Tesis Nuria-lq - digital

 FACTORES
QUE
AFECTAN
A
LA
COMPETENCIA ENTRE EL GALÁPAGO
LEPROSO
Y
EL
DE
N
(Mauremys
INTRODUCIDO
(Trachemys
FLORIDA
u
r
i
a
leprosa)
GALÁPAGO
P
o
l
o
C
TESIS DOCTORAL
scripta)
a
v
i
a
FACTORES QUE AFECTAN A LA
COMPETENCIA ENTRE EL GALÁPAGO
LEPROSO ( M auremys leprosa )
Y EL INTRODUCIDO GALÁPAGO
DE FLORIDA ( T rachemys scripta )
Nuria Polo Cavia
TESIS DOCTORAL
Madrid 2009
La presente tesis ha sido realizada en el Departamento de Ecología Evolutiva del Museo Nacional
de Ciencias Naturales (Consejo Superior de Investigaciones Científicas), Madrid, España. Diversos
proyectos financiados por el antiguo Ministerio de Educación y Ciencia y por el actual Ministerio
de Ciencia e Innovación, así como una beca predoctoral para la Estación Biológica de El
Ventorrillo (CSIC) y una beca de posgrado para la Formación del Profesorado Universitario
(MEC) han permitido el desarrollo de las investigaciones. Todos los experimentos cumplieron con
las leyes estatales y de las Comunidades Autónomas donde fueron llevados a cabo.
Ilustraciones: Nuria Polo Cavia
Foto de portada: Mauremys leprosa. Nuria Polo Cavia
UNIVERSIDAD AUTÓNOMA DE MADRID
FACULTAD DE CIENCIAS
Departamento de Biología
FACTORES QUE AFECTAN A LA COMPETENCIA
ENTRE EL GALÁPAGO LEPROSO (Mauremys leprosa)
Y EL INTRODUCIDO GALÁPAGO DE FLORIDA
(Trachemys scripta)
Memoria presentada por Nuria Polo Cavia para optar al Grado
de Doctor por la Universidad Autónoma de Madrid,
bajo la dirección del Dr. José Martín Rueda y de la Dra. Pilar López Martínez,
y la tutela académica del Dr. Francisco Javier de Miguel Águeda
Madrid, octubre de 2009
Nuria Polo Cavia
Vº Bº
José Martín Rueda
Vº Bº
Pilar López Martínez
Vº Bº
Fº Javier de Miguel Águeda
Nuria Polo Cavia
Departamento de Biología
Facultad de Ciencias
Universidad Autónoma de Madrid
Ciudad Universitaria de Cantoblanco
28049 Madrid, Spain
[email protected]
José Martín Rueda
Departamento de Ecología Evolutiva
Museo Nacional de ciencias Naturales, CSIC
José Gutiérrez Abascal, 2
28006 Madrid, Spain
[email protected]
Pilar López Martínez
Departamento de Ecología Evolutiva
Museo Nacional de ciencias Naturales, CSIC
José Gutiérrez Abascal, 2
28006 Madrid, Spain
[email protected]
Fº Javier de Miguel Águeda
Departamento de Biología
Facultad de Ciencias
Universidad Autónoma de Madrid
Ciudad Universitaria de Cantoblanco
28049 Madrid, Spain
[email protected]
A mis padres
Página siguiente
Un galápago de
Florida se aproxima
con determinación
al tronco sobre el
que descansan tres
galápagos leprosos
♥♦♣♠
The true
mystery of the world is
the visible, not the invisible.
—OSCAR WILDE, 1890
CONTENIDOS
Agradecimientos….………………………………………………………...
xiii
Introducción general………………………………………………..….…..
1
Las invasiones biológicas……………………………………..……
1
El galápago leproso…………………………………..…………….
16
El galápago de Florida………………………………………...........
18
Interacciones competitivas entre galápagos nativos e invasores....
20
Justificación y objetivos.……………………….…………………..
22
Procedimiento…………..………………………………..………...
26
Capítulos
1. Diferencias interespecíficas en las respuestas quimiosensoriales
de galápagos: consecuencias en la competencia entre especies
nativas e invasoras…………………………….…………………...
33
Interspecific differences in chemosensory responses of
freshwater turtles: consequences for competition between
native and invasive species……………………….……...……...…
35
2. Interacciones agresivas durante la alimentación entre especies
nativas e invasoras de galápagos…………………….……………..
49
Aggressive interactions during feeding between native and
invasive freshwater turtles………………………………………...
51
3. Interacciones competitivas durante la actividad de asoleamiento
entre especies nativas e invasoras de galápagos……………..….....
65
Competitive interactions during basking between native and
invasive freshwater turtle species…………………………………
67
4. Las diferencias interespecíficas en las tasas de intercambio de
calor pueden afectar a la competencia entre galápagos
introducidos y nativos……………………………………………..
85
Interspecific differences in heat exchange rates may affect
competition between introduced and native freshwater
turtles……………………………………………………………….
87
5. Relación entre el estado nutricional y los requerimientos de
asoleamiento de galápagos nativos e invasores……..……………..
105
Feeding status and basking requirements of freshwater turtles in
an invasion context………………………………………….……..
107
6. Efectos de la temperatura corporal en la respuesta de ‘giro’ de
galápagos nativos e invasores: consecuencias en la
competencia………………………………………..……………....
123
Effects of body temperature on righting performance of native
and invasive freshwater turtles: consequences for
competition…….…………….……………………….……………
125
7. Las diferencias interespecíficas en las respuestas al riesgo de
depredación pueden conferir ventajas competitivas a las especies
invasoras de galápagos……………………………….…………….
141
Interspecific differences in responses to predation risk may
confer competitive advantages to invasive freshwater turtle
species………………………………………………………………
143
8. La incapacidad de los renacuajos para reconocer depredadores
introducidos puede conferir ventajas competitivas a los
galápagos invasores…….………….……………………………….
157
Failed predator-recognition by tadpole prey may confer
competitive advantages to invasive turtle
predators…………………………………………….……………...
159
Síntesis de resultados y discusión………………………….….……………
173
Conclusiones………………………………………………………………..
185
Referencias………………………………………………………………….
187
Anexo…………………………………………………………………..……
199
Recuerdo con claridad el día en que llegué al Museo para comenzar mi
tesis doctoral. Acababan de concederme una beca predoctoral, y este
acontecimiento marcaría el inicio de una nueva etapa en mi vida. Sin
embargo, todo había empezado mucho antes, cuando ajena por completo al
mundo de la ciencia, comenzó a despertarse en mí el interés por la biología
evolutiva. Las preguntas más profundas sobre la vida, los organismos y
sus comportamientos tenían por fin una respuesta coherente con aquello
que observaba. Durante los últimos años de licenciatura, y más tarde, a lo
largo del doctorado, empecé a comprender los mecanismos que explican
el devenir de la historia natural, y a llamar a los procesos por su nombre.
Desde entonces, son muchas las personas que he encontrado en el camino
con las que he podido compartir mi pasión por comprender el verdadero
misterio de la vida. A ellas les debo en parte lo que soy, y desde luego, la
consecución de esta tesis.
En primer lugar, quiero expresar mi agradecimiento a mis directores, José
Martín y Pilar López, dos personas fundamentales que me han apoyado desde
el principio, guiando cada uno de mis pasos. A ellos les debo su confianza,
su paciencia conmigo, y el perdonármelo todo. Su continua orientación y
dedicación han hecho posible la realización de esta tesis.
Javier de Miguel ha sido un amigo incondicional durante todos estos años.
Desde que firmó mi tutela académica no he parado de importunarle (ya en
aquella ocasión le interrumpí en mitad de una reunión de departamento).
Sin embargo, aceptó con resignación mi marcha al Museo, recibiéndome
pacientemente cada vez que necesitaba resolver algún trámite universitario
y participando en cada uno de mis logros. De vuelta en la Autónoma, tengo
Ilustración | Galápagos exóticos se asolean sobre un tronco flotante
Agradecimientos
Agradecimientos
xiii
que agradecerle el compartir su despacho y sus jornadas conmigo, su
meticulosa revisión de erratas, y el aguantarme sin volverse loco durante
la edición y el maquetado de esta tesis.
A José Luis Rubio le debo muchos de mis conocimientos evolutivos y
el haberme descubierto el camino de la ciencia en el momento más oportuno,
lo bueno y lo malo de este mundo, las puertas a las que llamar y aquéllas de
las que huir. A Vicente Polo, el resolver mis problemas matemáticos al
aplicar la física a la biología, y a Santiago Merino, el ayudarme a discriminar
los diferentes tipos de leucocitos en los frotis sanguíneos (aunque ese
trabajo no aparezca reflejado en estas páginas). Alfonso Marzal me permitió
trabajar con total libertad en sus dehesas de Olivenza. Su generosidad y la
de los suyos facilitaron enormemente el trabajo de campo de esta tesis.
En California, el Dr. Tag Engstrom me abrió las puertas de su laboratorio,
dándome la oportunidad de ampliar mis perspectivas investigadoras. Les
estaré por siempre agradecida, a él y a todas las personas que hicieron de
aquélla una experiencia realmente fascinante. Gracias también a Luisma
Carrascal, por atender alguna que otra duda estadística, y a Luis Miguel Bautista
y a Antonio García-Valdecasas, por animarme con mi futuro posdoctoral.
A mis compañeros y amigos del Museo, Carlos, Adega y Marianne, les
estoy especialmente agradecida por todos los buenos momentos que
hemos compartido. Con vosotros me he reído tanto que habéis convertido
el trabajo de cada día en un verdadero placer. Gracias por apuntarme datos en
El Ventorrillo (a veces dos manos no son suficientes) y por cuidar de mis
galápagos en los momentos de ausencia. A Carlos le debo el actualizarme de
continuo “los últimos hallazgos científicos”, las conversaciones –largas y
acaloradas- sobre ciencia en las sobremesas de El Ventorrillo, el hacerme reír
con cualquier cosa y el aguantar mi mala costumbre de cuestionarlo todo
(a veces con razón, ¿eh?). A Adega, su extraordinaria colaboración en el
campo (¿recuerdas cuando cogimos el primer Mauremys en Colmenar?), el
preocuparse siempre por mí (sobre todo en Badajoz), las confidencias y esa
extraña confianza que existe entre las dos (sabes que puedes contar conmigo,
nena). A Marianne, el soportar mis “gloriosas” frases en francés y el
sorprenderme con su divertida forma de ver la vida. Gracias también a mis
compañeros de la “11 11” (y alrededores) y al resto de personal del Museo, que
hicieron más entretenidas las jornadas de trabajo y facilitaron los trámites, las
gestiones y el papeleo.
A todas las personas con las que coincidí en El Ventorrillo (becarios,
voluntarios e investigadores), gracias por todos los ratos estupendos que hemos
echado en la pradera y en los bares de Cercedilla y Navacerrada. Gracias, en
especial, a Nino, una persona encantadora, voluntariosa y diligente, siempre
presto a ayudarnos a todos. Sin él, El Ventorrillo no sería el mismo lugar.
xiv
Quiero agradecer también a mis compañeros de la Unidad de Zoología de
la Universidad Autónoma de Madrid el darme la oportunidad de trabajar
con ellos, de disfrutar de la docencia, y por qué no, de terminar esta tesis con
un poco más de tiempo y tranquilidad. Isabel, Raquel y Lucía son, además
de Javier, las personas con las que he compartido más tiempo, excursiones y
buenas conversaciones durante las comidas y los cafés, estrechando nuestra
amistad en el día a día.
A los organismos GREFA y EXOTARIUM, que cedieron voluntariamente
ejemplares de galápago para los experimentos de esta tesis, y al MNCN y a
la Estación Biológica de El Ventorrillo, que pusieron a mi disposición los
medios necesarios para que fuera posible llevar a cabo este proyecto.
Por último, mi más sincero agradecimiento a mi familia y amigos, por
animarme siempre y por comprender mis “perdonadme, estoy muy liada…”, y
muy en particular a mis padres, Arturo y Esperanza, quienes han sido un
verdadero estímulo para mi trabajo, demostrándome siempre su apoyo
incondicional y su confianza férrea.
Nuria Polo Cavia
Agradecimientos
Madrid, octubre de 2009
xv
xvi
— INTRODUCCIÓN GENERAL —
Las invasiones biológicas
L
a introducción de seres vivos fuera de su área de distribución natural
representa, tras la pérdida del hábitat, la segunda causa de amenaza a la
biodiversidad global (Wilcove et al. 1998; Gurevitch y Padilla 2004). Hoy
en día, gran cantidad de especies son transportadas diariamente por el ser
humano, de forma accidental o intencionada, estableciéndose en zonas
geográficas que no forman parte de sus rangos históricos, alterando la estructura
y el funcionamiento de los ecosistemas y desplazando especies nativas de sus
nichos ecológicos (Herbold y Moyle 1986; Williamson 1996). Este proceso es
conocido en biología de la conservación como invasión biológica. En el último
siglo, los fenómenos de invasión se han multiplicado sobremanera debido al
mayor desarrollo y a la creciente intervención humana en el ecosistema. Así,
una especie que por medios naturales necesitase del orden de miles de años para
alcanzar una nueva región biogeográfica, hoy podría lograrlo en tan sólo un día.
El aislamiento geográfico constituye una de las principales vías de especiación
natural (i.e., especiación vicariante, Mayr 1963). Barreras físicas tales como
océanos, valles, cadenas montañosas o placas de hielo representan límites que
impiden el desplazamiento de los individuos entre poblaciones de una misma
especie. Con el tiempo, las poblaciones que se mantienen separadas tienden a
divergir entre sí empujadas por las fuerzas de la deriva génica y la selección
natural, dando lugar a especies únicas bien diferenciadas. En una etapa
posterior, las barreras geográficas que motivaron la especiación pueden ser
eliminadas de forma natural por eventos climatológicos o alteraciones
geológicas, permitiendo la dispersión de estas nuevas especies y la expansión de
sus rangos. Por ejemplo, durante el Mioceno, cuando el istmo de Panamá
irrumpió la vía acuática de los trópicos americanos conectando Norte y Sur
América, los mamíferos norteamericanos migraron hacia el sur, mientras que las
aves y las plantas de los bosques lluviosos suramericanos expandieron sus rangos
de distribución hacia el norte (Marshall et al. 1982). Estas expansiones naturales,
INTRODUCCIÓN GENERAL: Las invasiones biológicas
BARRERAS GEOGRÁFICAS E INTRODUCCIONES HISTÓRICAS
1
inusualmente rápidas, han sido estudiadas por ecólogos y paleontólogos,
considerándose parte de la historia biológica de La Tierra.
Sin embargo, desde que el hombre ha tenido capacidad de dispersión entre
los continentes, las migraciones humanas han abierto brechas en las barreras
geográficas, interrumpiendo el aislamiento natural y permitiendo el flujo de
especies entre ámbitos muy alejados espacialmente. Muchos archipiélagos del
Mediterráneo y la Polinesia fueron poblados en tiempos prehistóricos antes del
Neolítico –en algunos casos incluso durante el Paleolítico-, manteniéndose la
comunicación entre las islas (Schüle 2000; Matisoo-Smith 2002; Hurles et al.
2003; Matisoo-Smith y Robins 2004). En la Antigüedad y la Edad Media, la
expansión de la agricultura y la navegación favorecieron el transporte de
materiales y la colonización, estableciéndose un flujo principal de Oriente hacia
Occidente. Pero fue tras las primeras expediciones transoceánicas del siglo XV,
y en especial tras el descubrimiento de América, cuando se abrieron las grandes
rutas comerciales marítimas que propiciaron la conexión intercontinental a gran
escala y la aceleración en la transferencia de organismos. Desde entonces,
millares de especies han sido regularmente transportadas junto con las personas,
los animales domésticos y las importaciones (Crosby 1986). Al igual que los
grupos de mamíferos, aves y plantas que expandieron sus rangos geográficos
durante el gran intercambio biótico americano (Marshall et al. 1982), algunas de
estas especies se establecieron en territorios que previamente se encontraban
fuera de su alcance, colonizando con éxito los nuevos ambientes. Pero esta vez,
en cambio, los colonizadores extendieron su distribución con la ayuda del
hombre.
INTRODUCCIONES MODERNAS
El protagonismo que el descubrimiento y la colonización del Nuevo Mundo
tuvieron en la introducción de nuevas especies en el viejo continente es
extremo, hasta el punto de que, en Europa, las especies introducidas se clasifican
en arqueófitos (introducidas antes de 1500) y neófitos (introducidas después de
1500). A raíz de la conquista de América, las potencias europeas impulsaron
enormemente sus viajes de exploración, a la par que la aclimatación de especies
exóticas se convirtió en una línea prioritaria tanto para naturalistas e
investigadores como para los propios colonos y las soberanías, que introducían
cultivos y otras especies de utilidad en el Nuevo y en el Viejo Mundo. Así,
además de los trasvases accidentales, empezaron a producirse intercambios
masivos intencionados por conveniencia del ser humano. A mediados del siglo
XIX, en el máximo apogeo de la revolución industrial y del colonialismo
moderno, proliferaron los jardines botánicos y las sociedades de aclimatación en
toda Europa y en las colonias, cuya misión última era la introducción y
2
aclimatación de animales y plantas para el abastecimiento humano y el mayor
bienestar económico (Lever 1992; Dunlap 1997). Ya en el último siglo, el
desarrollo económico, el progreso tecnológico y el avance de las comunicaciones
han disparado el impacto del hombre sobre el medio natural, incrementando el
número de vectores de introducción, y facilitando así la transferencia –intencional
o involuntaria- de una mayor cantidad de especies y su posterior supervivencia
en los nuevos territorios.
Al igual que la extinción de especies, las invasiones biológicas son un fenómeno
natural. Numerosas especies son capaces de atravesar grandes distancias
aprovechando los vientos favorables o las corrientes oceánicas (Bush 1991; Mack
y Lonsdale 2001; Mack 2004). En algunas ocasiones, incluso, las expansiones
históricas han ocurrido en periodos de tiempo relativamente cortos (Vermeij
2005). No obstante, los ecólogos diferencian entre expansiones naturales y
expansiones mediadas por el ser humano, al igual que distinguen las extinciones
naturales de aquellas otras en las que existe algún tipo de intervención antrópica.
La principal diferencia entre los procesos de colonización naturales y las
introducciones mediadas por el hombre radica en la magnitud de la velocidad y
la escala geográfica a la que se producen ambos sucesos. Las tasas de invasión
históricas han sido calculadas en islas oceánicas como Hawai o la isla de Gough,
al sur del Atlántico. Al comparar estas tasas con los ritmos de introducción
actuales, se encontró una aceleración asombrosa en el número de especies
nuevas por unidad de tiempo que han alcanzado estos remotos lugares en el
curso de la historia. La razón de tal incremento en las tasas de invasión es sin
duda el profundo cambio que el hombre ha inducido en los vectores de
transporte y en las vías de entrada de las especies exóticas, ampliándolas y
diversificándolas con respecto a las disponibles en los procesos de colonización
natural (ver Tabla 1, con diversos ejemplos de especies introducidas y sus
respectivas vías de entrada). Las especies exóticas pueden constituir una fuente de recursos (alimenticios,
medicinales, cinegéticos, silvícolas o experimentales), o ser de interés
ornamental (jardinería, mascotas, etc.). En estos casos, su transporte se realiza
deliberadamente, de forma legal o clandestina, con fines determinados. Estas
introducciones se consideran por tanto intencionadas. Por otra parte, en las
últimas décadas, la intensificación de los movimientos humanos, el comercio y
las alteraciones topográficas del paisaje han contribuido a acrecentar el trasvase
involuntario de numerosas especies. Este tipo de introducciones no
intencionadas se produce de forma accidental, pero siempre a través de agentes
antropogénicos. Así, por ejemplo, los vehículos, las embarcaciones y las aguas de
INTRODUCCIÓN GENERAL: Las invasiones biológicas
VÍAS DE ENTRADA
3
Tabla 1 Diversos ejemplos de introducciones y vías de entrada de especies exóticas
Tipo
Vía-Propósito
Producción de
alimento
Fines
medicinales
Producción de
madera
Procesos
industriales
Intencionadas
Caza y pesca
recreativa
Alimentación
de animales en
producción
4
Especie
Fuente
Achillea millefolium,
Rumex acetosella
Mack 2003
Opuntia ficus-indica
Capdevila-Argüelles y
Zilletti 2006
Lates niloticus
Goldschmidt et al. 1993;
Ogutu-Ohwayo 1993
Capra hircus
Genovesi 2005
Ovis aries
Genovesi et al. 2009
Sus scrofa
Vigne et al. 2003
Oryctolagus cuniculus
Flux y Fullagar 1992
Hypericum perforatum
Mack 2003
Pinus halepensis
Lavi et al. 2005
Acacia spp., Robinia
pseudoacacia
Capdevila-Argüelles y
Zilletti 2006
Artemia franciscana
Sorgeloos et al. 1986; Amat
et al. 2005
Anas platyrhynchos
Long 1981
Phasianidae
Lockwood 1999
Ovis orientalis
Pascal et al. 2003; SantiagoMoreno et al. 2004
Ammotragus lervia
Casinello 2000; Serrano et al.
2002
Cervidae
Lever 1985
Micropterus spp., Ictalurus
spp.
Moyle 2002
Salvelinus fontinalis
Elvira y Almodóvar 2001;
Moyle 2002
Oncorhynchus mykiss
Lever 1996; Elvira y
Almodóvar 2001
Esox lucius, Micropterus
salmoides, Perca fluviatilis,
Silurus glanis, Stizostedion
lucioperca
Elvira y Almodóvar 2001
Artemia franciscana
Sorgeloos et al. 1986
Pueraria montana
Miller y Edwards 1983
Caulerpa taxifolia,
Sargassum muticum
Siguan 2004
Acacia spp., Eichhornia
crassipes, Robinia
pseudoacacia,
Capdevila-Argüelles y
Zilletti 2006
Cyprinus carpio, Carassius
auratus
Elvira y Almodóvar 2001
Sturnus vulgaris
Dunlap 1997
Oxyura jamaicensis
Capdevila-Argüelles y
Zilletti 2006
Acacia spp.
Gardner 2001; Ferrari y
Wall 2004
Casuarina spp., Leucaena
leucocephala
Ferrari y Wall 2004
Freno de
erosión
Acacia dealbata, Chloris
gayana
Sanz-Elorza et al. 2004
Estabilización
dunar
Acacia melanoxylon,
Carpobrotus edulis
Sanz-Elorza et al. 2004
Euglandina rosea
Cowie 1998, 2001
Triops newberry
Su y Mulla 2002
Gambusia affinis
Lever 1996
Gambusia holbrooki
Elvira y Almodóvar 2001
Herpestes javanicus
Simberloff et al. 2000
Ornamentación
y paisajismo
Mejora del
suelo
Control de
plagas
Tipo
Procambarus clarkii
Gutiérrez-Yurrita et al. 1999
Declive y
sustitución de
especies nativas
Rutilus rutilus, Scardinius
erythrophthalmus,
Ameiurus melas, Lepomis
gibbosus
Elvira y Almodóvar 2001
Vía
Especie
Fuente
Fungi
Palm y Rossman 2004
Polychaeta
Hendrix y Bohlen 2002
Rhynchophorus
ferrugineus
Capdevila-Argüelles y
Zilletti 2006
Ascidiella aspersa
Carlton 1996
Hydroides spp.
Galil 2001
Womersleyella setacea
Boudouresque 2005
Dreissena polymorpha
Capdevila-Argüelles y
Zilletti 2006
Asociación a
sustrato
No
intencionadas
Embarcaciones
INTRODUCCIÓN GENERAL: Las invasiones biológicas
Tabla 1 - Continuación 5
Tabla 1 - Continuación Dreissena polymorpha
Capdevila-Argüelles y
Zilletti 2006
Rapana venosa
Zenetos et al. 2003
Callinectes sapidus
Galil et al. 2002
Dreissena polymorpha
Jiménez Mur 2001
Migraciones lessepsianas
Por 1978
Plasmodium relictum
Warner 1968; Van Riper et
al. 1986
Bothriocephalus
acheilognathi
Salgado-Maldonado y
Pineda-López 2003
Miconia calvescens
Medeiros et al. 1997
Transporte de
mercancías
Aedes albopictus
Eritja et al. 2005
Linepithema humile
Gómez y Espadaler 2004
Vía
Especie
Fuente
Caulerpa taxifolia
Meinesz 1999
Cerion spp.
Cowie y Robinson 2004
Cyprinodon diabolis
Sigler y Sigler 1987
Acipenser baerii, Gobio
gobio, Oncorhynchus
kisutch, Ictalurus
punctatus
Elvira y Almodóvar 2001
Mustela vison
Bravo y Bueno 1999
Myocastor coipus
Capdevila-Argüelles y
Zilletti 2006
Caulerpa taxifolia
Jousson et al. 2000
Opuntia tunicata
Escudero 2003
Trachemys scripta
Pleguezuelos 2002
Myiopsitta monachus,
Psittacula kramerii,
Estrilda astrild, Amandava
amandava
Martí y Del Moral 2003
Rana catesbeiana
Pleguezuelos 2002
Procyon lotor
Kahuala 1996
Myocastor coipus
Capdevila-Argüelles y
Zilletti 2006
Mustela vison
Bravo y Bueno 1999;
Hammershøj 2004
Aguas de lastre
Eliminación de
barreras
geográficas
Otros
organismos
como vectores
Tipo
Escapes de
granjas,
zoológicos,
jardines
botánicos o
centros de
investigación
Negligencias
Desechos de
jardinería
Liberación de
mascotas
Abandono de
explotaciones
Liberaciones
animalistas
6
lastre, o las propias personas, son susceptibles de transportar propágulos y
semillas, larvas, parásitos u otros organismos. De forma similar, la apertura de
canales ha permitido la entrada masiva de especies marinas originarias de unos
mares a otros (como fue el caso del canal de Suez o del canal de Panamá). A
estas dos formas principales de entrada hay que añadir las negligencias (escapes
de granjas, desechos de jardinería, liberación de mascotas, etc.), que sin ser
introducciones intencionadas (pues no se persigue el establecimiento de una
población silvestre), suceden con conocimiento de causa por falta de
concienciación o medidas de precaución.
Toda invasión comienza con la recolección de un grupo de individuos (a veces
incluso de un solo individuo), que es extraído de su rango original, transportado
a un nuevo territorio y liberado en el medio natural. Estos individuos deben
entonces ser capaces de establecerse como una población autónoma en su nuevo
hábitat, produciéndose la extinción en otro caso. Tras el establecimiento, la
población no nativa puede incrementar el número de individuos que la
sustentan y expandir su rango geográfico, o bien, mantener sus efectivos y su
distribución dentro de un margen restringido (Cuadro 1). En general, sólo
cuando una población no nativa ha conseguido expandirse y aumentar su
tamaño es capaz de ocasionar algún tipo de daño ecológico o económico, y por
tanto, puede ser considerada “invasora” (ver Cuadro 2 para más información
sobre la terminología utilizada en el contexto de las invasiones biológicas).
Aun cuando en la realidad estas etapas pueden confundirse, sobrepasar cada
una de ellas requiere la superación de ciertas barreras ecológicas que pueden
llegar a identificarse. Williamson (1996) fue uno de los primeros ecólogos en
representar el fenómeno de invasión como la progresión de una especie nueva
en un ecosistema a través de una serie de barreras. Uno de los puntos clave de
este modelo es la comprobación de que la mayoría de las especies no logran
transitar de una fase a otra del proceso de invasión. De acuerdo con las
investigaciones de Williamson (1996), sólo entre el 5 y el 20 % de las especies
no nativas consiguen alcanzar la siguiente fase, siendo el promedio del 10 %
(patrón que Williamson denominó “regla de los 10”). Si bien se ha demostrado
recientemente que este patrón no siempre se cumple (la identidad de la especie
invasora, las características del ecosistema receptor y la frecuencia de las
introducciones juegan un papel determinante), la aproximación de Williamson
sugiere dos importantes presunciones. En primer lugar, la estructura anidada de
las invasiones biológicas asegura que tan sólo una pequeña fracción del total de
especies que son introducidas fuera de sus rangos naturales causará un impacto
ecológico o económico. En segundo lugar, las barreras entre las fases de invasión
INTRODUCCIÓN GENERAL: Las invasiones biológicas
EL PROCESO DE INVASIÓN
7
Cualquier especie no nativa
debe superar una serie de
fases antes de ocasionar un impacto en el ecosistema (e.g., Kolar y Lodge
2001; Fig. 1). El conjunto de estas fases es lo que se ha dado en denominar
proceso de invasión. Diversos filtros actúan en las diferentes etapas del
proceso, evitando que las especies trasvasadas acaben invariablemente por
convertirse en especies invasoras ■
Figura 1 Fases discretas del proceso de invasión y alternativas
para cada fase. Fuente: modificado de Lockwood 2007
Cuadro 1 Modelo de Kolar y Lodge (2001), esquematizando las fases del proceso de invasión
son extraordinarias. Surge entonces una pregunta: ¿por qué unas especies son
capaces de rebasar exitosamente estas barreras mientras que otras no logran
culminar el proceso de invasión?
DE LA INTRODUCCIÓN A LA INVASIÓN: DETERMINANTES DEL ÉXITO
Como se ha visto, las invasiones biológicas constituyen sólo uno de los posibles
resultados de un proceso de fases anidadas que comienza cuando los organismos
son transportados desde sus hábitats originales a nuevas áreas locales. Así, las
consecuencias últimas de una introducción dependen tanto de la capacidad de la
especie introducida para adaptarse a un hábitat extraño como de la capacidad de
las especies nativas para acomodarse o resistir la presencia del invasor
(Lockwood 2007). En otras palabras, son tanto las características del invasor
como las propiedades de la comunidad que lo acoge las que determinan el éxito
o el fracaso de la invasión. Diversos experimentos en laboratorio han
demostrado que el orden de introducción de las especies en un ecosistema
8
La terminología utilizada en el marco de las invasiones biológicas
puede variar ligeramente de unos autores a otros (Tablas 2 y 3). Esta
variabilidad en el criterio de los autores, unida a la existencia de términos
sinónimos, ha generado cierta confusión semántica.
En general, los términos “introducida”, “exótica”, “alóctona”, “foránea” o “no
nativa” (“alien” en inglés) hacen referencia a una especie originaria de otra
región y pueden considerarse sinónimos (Vilà et al. 2008). En función de
la fase que alcanzan en el proceso de invasión, las especies trasvasadas
pueden calificarse como “transitorias” o “casuales”, si no han sido liberadas en
el medio; “adventicias”, si se ha producido su liberación (o escape), pero no
llegan a establecer poblaciones autosustentables en sus nuevos territorios,
sino que su persistencia depende de la proximidad a zonas antropizadas
y/o de la entrada continuada de nuevos individuos; “naturalizadas” o
“establecidas”, si son capaces de mantener sus poblaciones de forma
totalmente autónoma; o “invasoras”, en el caso de que se expandan a gran
velocidad lejos del foco de introducción. Cuando las especies invasoras
Especies que ocupan su área de distribución original
Nativas
Autóctonas
Indígenas
Especies que se encuentran fuera de su área de distribución
natural
Introducidas
Exóticas
Foráneas
Alóctonas
No nativas
Importadas
Especies introducidas que se extienden de forma autónoma, pero
dependientes de sistemas humanizados, o sin capacidad para
perdurar en los territorios ocupados
Adventicias
Subespontáneas
Casuales
Especies introducidas que se extienden a ecosistemas naturales,
donde tienen capacidad de mantener poblaciones de forma
autónoma
Naturalizadas
Establecidas
Especies naturalizadas con gran capacidad de propagación, en
número de individuos y/o en distancia
Invasoras
Especies naturalizadas con gran capacidad de propagación,
capaces de alterar sustancialmente los ecosistemas nativos y/o
ocasionar impactos económicos
Transformadoras
Pestes
Plagas
Cuadro 2 Terminología de las invasiones biológicas
INTRODUCCIÓN GENERAL: Las invasiones biológicas
Tabla 2 Términos más comunes relacionados con las especies invasoras. Fuente:
modificado de Vilà et al. 2008
9
generan un impacto ambiental o socioeconómico, se utilizan términos tales
como especies “transformadoras”, “pestes” o “plagas”, en función de la
magnitud del daño, rigiéndose por un criterio antropocéntrico. Otros
autores prefieren considerar como invasoras solamente a aquellas especies
que han alterado el medio natural, desplazando especies nativas, provocando
cambios en los ciclos de nutrientes, daños en las infraestructuras, etc. Sin
embargo, el impacto real de una especie introducida es en muchas
ocasiones desconocido, por lo que se recomienda utilizar conjuntamente
el criterio de expansión (en abundancia o distribución) de sus poblaciones
(Richardson et al. 2000; Colautti y MacIsaac 2004). En otros casos, se ha
dado en llamar invasoras a determinadas especies nativas que han
expandido sobremanera sus rangos tras beneficiarse de una variación en el
ambiente, en lugar de hablar de especies “colonizadoras” u “oportunistas” ■
Tabla 3 Listado de términos recopilados por Lockwood et al. (2007) a partir de varios
autores, utilizados para designar a las especies no nativas en relación a las fases del proceso
de invasión (transporte, establecimiento, expansión e impacto). Es interesante observar
que algunos de estos términos han sido aplicados también a las especies nativas. Fuente:
modificado de Lockwood et al. 2007 (basado en Colautti y MacIsaac 2004)
FASE DE INVASIÓN
Adventicias
Alien
Casuales
Colonizadoras
Criptogénicas
Escapadas
Establecidas
Exóticas
Foráneas
Importadas
Invasoras
Naturalizadas
No indígenas
Nocivas
Perturbadoras
Peste
Transformadoras
Transitorias
Translocadas
Transportadas
Trasplantadas
NATIVAS
NO NATIVAS
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
Transp.
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
Cuadro 2 - Continuación
10
Establ.
Expans.
Impacto
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
y
INTRODUCCIÓN GENERAL: Las invasiones biológicas
determina las relaciones entre especies y la estructura final de la comunidad
(Drake 1991; Price y Morin 2004). En este sentido, las especies nativas, así como
las no nativas previamente establecidas, pueden facilitar u obstaculizar el
establecimiento de nuevas especies exóticas, a través de interacciones bióticas
tales como la competencia, la depredación o el mutualismo, dando lugar a
asociaciones tanto positivas como negativas entre las especies recién
introducidas y las residentes. Así, por ejemplo, una especie exótica podría
recalar en un hábitat con bajos niveles de competencia y/o carente de
depredadores (o que albergue a un depredador de sus depredadores habituales),
o establecer una relación simbionte con una o más especies nativas que
favorezca su rápida proliferación (Hoopes 1999; Simberloff y Von Holle 1999;
Richardson et al. 2000; Facelly y Temby 2002; Kimball y Schiffman 2003; Adam
et al 2003). Por el contrario, esta nueva especie podría enfrentarse con eficaces
competidores y/o depredadores, o con la ausencia de un mutualista obligado, lo
que contendría su expansión en el nuevo hábitat (Nadel et al. 1992; Simberloff
et al 2002; Hunt y Behrens Yamada 2003; Green et al. 2004).
En general, las especies introducidas que acaban por convertirse en invasoras
suelen presentar una amplia valencia ecológica (capacidad de adaptación a
diversos hábitats), basan su ecología reproductiva en la estrategia de la r (amplia
procreación con escasa dedicación a las crías), tienden a asociarse con hábitats
antrópicos o situaciones de comensalismo con el hombre, y es común que su origen
se encuentre en continentes con faunas diversas y saturadas (Sax y Brown 2000;
Kolar y Lodge 2001). Por otro lado, un alto grado modificaciones de origen
antrópico en el medio, y la ausencia de enemigos de las especies introducidas
entre la fauna nativa, son características propias de las regiones que padecen
invasiones (Fox y Fox 1986; Smallwood 1994; Ewell 1999; Sax y Brown 2000).
Charles Elton (Cuadro 3) propuso en 1958 que las áreas con mayor
diversidad de especies indígenas presentan una mayor resistencia a las
invasiones biológicas que aquellas que albergan un menor número de especies
nativas (Elton 1958, The ecology of invasions by animals and plants). Esta
hipótesis se halla en consonancia con los modelos clásicos de competencia, que
sugieren que un gran número de competidores genera un intenso uso del
espacio y los recursos, dejando pocos nichos vacíos que puedan ser aprovechados
por nuevas especies. Desde un punto de vista ecológico, es también razonable
contemplar los puntos calientes de biodiversidad como espacios menos proclives
a sufrir invasiones (Kennedy et al. 2002). Sin embargo, la presunción de Elton
encierra una importante paradoja: los factores ecológicos que promueven una
mayor riqueza de especies nativas deberían favorecer también la diversidad de
especies no nativas. La solución a este dilema no es sencilla. Varios
experimentos a escala local (Tilman 1999; Kennedy et al. 2002) y algunos
modelos matemáticos (e.g., Case 1990) apoyan la hipótesis de Elton, mientras
11
Charles
Sutherland Elton
(1900-1991) —Biólogo y
naturalista inglés nacido en Manchester, se graduó en zoología por la
Universidad de Oxford en 1922. Fue uno de los primeros científicos en
estudiar los animales en su medio natural, desarrollando los conceptos de
cadena alimentaria y nicho ecológico, y estableciendo así los principios de
la ecología moderna. Su obra, The ecology of invasions by animals and
plants, escrita en 1958, pocos años antes de retirarse de su cargo en la
Universidad de Oxford, significó la consolidación de la ecología de las
invasiones como una disciplina nueva y diferenciada ■
Cuadro 3
que un gran número de estudios observacionales a gran escala y la mayoría de
los modelos matemáticos sostienen la relación contraria (Lonsdale 1999;
Stohlgren et al. 1999, 2003). Por ejemplo, comparando el número de especies no
nativas establecidas en un amplio grupo de regiones, Lonsdale (1999) encontró
tasas de establecimiento de especies exóticas mayores en las islas que en las
regiones continentales, y mayores en el Nuevo Mundo comparadas con las del
viejo continente. Lonsdale atribuyó estos resultados a la existencia de un patrón
geográfico subyacente. Pero su modelo sugería, además, que la riqueza de
especies nativas se halla positivamente correlacionada con la riqueza de especies
no nativas, con independencia de la ubicación o grado de protección del área
considerada. La razón de esta aparente contradicción entre los patrones
obtenidos a gran escala y los resultados de los experimentos a pequeña escala
descansa probablemente en la importancia relativa de las relaciones
interespecíficas a las diferentes escalas espaciales (Huston 1999; Davies et al.
2005; Lockwood 2007). Mientras que a escala local el establecimiento de nuevas
especies en la comunidad se encuentra principalmente limitado por factores
intrínsecos como la competencia, a gran escala las interacciones bióticas pierden
importancia, en contraposición a las fuerzas extrínsecas que determinan la
diversidad de especies en la comunidad, tales como la producción primaria o la
heterogeneidad de los recursos.
IMPACTO ECOLÓGICO
La introducción de especies exóticas constituye, tras la pérdida del hábitat, la
segunda causa de amenaza a la biodiversidad global (Wilcove et al. 1998;
Gurevitch y Padilla 2004). En numerosas ocasiones, las especies invasoras han
alterado comunidades terrestres y acuáticas, desviando flujos de energía y
desplazando especies nativas de sus nichos ecológicos (Herbold y Moyle 1986;
12
INTRODUCCIÓN GENERAL: Las invasiones biológicas
Williamson 1996). Los efectos de estas introducciones son generalmente
impredecibles (a no ser que la demografía, el uso de los recursos y las relaciones
bióticas de las especies hayan sido cuidadosamente investigados), pero procesos
tales como la contaminación genética, la depredación, la transmisión de
patógenos y/o la competencia entre especies nativas e invasoras aparecen con
frecuencia a consecuencia de este tipo de alteraciones (Dodd y Seigel 1991;
Shigesada y Kawasaki 1997; Butterfield et al. 1997; Manchester y Bullock 2000;
Mack et al. 2000; Lockwood et al. 2007).
A nivel genético, las especies exóticas pueden afectar a la integridad
genética de las especies indígenas, vía hibridación o introgresión (Krueger y
May 1991). Los cruzamientos entre especies nativas e invasoras pueden generar
descendencia estéril, lo que supone una reducción en la reproducción de los
individuos nativos debido al desperdicio de gametos (Rhymer y Simberloff
1996), o fértil, en cuyo caso los híbridos pueden constituir un nuevo genotipo
invasor (Anttila et al. 1998; Ayres et al. 2004). Además, la descendencia fértil
puede hibridar con las especies parentales, dando lugar a la introgresión y al
flujo génico entre especies, pudiendo conducir incluso a la extinción del
genotipo nativo (Dowling y Childs 1992; Rhymer et al. 1994).
Los impactos a nivel individual comprometen la supervivencia y el éxito
reproductor de los individuos. Producto de estos impactos son los cambios en la
morfología, los patrones de comportamiento y/o la demografía de las
poblaciones nativas a consecuencia de la introducción de depredadores,
competidores o transmisores de enfermedades (Parker et al. 1999; Mattila y Otis
2003; Orrock y Danielson 2004; Marra et al 2004). Así, los impactos ocasionados
sobre los individuos acaban por afectar a la estructura y distribución de las
poblaciones, cuyas densidades pueden verse fuertemente reducidas (Cree et al.
1995; Lesica y Shelly 1996; Pell y Tiedemann 1997). En casos de especies raras o
vulnerables, la especie nativa puede ser empujada a la extinción si los efectos
negativos se producen sobre su rango completo de distribución, o si persisten
durante el tiempo suficiente. No obstante, la extinción es la forma más extrema
de impacto a nivel poblacional.
Los impactos poblacionales generalizados sobre varias especies nativas
pueden traducirse en cambios sustanciales a nivel de la comunidad. Los
mamíferos herbívoros domésticos (i.e., Capra hircus, Ovis aries, Equus caballus,
Sus domestica, Oryctolagus cuniculus, entre otros) se encuentran entre las
especies causantes de las mayores transformaciones acaecidas en las
comunidades nativas, especialmente en ecosistemas insulares (Courchamp et al.
2003). El impacto de estos herbívoros introducidos se concentra en la base de la
cadena trófica, afectando en consecuencia a una gran cantidad de especies. La
presencia de invasores conduce por lo general a una “cascada” de alteraciones en
la estructura y composición de la comunidad (Porter y Savignano 1990; Allen et
13
al. 2001; Morrison 2002; Ness y Bronstein 2004; Orrock y Danielson 2004;
Smith et al. 2004; Lockwood et al. 2007 realiza una completa revisión de los
efectos derivados de la introducción de la hormiga Solenopsis invicta en el
sureste de los Estados Unidos). En algunos casos, las especies invasoras han
ocasionado impactos de tal magnitud que han llegado a provocar la extinción en
masa de un sinfín de especies nativas (la introducción de la perca del Nilo, Lates
niloticus, en el Lago Victoria a mediados del siglo XX constituye uno de los
ejemplos clásicos de extinción en masa a consecuencia de las invasiones
biológicas. La entrada de este depredador en la comunidad supuso la
desaparición de aproximadamente 200 especies de peces nativos; Witte et al.
2000). Estas extinciones han ocurrido con mayor frecuencia en ecosistemas
evolutivamente aislados, en los que la radiación adaptativa se ha producido en
ausencia de grandes depredadores o herbívoros.
Los cambios en el comportamiento de los individuos, la dinámica
poblacional y la estructura de las comunidades pueden finalmente generar
impactos a nivel de ecosistemas, transformando el medio físico o creando
nuevos regímenes de perturbación. Así por ejemplo, las especies invasoras son
capaces de alterar la salinidad de los hábitats riparios (Di Tomaso 1998), los
ciclos de nutrientes (Ehrenfeld 2003) y la disponibilidad de los recursos
(Vitousek 1990; Gardner 1995; Simon y Townsend 2003). Un caso particular es
el del mejillón cebra, Dreissena polymorpha, capaz de modificar los niveles de
nitrógeno, fósforo y carbono disponibles en el medio. Mediante el filtrado de
cantidades ingentes de agua a través de su tracto digestivo, este invasor genera
un incremento en la disponibilidad de nitrógeno y fósforo en la columna de
agua, a la vez que el carbono es desplazado hacia el fondo (Gardner 1995). De
forma similar, las plantas fijadoras de nitrógeno establecidas fuera de sus rangos
pueden alterar la disponibilidad de los recursos, mediando en la competencia
entre la flora nativa y la invasora, afectando a los procesos de sucesión y
transformando los ecosistemas (Vitousek 1990).
Aun cuando la mayor parte de las invasiones biológicas va ligada a la
pérdida de biodiversidad, numerosas áreas locales han experimentado un
incremento en la riqueza de especies tras la introducción de especies exóticas
(Sax et al. 2002; Sax y Gaines 2003). Sin embargo, el incremento y la reducción
de la diversidad no se producen de manera uniforme en los distintos grupos
taxonómicos. Las especies asociadas con los sistemas antrópicos son transportadas
con mayor probabilidad fuera de sus hábitats originales, y sus posibilidades de
supervivencia en los nuevos territorios son también mayores. En el otro extremo,
las especies endémicas que han evolucionado en ausencia de competidores,
depredadores o patógenos, o en ambientes ajenos a las perturbaciones humanas,
son proclives a sufrir recesiones. Esta pérdida de especies endémicas y el
aumento de las especies invasoras comporta un patrón bipolar emergente a gran
14
escala: un gran grupo de especies que desaparecen frente a un grupo reducido de
especies que prosperan a nivel global, haciéndose más y más numerosas
(McKinney y Lockwood 1999). En consecuencia, unas pocas especies comienzan
a estar presentes en casi todas las regiones del mundo, al tiempo que la fauna y
la flora de los ecosistemas que han sido invadidos se vuelven cada vez más
parecidas, especialmente entre aquellas regiones que comparten características
climáticas. Este proceso, conocido como homogeneización biótica (McKinney y
Lockwood 1999), avanza con sutileza, lo que dificulta en gran medida su
detección.
La preocupación por los problemas causados por las especies exóticas invasoras
es bastante reciente, en comparación con otras amenazas ambientales como la
contaminación, la erosión o la deforestación. En muchos países, la
Administración y la opinión pública son aún indiferentes a la necesidad de
prevención de las introducciones biológicas (De Klemm 1996). No obstante, el
interés de las autoridades e instituciones hacia la naturaleza y los problemas
ambientales se ha acrecentado en las últimas décadas. Este hecho, unido al
incremento en la concienciación social, ha favorecido un cambio en el panorama
de las invasiones biológicas, tanto a nivel de legislación, como en el número de
estudios científicos y artículos de divulgación que se han publicado en los
últimos años (Pleguezuelos 2002).
Así, las especies exóticas invasoras son actualmente una de las mayores
preocupaciones ecológicas a nivel internacional, objeto de esfuerzos de
numerosas instituciones protectoras de la biodiversidad. El papel de la Unión
Internacional para la Conservación de la Naturaleza (UICN) es clave en la
preservación de la fauna y de la flora nativas, evitando que se produzcan
mayores daños en los ecosistemas. Recientemente, un proyecto de investigación
en el que han participado más de 100 científicos europeos ha visto la luz en el
marco de la Unión Europea. Más de 11.000 especies exóticas, sus impactos y
consecuencias sobre el ambiente y la sociedad, han sido catalogados por DAISIE
(Delivering Alien Invasive Species Inventory for Europe)1. Hasta el momento se
conoce el impacto ecológico de 1.094 de estas especies (el 10 % del total), y
1.347 (aproximadamente el 13 % de las registradas) generan daños económicos
(DAISIE Handbook of alien species in Europe 2009; Cuadro 4).
Es probable que muchas de las especies potencialmente invasoras,
introducidas en el momento actual, no se hayan detectado o reconocido todavía,
por lo que se prevé que en un futuro próximo la tasa de invasiones se incremente,
En el Anexo se incluye un listado con las 100 especies invasoras más dañinas de Europa
1
INTRODUCCIÓN GENERAL: Las invasiones biológicas
SITUACIÓN ACTUAL DE LAS ESPECIES EXÓTICAS INVASORAS
15
Las cifras
ƒ
En Europa habitan 11.000 especies invasoras
ƒ
Más del 10 % de estas especies son dañinas para los ecosistemas y/o la
economía del continente europeo
ƒ
El Mediterráneo es el área marina más perjudicada, con una
superficie afectada de 2.500.000 Km2 y 1.313 de las especies
registradas
ƒ
Las plantas y los invertebrados terrestres son los taxones con mayor
número de especies invasoras (6.630 y 2.535 respectivamente) que
causan impactos en los ecosistemas
ƒ
España cuenta con 1.467 especies foráneas
Datos revelados por el primer registro de especies invasoras de Europa, elaborado
dentro del proyecto europeo DAISIE (Delivering Alien Invasive Species Inventories for Europe).
Fuente: DAISIE-project, disponible on-line en: www.europe-aliens.org
Cuadro 4
afectando a nuevos ecosistemas y regiones geográficas. Por otra parte, la
creciente movilidad de las personas y mercancías, y el fenómeno de la
globalización, en pleno desarrollo, favorecerán la transferencia a escala global de
un gran número de especies en las próximas décadas (Mack 1991; Jenkins 1996;
Ruiz et al. 2000). La prevención, evitando la introducción de nuevas especies y
actuando antes de que se produzca la colonización de nuevas áreas, es la forma
más eficiente y económica de enfrentarse a las invasiones biológicas venideras.
En los casos en los que ya se ha producido la introducción, una detección
temprana y una respuesta rápida en las primeras fases de la colonización pueden
impedir el establecimiento de la especie invasora y lograr su erradicación
(Genovesi y Shine 2004).
El galápago leproso
P
erteneciente a la familia de los batagúridos, el galápago leproso
(Mauremys leprosa, Schweiger 1812) es una especie de carácter
termófilo, distribuida por el suroeste de Europa y el noroeste de África
(Da Silva 2002). En la Península Ibérica es mucho más común en la mitad sur,
escaseando en la meseta septentrional y siendo muy rara su presencia en el
norte, encontrándose poblaciones aisladas en puntos dispersos, quizá debidas a
16
INTRODUCCIÓN GENERAL: El galápago leproso
escapes y/o introducciones (Bea 1998;
Gosá y Bergerandi 1994; Galán 1999) (Fig.
2). Habita preferentemente charcas y
arroyos de torrentera con vegetación de
rivera, siendo menos común en grandes
ríos y embalses. Tolera muy bien las
aguas salobres, y en cierta medida la
contaminación, pero tiende a desaparecer
cuando ésta es excesiva (Andreu y LópezJurado 1998; Da Silva 2002). El
Figura 2 Distribución del galápago
caparazón, que puede alcanzar los 21 cm,
leproso, M. leprosa, en la P. Ibérica.
es pardo oliváceo, y el plastrón, amarillo o
Basado en Andreu y López-Jurado 1998
crema con manchas oscuras. Los jóvenes
presentan rayas anaranjadas muy patentes en la cabeza, cuello y patas, que
tienden a disolverse con la edad. Las hembras alcanzan tamaños mayores que los
machos, y carecen de la patente concavidad que éstos presentan en el plastrón.
La porción anterior de la cola, desde la base a la cloaca, es mayor en los machos
(Andreu y López-Jurado 1998). Los machos adquieren la madurez sexual en torno
a los siete años (cuando alcanzan tamaños de entre 135 y 140 mm), mientras que
las hembras la adquieren a edades próximas a los 10 años (con longitudes entre
los 140 y los 160 mm) (Pérez et al. 1979). La puesta, de entre 1 y 13 huevos,
tiene lugar en primavera, durante los meses de mayo y junio. Las crías miden
unos 20 mm al nacer, entre 4 y 16 semanas después de la puesta (Andreu y
Ilustración | Mauremys leprosa
17
López-Jurado 1998; Arnold y Ovenden 2002). La alimentación de esta especie,
muy variada, se compone de insectos, pequeños moluscos y crustáceos, anfibios,
peces, plantas, carroña e incluso excrementos (Salvador 1985; Oliveira y Crespo
1989). Los ejemplares pueden vivir hasta 20 años en cautividad.
La especie se encuentra actualmente catalogada como Vulnerable según los
criterios de UICN (Da Silva 2002), al estar desapareciendo en determinadas áreas
de su distribución. Su regresión se debe fundamentalmente a la intensa
transformación del hábitat y a la excesiva contaminación de las zonas agrícolas e
industriales (Da Silva 2002). A estos factores se suma la introducción en las
últimas décadas de especies exóticas de galápagos competidores, principalmente
el galápago de Florida.
El galápago de Florida
T
ambién conocido como galápago americano o tortuga de orejas rojas, el
galápago de Florida (Trachemys scripta elegans, Wied 1839) es un
quelonio perteneciente a la familia de los emídidos. Originario del
sureste de los EEUU y noreste de Méjico, posee un rango geográfico muy
amplio, extendiéndose por la cuenca del Mississippi, desde Illinois hasta el Golfo
de Méjico (Fig. 3). Se trata de una especie semiacuática, generalista y ubiquista,
que habita lagunas, canales, áreas pantanosas, arroyos intermitentes y otras
zonas húmedas con abundante vegetación (Carr 1952; Gibbons 1990). Se
caracteriza por poseer una intensa mancha roja postorbital (de ahí el
sobrenombre de “orejas rojas”), estrechas bandas gulares y una banda amarilla
transversal en cada escudo pleural (Ernst y Barbour 1989). Su dimorfismo sexual
es observable en las uñas de las extremidades anteriores y en la longitud de la
cola (en ambos casos más largas en los
machos), así como en el pequeño tamaño
de los machos en comparación con las
hembras (Gibbons 1990). Los individuos
pueden sobrepasar los 30 cm de longitud
(N. Polo-Cavia, pers. obs.), y vivir hasta
40 años en condiciones de cautividad
(Capdevila-Argüelles y Zilletti 2006). En
los machos, la madurez sexual se
adquiere al alcanzar un tamaño
determinado (80-130 mm en la longitud
Figura 3 Área de distribución original
del plastrón), mientras que en las
del galápago de Florida, T. scripta.
Basado en Gibbons 1990
hembras, la madurez parece estar más
18
Durante las últimas décadas, un gran número de juveniles de T. scripta han
sido importados en masa por diferentes países, como parte del comercio de
mascotas, lo que ha dado lugar a frecuentes introducciones. La especie se
encuentra actualmente establecida en
diversas regiones de África, Asia y
Europa (Tiedemann 1990; Chen y Lue
1998),
especialmente
en
países
mediterráneos (Luiselli et al. 1997; Chen
y Lue 1998; Pleguezuelos 2002), donde
coloniza todo tipo de masas de agua,
incluso algunas muy contaminadas,
gracias a su gran capacidad de adaptación
(Gibbons 1990). Su reproducción en el
medio natural ha sido constatada en
Figura 4 Presencia del galápago de
varias de estas áreas (Luiselli et al. 1997;
Florida, T. scripta, en la P. Ibérica. Basado
Martinez-Silvestre et al. 1997; Cadi et al.
en Pleguezuelos 2002; Loureiro et al. 2008
Ilustración | Trachemys scripta elegans
INTRODUCCIÓN GENERAL: El galápago de Florida
relacionada con la edad (las primeras puestas suelen producirse entre los 5 y los
7 años) (Gibbons y Greene 1990). La reproducción tiene lugar en primavera, con
puestas de 2 a 18 huevos que las hembras entierran en el suelo (Gibbons y
Greene 1990). Los huevos eclosionan al cabo de unos tres meses, pero los recién
nacidos permanecen en el nido por lo general hasta pasado el invierno (Gibbons
y Nelson 1978). Aproximadamente un año después de la puesta, las crías se
desplazan hasta el agua y comienzan a alimentarse (Clark y Gibbons 1969). Los
juveniles son preferentemente carnívoros, al igual que los adultos cuando existe
disponibilidad proteica en el medio (Parmenter 1980).
19
2004). En la Península Ibérica se ha producido una gran expansión de la especie,
existiendo poblaciones autónomas de mayor o menor densidad en diversas
marismas y humedales de la franja litoral, así como en puntos dispersos del
interior (Pleguezuelos 2002; Fig. 4). Estas poblaciones son susceptibles de causar
importantes impactos sobre los ecosistemas, pudiendo interferir con las
poblaciones de galápagos nativos.
Interacciones competitivas entre
galápagos nativos e invasores
A
lgunas observaciones indican que el galápago de Florida es una especie
que compite con los galápagos autóctonos ibéricos (el europeo, Emys
orbicularis y el leproso, Mauremys leprosa). Sin embargo, la forma en
que se puedan estar produciendo las interacciones entre especies no está clara.
Tanto los galápagos nativos como el americano ingieren materia animal de
manera constante –todos depredan sobre anfibios ibéricos-, dedican gran parte
del tiempo a asolearse y coinciden en las épocas de reproducción (Gibbons 1990;
Andreu y López-Jurado 1998; Pleguezuelos 2002), por lo que es probable que
exista competencia por los recursos tróficos, los lugares de asoleamiento o los de
nidificación (Crucitti et al. 1990; Cadi y Joly 2003, 2004). La introducción de
patógenos por parte de los galápagos exóticos que ataquen a los nativos es otra
de las interacciones posibles (Hidalgo Vila et al. 2009). Entre las ventajas
potenciales de T. scripta sobre las especies nativas se han citado una mayor
tolerancia a la contaminación y a la presencia humana, lo que podría permitirle
una distribución más amplia (Pleguezuelos 2002). Además, el galápago de Florida
se muestra activo a temperaturas inferiores del agua, por lo que puede comenzar
antes su actividad anual, alcanza tallas superiores a las de los galápagos
autóctonos, produce una mayor descendencia, tiene una madurez sexual más
temprana y una dieta más variada (Gibbons 1990; Pleguezuelos 2002).
En diversas áreas de la Península Ibérica se han encontrado ejemplares de
galápago de Florida conviviendo en sintopía con galápagos leprosos, incluso
compartiendo los mismos lugares de asoleamiento (Aceituno 2001; Ayres 2001;
Balset 2001; Martínez-Silvestre et al. 2001; Díaz-Paniagua et al. 2002). Tanto M.
leprosa como T. scripta son especies principalmente acuáticas, pero abandonan
el agua para asolearse. Durante estos momentos, los galápagos son presas
potenciales de diversos depredadores, como algunas aves o mamíferos terrestres
(Greene 1988; Martín y López 1990), por lo que se muestran muy cautelosos,
especialmente los leprosos, estando expectantes y en constante alerta, y
sumergiéndose en el agua ante la menor señal de peligro (López et al. 2005). Por
20
INTRODUCCIÓN GENERAL: Interacciones competitivas entre galápagos nativos e invasores
esta razón, los lugares preferidos para el asoleamiento son piedras y troncos
emergidos en las áreas centrales de las charcas o arroyos, rodeados de agua
profunda (Cadi y Joly 2003). El desplazamiento de E. orbicularis de estos lugares
por parte del introducido T. scripta ha sido comprobado experimentalmente
(Cadi y Joly 2003), y las observaciones de campo sugieren que es muy posible
que la competencia durante el asoleamiento se produzca también entre M.
leprosa y T. scripta, puesto que los recursos son limitados y las dos especies se
ven obligadas a compartirlos (Díaz-Paniagua et al. 2002; Pleguezuelos 2002;
Cadi y Joly 2003). Así, el galápago de Florida podría monopolizar los lugares más
aptos para el asoleamiento, impidiendo la adecuada termorregulación de los
galápagos nativos, lo que podría afectar gravemente a la eficiencia de sus
funciones fisiológicas, especialmente la de aquellas relacionadas con la digestión
(Parmenter 1981; Meek y Avery 1988; Avery et al. 1993; Koper y Brooks 2000).
Tales efectos negativos, derivados de una actividad de asoleamiento deficiente,
podrían afectar últimamente al crecimiento y a la reproducción de los galápagos
autóctonos (Obbard y Brooks 1979; Avery et al. 1993). En este sentido, Cadi y
Joly (2004) encontraron una significativa pérdida de peso y una elevada
mortalidad en el galápago europeo tras someterlo experimentalmente a un largo
periodo de competencia con el galápago de Florida.
El desplazamiento de M. leprosa debido a la introducción de T. scripta ha
sido observado en algunos enclaves ibéricos. Por ejemplo, en la Laguna del
Acebuche (Parque Nacional de Doñana), al extraer galápagos americanos de las
zonas más profundas, con menor riesgo de depredación, éstas fueron reocupadas por el galápago leproso, lo que indica que la presencia del invasor está
afectando al uso del espacio y a la selección de hábitat de los galápagos nativos,
llegando incluso a excluirlos de los espacios más favorables (Díaz-Paniagua et al.
2002). Si la competencia con el galápago de Florida supone desventajas para los
galápagos autóctonos, es muy posible que M. leprosa evite el contacto directo
con T. scripta, utilizando en consecuencia recursos subóptimos y favoreciendo
así la expansión de la especie exótica.
Dado que las características específicas de M. leprosa y T. scripta han
evolucionado en sus respectivos hábitats naturales, las adaptaciones originales
de cada especie podrían conferir ventajas o desventajas a los galápagos en una
nueva situación ecológica en la que la especie introducida ocupa un hábitat
desconocido y la nativa se enfrenta a la competencia con el invasor. En este
sentido, el origen de T. scripta en un medio especialmente competitivo (i.e., la
coexistencia de numerosas especies competidoras de galápagos en sintopía es
habitual en muchos ecosistemas de Norteamérica; Gibbons 1990) podría dotarle
de ciertas habilidades competitivas de las que podrían carecer los galápagos
autóctonos, adaptados a ambientes de escasa o nula competencia (tan sólo dos
especies de galápagos nativos, op.cit., habitan en la Península Ibérica). En
21
consecuencia, una mayor voracidad, agresividad y/o dominancia del galápago de
Florida podrían ser la causa principal del desplazamiento que sufre la especie
nativa. No obstante, otras diferencias interespecíficas en la morfología, fisiología
y comportamiento de los galápagos –hasta ahora inexploradas-, podrían afectar
también al resultado de la competencia entre la especie nativa y la invasora. Así,
por ejemplo, el galápago de Florida podría beneficiarse de determinadas
ventajas termorreguladoras, menores requerimientos energéticos o estrategias
depredatorias y/o antidepredatorias de mayor eficacia, producto de la adaptación
a sus hábitats naturales, que le permitieran competir ventajosamente con los
galápagos nativos en los nuevos territorios en los que ha sido introducido.
Justificación y objetivos
L
as características morfológicas, ecológicas y el comportamiento de los
organismos han sido modelados por la selección natural a lo largo de la
historia evolutiva de cada especie, permitiendo una mayor adaptación de
los individuos al conjunto de condiciones bióticas y abióticas de su entorno. Sin
embargo, en ambientes que han sufrido una rápida alteración, estas
características, anteriormente asociadas con el éxito reproductor y la
supervivencia de los organismos (Williams y Nichols 1984), pueden perder
repentinamente su valor adaptativo (Schlaepfer et al. 2005). En este sentido, las
22
Ilustración | Galápagos exóticos se asolean sobre la vegetación palustre
INTRODUCCIÓN GENERAL: Justificación y objetivos
especies invasoras constituyen una seria amenaza para los ecosistemas, en tanto
que generan nuevos contextos ecológicos en los que las respuestas de los
organismos nativos, otrora adaptativas, pueden carecer de funcionalidad
(Callaway y Aschehoug 2000; Shea y Chesson 2002). Como consecuencia de este
desajuste, las especies nativas son susceptibles de sufrir un detrimento en sus
tasas de supervivencia y/o reproducción (Schlaepfer et al. 2002).
Sin embargo, bajo circunstancias favorables, los organismos nativos pueden
adquirir mecanismos (por evolución o aprendizaje), que les permitan hacer
frente a las invasiones y mantener sus poblaciones (Ancel Meyers y Bull 2002).
Así, las especies nativas pueden alterar su comportamiento y/o morfología,
como resultado de las interacciones con las especies introducidas (Reznick y
Endler 1982; Singer et al. 1993; Singer y Thomas 1996; Carroll et al. 1997, 1998;
Magurran 1999). A pesar de ello, el comportamiento y los procesos evolutivos
rara vez son integrados explícitamente en los planes y en las estrategias de
conservación (e.g., Watters et al. 2003), tal vez debido a la presunción
generalizada de que tales procesos operan a escalas espaciales y temporales que
escapan a las posibilidades de actuación humana (Ashley et al. 2003). No
obstante, existen numerosos ejemplos de rápida adquisición de comportamientos
en respuesta a las modificaciones del ambiente (e.g., Griffin 2004), y algunos
casos documentados de evolución en tiempo real (i.e., en el orden de años y
décadas) inducidos por la actividad antrópica (Ashley et al. 2003; Rice y Emery
2003; Stockwell et al. 2003). Estos ejemplos ofrecen una nueva visión de las
invasiones biológicas, así como la posibilidad de gestionar estas alteraciones en
base a los regímenes de selección, al comportamiento y a la plasticidad de las
especies nativas, con el fin de asegurar su persistencia a largo plazo (lo que se ha
denominado en inglés evolutionarily enlightened management; Ashley et al.
2003). Integrar este tipo de gestión en los planes de intervención actuales es
esencial para preservar la riqueza de especies nativas, especialmente en los casos
en los que la erradicación de la fauna o la flora exótica es económica o
biológicamente imposible. Un plan de actuación eventual, que garantice la
permanencia de las especies nativas mientras se produce el tránsito a sus nuevos
regímenes selectivos será, probablemente, menos costoso y más efectivo a largo
plazo que los indefinidos intentos de erradicación de las especies invasoras.
La presente tesis pretende servir a este propósito, abordando en un contexto
evolutivo diversos aspectos de la biología, ecología y comportamiento del
galápago ibérico Mauremys leprosa, y comparándolos con los del galápago de
Florida, Trachemys scripta, con el objetivo de contribuir a esclarecer la
naturaleza de las interacciones competitivas que se puedan estar produciendo
entre la especie nativa y la invasora. A lo largo de sus ocho capítulos, se han
explorado diversos factores que pueden afectar al resultado de la competencia
entre estas dos especies, analizando los potenciales efectos adversos que el
23
galápago introducido pudiera generar en las poblaciones nativas de galápago
leproso2.
Los tres primeros capítulos se han dedicado a examinar algunas de las
posibles formas de interferencia directa por parte del galápago de Florida en tres
aspectos clave de la ecología y el comportamiento del galápago leproso: uso del
espacio, eficiencia de la alimentación y eficiencia termorreguladora. En los
siguientes cuatro capítulos se analizan diferentes factores relacionados con el
potencial y la habilidad competitiva específicos de cada especie, que podrían
afectar indirectamente al resultado de la competencia (i.e., ventajas
termorreguladoras, fisiológicas y comportamentales). Finalmente, en el último
capítulo se analizan las potenciales ventajas que una trampa evolutiva (i.e., la
incapacidad de los renacuajos presa para reconocer depredadores introducidos)
podría conferir a los galápagos invasores.
Se han planteado los siguientes
OBJETIVOS
ƒ
Capítulo 1: En muchas especies de galápagos, las sustancias químicas
secretadas por diferentes glándulas facilitan el reconocimiento específico y
sexual, pudiendo afectar al uso del espacio y a la selección de hábitat de los
individuos. El objetivo de este capítulo es analizar la capacidad de M. leprosa
y T. scripta para reconocer secreciones químicas de machos y hembras
coespecíficos y heteroespecíficos disueltas en el agua, y determinar si la
detección de señales químicas de especies competidoras afecta al uso del
espacio por parte de los galápagos nativos.
ƒ
Capítulo 2: El galápago de Florida es una especie agresiva que podría
desplazar a los galápagos nativos durante el desarrollo de actividades
competitivas tales como la alimentación. Los objetivos de este capítulo son:
comparar las tasas de ingestión de M. leprosa y T. scripta en situaciones de
competencia intra e interespecífica, analizar el nivel de agresividad y la
dominancia establecidos durante la alimentación entre individuos
coespecíficos y heteroespecíficos, y determinar si existe relación entre el
comportamiento agonístico de T. scripta y el posible desplazamiento de M.
leprosa.
2Los
capítulos reproducen el texto íntegro de manuscritos que han sido publicados en revistas
científicas internacionales, o que se hallan en fase de revisión en el momento presente. Por esta
razón se presentan en inglés, idioma original en el que fueron redactados. No obstante, en cada
uno ellos se ha incluido un resumen en castellano.
24
Capítulo 3: La eficiencia termorreguladora de los galápagos nativos podría
verse comprometida en una situación de competencia con el galápago de
Florida. El objetivo de este capítulo es determinar si la competencia por los
recursos de asoleamiento entre las dos especies, ocasional o a largo plazo,
supone una alteración en el tiempo disponible que los galápagos nativos
pueden dedicar a asolearse, y si T. scripta desplaza a M. leprosa en la
competencia por estos recursos.
ƒ
Capítulo 4: Las diferencias morfológicas interespecíficas podrían influir
significativamente en las tasas de calentamiento y enfriamiento de los
galápagos, pudiendo derivarse ventajas termorreguladoras para el galápago
de Florida. El objetivo de este capítulo es comparar la relación superficievolumen de M. leprosa y T. scripta a partir de medidas biométricas y
analizar los efectos de su morfología específica en las tasas de intercambio de
calor.
ƒ
Capítulo 5: Un comportamiento de asoleamiento deficiente a consecuencia
de la competencia con el galápago de Florida podría ocasionar diversas
alteraciones en el metabolismo de M. leprosa. Los objetivos de este capítulo
son: comparar los requerimientos de asoleamiento de M. leprosa y T. scripta
en condiciones de alimentación ad líbitum vs. ayuno prolongado,
determinar el efecto de la privación de alimento en la temperatura preferida
de asoleamiento de cada especie, y analizar la relación entre la morfología
de los galápagos y esta temperatura.
ƒ
Capítulo 6: La habilidad de los galápagos para recuperar su posición natural
cuando son volteados accidentalmente es crítica para su supervivencia. En
consecuencia, las posibles diferencias interespecíficas en el comportamiento
de ‘giro’ de M. leprosa y T. scripta podrían contribuir a explicar la mayor
capacidad competitiva del galápago introducido. El objetivo de este capítulo
es comparar la respuesta de ‘giro’ (en su fase comportamental y mecánica) de
ambas especies de galápagos y analizar los efectos de la temperatura corporal
y la morfología en la respuesta de ‘giro’ de cada especie.
ƒ
Capítulo 7: En ambientes alterados antrópicamente, potenciales diferencias
en la percepción del riesgo de depredación entre M. leprosa y T. scripta
podrían beneficiar a la especie invasora. El objetivo de este capítulo es
analizar si existen diferencias interespecíficas en su comportamiento
antidepredatorio comparando el tiempo que ambas especies pasan refugiadas
en el caparazón tras la amenaza de un depredador en respuesta a diversos
factores de riesgo.
INTRODUCCIÓN GENERAL: Justificación y objetivos
ƒ
25
ƒ
Capítulo 8: Tanto los galápagos nativos como los invasores depredan
habitualmente sobre renacuajos de diversas especies de anuros. Estos
renacuajos son capaces de reconocer y responder de forma innata a las
señales químicas de los depredadores locales, pero su incapacidad para
detectar nuevos depredadores podría conferir ventajas competitivas a los
galápagos introducidos. El objetivo de este capítulo es analizar la capacidad
de cuatro especies de renacuajos de anuros ibéricos para reconocer y
responder a estímulos químicos de varias especies de galápagos nativos e
invasores presentes en la Península.
Procedimiento
D
urante las primaveras de 2005 a 2008 se capturaron ejemplares de
galápago leproso en diversas localidades de las Comunidades de Madrid
y Extremadura. Así mismo, se obtuvieron galápagos de Florida
procedentes de varios centros de recuperación de fauna, donde eran mantenidos
en condiciones de semilibertad. Estos galápagos habían sido extraídos de
poblaciones introducidas en el medio natural, con el fin de evitar efectos
adversos sobre las poblaciones nativas de galápagos. Los sujetos experimentales
fueron trasladados a la Estación Biológica de El Ventorrillo (CSIC), próxima a
Navacerrada (Madrid), donde se realizaron los experimentos. Los galápagos
fueron alojados individualmente en acuarios (60 x 40 x 30 cm) situados al aire
libre, que contenían agua y piedras que les permitían asolearse. El fotoperiodo y
la temperatura fueron los mismos que los de las zonas de alrededor. Durante el
tiempo que permanecieron en cautividad, los galápagos fueron alimentados tres
veces por semana con carne picada, lombrices y babosas. Los animales se
encontraban en buen estado de salud durante los experimentos, tras los cuales
fueron devueltos a sus lugares exactos de captura (galápagos leprosos) o a los
centros de recuperación de los que procedían (galápagos exóticos). Los
experimentos cumplieron todas las leyes actuales de España y de los Organismos
Medioambientales de la Comunidad de Madrid y de la Junta de Extremadura
donde fueron llevados a cabo.
Capítulo 1: La capacidad de M. leprosa y T. scripta para reconocer secreciones
químicas de individuos coespecíficos y heteroespecíficos disueltas en el agua se
analizó comparando el tiempo que los galápagos permanecían en acuarios con
agua limpia vs. el tiempo que permanecían en acuarios con los diferentes
estímulos químicos. Dos acuarios experimentales (70 x 60 x 15 cm) fueron
unidos por rampas que permitían a los galápagos desplazarse fácilmente de uno a
26
otro acuario. En las pruebas, uno de los acuarios contenía siempre agua limpia
mientras que en el otro se alternaron los tratamientos con los diferentes olores.
A cada individuo se le aplicaron todos los tratamientos experimentales en orden
aleatorio. Las posiciones de los acuarios fueron también aleatorizadas a lo largo de
los experimentos, y se controló que la temperatura, la iluminación y la profundidad
del agua fueran similares en todas las pruebas (De Rosa y Taylor 1980).
Capítulo 3: Para analizar experimentalmente la actividad de asoleamiento de M.
leprosa y T. scripta en situaciones de competencia intra e interespecífica por los
lugares de asoleamiento se utilizaron acuarios (60 x 40 x 30 cm) provistos de una
única plataforma (24 x 11,5 x 7 cm) para el asoleamiento. Los acuarios fueron
colocados al aire libre y en cada uno de ellos se introdujo una pareja de
individuos coespecíficos o heteroespecíficos de tamaño similar. Los patrones de
asoleamiento de ambas especies fueron comparados entre tratamientos (i.e.,
competencia intraespecífica vs. competencia interespecífica), así como el tiempo
que los galápagos se asolearon en solitario con el tiempo que compartieron las
plataformas, asoleándose uno sobre otro. Los galápagos eran alimentados ad
líbitum al final de cada prueba, pero no se les alimentó durante las
observaciones, con el fin de evitar los efectos del estado nutricional en el
comportamiento de asoleamiento (Hammond et al. 1988, Dubois et al. 2008).
Los tratamientos fueron aleatorizados y se controló que la temperatura, la
iluminación y la profundidad del agua fueran similares en todas las pruebas.
Capítulo 4: La relación superficie-volumen de los galápagos fue calculada a
partir de medidas biométricas, aproximando la forma de su caparazón a la de un
semielipsoide de revolución. La superficie y el volumen de los galápagos se
estimaron a partir de ecuaciones que fueron validadas cubriendo el caparazón de
INTRODUCCIÓN GENERAL: Procedimiento
Capítulo 2: Las tasas de ingestión de M. leprosa y T. scripta, así como la
frecuencia de las interacciones agresivas entre los galápagos durante la
alimentación, fueron comparadas en situaciones de competencia intra e
interespecífica en acuarios (60 x 40 x 30 cm) situados al aire libre. Cada galápago
competía en cada prueba con un individuo coespecífico o heteroespecífico de
tamaño similar por 6 bolas de pienso compuesto, similares en apariencia y
dinámica de flotación a determinados componentes de la dieta de los galápagos
(i.e., trozos de algas, pequeños moluscos, etc.). Las pruebas se replicaron 5 veces
en orden aleatorio en diferentes días, de forma que cada galápago compitió por
30 bolas de pienso en cada tratamiento experimental (i.e., competencia
intraespecífica vs. competencia interespecífica). Al final de cada prueba los
galápagos eran alimentados ad líbitum, y una vez saciados, mantenidos en ayuno
en acuarios individuales hasta la siguiente prueba.
27
los galápagos con rectángulos de papel y calculando la suma total de sus áreas, y
calculando el volumen de agua desplazada por los galápagos al sumergirlos en
un recipiente. Para estimar las tasas de enfriamiento en aire de M. leprosa y T.
scripta se utilizó una cámara de frío a 15 °C. Para las tasas de calentamiento y de
enfriamiento en agua se utilizaron acuarios (60 x 40 x 30 cm) con agua a 15 °C,
provistos de una plataforma emergente (24 x 11,5 x 7 cm) sobre la que pendía
una lámpara de infrarrojos (250 W, 250 V). Los galápagos eran fijados a la
plataforma hasta que su temperatura se estabilizaba en torno a los 30 °C y
después liberados en el agua. La temperatura cloacal de los galápagos fue
controlada continuamente durante las pruebas por medio de registradores
conectados a una sonda (Mrosovsky 1980). Las tasas de intercambio de calor se
calcularon a partir de los incrementos de temperatura registrados, ajustando
ecuaciones de Bertalanffy (Von Bertalanffy 1960; Kaufman 1981).
Capítulo 5: Los requerimientos térmicos de ambas especies de galápagos se
analizaron comparando las temperaturas preferidas de asoleamiento (i.e., la
temperatura corporal a la cual cesa esta actividad) de M. leprosa y T. scripta en
condiciones de alimentación vs. ayuno. Dependiendo del tratamiento, los
galápagos fueron alimentados ad líbitum con pienso compuesto una vez al día
durante los 7 días previos a las pruebas, o bien mantenidos en ayuno durante
estos 7 días (Bennet y Dawson 1976; Gatten 1974). A cada individuo se le
aplicaron ambos tratamientos en orden aleatorio. Durante las pruebas, se
permitió a los galápagos asolearse libremente en acuarios (60 x 40 x 30 cm) con
agua a temperatura ambiente, provistos de una plataforma emergente (24 x 11,5
x 7 cm) y una lámpara de infrarrojos (250 W, 250 V). Las temperaturas
corporales de los galápagos fueron medidas continuamente durante 1 h por
medio de registradores conectados a sondas cloacales. Las temperaturas
preferidas de asoleamiento quedaban registradas en el momento en el que los
galápagos se sumergían en el agua.
Capítulo 6: Para determinar la influencia de la temperatura en la respuesta de
‘giro’ de M. leprosa y T. scripta se midió el tiempo que los galápagos tardaban en
darse la vuelta tras ser depositados con el plastrón hacia arriba sobre un sustrato
de hierba uniforme, a tres temperaturas experimentales: 15 y 20 °C, y la
temperatura preferida de asoleamiento respectiva de cada especie (esta
temperatura se determinó siguiendo el mismo procedimiento que en el capítulo
5). Cada individuo fue observado a las tres temperaturas experimentales en
orden aleatorio. Antes de cada prueba, los galápagos eran introducidos en una
cámara termostática hasta que su temperatura corporal se estabilizaba a la
temperatura correspondiente. Acto seguido, los galápagos eran depositados
sobre el sustrato. Desde este momento se medía 1) el tiempo de latencia: tiempo
28
que los galápagos permanecían inmóviles, y 2) la respuesta mecánica: el tiempo
transcurrido desde el primer movimiento hasta que los galápagos completaban
el giro.
Capítulo 7: Las respuestas antidepredatorias de M. leprosa y T. scripta a los
diferentes factores de riesgo se analizaron simulando ataques de diferente
intensidad, manipulando a los galápagos durante 2 ó 25 s (‘riesgo bajo’ vs. ‘riesgo
alto’) y depositándolos después en contenedores (70 x 60 x 15 cm) provistos de
un sustrato de hierba, o bien conteniendo 4 cm de agua limpia (‘tierra’ vs.
‘agua’). Tras liberar a los galápagos, el experimentador se mantenía cerca (1 m),
simulando la persistencia en el ataque, o se retiraba a una posición alejada (8 m),
simulando el abandono de la presa (‘cerca’ vs. ‘lejos’). A partir de este momento
se medía 1) el tiempo de aparición: tiempo desde que los galápagos eran
liberados hasta que la cabeza y los ojos emergían del caparazón, y 2) el tiempo
de espera: desde que los ojos eran visibles hasta que los galápagos iniciaban la
huida.
— ‚ƒ‚ —
INTRODUCCIÓN GENERAL: Procedimiento
Capítulo 8: La capacidad de los renacuajos para reconocer y responder a
estímulos químicos de galápagos nativos e invasores se analizó comparando sus
niveles de actividad basal en canaletas (101 x 11,4 x 6,4 cm) con agua limpia vs.
agua con los diferentes estímulos químicos de galápagos depredadores (nativos y
exóticos) y vs. agua con los estímulos de un pez exótico no depredador. A cada
renacuajo se le aplicaron los distintos tratamientos en orden aleatorio. La
duración de las pruebas fue de 30 min y se permitió a los renacuajos descansar
durante 24 h entre prueba y prueba. En las canaletas se trazaron líneas que
permitían registrar la posición de los renacuajos cada minuto. Los niveles de
actividad fueron estimados en cada tratamiento a partir del número de líneas
cruzadas por los renacuajos durante el tiempo total de las pruebas (Rohr y
Madison 2001; Gonzalo et al. 2007).
29
30
Capítulos
32
Capítulo
1
Diferencias interespecíficas en las respuestas quimiosensoriales de galápagos: consecuencias en la competencia entre especies nativas e invasoras Nuria Polo Cavia, Pilar López y José Martín
Biological Invasions 11 (2009) 431-440
RESUMEN
34
El galápago de Florida (Trachemys scripta elegans) es una
especie invasora, actualmente introducida en diversos países
mediterráneos, donde está desplazando poblaciones nativas
de galápago leproso (Mauremys leprosa). Sin embargo, la
forma en la que se producen las interacciones competitivas
entre estas dos especies permanece relativamente
inexplorada. En muchas especies de galápagos, las sustancias
secretadas por diferentes glándulas facilitan el reconocimiento
específico y sexual. De este modo, es posible que la detección
química de especies competidoras afecte al uso del espacio y a
la selección de hábitat de los galápagos nativos. En este
trabajo se analizó la capacidad de T. scripta y M. leprosa para
reconocer señales químicas disueltas en agua, secretadas por
machos y hembras coespecíficos y heteroespecíficos. Se
comparó el tiempo que los galápagos permanecían en acuarios
con agua limpia vs. el tiempo que permanecían en acuarios
que contenían diferentes estímulos químicos. T. scripta no
prefirió ni evitó los acuarios con estímulos químicos
secretados por M. leprosa, lo que podría favorecer la
expansión de la especie invasora. En contraste, M. leprosa
prefirió agua con estímulos químicos de coespecíficos y evitó
el agua con estímulos secretados por T. scripta, lo que sugiere
que las señales químicas podrían ser usadas por los galápagos
nativos para evitar áreas ocupadas por los galápagos exóticos.
Sugerimos que este comportamiento de la especie nativa, M.
leprosa, puede ser una de las causas que contribuya al
desplazamiento observado de sus poblaciones por la especie
invasora, T. scripta ■
INTERSPECIFIC DIFFERENCES IN CHEMOSENSORY RESPONSES OF
FRESHWATER TURTLES: CONSEQUENCES FOR COMPETITION
BETWEEN NATIVE AND INVASIVE SPECIES
Abstract The red-eared slider (Trachemys scripta elegans) is an introduced invasive species in
many Mediterranean countries that is displacing the populations of native endangered Spanish
terrapins (Mauremys leprosa). However, it is relatively unknown how potential competitive
interactions could be taking place. In many freshwater turtles, semiochemicals from different
glands might facilitate species and sex recognition. We hypothesized that chemosensory detection
of competitor species might affect space use and habitat selection by freshwater turtles. We
analyzed whether T. scripta and M. leprosa turtles recognized chemical cues from male and
female conspecifics and heterospecifics in water. We compared time spent by turtles in clean
water pools vs. water pools containing the different chemical stimuli. Introduced T. scripta did
not avoid nor prefer water pools with chemical stimuli of native M. leprosa terrapins, which
might favor the expansion of the invasive species. In contrast, M. leprosa preferred water with
chemical stimuli of conspecifics and avoided water with chemical cues of T. scripta, which
suggests that chemical cues could be used by native M. leprosa to avoid water pools occupied by
introduced T. scripta. We suggest that this avoidance behavior of native M. leprosa may be one of
the causes that contribute to the observed displacement of their populations by invasive T.
scripta.
Keywords
Chemoreception • Freshwater turtles • Invasive species • Mauremys leprosa •
Trachemys scripta • Use of space
CAPÍTULO 1: Reconocimiento químico
T
he introduction of species outside their natural ranges represents the
second greatest threat to biodiversity after habitat destruction (Wilcove
et al. 1998). Alien species may displace native species through
predation, hybridization, introduction of pathogens, or competition for
resources (Williamson 1996; Shigesada and Kawasaki 1997). For example, the
American red-eared slider (Trachemys scripta elegans) is currently introduced
as a breeding species in many countries of Africa, Asia and Europe, especially in
the Mediterranean area, where sliders have been uncontrollably released in
diverse aquatic habitats after having been imported and sold as pets (Luiselli et
al. 1997; Pleguezuelos 2002). Many observations indicate that introduced sliders
are competing with native European species of freshwater turtles, such as the
European pond terrapin (Emys orbicularis) and the Spanish terrapin (Mauremys
leprosa) (Pleguezuelos 2002; Cadi and Joly 2003, 2004). In the Iberian
Peninsula, the populations of native Spanish terrapins, M. leprosa, have
considerably declined and this terrapin is now considered as an endangered
species in some areas (Pleguezuelos et al. 2002). Although habitat destruction
and human pressure are major causes for this decline, competition with
introduced species, mainly T. scripta, might be worsening the conservation state
of native Iberian turtles (Da Silva and Blasco 1995; Pleguezuelos et al. 2002).
35
However, it is not clear how these interactions between native and
introduced terrapins are taking place. It is possible that direct competition for
food, refuge or basking places occurs (Cadi and Joly 2003, 2004). Also, the
advantages of sliders over native freshwater turtles might be larger adult body
size, more diverse diet, higher fecundity, and a greater tolerance to pollution
and human presence (Pleguezuelos 2002; Polo-Cavia et al. 2008). Field
observations showed that introduced T. scripta displaced native M. leprosa in
some places, and that after removing T. scripta, these same places were reoccupied by M. leprosa, which indicates exclusion of the native species by the
introduced one (Díaz-Paniagua et al. 2002). We hypothesized that, if direct
competitive interactions are disadvantageous for native terrapins, they would
likely avoid water pools in which they detected the presence of T. scripta, thus
favoring the expansion of the invasive species. Freshwater turtles often inhabit
quiet and stagnant waters, where dense vegetation and turbidity can make
visual cues unreliable, and this would favor chemical detection of conspecifics
or competitor species when visual cues are limited (Mason 1992; Muñoz 2004).
If scents of T. scripta were aversive for M. leprosa, dispersal would be a logical
result in a natural environment. Similarly, in the desert tortoise (Gopherus
agassizi), the presence of urine from conspecifics at their sleeping areas do not
significantly affect their aggregation behavior, but spreading urine of males of
the related Texas tortoise (G. berlandieri) over the sleeping site cause G. agassizi
to leave the site and sleep open (Patterson 1971).
However, although chemical communication is widespread among aquatic
vertebrates (Müller-Schwarze 2006), very little is known of the chemical
communication of freshwater turtles (see Mason 1992). Nevertheless,
comparative neurology asserts that many turtles are well equipped anatomically
for chemosensory detection (i.e., well developed olfactory and vomeronasal
systems; Halpern 1992; Hatanaka and Matsuzaki 1993), and many turtle
behaviors seem to be mediated by chemical signals (e.g., Graham et al. 1996;
Quinn and Graves 1998; Poschadel et al. 2006; Müller-Schwarze 2006; see
reviews in Mason 1992). Many turtles have several specialized glands that
secrete potential semiochemicals (Ehrenfeld and Ehrenfeld 1973; Winokur and
Legler 1975; Solomon 1984; Legler 1993). These glands are quiescent in
juveniles, sexually dimorphic (larger in males), and active during the breeding
season only (Rose et al. 1969). Cloacal secretions and faeces are also considered
as possible sources of semiochemicals (Mason 1992). Some turtles use chemicals
from these glands in foraging, homing behavior, aggregation, aggressive
interactions between males, and mating behavior (reviewed in Mason 1992;
Müller-Schwarze 2006). Chemical stimuli may also play a major role in sex and
species identification (Harless 1979).
36
The olfactory anatomy and some behavioral observations suggest that
freshwater turtles can detect chemicals in water. Spanish terrapins (M. leprosa)
have mental and inguinal Rathke’s glands, clearly visible in males, show
frequent and conspicuous sniffing behavior similar to that of related species
(Ernst 1971; Seigel 1980; Kramer and Fritz 1989; Kaufmann 1992), and can
discriminate between water with chemical cues of male or female conspecifics
(Muñoz 2004). Also, male European pond turtles (E. orbicularis) prefer water
with the odor of a female over clean water, and can assess female body size
based on chemical cues (Poschadel et al. 2006). Sliders (T. scripta elegans) seem
to be also able of detecting odors underwater (Cagle 1950; Boycott and Guillery
1962; Parmenter 1980). Early experiments showed that sliders can be trained to
make discriminations based on chemical cues (Boycott and Guillery 1962).
However, sliders lack inguinal and mental glands, and preliminary comparative
tests suggested that they may be less responsive to chemical cues than other
freshwater turtles (Cagle 1950).
In this paper, we aimed to explore whether attraction or repulsion for water
with conspecific or heterospecific chemical cues might affect space use by
freshwater turtles, which might have consequences for the outcome of
competition between native and invasive species. We specifically analyzed
whether M. leprosa and T. scripta were able to recognize chemical cues from
conspecifics and heterospecifics in water. We firstly analyzed in the laboratory
the use by T. scripta of pools with clean water compared with pools with water
with their own chemical stimuli, or with chemical stimuli from male or female
conspecifics. Similar data for M. leprosa are already available (Muñoz 2004).
Then, we compared time spent by male and female M. leprosa and T. scripta in
pools with clean water vs. time spent in pools with water containing chemical
cues from conspecific or heterospecific males or females.
Study animals
We obtained red-eared sliders (T. scripta) (carapace length: mean ± SE = 15 ± 1
cm, n = 38), from a large outdoor pond located in Madrid Province (central
Spain), where they had been maintained under seminatural conditions by the
conservationist private organization ‘‘Grupo de Rehabilitación de la Fauna
Autóctona y su Hábitat’’ (GREFA). These sliders had been recently extracted
from introduced populations in central Spain to avoid aversive effects on
populations of native terrapins. We captured with funnel traps Spanish
terrapins (M. leprosa) (carapace length: mean ± SE = 16 ± 2 cm, n = 15) in
CAPÍTULO 1: Reconocimiento químico
METHODS
37
several ponds and creeks of the Manzanares river (Madrid Province, Spain),
where introduced sliders can be also found.
All turtles were individually housed at ‘‘El Ventorrillo’’ Field Station
(Navacerrada, Madrid Province), in outdoor aquaria (60 x 40 x 30 cm) filled
with water and containing stones that allowed turtles to bask. Temperature and
photoperiod were those of the surroundings. Turtles were fed mince meat,
worms and slugs three times a week. Turtles were held in their home-aquaria
for at least two weeks before testing, so that they became familiarized with
captivity conditions. At the end of experiments, all turtles had maintained or
increased their body mass, and were returned to the GREFA’s pond (sliders) or
to their exact field capture sites (Spanish terrapins).
Experimental procedure
In a first experiment, we analyzed the use by T. scripta of pools with water with
chemical stimuli from conspecific males or females, or with their own chemical
stimuli. We carried out the experiments outdoor using two artificial pools (i.e.,
two plastic containers of 70 x 60 x 15 cm each) that were joined by stone ramps,
which allowed turtles to move easily from one pool to the other. One pool was
always filled with clean water, and the other was filled with water with one of
the different chemical stimuli taken from either the home-aquaria of individual
donor turtles of the same or the opposite sex of the subject turtle, or from the
own home-aquaria of the subject turtle. We tested each subject turtle in three
treatments (‘clean vs. same sex stimulus’, ‘clean vs. opposite sex stimulus’, ‘clean
vs. own stimulus’) in a random sequence. Clean water was obtained from a
nearby mountain stream that does not contain turtles. Home-aquaria of donor
turtles had been filled with 15 cm deep clean water, and the donor turtle had
been maintained there for 3 days without being fed. Thus, original clean water
was pervaded with the donor turtle’s scents alone. The position of the pools
with clean and stimulus water was randomized. We also monitored at the
beginning of the tests water and air temperatures (with digital thermometers;
precision ± 0.1 °C), the extent of illumination by sunlight, and water depth to
ensure that they were similar in both pools during all the tests and did not
affect the turtle responses (De Rosa and Taylor 1980). To avoid odor
contamination, after each trial, we cleaned the pools and the ramps with clean
water, and let them dried outdoor for 12 h. Trials were spaced in time for at
least 2 days so that possible stress resulting from one test did not affect
subsequent tests. The experiment was repeated with different responding
individuals during the mating (April) and non-mating (July) seasons (Gibbons
and Greene 1990).
38
Statistical analyses
We used repeated measures analyses of variance (ANOVAs) to analyze the
differences in use of water pools with different chemical cues across treatments
by the same individual subject turtle. Data from the first experiment were
analyzed with a three-way repeated measures ANOVA with the experimental
treatment (‘same sex stimulus’ vs. ‘opposite sex stimulus’ vs. ‘own stimulus’) as a
within subject factor, and the sex of the subject turtle and the season as two
between-subjects factors. In the second experiment, we used a four-way
repeated measures ANOVA with the chemical cues treatments, species
(‘conspecific stimulus’ vs. ‘heterospecific stimulus’) and sex (‘same sex stimulus’
CAPÍTULO 1: Reconocimiento químico
Before the trials, turtles were allowed to bask for at least 2 h in their homeaquaria, so turtles could attain an optimal body temperature. At the beginning
of the trials, each turtle was placed over the ramps, in the middle of the
experimental pools, so it was given the choice between the two water pools.
Turtles usually explored the two pools, changing from one to the other, very
often at the beginning of the trial and less frequently as the experiment
progressed. We used the instantaneous scan sampling method to monitor each
turtle during 3 h, scanning from a hidden position, and recording every 15 min
the location of the turtle (12 scans per turtle in total). In each scan, if the turtle
was situated in one of the two pools (clean or with chemical stimulus), we
assumed that it had chosen that pool, whereas if it was located in a non-specific
position (e.g., on the ramps), we assumed that it had made no choice. We
assessed the ‘preferences’ of each turtle for each chemical cue from the
percentage of time (excluding time spent in the non-choice area) that the turtle
spent in each water pool (clean vs. stimulus). Then, we compared the
percentage of time that turtles spent in water with different chemical cues to
estimate differences in ‘preferences’ between treatments. Preliminary trials
showed that there were no significant differences in percentage of use between
two clean-water pools.
In a second experiment, we compared the use by M. leprosa and T. scripta
of water with conspecific or heterospecific chemical cues. We followed the
same procedures as in the first experiment, but the stimulus pool was filled with
water from the home-aquaria of individual donor turtles that were either (1) a
conspecific of the same sex, (2) a conspecific of the opposite sex, (3) a
heterospecific of its same sex, or (4) a heterospecific of the opposite sex. Thus,
we tested each subject turtle in four experimental treatments in a random order
(‘clean vs. same sex conspecific stimulus’, ‘clean vs. opposite sex conspecific
stimulus’, ‘clean vs. same sex heterospecific stimulus’ and ‘clean vs. opposite sex
heterospecific stimulus’).
39
vs. ‘opposite sex stimulus’), as two within-subjects factors. The sex and the
species of the subject turtle were included as between-subjects factors.
Data normality was verified by Shapiro-Wilk’s test and tests of
homogeneity of variances (Levene’s test) showed that variances were not
significantly heterogeneous. Pairwise comparisons were made using Tukey’s
honestly significant difference tests (Sokal and Rohlf 1995).
RESULTS
Responses of T. scripta to conspecific and own scents
There were significant differences between seasons in the overall time that T.
scripta spent in pools with water with chemical cues from conspecifics or water
from their home-aquaria (three-way repeated measures ANOVA, season: F =
7.33, df = 1,31, P = 0.01) (Fig. 1.1). Thus, sliders spent less time in water with
conspecific or own chemical stimuli during the mating season (38 ± 3 %) than
during the non-mating season (49 ± 3 %). Sliders tended to prefer water with
their own odor in both seasons, but differences between treatments did not
reach statistical significance (treatment: F = 2.69, df = 2,62, P = 0.08). The
interaction between treatment and season was non-significant (F = 2.05, df =
2,62, P = 0.14). Sex of the subject turtle did not influence the use of water pools
(sex: F = 0.11, df = 1,31, P = 0.75). The rest of the interactions were all nonsignificant (P > 0.40 in all cases).
Between-species comparison
Overall percent time spent by turtles in pools with different types of water did
not differ significantly depending on the species or sex of the subject turtle, and
the interaction between these two factors was non-significant (Table 1.1).
However, the significant differences between conspecific and heterospecific
stimulus and a significant interaction term (species stimulus x species subject)
indicated that T. scripta did not show significant differences in the use of pools
with water with conspecific or heterospecific chemical cues (Tukey’s test, P =
0.98), but M. leprosa had significantly greater preferences for water with
conspecific chemicals than for water with chemicals of T. scripta (P = 0.0003).
Time spent in pools with conspecific chemical cues was significantly higher in
M. leprosa than in T. scripta (P = 0.0006), while time spent in pools with
heterospecific chemical cues was significantly lower in M. leprosa than in T.
scripta (P = 0.03) (Fig. 1.2; Table 1.1).
40
a)
100
Figure 1.1 Percent time (mean ± SE) spent
by T. scripta in pools with water with
Males
Females
chemical cues stimuli from conspecific
donor turtles of the same or opposite sex, or
with their own chemicals, during (a) mating
and (b) non-mating seasons
Time (%)
80
60
40
20
0
Same sex
b)
Opposite sex
Own odor
Opposite sex
Own odor
100
Males
Females
Time (%)
80
60
40
20
Same sex
100
Figure 1.2 Percent time (mean ± SE) spent
by T. scripta and M. leprosa in pools with
water with chemical cues stimuli from
conspecific or heterospecific donor turtles
Conspecific
Heterospecific
Time (%)
80
60
40
20
0
T. scripta
M. leprosa
CAPÍTULO 1: Reconocimiento químico
0
41
Table 1.1 Results from a four-way repeated measures ANOVA examining the effects of the sex
and species of the responding subject turtle, and sex and species of the donor turtle that provided
the chemical cues stimulus, on the levels of preference of water with chemical stimuli by subject
turtles (df = 1,31 in all cases)
Effect
Species subject
Sex subject
Species stimulus
Sex stimulus
Species subject x sex subject
Species stimulus x species subject
Species stimulus x sex subject
Sex stimulus x species subject
Sex stimulus x sex subject
Species stimulus x sex stimulus
Species stimulus x species subject x sex subject
Sex stimulus x species subject x sex subject
Species stimulus x sex stimulus x species subject
Species stimulus x sex stimulus x sex subject
Species stimulus x sex stimulus x species subject x sex subject
F
P
3.48
0.83
32.98
1.40
0.86
25.10
0.27
0.06
1.60
2.63
0.19
0.01
0.04
2.25
6.63
0.07
0.37
< 0.0001
0.25
0.36
< 0.0001
0.61
0.80
0.22
0.11
0.67
0.99
0.84
0.14
0.02
There were no significant overall differences between preferences for
chemicals of the same or the opposite sex, and neither the interactions between
species of the subject turtle, or sex of the subject turtle, and preferences for sex
stimulus were significant. All of the three factors interactions were nonsignificant (Table 1.1). In addition, there was a significant four way interaction between species
and sex of the donor turtle and species and sex of the subject turtle (Fig. 1.3;
Table 1.1). Thus, preferences of both male and female T. scripta were not
significantly different for any stimuli (Tukey’s tests, P > 0.97 in all cases).
However, male M. leprosa had significantly greater preferences for conspecific
female chemical cues than for heterospecific female (P = 0.0002) and
heterospecific male chemical cues (P = 0.002), and significantly greater
preferences for conspecific male chemical cues than for heterospecific male (P =
0.03) and female chemical cues (P = 0.003). In contrast, female M. leprosa had
significantly greater preferences for conspecific female chemical cues than for
heterospecific female (P = 0.0004) and heterospecific male cues (P = 0.003), but
preferences for conspecific and heterospecific male chemical cues were not
significantly different (P = 0.40).
42
a)
T. scripta
100
Figure 1.3 Percent time
Conspecific
Heterospecific
(mean ± SE) spent by
males and females (a) T.
scripta and (b) M. leprosa
in pools with water with
chemical cues stimuli
from conspecific or
heterospecific donor
turtles of the same or
opposite sex
Time (%)
80
60
40
20
0
Same sex
Opposite sex
Males
b)
Same sex
Opposite sex
Females
M. leprosa
100
Conspecific
Heterospecific
Time (%)
80
60
40
20
0
Opposite sex
Males
Same sex
Opposite sex
Females
DISCUSSION
Our results first suggest that red-eared sliders, T. scripta, are able to detect
chemical cues from conspecifics in water and to vary seasonally their responses,
such that sliders spent more time in clean water without conspecific chemical
stimuli during the mating season. During breeding, sliders may exhibit
aggressive behavior towards each other, with males fighting each other or
harassing females (Evans 1952). Thus, sliders may avoid water with conspecific
chemical cues during the mating season to avoid potential aggressive encounters
with conspecifics. However, sliders did not show a clear significant
CAPÍTULO 1: Reconocimiento químico
Same sex
43
discrimination of the different conspecific chemical stimuli, nor of their own
scents, which suggests that these different chemical stimuli were not
discriminated, or that the discrimination did not affect their space use. In
contrast, a similar experiment showed that Spanish terrapins, M. leprosa, clearly
discriminate between male and female conspecific chemical stimuli, especially
during the mating season (Muñoz 2004). Therefore, when deciding space use,
sliders seem to be less chemosensory dependent than Spanish terrapins, whose
reproductive behavior seems based greatly on chemical signals. For example,
male head bobbing, which may help to spread scent from mental glands to
females (Auffenberg 1966) is a normal behavior of M. leprosa during courtship
(N. Polo-Cavia, unpubl. data). Also, throat pumping behavior, a mechanism for
moving water across chemoreceptors in the mouth or nasal cavities for chemical
sampling (Walker 1959), has been observed in M. leprosa (N. Polo-Cavia,
unpubl. data), which suggests a greater use of olfactory senses in this turtle
species. In contrast, T. scripta lacks mental glands, and courtship involves a
visual dance where the male vibrates his claws on the female’s head (Jackson
and Davis 1972). However, olfaction seems to be also used by T. scripta, as one
third of the telencephalon is occupied by the olfactory bulbs (Scott 1979), sex
recognition seems to depend on chemical cues (Cagle 1950) and sniffing has
been observed during courtship (Jackson and Davis 1972). Olfaction also may
play a role in prey detection; Parmenter (1980) showed that T. scripta responds
to odors from fish-meat baits placed in perforated containers, indicating that
location of carrion can be facilitated by olfactory cues.
Our results further indicate that M. leprosa was able to identify scents of
conspecifics and heterospecific T. scripta in water, and that M. leprosa avoided
water with these heterospecific chemical stimuli. In contrast, T. scripta did not
avoid, but neither prefer, water with scent from M. leprosa. The absence of
response in T. scripta may be due to inability to detect heterospecific chemical
cues, or simply to that, although detected, these cues are not avoided because
M. leprosa does not represent a threat for the invasive T. scripta. Preliminary
comparative tests suggested that sliders may be less responsive to olfactory cues
than other freshwater turtle species (Cagle 1950). However, the ability of sliders
to discriminate different olfactory stimulus was established by Boycott and
Guillery (1962), who successfully trained sliders to discriminate an olfactory
stimulus (i.e., amylacetate, vanillin, or eucalyptus oil) that was presented in
water containing also food. It is likely that T. scripta might be able to
discriminate scents of M. leprosa too, and that the absence of responses in the
use of water pools in our experiment could be due to the absence of negative
stimuli associated to the chemical cues of M. leprosa.
On the other hand, the preferences of M. leprosa for water with conspecific
chemical stimuli and the avoidance of water with scent of T. scripta suggest that
44
This behavior may be applicable to natural habitats because concentrations of
the chemical stimuli used in our laboratory experiment may resemble the effect
that a new population of introduced sliders, spreading continuously their
chemical cues, may cause in a natural body of relatively quiet water. Thus, it is
likely that M. leprosa may also identify the presence of chemical cues of T.
scripta in natural ponds, and use this information to avoid these areas.
The ability to recognize conspecific scents has been reported in many
animal species, and may contribute to decrease the costs of aggressive
interactions, or facilitate reproductive interactions (Mason 1992; MüllerSchwarze 2006). However, recognition of heterospecific chemical cues in water
may help to assess risk posed by predators or aversive competitor species in
many aquatic animals (for reviews see Dodson et al. 1994; Kats and Dill 1998).
Prey species often respond to predator or aversive stimuli by reducing activity
or seeking refuge, but, in many different animal species, a simpler avoidance
response of areas with aversive chemicals is the primary response after
chemosensory detection (Kats and Dill 1998). The effects of predator and
aversive chemical cues on avoidance behavior have been examined in many
terrestrial reptiles (e.g., Downes 2002; Amo et al. 2004), but rarely on aquatic
ones. In turtles, Jackson (1990) found that two species of musk turtles
(Sternotherus spp.) avoid odors of their predator, the alligator snapping turtle
(Macrochelys temminckii). Speed of movement, the frequency of gular
pumping behavior, and percentage of time spent by musk turtles in water with
chemicals of alligator snapping turtles were lower than those in water with
odor of a non-predator turtle species (Pseudemys sp.). This suggests that musk
turtles may detect and avoid proximity with water used by the predator turtle
species.
In many cases, animals can acquire recognition of an odor as dangerous
when they simultaneously detect this odor and known indicators of risk such as
the antipredator behavior, or injury-released chemicals, of conspecifics (e.g.,
Magurran 1989; Mathis et al. 1996; Chivers and Smith 1998). In this context,
there are only a few documented cases of native prey able to learn the ability to
avoid invasive species. For example, predator-avoidance behavior can propagate
through a naïve population of fish in less than two weeks after the introduction
of a novel predator (Chivers and Smith 1995). Also, juvenile Pacific treefrogs
(Hyla regilla) from a population that co-occurred with introduced bullfrogs
(Rana catesbeiana) showed a strong avoidance of chemical cues of bullfrogs
(Chivers et al. 2001). It is likely that the presence of an introduced aversive
competitor species might have an effect similar to a novel predator. Native
species might learn to avoid odors from invasive species if these odors were
previously associated with an overt behavioral aggressive response, or
CAPÍTULO 1: Reconocimiento químico
M. leprosa may use chemoreception to avoid water pools occupied by T. scripta.
45
unsuccessful use of resources. For example, two mice species show avoidance
response to heterospecific odors in spring, but not in autumn, probably to avoid
interspecific aggressive encounters due to competition for habitat resources
during the breeding season (Simeonovska-Nikolova 2007). Since T. scripta
seems more aggressive than native European turtles in heterospecific
encounters competing for food or basking places (Cadi and Joly 2003; PoloCavia et al. in press; chapter 2), the avoidance response of native M. leprosa to
heterospecific odors of T. scripta might serve as a spacing mechanism to avoid
aggressive encounters with the alien species in a situation of competitive
disadvantage. Native M. leprosa might acquire information from chemicals in
water, and use this information to distinguish between conspecifics and
heterospecifics, thereby avoiding to spent time and energy in unfavorable
competitive interactions with invasive American turtles. By keeping away from
water pools with odors of T. scripta, M. leprosa might evade costly aggressive
encounters with this invasive species under severe interspecific competition for
limited resources. However, this chemically-mediated avoidance behavior could
result in the displacement and progressive replacement of M. leprosa
populations by the alien T. scripta, which expansion might be further favored
by their lack of chemosensory responses towards native turtle species.
Acknowledgements We thank an anonymous reviewer for helpful comments, the ‘‘Grupo de
Rehabilitación de la Fauna Autóctona y su Hábitat’’ (GREFA) for providing sliders, and ‘‘El
Ventorrillo’’ MNCN Field Station for use of their facilities. Financial support was provided by the
MEC project CGL2005-00391/BOS, and by an ‘‘El Ventorrillo’’ CSIC grant and a MEC-FPU grant
to N. P.-C. The experiments enforced all the present Spanish laws and of the Environmental
Organisms of Madrid Communities where they were carried out.
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48
Capítulo
2
Interacciones agresivas durante la alimentación entre especies nativas e invasoras de galápagos Nuria Polo Cavia, Pilar López y José Martín
En revisión
RESUMEN
50
El galápago de Florida (Trachemys scripta elegans) es una
especie altamente invasiva a nivel mundial, actualmente
introducida en la gran mayoría de los humedales debido al
comercio masivo de mascotas. En la Península Ibérica, esta
especie compite y desplaza al galápago leproso (Mauremys
leprosa), especie autóctona protegida. El galápago de Florida
está considerado como una especie ecológicamente agresiva,
capaz de amenazar o morder a otros individuos mientras
realiza actividades competitivas tales como la alimentación.
Este comportamiento agonístico de los galápagos introducidos
dirigido hacia los galápagos nativos podría afectar
negativamente a la eficiencia nutricional de la especie
indígena M. leprosa. En este trabajo, se compararon las tasas
de ingestión de los galápagos nativos e invasores, y las
interacciones agresivas ocurridas durante la alimentación, en
situaciones de competencia intra e interespecífica. La
cantidad de alimento ingerida por M. leprosa y T. scripta fue
similar cuando compitieron con individuos conespecíficos.
Sin embargo, en condiciones de competencia interespecífica,
la especie invasora ingirió una mayor proporción del
alimento suministrado. Además, los galápagos introducidos
cometieron la mayor parte de las agresiones observadas
durante la actividad de la alimentación, y las agresiones
fueron dirigidas con mayor frecuencia hacia individuos
heteroespecíficos. Nuestros resultados sugieren una mayor
agresividad y un comportamiento más competitivo del
introducido galápago de Florida en la pugna por los recursos
alimenticios, lo que podría contribuir a explicar el
desplazamiento de las poblaciones nativas de M. leprosa ■
AGGRESSIVE INTERACTIONS DURING FEEDING BETWEEN NATIVE
AND INVASIVE FRESHWATER TURTLES
Abstract The red-eared slider (Trachemys scripta elegans) is a worldwide highly invasive species,
currently introduced in most freshwater habitats as a consequence of massive pet trade. In the
Iberian Peninsula, this species is competing and displacing the endangered native Spanish
terrapin (Mauremys leprosa). Sliders are considered environmentally-aggressive turtles, capable
of threatening or biting other individuals during competitive activities such as feeding. We
hypothesized that agonistic behavior of introduced sliders against native terrapins might
negatively affect the feeding efficiency of M. leprosa. We compared food ingestion of turtles and
aggressive interactions during feeding, under situations of conspecific and heterospecific
competition. The amount of food ingested by native and introduced turtles was similar under
conspecific competition, but T. scripta ingested a greater percentage of food supplied under
heterospecific competition. Also, introduced sliders initiated most of the aggressions observed
during feeding activity, and aggressions were more frequently directed to heterospecifics. Our
results suggest a more aggressive and competitive behavior of introduced T. scripta in vying for
food resources, which might contribute to explain the observed displacement of native
populations of M. leprosa.
S
pecies are being increasingly introduced by humans outside their natural
ranges, competing and displacing native organisms from their ecological
niches (Herbold and Moyle 1986; Williamson 1996; Mooney and Hobbs
2000; Lockwood et al. 2007). These introductions have altered terrestrial and
aquatic communities worldwide, constituting the second greatest threat to
biodiversity after habitat destruction (Wilcove et al. 1998; Gurevitch and
Padilla 2004). Alien species may displace native species through predation,
hybridization, pathogens transmission, or competition for resources (Dodd and
Seigel 1991; Shigesada and Kawasaki 1997; Butterfield et al. 1997; Manchester
and Bullock 2000).
An example of biological invasion is the red-eared slider (Trachemys scripta
elegans), which has been commonly exported from the USA as part of the pet
trade, being introduced in many countries of Africa, Asia and Europe, especially
in Mediterranean habitats (Luiselli et al. 1997; Chen and Lue 1998; Pleguezuelos
2002). In the Iberian Peninsula, T. scripta has been released in diverse aquatic
ecosystems, where it is displacing the native Spanish terrapin (Mauremys
leprosa) (Da Silva and Blasco 1995; Pleguezuelos 2002; Vilà et al. 2008). This
native species has suffered a considerable recession during the last decades,
being currently considered as endangered species (Pleguezuelos et al. 2002).
Recent studies have pointed out to diverse competitive advantages of sliders
over Spanish terrapins, such as a more accurate assessment of predatory risk in
CAPÍTULO 2: Interacciones agresivas durante la alimentación
Keywords Aggressiveness • Freshwater turtles • Invasive species • Mauremys leprosa • Feeding
competition • Trachemys scripta
51
altered habitats, displacement of native turtles mediated by chemical cues
avoidance, or a greater thermal inertia that favors heat retention (Polo-Cavia et
al. 2008, 2009a,b). Also, turtles may compete for food, nesting sites or basking
places (Cadi and Joly 2003, 2004; N. Polo-Cavia, unpubl. data). Sliders are
aggressive omnivores with high preferences for a carnivorous diet (growth rates
significantly decline when individuals subsist on a vegetative diet, Parmenter
1980; Gibbons 1990), and might likely be involved in interference competition
for food with Spanish terrapins, since M. leprosa consumes mainly animal
matter and the two turtle species overlap in diet and feeding areas (Keller and
Busack 2001; Pleguezuelos 2002).
The ideal free distribution model (IFD, Fretwell and Lucas 1970) predicts
that foragers will distribute themselves among resource patches in relation to
the quantity of food available in such patches. However, systematic deviations
from IFD are expected when competitive asymmetries exist between foragers,
and so, the access to resource patches is constrained by dominant individuals
(Holmgren 1995; Moody and Houston 1995; Spencer et al. 1995). For example,
in habitats with low food availability and difficulties for spatial segregation,
patterns of habitat use by tits (Parus spp.) have been shown to be affected by
intra and interspecific dominance (Alatalo et al. 1986; Alatalo and Moreno
1987). Similarly, experimental studies on the social rank of the juvenile Atlantic
salmon (Salmo salar) showed that dominant fishes occupy the high quality
patches, while subordinates are forced out (Huntingford et al. 1993;
Huntingford and García de Leániz 1997). Furthermore, under interspecific
competition, salmonid fish species with greater innate competitive ability
occupy the more suitable habitats while subordinate species are displaced,
which cause dominant species to gain higher growth rates than subordinates
(Fausch 1984; Nakano 1995).
Several studies addressing overlap food preferences between sympatric
species of turtles suggest that food niche separation is common among turtle
species with overlapping diets (Moll 1976a; Vogt and Guzman 1988). Williams
and Christiansen (1981) found that two species of turtles of the genus Trionyx
with high degree of food overlap partitioned the habitat by one being a bottom
forager and the other feeding in the water column. However, differences in
growth rates and reproductive patterns between populations of the same species
are often correlated with different levels of interspecific competition and
displacement in the feeding niche (Moll 1976b; Bury 1979; Gibbons et al 1979;
Vogt and Guzman 1988), what suggest that interspecific dominance
relationships may lead to the lower survival of turtle species enduring high
competitive pressures.
Displacement between competitors is mainly expected to occur through
aggressive interactions, although subordinates have been observed to
52
METHODS
Study animals
During May 2006, we captured 16 Spanish terrapins (M. leprosa) (carapace
length: mean ± SE = 14.2 ± 1.9 cm, range = 10.0-16.6 cm) in several ponds and
creeks of the Manzanares River (Madrid Province, Spain), using funnel traps
baited with fresh pet food and raw fish. We also obtained 16 red-eared sliders
(T. scripta) (carapace length: mean ± SE = 14.5 ± 2.2 cm, range = 10.9-17.4) from
a large outdoor pond (Madrid Province, central Spain), where they had been
maintained under seminatural conditions by the conservationist organization
“Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat” (GREFA). These
turtles had been recently extracted from introduced populations in Central
Spain to avoid aversive effects on the original ecosystem balance. Sliders were
selected basing on their body sizes, which were similar to those of native
Spanish terrapins captured in the field. Both samples of M. leprosa and T.
scripta were sex-balanced.
CAPÍTULO 2: Interacciones agresivas durante la alimentación
voluntarily displace themselves when dominant individuals approach
(Huntingford and Turner 1987; Lindeman 1999; Polo-Cavia et al. 2009a).
Aggressive behaviors such as open-mouth gestures, biting and pushing have
been reported in a variety of turtle species, including T. scripta, when resources
are limiting (Boice 1970, Lovich 1988; Kaufmann 1992, Lindeman1999).
Introduced sliders are considered especially competitive turtles, capable of
threatening or biting conspecific and heterospecific individuals during
competitive activities (Arvy and Servan 1998, Lindeman 1999). In consequence,
T. scripta turtles might impede M. leprosa terrapins to adequately forage, or
exclude them from areas with more profitable feeding resources through
aggressive interactions. We hypothesized that the higher aggressiveness of
introduced sliders might negatively affect the feeding efficiency of native
Spanish terrapins. We compared experimentally the food ingestion of both M.
leprosa and T. scripta under situations of conspecific and heterospecific
competition, analyzing aggressive interactions between turtles during feeding
activity. The purpose of this paper was to determine 1) the feeding efficiency of
M. leprosa when competition for food resources occurs between conspecific
individuals, as opposed to a situation of interspecific competition with
introduced sliders, 2) the level of aggressiveness and dominance among
conspecific vs. heterospecific turtles during feeding competition, and 3) the
relationship between the agonistic behavior of introduced T. scripta and the
possible displacement from food resources of native M. leprosa.
53
All turtles were individually housed at “El Ventorrillo” Field Station
(Navacerrada, Madrid Province), in outdoor home aquaria (60 x 40 x 30 cm),
filled with water and containing stones that allowed turtles to bask. The
temperature and photoperiod were those of the natural surroundings. Turtles
were held in captivity for at least two weeks before experiments, to allow them
to familiarize with captivity conditions. During this time, turtles were fed ad
libitum small pieces of commercial compound feed (dehydrated meat) three
times a week, so that they became habituated to the food supplied in the
experiments. All turtles were healthy during the trials and all maintained their
body mass. At the end of experiments, turtles were returned to the GREFA’s
ponds (sliders) or to their exact field capture sites (Spanish terrapins).
Experimental procedure
We compared food ingestion of M. leprosa and T. scripta and frequencies of
aggressive interactions between turtles during feeding activity, under situations
of conspecific and heterospecific competition, and with competitors of the same
and the opposite sex. We performed experiments outdoor, in aquaria exact to
home aquaria, but that had not housed any turtle before the trials. For the
experiments, each turtle was paired, according with its body size, with (1) a
conspecific of the same sex, (2) a conspecific of the opposite sex, (3) a
heterospecific of its same sex, and (4) a heterospecific of the opposite sex. Thus,
we tested each subject turtle in four experimental treatments in a random order.
Both members of the pairs were introduced together in the experimental
aquaria right before the trial took place. During trials, we supplied 6 pieces of
commercial compound feed to each pair of turtles (the amount of food provided
was restricted to elicit competition within pairs). Turtles were used to
experimental conditions and experimental food and they were hungry during
the trials, so they fought for the pellets and always ate them all in few minutes).
We considered that competition for compound feed pellets in captivity properly
reflected competition for food in the wild, since these food pellets are similar in
appearance, smell and floating dynamic to several food items commonly
consumed by M. leprosa and T. scripta turtles, such as shards of algae, pieces of
carrion, or slow-moving prey such as snails and other small mollusks (Newbery
1984; Parmenter and Avery 1990; Arnold and Ovenden 2002). From a hidden
position, an experimenter recorded the number of food pellets that each turtle
ingested, and the number of aggressive interactions (i.e., bites specifically
directed to the competitor) that took place between the two members of the
pair until all the food was consumed. Then, paired turtles were separated again
and returned to their individual home aquaria, where they were fed ad libitum
and ate their fill. Trials were replicated 5 times in different days, so that each
54
turtle competed for 30 pieces of food within each experimental treatment
throughout the whole experiment. Tests were spaced in time for two days so
that possible stress resulting from one partner did not affect subsequent
behavior with other partners. We did not fed turtles during these two days to
encourage them to compete for food in the following trial.
To compare number food pellets ingested by each individual subject turtle
across treatments, we used a three-way repeated measures analysis of variance
(ANOVA), with the experimental treatments, competitor species (‘conspecific
competitor’ vs. ‘heterospecific competitor’) and competitor sex (‘same sex
competitor’ vs. ‘opposite sex competitor’), as two within-subjects factors. The
species of the subject turtle was included as a between-subjects factor. Previous
analyses showed that size differences between turtles were non-significant, as
we intended in the selection of the experimental turtles based on similar body
sizes. Therefore, size was not included in further analyses. Also, the sex of the
subject turtle did not influence the food ingested by turtles, and thus, sex was
not considered in final analysis. We verified data normality using ShapiroWilk’s test and tested for homogeneity of variances (Levene’s test). Pairwise
comparisons were made using Tukey’s honestly significant difference tests
(Sokal and Rohlf 1995).
To analyze agonistic behavior between turtles during feeding activity, we
used log-linear models to compare the frequency of aggressive interactions
across treatments (Sokal and Rohlf 1981). A four-way contingency table was
generated by the factors species of the aggressor, sex of the aggressor, species of
the subordinate (‘conspecific subordinate’ vs. ‘heterospecific subordinate’) and
sex of the subordinate (‘same sex subordinate’ vs. ‘opposite sex subordinate’).
Dominance between the two members of the pairs was established following
the criterion of aggressions inflicted less aggressions suffered for each turtle of
each pair, computing the 5 replicas of each trial, and defining the turtle with
the highest positive sum as the dominant individual (Martín and Salvador
1993). Then, we used chi-square and binomial tests to compare dominance of
turtles under intra vs. interspecific competition.
We used Spearman’s rank-order correlations to analyze the relationship
between total amount of food ingested and aggressions inflicted and suffered by
M. leprosa and T. scripta turtles, under both situations of intra and interspecific
competition.
CAPÍTULO 2: Interacciones agresivas durante la alimentación
Data analyses
55
RESULTS
We found significant differences between M. leprosa and T. scripta in total
amount of food ingested (three-way repeated measures ANOVA, F = 14.43, df =
1,30, P < 0.001), with a greater overall percentage of food ingested by
introduced sliders (55 ± 2 %) than by native terrapins (45 ± 2 %). There were no
significant differences in food ingested by turtles under conspecific and
heterospecific competition (F = 0.01, df = 1,30, P = 0.99), and the effect of the
sex of the competitor was not significant (F = 0.01, df = 1,30, P = 0.99).
However, the interaction between species of the subject turtle and species of
the competitor was significant (F = 26.15, df = 1,30, P < 0.0001). Thus, food
ingestion was similar between M. leprosa and T. scripta turtles under
conspecific competition (Tukey’s test, P = 0.99), but under heterospecific
competition, sliders ingested a greater percentage of food than Spanish terrapins
(P = 0.004) (Fig. 2.1). Also, under heterospecific competition, M. leprosa turtles
tended to reduce the amount of food ingested while T. scripta tended to
increase it (P = 0.07 in both cases) (Fig. 2.1). The rest of the interactions were
non-significant (F ≤ 0.013, df = 1,30, P ≥ 0.91).
Figure 2.1 Percentage of food (mean ± SE)
ingested by introduced T. scripta and native
M. leprosa under situations of conspecific
100
Conspecific
Heterospecific
(open rectangle) and heterospecific (dotted
rectangle) feeding competition.
Food ingestion (%)
80
60
40
20
0
T. scripta
M. leprosa
We observed 27 aggressive interactions in total during feeding competition.
Aggressions were more frequently inflicted by introduced T. scripta than by
native M. leprosa, and occurred more frequently between heterospecific
individuals (Table 2.1). These differences were statistically significant, as shown
by the fit of log-linear models to the four-way contingency table crossing the
effects of the species of the aggressor, the sex of the aggressor, the species of the
56
subordinate and the sex of the subordinate. The sex of the aggressor did not
significantly influence aggressiveness of turtles during feeding activity, but
there was a tendency of male and female turtles close to signification to attack
competitors of the opposite sex more often than competitors of the same sex.
The rest of the interactions were non-significant (Table 2.2).
Overall dominance of turtles varied depending on the experimental
treatment (intraspecific vs. interspecific competition); under intraspecific
competition, dominance was established in 5/32 monospecific pairs of turtles
(dominance was observed in 2/16 M. leprosa pairs and in 3/16 T. scripta pairs),
while under interspecific competition, we observed dominance in 11/32 mixed
Frequency of aggressions (bites within experimental pairs) observed during feeding
competition between M. leprosa and T. scripta turtles, directed to conspecific and heterospecific
individuals of the same and the opposite sex.
Table 2.1
Subordinate
Conspecific
Same sex
Opposite sex
Heterospecific
Same sex
Opposite sex
T. scripta
Male
Female
Male
Female
1
1
0
0
0
3
0
0
0
2
1
0
2
6
4
7
Table 2.2 Results of the fit of log-linear models for the four-way contingency table generated by
the factors species of the aggressor, sex of the aggressor, species of the subordinate and sex of the
subordinate (df = 1 in all cases). Raw data are shown in Table 2.1.
Effect
G2
P
Species of the aggressor
Sex of the aggressor
Species of the subordinate
Sex of the subordinate
Species of the aggressor x sex of the aggressor
Species of the aggressor x species of the subordinate
Species of the aggressor x sex of the subordinate
Sex of the aggressor x species of the subordinate
Sex of the aggressor x sex of the subordinate
Species of the subordinate x sex of the subordinate
Species of the aggressor x sex of the aggressor x species of the subordinate
Species of the aggressor x sex of the aggressor x sex of the subordinate
Species of the aggressor x species of the subordinate x sex of the subordinate
Sex of the aggressor x species of the subordinate x sex of the subordinate
8.62
0.003
0.26
8.62
3.52
0.44
1.50
0.80
2.25
1.42
0.002
0.12
0.27
0.37
0.014
0.61
0.003
0.06
0.51
0.22
0.37
0.13
0.23
0.97
0.73
0.60
0.54
0.91
CAPÍTULO 2: Interacciones agresivas durante la alimentación
M. leprosa
57
pairs of M. leprosa and T. scripta (Pearson’s chi-square test, χ2 = 8.53, P = 0.004).
Under interspecific competition, dominance of M. leprosa was observed in a
lower number of pairs than under intraspecific competition (1/11 vs. 2/5), and
dominance of T. scripta was observed in a higher number of pairs than under
intraspecific competition (10/11 vs. 3/5) (χ2 = 4.38, P = 0.04). Within
heterospecific pairs in which dominance could be established, T. scripta was
clearly dominant over M. leprosa (10/11; two-tailed binomial test, P = 0.012).
Total amount of food ingested by M. leprosa under interspecific competition
correlated positively with level of aggressiveness suffered by native terrapins
(Spearman’s rank-order correlations, rs = 0.53, n = 16, P = 0.04). The rest of the
correlations analyzing the relationship between food ingestion and suffered or
inflicted aggressiveness were non-significant (M. leprosa: -0.41 ≤rs ≤ 0.25, n =
16, P ≥ 0.11 in all cases; T. scripta: -0.36 ≤ rs ≤ 0.19, n = 16, P ≥ 0.16 in all cases).
DISCUSSION
In contrast with the ideal free distribution (IFD) model assumption that all
foragers are equal in competitive skills, differing competitive abilities among
individual foragers is widespread in nature (Holmgren 1995; Moody and
Houston 1995; Spencer et al. 1995). In consequence, some competitors are able
to exclude others through aggressive interactions (Schoener 1983). The results
of this study show that feeding competition between native Spanish terrapins
and introduced red-eared sliders follows this asymmetrical pattern. M. leprosa
and T. scripta did not differ in total amount of food ingested under intraspecific
competition but, when the two turtle species were forced to forage together,
the access of M. leprosa to feeding resources was significantly restricted by T.
scripta, which ingested a higher percentage of the food supplied. This suggests a
greater competitive ability of introduced sliders in vying for feeding resources.
Our results further indicate that introduced T. scripta is a more aggressive
species than native M. leprosa. Observed aggressions during feeding were
mainly committed by sliders (more than 81 %), and aggressive interactions were
much scarcer under intraspecific competition: less than 14 % of the aggressions
committed by T. scripta were directed to conspecific competitors, while the rest
of its agonistic behavior was directed to M. leprosa, which attacked sliders only
in 3 occasions. Although escalated aggressive behavior was minority across the
whole experiment, such a high percentage of aggressions directed by sliders to
Spanish terrapins suggests that T. scripta is highly dominant over M. leprosa.
Indeed, dominance by means of aggressiveness was significantly greater within
pairs subjected to interspecific competition, in which T. scripta widely
overcame M. leprosa. Moreover, heterospecific aggressions were consistently
initiated by sliders and were never responded by native terrapins. In contrast, in
58
CAPÍTULO 2: Interacciones agresivas durante la alimentación
the 3 exceptional cases in which M. leprosa attacked T. scripta, sliders
immediately after established their superiority by displaying aggressive
behavior (e.g., in one instance, a Spanish terrapin targeted the red spot behind
the ear of its slider competitor, most probably confounding this characteristic
spot with a food pellet. Immediately afterward, the slider responded biting the
native terrapin).
The sex of the competitors had no significant effect either in the amount of
food ingested, or in their aggressive behavior. However, turtles tended to attack
more frequently competitors of the opposite sex, regardless their species
identity. Males of both turtle species show lower volumes and weights than
females for same body sizes (Polo-Cavia et al. 2009b). Because turtles were
paired minimizing differences in body size, females might perceive other
females as heavier and more dangerous competitors than males, thus avoiding
intrasex confrontations. On the other hand, males might likely evade fighting
with other males that might represent a double threat, since competition among
males entails not only food resources but also females. Nevertheless, the last
would imply sex recognition of heterospecific individuals, which has been
poorly supported (Jackson and Davis 1972, Gibbons 1990).
Agonistic behavior during trials was possibly triggered by experimental
conditions, since turtles were confined in experimental aquaria and food
resources were highly limited in order to force competition. However, in
sympatric populations in nature, dominance of introduced sliders over native
terrapins might result in displacement of M. leprosa from preferred feeding
areas by means of avoidance behavior. Avoidance is known to be used by
inferior competitors to reduce interference from more competitive species
(Menge and Menge 1974; Sloan 1984; Gaymer et al. 2002). This prediction is
consistent with our previous observations that native M. leprosa avoids water
pools with chemical stimuli of introduced T. scripta (Polo-Cavia et al. 2009a),
presumably as a mechanism to evade aggressive encounters with sliders. By
shifting to less profitable habitats, or by directly abandoning food resources,
Spanish terrapins might evade costs of hostile interactions with aggressive
sliders. Interestingly, percentage of food ingested by M. leprosa under
interspecific competition correlated positively with level of aggressiveness
suffered by native terrapins. We observed that daring M. leprosa which
incurred in active competition for food pellets were harshly punished by
aggressive sliders, while shier individuals that displayed a subordinate role were
less attacked. This suggests the existence of a trade-off between feeding
efficiency and costs of aggressive competition with sliders, which might lead M.
leprosa to avoid feeding areas in where T. scripta forages and move away to look
for alternative food sources, thus transferring the benefit of exploiting preferred
areas to the introduced competitor.
59
Many authors have suggested that resources partitioning and microhabitat
use reduce interspecific competition for food among sympatric turtles (Moll
1976a; Vogt 1981; Williams and Christiansen 1981; Vogt and Guzman 1988).
However, switching of inferior competitors to alternative less profitable diets
and habitats widely occurs in nature as consequence of asymmetrical
interaction between species (Abramsky et al. 1990; Nakano 1995; Gaymer 2001;
Ovadia and zu Dohna 2003), and sometimes is hard to elucidate what is
partition and what displacement (Kronfeld-Schor and Dayan 1999). For
example, consume of animal prey by the omnivorous generalist musk turtle
Kinosternon leucostomum has been observed to considerably decrease in
localities in which this species coexists with a more specialized competitor
(Staurotypus triporcatus), with negative consequences in growth and
reproductive output (Vogt and Guzman 1988). Temporal partitioning (usually
asymmetrical) is another viable mechanism for coexistence between
competitive species (Kronfeld-Schor and Dayan 1999, 2003; Weinstein 2003).
For example, interspecific displacement from preferred activity time for
foraging has been observed among co-occurring gerbil species (Ziv et al. 1993).
However, evolutionary constraints may limit the use of this diel niche axis.
When partition occurs, the subordinate species normally experiences a cost in
its efficiency of resource exploitation. Thus, interference and niche
displacement is underlying the coexistence of many competitive species.
We consider that competition between native and introduced turtles
observed in our experiment may be representative of interspecific competitive
interactions occurring in the wild, for two main reasons. First, we used small
pieces of commercial compound feed that may resemble food items that are part
of the natural diet of M. leprosa and T. scripta turtles. Second, direct
competition for food between M. leprosa and T. scripta is likely to occur in
nature, since both turtle species are opportunistic omnivores, mainly predatory.
Although more phytophagous than native terrapins, sliders are preferential
carnivores when a high-protein diet is available (Gibbons 1990; Díaz-Paniagua
et al. 2002; Pleguezuelos 2002). The two turtle species hunt in the same areas
–shallow waters with abundant vegetation-, although M. leprosa may also
forage in more open waters (Arnold and Ovenden 2002; Hart 1983). Also, the
preferred activity time for feeding seems to overlap between native and
introduced turtles. T. scripta eats at any time of the day, but usually in early
morning and late afternoon (Cagle 1950; Newbery 1984), very likely interfering
on feeding habits of M. leprosa (J.L. Rubio, unpubl. data). In addition, diurnal
trapping produced few Spanish terrapins, while tending traps in early evening
and prolonging trapping until next morning increased trapping success,
probably indicating a more crepuscular or morning feeding activity of M.
leprosa.
60
Acknowledgements
We thank the “Grupo de Rehabilitación de la Fauna Autóctona y su
Hábitat” (GREFA) for providing sliders and “El Ventorrillo” MNCN Field Station for use of their
facilities. Financial support was provided by the MEC project CGL2005-00391/BOS and the MCI
project CGL2008-02119/BOS, and by a MEC-FPU grant to N. P.-C. The experiments comply with
all the present Spanish laws of the Environmental Organisms of the “Comunidad de Madrid”
where they were performed.
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64
Capítulo
3
Interacciones competitivas durante la actividad de asoleamiento entre especies nativas e invasoras de galápagos Nuria Polo Cavia, Pilar López y José Martín
Biological Invasions (2009) In press
RESUMEN
66
El galápago de Florida (Trachemys scripta elegans) se
encuentra actualmente introducido en diversos países
mediterráneos, donde se comporta como especie invasora,
compitiendo y desplazando poblaciones nativas del protegido
galápago leproso (Mauremys leprosa). Sin embargo, la forma
en la que se producen las interacciones competitivas entre las
dos especies es relativamente desconocida. Factores tales
como un mayor tamaño corporal o adaptaciones preexistentes, originadas en hábitats con alto grado de
competencia interespecífica, podrían conferir ventajas
competitivas al introducido T. scripta durante la actividad de
asoleamiento. Así pues, la eficiencia termorreguladora de los
galápagos nativos podría verse comprometida en una
situación de competencia por los recursos de asoleamiento
con el introducido galápago americano. En este trabajo, se
analizó experimentalmente la actividad de asoleamiento de T.
scripta y M. leprosa en situaciones de competencia intra e
interespecífica por lugares de asoleamiento, ocasional y a
largo plazo. Los galápagos nativos sometidos a competencia
interespecífica redujeron su actividad de asoleamiento, se
asolearon por periodos más cortos que los galápagos exóticos
y evitaron compartir los lugares de asoleamiento con la
especie introducida. Nuestros resultados sugieren el
desplazamiento del galápago leproso durante el asoleamiento
por parte del introducido galápago de Florida. Este
detrimento en el comportamiento termorregulador de los
galápagos nativos cuando se produce competencia directa por
los recursos de asoleamiento con los galápagos exóticos podría
conducir a una pérdida de eficiencia en las funciones
fisiológicas de M. leprosa ligadas a la termorregulación, tales
como la digestión o la respuesta locomotora, favoreciéndose
así la expansión de la especie invasora ■
COMPETITIVE INTERACTIONS DURING BASKING BETWEEN NATIVE
AND INVASIVE FRESHWATER TURTLE SPECIES
Abstract The red-eared slider (Trachemys scripta elegans) is currently introduced in many
Mediterranean countries, where it behaves as an invasive species that competes and displaces
native populations of the endangered Spanish terrapin (Mauremys leprosa). However, the nature
of competitive interactions is relatively unknown. During basking activity, factors like greater
body size or pre-existing behavioral adaptations to an original habitat with higher levels of
interspecific competition might confer competitive advantages to introduced T. scripta with
respect to native terrapins. We hypothesized that competition for basking places with the
introduced T. scripta might negatively affect the efficiency of basking and thermoregulation of
the native Spanish terrapin. We experimentally analyzed the basking activity of T. scripta and M.
leprosa under occasional and long-term situations of intra and interspecific competition. Native
M. leprosa subjected to interspecific competition reduced their basking activity, basked for
shorter periods than T. scripta, and avoided basking stacked with the exotic turtles. These results
suggested the displacement from the basking sites of the native terrapin by the introduced T.
scripta. The decreased basking activity of native M. leprosa when competing directly for basking
places with introduced sliders may lead native terrapins to a loss in the efficiency of physiological
functions related to ineffective thermoregulation, such as digestion or locomotor performance,
thus favoring the expansion of the invasive species.
Keywords Basking • Freshwater turtles • Invasive species • Mauremys leprosa • Thermoregulation
• Trachemys scripta
CAPÍTULO 3: Competencia durante el asoleamiento
F
reshwater turtles spend much of their diel activity cycle basking on logs
and stones that emerge from the water (Boyer 1965). As in most
ectotherms, basking atmospherically serves as the main mechanism to
achieve thermoregulation in aquatic turtles (Boyer 1965; Crawford et al. 1983;
Schwarzkopf and Brooks 1985; Meek and Avery 1988). Physiological processes
occur optimally at the mean selected temperature of a species, and basking
allows turtles to attain and maintain body temperatures close to this optimal
temperature (Dawson 1975; Avery 1982; Huey 1982; Edwards and BlouinDemers 2007). Turtles that bask benefit from a raised metabolic rate (Jackson
1971; Kepenis and McManus 1974; Dubois et al. 2008) that facilitates and
increases the efficiency of their physiological processes (Crawford et al. 1983;
Hammond et al. 1988; Ben-Ezra et al. 2008). Basking is especially important to
maximize digestive processes (Moll and Legler 1971; Parmenter 1981;
Gianopulos and Rowe 1999). Dermal synthesis of vitamin D (Pritchard and
Greenhood 1968; Avery 1982) and secondary functions have also been
attributed to aerial basking behavior, such as conditioning of the skin and shell
by drying and ectoparasite removal (Cagle 1950; Neill and Allen 1954; Boyer
1965).
67
The Spanish terrapin (Mauremys leprosa) is a semiaquatic medium-sized
turtle that actively bask outside of water to achieve and maintain body
temperatures within the intervals necessary for its daily activities (Meek 1983).
M. leprosa is widespread in the southern and central Iberian Peninsula and
northwestern Africa (Keller and Busack 2001), but its populations have
considerably declined during recent decades, and it is currently considered an
endangered species (Da Silva 2002). Habitat destruction and human pressure are
the major factors responsible for this decline, but competition with exotic
introduced turtles, mainly the American red-eared slider (Trachemys scripta
elegans), might be worsening the state of the remaining populations (Da Silva
and Blasco 1995; Pleguezuelos 2002). Although the nature of the interaction
between sliders and Spanish terrapins is not clear, it is possible that direct
competition for food, refuges or basking places is present (Crucitti et al. 1990).
Recent studies indicated that sliders have diverse advantages over Spanish
terrapins (Polo-Cavia et al. 2008, 2009a,b). Competition for basking sites has
been described between sliders and the European pond turtle (Emys orbicularis)
(Cadi and Joly 2003), and field observations suggest that competition is very
likely to occur also between sliders and the Spanish terrapin, as both turtle
species are commonly forced to share basking sites (Díaz-Paniagua et al. 2002;
Pleguezuelos 2002), such as emergent rocks or logs, which may be a restricted
resource in the wild (Cadi and Joly 2003).
Competition for space may occur among conspecific or heterospecific
turtles if basking substrates are limiting (Bury and Wolfheim 1973; Auth 1975;
Bury et al. 1979; Pluto and Bellis 1986; Lovich 1988; Lindeman 1999). In such
situations, body size may play an important role in determining the outcome of
the competitive interaction (Bury and Wolfheim 1973; Auth 1975; Lindeman
1999). Consequently, differences in body size between sliders and native turtles
might possibly favor invasive species during basking interactions, since T.
scripta reaches larger adult body size on average than native freshwater turtles
(Da Silva and Blasco 1995; Arvy and Servan 1998). If direct competitive
interactions are disadvantageous for native terrapins, they would likely avoid
basking places occupied by T. scripta, thus favoring the invasive species. Also,
in the original habitats of T. scripta, the species richness of most chelonian
assemblages is dramatically higher compared with that of the Iberian
assemblages (only two turtle species: M. leprosa and E. orbicularis), which may
confer competitive advantages to invasive sliders over native Iberian terrapins.
Adapted to environments with greater levels of interspecific competition and
aggressiveness, sliders can easily monopolize the most suitable basking sites in
their new habitats, where they have been introduced, impeding basking by
native turtles (Cadi and Joly 2003), probably contributing to the loss of weight
and decreased survival of native terrapins after long-term competition with
68
sliders (Cadi and Joly 2004). Since basking is a vital activity in regions where
mean temperatures fall below minimum thermal requirements (Hutchison and
Maness 1979; Crawford et al. 1983), interference in basking behavior of Spanish
terrapins caused by sliders might severely affect the efficiency of
thermoregulation and physiological functions of the native species. A decrease
in thermoregulatory behavior of native M. leprosa might be one of the causes
that contribute to the observed displacement of their populations.
In this study, we experimentally tested the hypothesis that competitive
interactions occur between the introduced red-eared slider (T. scripta) and the
Spanish terrapin (M. leprosa) during basking activity when basking resources
were limited. Our objectives were to determine 1) whether alteration in time
spent basking by native Spanish terrapins occurred under occasional and/or
long-term interspecific competition with sliders, in comparison with situations
of intraspecific competition, and 2) whether invasive sliders had a consistent
advantage over Spanish terrapins in competition for basking space.
METHODS
During spring, as a part of a long-term study, we captured Spanish terrapins (M.
leprosa) with baited funnel traps in several ponds and tributary streams of the
Manzanares River (Madrid Province, Spain). We also obtained red-eared sliders
(T. scripta) from a large seminatural outdoor pond (Madrid Province, Spain),
where they had been maintained by the conservationist organization “Grupo de
Rehabilitación de la Fauna Autóctona y su Hábitat” (GREFA). These turtles
originated from introduced populations in central Spain.
All turtles were housed in outdoor aquaria at “El Ventorrillo” Field Station
(Navacerrada, Madrid Province), about 20-30 km from the capture sites. The
temperature and photoperiod were the same as the natural surroundings.
Turtles were fed mince meat, earthworms and slugs three times a week. Turtles
were held in captivity for at least two weeks before experiments to allow them
to habituate to captivity conditions. At the end of experiments, all turtles had
maintained their body mass and were returned to the GREFA ponds (sliders) or
to their exact field capture sites (Spanish terrapins). The experiments enforced
all the present Spanish laws of the Environmental Organisms of Madrid and
Community where they were carried out.
Occasional competition
In a first experiment, we compared the use of basking sites by M. leprosa in
situations of both intra and interspecific competition and with competitors of
CAPÍTULO 3: Competencia durante el asoleamiento
Study animals
69
the same and the opposite sex. Spanish terrapins (straight-line carapace length:
mean ± SE = 15.2 ± 0.4 cm, range = 10.0-20.4 cm, n = 27) were individually
housed in home aquaria (60 x 40 x 30 cm) that were filled with water and
contained a single brick (24 x 11.5 x 7 cm) emerging 1 cm above water surface.
Turtles were completely free to bask on the brick before and after the
experiments.
Trials took place outdoors, in aquaria like the home aquaria, but that had
not housed any experimental turtle before the trials. For the trials, each Spanish
terrapin was paired, according with its body size, with (1) a conspecific of the
same sex, (2) a conspecific of the opposite sex, (3) a heterospecific (T. scripta) of
the same sex, and (4) a heterospecific of the opposite sex. Each M. leprosa
subject was tested once in each of the four experimental treatments in a random
order. Both members of the pairs were introduced together in the experimental
aquaria. During the trials, turtles were able to bask on the brick, one at a time,
or stacked one on top of the other, given the small surface area available for
basking. After each trial, paired turtles were separated again and returned to their
individual home aquaria. Tests were spaced in time for at least two days so that
possible stress resulting from one partner did not affect subsequent behavior in
further tests. Turtles were not fed the day that they were tested. An
instantaneous scan sampling method was used and each pair of turtles was
monitored during 3 h, recording every 5 min the location of each M. leprosa
subject (36 scans per turtle per day in total). We checked that water and air
temperatures, illumination, and water depth were similar among tests.
Long-term competition
In a second experiment, the basking patterns of M. leprosa and T. scripta were
analyzed, in long-term situations of intra and interspecific competition, when
they shared their home aquaria with a conspecific or a heterospecific partner
respectively. We used 13 M. leprosa (straight-line carapace: mean ± SE = 14.6 ±
0.4 cm, range = 12.3-16.6 cm) and 11 T. scripta (straight-line carapace: mean ±
SE = 13.7 ± 0.6 cm, range = 10.9-16.4 cm) to compose experimental and control
pairs of turtles. Each pair was placed into one home aquarium (60 x 40 x 30 cm).
Experimental pairs consisted of one Spanish terrapin and one slider of the same
sex and similar size, whereas the control pairs were made up of two individuals
of the same species and sex, and similar size. A single brick (24 x 11.5 x 7 cm) in
each home aquarium forced turtles to compete for basking, as in the first
experiment. All turtles were simultaneously introduced into the aquaria, which
they occupied during the whole experiment. Turtles remained untested for two
weeks prior to observations to allow them to accustom to the competition
situation. All turtles had been fed ad libitum the day before the trials and every
70
day after finishing the observations, but turtles were not fed during the
observations to standardize hunger levels and avoid effects of feeding status on
basking activity (Hammond et al. 1988, Dubois et al. 2008).
We used the instantaneous scan sampling method to monitor each pair of
turtles from 11:00 to 13:30 h, scanning continuously from a hidden position,
and recording every 10 min the location of the turtles (16 scans per pair per day
in total). Water and air temperatures were also recorded with digital
thermometers (precision ± 0.1 °C). We replicated observations of basking
behavior of each pair of control or experimental turtles for 10 non-consecutive
days. From the scans, we calculated the percentage of basking activity at each
time of day and the average and maximum length of basking events for each
turtle, halfway through the 10 days. Length of basking bouts was ensured by
confirming visually the persistence of each turtle’s location during the interscan intervals. The dates for observation were selected depending on the
meteorological conditions (i.e., sunny weather). The interval between tests was
of at least 24 h. We controlled the extent of illumination by sunlight and water
depth to ensure that they were similar in all home aquaria during the tests and
did not affect the turtle responses (De Rosa and Taylor 1980). Terraria with the
different treatments were placed randomly, and turtles in all the treatments
were tested in parallel in each day.
In the first experiment, we used a three-way repeated measures analysis of
variance (ANOVA) to analyze the differences in number of observations in
which basking was occurring (‘basking activity’) across treatments by the same
individual subject M. leprosa. The experimental treatments, competitor species
(‘conspecific competitor’ vs. ‘heterospecific competitor’) and competitor sex
(‘same sex competitor’ vs. ‘opposite sex competitor’), were included as two
within-subjects factors. The sex of the subject turtle was included as a betweensubjects factor.
In the second experiment, we used a three-way repeated measures ANOVA
to test for differences in basking patterns of M. leprosa and T. scripta under
control and experimental treatments (‘intraspecific competition’ vs.
‘interspecific competition’) in each instantaneous scan. Percent time of basking
activity was calculated for each turtle in each time of day as the proportion of
days that turtles were observed basking in each one of the respective scans.
Time of day was included as a within-subjects factor. The species of the subject
turtle and the treatment were included as two between-subjects factors. To
analyze differences in continuity of basking activity between the two turtle
species (measured as the average length of basking events and maximum length
CAPÍTULO 3: Competencia durante el asoleamiento
Data analyses
71
of basking events halfway through the 10 days), we used two-ways repeated
measures ANOVAs with the species of the subject turtle and the treatment
(‘intraspecific competition’ vs. ‘interspecific competition’) as two betweensubjects factors.
To test for differences between basking activity of M. leprosa in both ‘alone’
and ‘stacked’ situations, we analyzed data from the first experiment with a fourway repeated measures ANOVA with the sex of the subject turtle and the sex
and species of the competitor as described above, but we also included the
basking situation (‘alone’ vs. ‘stacked’) as an additional within-subjects factor.
In all cases, data normality was verified by Shapiro-Wilk’s test and tests of
homogeneity of variances (Levene’s test) showed that variances were not
significantly heterogeneous. Pairwise comparisons were made using Tukey’s
honestly significant difference tests (Sokal and Rohlf 1995).
RESULTS
Basking activity of M. leprosa in situations of occasional competition
The species of the competitor significantly influenced the percent time that
individual M. leprosa spent basking in transitory situations of competition
(three-way repeated measures ANOVA, competitor species: F = 8.21, df = 1,25,
P = 0.008). Individual M. leprosa clearly reduced their basking activity when
the competitor was a T. scripta (average basking activity with conspecific
competitors: mean ± SE = 66 ± 8 %; with heterospecific competitors: 55 ± 8 %)
(Fig. 3.1a). No significant differences between male and female M. leprosa were
observed in overall percent time that turtles spent basking (subject sex: F = 0.34,
df = 1,25, P = 0.57), and the sex of the competitor did not significantly influence
basking activity of individual M. leprosa (competitor sex: F = 0.55, df = 1,25, P =
0.47). Male M. leprosa showed a tendency to reduce their basking activity
when the competitor was a female, while female M. leprosa tended to increase
the time spent basking when the competitor was a male, but differences did not
reach statistical significance (subject sex x competitor sex: F = 3.08, df = 1,25, P =
0.09) (Fig. 3.2). All other interactions were non-significant (subject sex x
competitor species: F = 0.60, df = 1,25, P = 0.45; competitor sex x competitor
species: F = 0.22, df = 1,25, P = 0.64; subject sex x competitor sex x competitor
species: F = 0.21, df = 1,25, P = 0.65). Thus, basking activities of male and female
M. leprosa were similarly restricted under occasional competition by
heterospecific T. scripta competitors independently of the sex of the competitor
(Fig. 3.2).
72
Occasional competition
a)
100
90
Basking activity (%)
80
70
60
50
Figure 3.1 Percent time (mean ± SE) spent
basking by (a) M. leprosa in occasional
situations of intra (open rectangle) and
interspecific (dotted rectangle) competition,
and (b) T. scripta and M. leprosa under longterm competition situations, when they
shared the home aquaria and the basking
site with a conspecific (open rectangle) and a
heterospecific (dotted rectangle) competitor
40
30
20
10
0
M. leprosa
Long-term competition
b)
100
90
Basking activity (%)
80
70
60
50
40
30
20
10
Significant differences were observed in overall percent time spent in basking
activity by T. scripta and M. leprosa under prolonged situations of competition
(three-way repeated measures ANOVA, species: F = 5.64, df = 1,20, P = 0.028).
Thus, sliders spent more time basking (mean ± SE = 69 ± 7 %) than Spanish
terrapins (46 ± 7 %) during the whole experiment. The effect of the treatment
was non-significant (treatment: F = 0.65, df = 1,20, P = 0.43), but the interaction
between species and treatment was significant (F = 4.65, df = 1,20, P = 0.043)
(Fig. 3.1b). T. scripta spent more time basking than M. leprosa under interspecific
competition (Tukey’s test, P = 0.031), but there were no significant differences
CAPÍTULO 3: Competencia durante el asoleamiento
0
73
T. scripta
Conspecific
M. leprosa
Heterospecific
Basking patterns of T. scripta and M. leprosa under long-term competition
100
90
Basking activity (%)
80
70
60
50
40
30
20
10
0
Same sex
Opposite sex
Same sex
Males
Opposite sex
Females
Conspecific
Heterospecific
Figure 3.2 Percent time (mean ± SE) spent basking by male and female M. leprosa when they
shared the basking site with a conspecific (open rectangle) or a heterospecific (dotted rectangle)
of the same and the opposite sex
between the two species under intraspecific competition (P = 0.99). Differences
in basking activity between treatments were non-significant for T. scripta (P =
0.23) and neither were significant for M. leprosa (P = 0.74).
Significant differences were observed in overall basking activity of turtles
through the day (time of day: F = 10.47, df = 15,300, P < 0.001), which is
explained by the increased basking activity as a result of a lower water
temperature than air temperature (Spearman’s rank-order correlation between
basking activity and time of day; rs = 0.90, n = 8, P = 0.0024). Basking activity
decreased when water temperature became greater than air temperature (rs = 0.95, n = 8, P = 0.0003) (Fig. 3.3). All the interactions between time of day and
species or treatments were no significant (time of day x species: F = 0.60, df =
15,300, P = 0.87, time of day x treatment: F = 0.42, df = 15,300, P = 0.97; time of
day x species x treatment: F = 1.04, df = 15,300, P = 0.42) (Fig. 3.4).
There were significant differences in the average length of basking events
between species (two-way repeated measures ANOVA, species: F = 6.55, df =
1,20, P = 0.019), with sliders basking for longer periods on average (mean ± SE =
98 ± 12 min) than Spanish terrapins (58 ± 11 min). Differences between
treatments were non-significant (treatment: F = 0.42, df = 1,20, P = 0.52), but
the interaction between species and treatment was significant (F = 5.02, df =
1,20, P = 0.037). Under interspecific competition, average basking events of T.
74
scripta (121 ± 19 min) were significantly longer than those of M. leprosa (45 ±
14 min) (Tukey’s test, P = 0.021), but average duration of basking events did not
significantly differ between species under intraspecific competition (T. scripta:
76 ± 14 min; M. leprosa: 71 ± 15 min) (P = 0.99). There were no significant
differences between intraspecific and interspecific competition in average
length of basking periods in either species (T. scripta: P = 0.25; M. leprosa: P =
0.63).
a)
26
Figure 3.3 (a) Daily temporal variation
(mean ± SE) of air and water temperatures
during the trials, and (b) associated
variation in overall basking activity of
turtles. Linear fit breaks at the point in
which air and water temperatures coincide
Temperature (ºC)
24
22
20
18
16
14
12
11:00
11:30
12:00
12:30
13:00
13:30
Time of day
100
4
90
3
Basking activity (%)
80
2
70
1
60
50
0
40
-1
30
-2
20
-3
10
0
-4
11:00
11:30
12:00
12:30
13:00
Time of day
Average basking activity
Air - Water Temperature
13:30
Air - Water Temperature (ºC)
b)
Water
CAPÍTULO 3: Competencia durante el asoleamiento
Air
75
T. scripta
M. leprosa
100
Basking activity (%)
90
80
70
60
50
40
30
20
10
0
11:00
11:30
12:00
12:30
13:00
13:30
11:00
11:30
Time of day
12:00
12:30
13:00
13:30
Time of day
Conspecific
Heterospecific
Figure 3.4 Daily basking patterns of T. scripta and M. leprosa (mean ± SE of percent time spent
basking for each time of day), under long-term situations of intra and interspecific competition
Differences in overall longest basking event between species were
significant (two-way repeated measures ANOVA, species: F = 6.50, df = 1,20, P =
0.019). Maximum length of T. scripta basking events (mean ± SE = 104 ± 12
min) was greater than maximum length of M. leprosa basking events (64 ± 10
min). The effect of the treatment was non-significant (treatment: F = 0.62, df =
1,20, P = 0.44), but the interaction between species and treatment was
significant (F = 5.27, df = 1,20, P = 0.033). Significant differences between
maximum length of T. scripta and M. leprosa basking events under interspecific
competition was observed (129 ± 19 min vs. 53 ± 14 min respectively, Tukey’s
test, P = 0.02), but not under intraspecific competition (80 ± 14 min vs. 76 ± 15
min, P = 0.99). Differences between intraspecific and interspecific competition
were not significant for either species (P ≥ 0.20 in both cases).
Alone and stacked basking activity of M. leprosa
Overall percent time that M. leprosa spent basking alone (mean ± SE = 18 ± 4 %)
was significantly lower than overall percent time that it spent basking stacked
(41 ± 8 %) (four-way repeated measures ANOVA, basking situation: F = 27.70,
df = 1,25, P < 0.001). The sex of the subject turtle did not influence the basking
situation (basking situation x subject sex: F = 0.28, df = 1,25, P = 0.60), and
neither did the sex of the competitor (basking situation x competitor sex: F =
76
0.11, df = 1,25, P = 0.75), but the species of the competitor had a significant
effect on basking situation (basking situation x competitor species: F = 5.81, df =
1,25, P = 0.024) (Fig. 3.5). When the competitor was a conspecific, percent time
spent by individuals M. leprosa basking alone was significantly lower than
percent time spent basking stacked (Tukey’s test, P = 0.004), but there were no
significant differences in basking activity between alone and stacked situations
when the competitor was a heterospecific (P = 0.50). Differences in alone or
stacked basking activity between basking with conspecific and heterospecific
competitors were non-significant (basking alone: P = 0.92; basking stacked: P =
0.31). The interaction between sex of the subject turtle, sex of the competitor
and basking situation was non-significant (F = 3.35, df = 1,25, P = 0.08), but
males showed a tendency to spend more time basking alone with a competitor
of the same sex while females tended to spend more time basking alone with a
competitor of the opposite sex. The rest of the interactions were non-significant
(F ≤ 1.72, df = 1,25, P ≥ 0.20 in all cases).
Figure 3.5 Percent time (mean ± SE) spent
basking alone and stacked by M. leprosa
when they competed for the basking site
with a conspecific (open rectangle) or a
heterospecific (dotted rectangle)
100
90
70
60
50
40
30
20
10
0
alone
Conspecific
stacked
Heterospecific
DISCUSSION
The results of our experiments suggest that the presence of invasive sliders
alters the basking behavior of native Spanish terrapins. Basking activity of
native terrapins subjected to occasional competition situations was significantly
lower when the competitor was a slider than when it was a conspecific (first
experiment; see Fig. 3.1). Results from the second experiment showed that
CAPÍTULO 3: Competencia durante el asoleamiento
Basking activity (%)
80
77
basking activity of M. leprosa was similar to basking activity of T. scripta when
turtles shared their home aquaria with conspecific competitors, but when
turtles underwent a situation of long term interspecific competition, significant
differences in continuity and total time devoted to basking appeared between
the two species. In such situation, average and maximum length of the basking
events and percent time spent basking by T. scripta were greater than those of
M. leprosa. Although differences in continuity and total activity of basking
between intra and interspecific competition did not reach statistical significance
for either species, T. scripta showed a more efficient occupation of basking
resources than M. leprosa under inter but not under intraspecific competition,
suggesting the dominance of the introduced species over the native one.
Similarly, Cadi and Joly (2003) found that T. scripta outcompeted the European
pond turtle, Emys orbicularis, for preferred basking places of experimental
ponds (i.e., floating platforms in middle position, surrounded by deep water) in
mixed-species groups.
Differences in the magnitude of the effects between the two experiments
might be due to the different kinds of competition turtles encountered. While
in the second experiment turtles were subjected to prolonged maintained
conditions of intra and interspecific competition, in the first experiment, the
effect of competition for basking places with a more competitive species might
be amplified by the transitory and the new nature of the competition. We
hypothesize that M. leprosa had less incentive to compete with sliders for
basking sites in the first experiment, given that their basking requirements were
regularly satisfied before the trials (because they were housed individually). On
the other hand, in the second experiment, M. leprosa suffering from the
cumulative effects of deficient basking during several consecutive days might be
able to assess the costs of a long-lasting competition with sliders and
consequently increase their investment in basking competitive interactions,
thus reducing the differences in basking behavior between situations of intra
and interspecific competition. Further experiments addressing this hypothesis
would be interesting. Nevertheless, negative effects of long-term competition
with exotic turtles are expected to persist in the wild, since basking sites are
limited, and optimal time for basking is restricted on an annual basis, especially
in Mediterranean countries. Thus, native M. leprosa could hardly optimize
basking by intercalating their basking bouts within the activity of a more
competitive species.
Although time devoted to basking activity of native turtles was similarly
restricted by invasive competitors through the whole time of the trials,
interferences in temporal patterns of basking of the two species did not occur.
Thus, patterns of basking throughout the day performed by invasive and native
turtles under interspecific competition were similar to those performed by each
78
CAPÍTULO 3: Competencia durante el asoleamiento
species under intraspecific competition; both sliders and Spanish terrapins
regularly basked atmospherically while air temperature was higher than water
temperature and both species reduced their basking activity and spent more
time immersed in the water once water temperature became greater than air
temperature. This fact supports the hypothesis that thermoregulation is the
primary function of basking behavior in freshwater turtles (Boyer 1965; Moll
and Legler 1971; Standora 1982; Crawford et al. 1983; Meek and Avery 1988).
Therefore, competition for basking sites and decreased basking periods of native
terrapins may have important consequences for thermoregulation, with
subsequent physiological costs (e.g., Huey 1982; Hammond et al. 1988; BenEzra et al. 2008).
Sex did not appear to affect basking activity of native turtles. Male and
female M. leprosa clearly reduced their efficiency in occupying basking sites
when competing with sliders, independently of the sex of the competitor, thus
indicating that male and female exotic turtles may pose similar dominance over
native terrapins. However, male and female M. leprosa tended to spend less
time basking when the competitor (conspecific or heterospecific) was a female,
likely due to the minimum differences remaining in body size between
competitors. Females, which are usually larger than males, might be more
successful when competing for basking sites. Higher basking requirements of
females related to egg production might be an alternative explanation for this
tendency (Lefevre and Brooks 1995; Krawchuk and Brooks 1998; Carrière et al.
2008).
Regarding alone and stacked basking, male and female M. leprosa contrarily
tended to spend more time basking stacked with a female competitor
(conspecific or heterospecific), which suggests avoidance of physical contact
with males by females and between males during basking events. However,
there was no statistical significance. Also, native turtles spent more time
basking stacked with conspecific competitors than basking alone, but percent
times that native turtles spent basking alone and stacked with heterospecific
competitors were similar. Considering that the availability of empty basking
sites was half the availability of shared ones, M. leprosa terrapins seemed
reluctant to share basking sites with heterospecifics, while they did not avoid
sharing them with conspecifics. In this regard, Cady and Joly (2003) reported
that E. orbicularis shied away from climbing onto a basking site that was
already occupied by a T. scripta. They suggested remote identification and
active avoidance of interactions with heterospecific competitors by the native
species. Also, avoidance by M. leprosa of water with chemical cues of T. scripta
has been experimentally demonstrated (Polo-Cavia 2009a), which suggests that
Spanish terrapins actively avoid areas occupied by introduced sliders.
79
If direct competitive interactions with a more aggressive competitor are
disadvantageous for native terrapins, they would likely avoid basking sites
occupied by sliders, thus reducing considerably the availability of basking
resources for the native species and favoring the exploitation of basking sites by
the invasive one. A restricted occupation of basking sites might lead to a
detriment in efficiency of thermoregulatory behavior of M. leprosa.
Deficiencies in thermoregulation negatively affect physiological functions such
as food ingestion and digestion (Parmenter 1981; Zimmerman and Tracy 1989;
Gianopulos and Rowe 1999), dermal synthesis of vitamin D (Pritchard and
Greenhood 1968; Avery 1982), conditioning of the skin and the shell (Cagle
1950; Boyer 1965; Vogt 1979), and may also retard maturation of ova (Ganzhorn
and Licht 1983; Mendonca 1987; Sarkar et al. 1996; Rollinson and Brooks 2007).
Similarly, such negative consequences of inefficient basking may explain the
lower survival rates of E. orbicularis when competing with sliders (Cadi and
Joly 2004). In our experiment, native terrapins subjected to interspecific
competition ultimately spent insufficient time basking and they basked for
shorter periods than T. scripta, which suggests not only avoidance behavior by
M. leprosa but also superimposition and active displacement by sliders.
However, it is probable that wild Spanish terrapins simply avoid disturbance by
shifting their basking activity to less preferred basking sites (Cady and Joly
2003) or to the shores of the ponds, in contrast to the safer basking places
emerging in open deep water in the center of the ponds, thus incurring
additional costs such as higher predation risk (López et al. 2005; Polo-Cavia et
al. 2008). This avoidance behavior and consequent detriment in basking activity
of M. leprosa might play an important role in explaining the observed
displacement of their populations by the invasive T. scripta.
Our study further clarifies the nature of the basking interactions between
the introduced sliders and the Iberian turtle species. The results of our
experiments coincide and reinforce those recorded by Cadi and Joly (2003),
who observed that native E. orbicularis sharing experimental ponds with sliders
occupied basking places of lower quality, while sliders monopolized the
preferred basking sites, in absence of agonistic behavior. Factors like differences
in body size or a higher aggressiveness, probably due to a “more competitive”
original habitat, might explain why T. scripta appear more competitive than the
two Iberian turtle species during basking activity. Body size has been shown to
play a role in determining the outcome of competitive interactions (Bury and
Wolfheim 1973; Auth 1975; Lindeman 1999). Although wild red-eared sliders
reach larger body sizes in adulthood than Iberian freshwater turtles (Da Silva
and Blasco 1995; Arvy and Servan 1998), turtles from our experiments were
paired basing on body size criteria, thus minimizing these differences between
the two members of the pair. Consequently, we suggest that other factors such
80
Acknowledgements We thank two anonymous reviewers for helpful comments, the “Grupo de
Rehabilitación de la Fauna Autóctona y su Hábitat” (GREFA) for providing sliders, and “El
Ventorrillo” MNCN Field Station for use of their facilities. Financial support was provided by the
MEC project CGL2005-00391/BOS and the MCI project MCI-CGL2008-02119/BOS, and by an “El
Ventorrillo” CSIC grant and a MEC-FPU grant to N. P.-C.
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Capítulo
4
Las diferencias interespecíficas en las tasas de intercambio de calor pueden afectar a la competencia entre galápagos introducidos y nativos Nuria Polo Cavia, Pilar López y José Martín
Biological Invasions 11 (2009) 1755–1765
RESUMEN
86
En la Península Ibérica, el galápago de Florida (Trachemys
scripta elegans) es una especie introducida que se comporta
como invasora, desplazando a las poblaciones nativas de
galápago leproso (Mauremys leprosa), una especie protegida.
Sin embargo, la naturaleza de las interacciones competitivas
entre las dos especies no se conoce con seguridad. En zonas
templadas, los mecanismos que maximicen la retención de
calor corporal podrían resultar selectivamente ventajosos para
las especies de galápagos, puesto que los individuos tienden a
perder rápidamente el calor adquirido mediante asoleamiento
al entrar en el agua. Así, es posible que ciertas diferencias en
la morfología, y por tanto en las tasas de calentamiento y
enfriamiento, puedan conferir ventajas competitivas al
introducido T. scripta. En este trabajo, comparamos la
relación superficie-volumen de ambas especies de galápagos a
partir de medidas biométricas, y sus efectos en las tasas de
intercambio de calor. T. scripta presenta una forma más
redondeada, una menor relación superficie-volumen y una
mayor inercia térmica, lo que facilita la retención de calor y
favorece el desarrollo de actividades y funciones fisiológicas
tales como la búsqueda de alimento o la digestión. Estas
características del galápago invasor podrían permitirle
competir ventajosamente con los galápagos nativos en los
hábitats mediterráneos ■
INTERSPECIFIC DIFFERENCES IN HEAT EXCHANGE RATES
MAY AFFECT COMPETITION BETWEEN INTRODUCED AND NATIVE
FRESHWATER TURTLES
Abstract
In the Iberian Peninsula, the red-eared slider (Trachemys scripta elegans) is an
introduced invasive species that is displacing the endangered native Spanish terrapin (Mauremys
leprosa). However, the nature of competitive interactions is relatively unclear. In temperate
zones, mechanisms for maximizing heat retention could be selectively advantageous for aquatic
turtle species, since individuals usually lose the heat gained from basking very rapidly when
entering the water. We hypothesized that interspecific differences in morphology, and thus, in
heating and cooling rates, might confer competitive advantages to introduced T. scripta. We
compared the surface-to-volume ratios of both, introduced and native turtles, basing on biometric
measures, and their effects on thermal exchange rates. T. scripta showed a more rounded shape, a
lower surface-to-volume ratio and a greater thermal inertia, what facilitates body heat retention
and favors the performance of activities and physiological functions such as foraging or digestion,
thus aggravating the competition process with native turtles in Mediterranean habitats.
Keywords Freshwater turtles • Heat exchange rates • Invasive species • Mauremys leprosa •
Thermoregulation • Trachemys scripta
CAPÍTULO 4: Diferencias en las tasas de intercambio de calor
T
hermoregulation in aquatic turtles, as in most ectotherms, is primarily
achieved through behavioral changes (Hutchison and Maness 1979;
Sturbaum 1982; Meek and Avery 1988). Freshwater turtles simply
achieve preferred body temperatures switching between basking outside of
water and water immersion, avoiding extreme thermal environments. Although
basking behavior of aquatic turtles has long been known, there has been
considerable speculation around this behavior, and their specific functions
remain unclear. The consensus is that the primary function of basking is
thermoregulatory (Boyer 1965; Moll and Legler 1971; Standora 1982; Crawford
et al. 1983; Meek and Avery 1988) though more recent studies have pointed out
contradictory results (Manning and Grigg 1997). Increased body temperature
speeds digestion (Parmenter 1981; Gianopulos and Rowe 1999), and may also
speed maturation of ova (Obbard and Brooks 1979; Whittow and Balazs 1982).
Cagle (1950) suggested that basking serves a variety of needs in turtles apart
from thermoregulation, as conditioning of the skin and shell, avoiding
infections by drying and the antibiotic effects of the ultraviolet component of
sunlight. Basking also contributes to dermal synthesis of vitamin D (Pritchard
and Greenhood 1968; Avery 1982). An interesting point is that freshwater
turtles usually lose the heat gained from basking very rapidly when they reentry to water (Avery 1982; Bartholomew 1982). Turtles that have achieved
high body temperatures basking in air may be exposed abruptly to chilling
conditions when they dip into water, particularly during spring and fall in
87
middle latitudes. Consequently, mechanism for maximizing heat retention, or
even heat production could be selectively advantageous for aquatic species.
Basically, turtles’ abilities to retain and produce heat rest on morphological
and physiological specific determining factors (Ernst 1972; Hutchison 1979).
The hemispherical shape of turtles gives them relatively small surface-tovolume ratios when compared with other reptiles of the same size, thus
minimizing their rates of heat exchange with the environment, and increasing
the inertial homeothermy as bigger they are (Bartholomew 1982). Boyer (1965)
demonstrated the influence of shell shape on heating rates of freshwater turtles
belonging to different genera. Body size and surface-to-volume ratio are clearly
correlated with thermal rates in aquatic turtles (Spray and May 1972; Gronke et
al. 2006). Also, the presence of a bony shell may influence thermal gradients
following insolation. On the other hand, when behavioral strategies are not
sufficient to maintain optimal body temperatures within required limits, some
turtles can use physiological mechanisms of control of body temperatures for
short periods of time. For example, physiological thermoregulatory systems
could be based on heat transference mediated by thermal conductivity
(Weathers 1970; Weathers and White 1971; Cloudsley-Thompson 1974),
respiratory responses to hyperthermia (Sturbaum 1982) or vasomotor responses
with adjustments of blood flow within the body (Bartholomew 1982; Turner
1982). Although small differences in morphology and physiological control of
rate of change in body temperature are almost trivial when compared with the
control by postural adjustments and choice of microhabitat, we should not
discard their implications in thermoregulatory behavior of freshwater turtles.
The Spanish terrapin (Mauremys leprosa) is a semiaquatic medium-sized
turtle widespread in the South and Central Iberian Peninsula and northwestern
Africa (Keller and Busack 2001). These turtles are predominantly aquatic, but
they need to come to land for basking to achieve and maintain body
temperature within the intervals necessary for their daily activities (Meek
1983). This is an endangered species which populations have considerably
declined during the last decades (Pleguezuelos et al. 2002). Habitat destruction
and human pressure are the major responsible for this decline, but competition
with exotic introduced turtles, mainly the American red-eared slider
(Trachemys scripta elegans), might be worsening the state of the remainder
populations (Da Silva and Blasco 1995; Pleguezuelos 2002). However, it is not
clear how interspecific competitive interactions with sliders are taking place. It
is possible that direct competition for food, refuges or basking places is present
(Crucitti et al. 1990). Competition for basking places has been described
between sliders and the European pond turtle (Emys orbicularis) (Cadi and Joly
2003), and it also occurs between sliders and the Spanish terrapin (Polo-Cavia et
al. in press). Sliders can monopolize the most suitable basking places, impeding
88
METHODS
Study animals
During spring 2007, we captured with funnel traps Spanish terrapins (M.
leprosa) in several ponds and tributary streams of the Guadiana river, located
inside dehesa woodlands with scattered holm oak (Quercus ilex) at Olivenza
(Badajoz Province, southwestern Spain). We selected 5 females of similar body
size for carrying out experiments (carapace straight length: mean ± SD = 15.9 ±
0.4 cm, range = 15.2-16.2 cm). We also obtained 5 female red-eared sliders (T.
scripta) of equivalent body size (carapace straight length: mean ± SD = 15.8 ± 0.2
cm, range = 15.6-16.1 cm) from a large seminatural outdoor pond located in
Madrid Province (Central Spain) where they had been maintained by the
conservationist organization ‘‘Grupo de Rehabilitación de la Fauna Autóctona y
CAPÍTULO 4: Diferencias en las tasas de intercambio de calor
native turtles to adequately bask (Cadi and Joly 2003). However, the effects of
morphological and physiological differences, per se, between species on
thermoregulatory abilities of native and invasive species of aquatic turtles have
never been analyzed. This can be, however, important for the outcome of
competitive interactions between freshwater turtles. While each turtle species
has probably evolved to optimize their thermal exchange rates in their natural
habitat and original conditions, the new situation caused by man (i.e., the
introduced species occupies new environmental conditions and the native
species faces competition with it) might result in that the original
thermoregulatory adaptations conferred advantages or disadvantages to each
species in the new ecological situation. Thus, we hypothesized that interspecific
intrinsic differences in thermal exchange rates may affect the efficiency of
thermoregulation in the new situation, which might finally affect to the result
of indirect competitive interactions between the introduced and the native
freshwater turtles.
In this study, we compared in the laboratory the rates of heat exchange
(heating and cooling rates) of the American red-eared slider (T. scripta) and the
Spanish terrapin (M. leprosa), following exposure of turtles to step changes of
ambient temperature in air and water. The step changes simulated thermal
alterations that turtles experience under natural conditions during basking
outside of water and when turtles posteriorly entered into water for foraging or
other activities. Morphological differences in body and carapace size and shape
between these two species of turtles might result in differences in heat
exchange rates. Thus, we also compared the surface-to-volume ratios of the two
species, basing on biometric measures, and their effects on thermal exchange
rates.
89
su Hábitat’’ (GREFA). These turtles had been extracted from introduced
populations in Spain, with the purpose of preserving the original ecosystem
balance.
The turtles were transported to ‘‘El Ventorrillo’’ Field Station (Navacerrada,
Madrid Province), and individually housed in outdoor aquaria (60 x 40 x 30 cm)
with water and stones that allowed them to bask. The temperature and daylength cycle of light were the same as the natural surroundings. Turtles were
fed mince beef, earthworms and slugs three times a week. Turtles were
habituated to captivity conditions at least two weeks before experiments took
place. At the end of the tests, all turtles had maintained their body mass, and
were returned to the GREFA ponds (sliders) or to their exact field capture sites
(Spanish terrapins).
Surface-to-volume ratio
To estimate the surface-to-volume ratio of both species of turtles, we used
biometric measures of a large set of individuals from the same areas (carapace
straight length, M. leprosa: mean ± SE = 14.9 ± 0.2 cm, n = 60; T. scripta: mean ±
SE = 15.0 ± 0.3 cm, n = 46). We considered that the hemispherical shape of the
carapace of these freshwater turtles resembles a scalene semiellipsoid of
revolution where the three semiaxes (a, b, c) are distinct. We approached the
shape of turtles to a semiellipsoid whose axes 2a, 2b, 2c were given by CL
(carapace straight length), CW (carapace straight width, measured at the 6-7
marginal scutes joint) and 2CH (maximum carapace height), respectively.
Unlike the area of a sphere, the surface area of a general ellipsoid cannot be
expressed exactly by an elementary function. The surface area of a scalene
ellipsoid is given by:
⎫
⎧
bc 2
(
)
ο
ε
SA = 2π ⎨c 2 + b a 2 − c 2 E (οε , m ) +
,
F
m
⎬
a2 − c2
⎭
⎩
where
οε = arccos ( a / c ) ;
m=
b2 − c2
2
b 2 sin (οε ) ;
a>b>c>0
m is the modular angle, or angular eccentricity and E (οε , m ) , F (οε , m ) are the
Legendre elliptic integrals of the first and second kind (Legendre 1811).
An expression that approximates the true surface area of an arbitrary
ellipsoid is given by Klamkin (1971):
90
SA ≈ 4π
{( a b
2 2
) }
+ a 2c 2 + b 2c 2 / 3
1/ 2
To asses the surface area of turtles, we adapted Klamkin’s equation for a
semiellipsoid:
SA ≈ 2π
{( a b
2
) }
+ a 2c 2 + b 2c 2 / 3
2
1/ 2
+ π ab
We validated this adapted equation, both in M. leprosa and T. scripta, by
covering turtle carapaces with rectangles (1 cm width) and computing their
summatory area (observed vs. predicted R 2 = 0.946).
To assess volume of the turtles’ body, we first calculated values of volume
displacement by submerging turtles in water. Then we used these values to
obtain an interpolated equation which approaches the volume of the turtles
from their shell dimensions (CL, CW, and CH) (non-linear estimation, observed
vs. predicted R 2 = 0.999; coefficient values: i = 0.381299, j = 53.3286, k = 2.360010, l = -0.169371):
V ≈ iπ (CL / 2 + j )(CW / 2 + k )(CH / 2 + l )
13
⎛ qr ⎞
SI = ⎜⎜ 2 ⎟⎟
⎝p ⎠
FI =
p+q
2r
where p, q and r were given by CL, CW and CH respectively. Higher values of
sphericity index and lower values of flatness index mean a lower surface-tovolume ratio. Higher values of sphericity index and lower values of flatness
index mean a lower surface-to-volume ratio.
Heating and cooling rates
Experiments took place under indoor laboratory conditions. Ambient air
temperature in the room was kept at 20 ± 1 °C. To monitor the body
temperature (Tb) of turtles during the whole tests, we used HOBO U-12 data
loggers with HOBOware Pro Software for Windows (Onset Computer
Corporation). A cloacal probe (38 ga copper-constantan thermocouple;
temperature range: -200 to 100 °C; precision: ± 1.5 °C; resolution: 0.1 °C) was
CAPÍTULO 4: Diferencias en las tasas de intercambio de calor
We also estimated sphericity and flatness indexes for both species of turtles,
using Krumbein’s Sphericity Index (SI) (Krumbein 1941) and Cailleux’s Flatness
Index (FI) (Cailleux 1947):
91
inserted into each turtle’s cloaca to approximately a third of the total length of
the plastron (Mrosovsky 1980). To prepare the thermally sensitive probe, we
entwined the leads at one end of the thermocouple, fused the entwined leads
together at the tips, and encapsulated the end in epoxy resin. We used duct tape
to secure the exiting thermocouple wire to the turtle’s carapace (Do Amaral et
al. 2002). Previous studies have shown that cloacal temperatures of turtles were
highly correlated with air and water temperatures immediately surrounding
turtles (Obbard and Brooks 1981; Ernst 1982; Wilson 1994). Therefore, we
assumed that cloacal temperature was a reasonably accurate estimate of turtles
Tb.
To achieve initial body temperatures of turtles, we used a thermostatic
chamber that was maintained at 15 ± 1 °C. For the heating experiments, each
turtle was initially cooled to a Tb of 15 °C inside the cooling chamber, and then
rapidly placed in an aquarium equal to the ones used to house them. The
aquarium was filled with 10 L water at 15 °C, and a brick (24 x 11.5 x 7 cm) was
placed in the center, emerging 3 cm above the water surface. The turtle was
fixed lying on the plastron over the brick’s surface using duct tape. An infrared
heat reflector (250 W, 250 V) was situated hanging 52 cm over the brick in the
center of the aquarium. In this way, we simulated a basking place located in a
body of water reflecting natural temperature conditions. We kept the turtle in
this heating experiment until its Tb stabilized. For cooling experiments in air,
we quickly removed the turtle from the aquarium and place it into the cooling
chamber until its Tb decreased at 15 °C again. For cooling experiments in water,
we followed the same procedure for heating until the turtle Tb stabilized, but
then we removed the brick and placed the turtle inside the water of the
aquarium (15 ± 1 °C) and monitored Tb until it stabilized at water temperature.
Analytical model of thermal exchange rates
When an ectotherms animal basks, its Tb gradually increases, as time spent
basking increases. Therefore, to fit the increment in Tb described by turtles
during the heating experiments (i.e., heating rates), we used a Bertalanffy
equation (Von Bertalanffy 1960; Kaufman 1981):
⎡
1 ⎤
Tb = u + v ⎢1 −
⎥
⎣ cosh( st ) ⎦
where u was the initial Tb (°C) and v the total increment over the initial Tb at
the equilibrium time (°C). s is the slope of the function, defined as the heating
rate, and t is the time (min).
92
For the cooling experiments, we used a similar Bertalanffy equation
describing gradually decreasing Tb:
⎡ 1 ⎤
Tb = w − v ⎢
⎥
⎣ cosh( st ) ⎦
where w and v were respectively the Tb at the equilibrium time and the total
negative increment over the initial Tb (°C). s is the cooling rate and t is the time
(min).
Statistical analyses
To analyze differences in morphological parameters between both species of
turtles, we used general lineal models (GLM) with surface-to-volume ratio, or
sphericity or flatness index as dependent variable, species and sex as categorical
predictors and body size as continuous predictor. For turtles tested in the
thermal exchange experiment, we used Mann-Whitney’s U-tests to analyze
differences between species in body size, weight, surface-to-volume ratio,
sphericity and flatness indexes, and heating and cooling rates (Sokal and Rohlf
1995). Pairwise comparisons were made using Tukey’s honestly significant
difference tests.
Surface-to-volume ratio
Surface-to-volume ratio was significantly and negatively correlated with body
size of turtles (r = -0.67, F = 152.36, df = 1,101, P < 0.001). We found significant
differences between the two species of turtles in surface-to-volume ratio after
controlling by body size differences (GLM, F = 99.10, df = 1,101, P < 0.001),
with higher values of surface-to-volume ratio for M. leprosa than for T. scripta.
Males of both species of turtles showed significantly higher values of surface-tovolume ratio than females (F = 13.81, df = 1,101, P < 0.001), and this difference
was greater for M. leprosa than for T. scripta (interaction: F = 4.87, df = 1,101, P
= 0.03).
There were no significant correlations between body size and sphericity
index (r = -0.14, F = 2.05, df = 1,104, P = 0.16) or flatness index (r = -0.05, F =
0.26, df = 1,104, P = 0.61), so we did not include body size in further analyses.
The two turtle species differed significantly in both sphericity (GLM, F = 9.89,
df = 1,102, P < 0.001) and flatness indexes (F = 9.84, df = 1,102, P = 0.002) with
CAPÍTULO 4: Diferencias en las tasas de intercambio de calor
RESULTS
93
higher values of flatness and lower values of sphericity for M. leprosa than for
T. scripta. Males showed also higher flatness and lower sphericity indexes than
females (F = 14.02, df = 1,102, P < 0.001 and F = 20.08, df = 1,102, P < 0.001,
respectively). The interaction between sex and species was non-significant for
flatness index (F = 0.43, df = 1,102, P = 0.52) but it was significant for sphericity
index (F = 8.80, df = 1,102, P = 0.004). Thus, there were significant differences
in sphericity between male and female M. leprosa (higher values for females,
Tukey’s test, P < 0.001), but not between male and female T. scripta (P = 0.72).
Heating and cooling rates
Mann-Whitney’s U-tests analyzing turtles tested in the thermal exchange
experiment showed significant differences between species in body weight,
surface-to-volume ratio, and sphericity and flatness indexes, being T. scripta
heavier and more spherical and with lower values of surface-to-volume ratio
and flatness than M. leprosa (Table 4.1). Size differences were non-significant,
as we intended in the selection of the experimental individual turtles based on
similar body sizes. Also, there were significant differences between M. leprosa
and T. scripta in heating and cooling rates (Table 4.1; Fig. 4.1). T. scripta
showed a lower heating rate and also lower cooling rates, both in air and water,
than M. leprosa. Values of heating and cooling rates for each individual turtle
are provided in Table 4.2. All thermal exchange rates were positively correlated
with the surface-to-volume ratio (Spearman’s rank-order correlations, heating
rate: rs = 0.79, n = 10, P = 0.006; cooling rate in air: rs = 0.82, n = 10, P = 0.004;
cooling rate in water: rs = 0.66, n = 10, P = 0.038).
DISCUSSION
Our results revealed differences between native M. leprosa and introduced T.
scripta turtles in heating and cooling rates. T. scripta showed lower heating
rates but also lower cooling rates, both in air and water, thus taking more time
than M. leprosa in heating and cooling processes. Although we cannot discard
that unknown physiological mechanisms are also playing a role in interspecific
differences in thermal exchange rates, our results show that these differences
are closely related to differences between turtle species in characteristic shape
and morphology. Shape has been established as a critical factor in the ability of
organisms to thermoregulate (Bogert 1949; Gould 1966). We found that M.
leprosa turtles were flatter than T. scripta, which showed a more spherical shell
shape. Thus, M. leprosa have smaller body sizes and higher surface-to-volume
ratios for the same body lengths than T. scripta. Since rates of thermal exchange
depend upon absolute body size (Grigg et al. 1979; Seebacher et al. 1999), and
b)
94
Table 4.1 Results from Mann-Whitney U test examining the effect of the turtle specie on size,
weight, surface-to-volume ratio, sphericity and flatness indexes, and heating and cooling rates in
tested turtles (mean ± SD; n1= n2 = 5 in all cases)
Size (cm)
Weight (g)
Surface-to-volume ratio (cm-1)
Sphericity Index
Flatness Index
Heating rate (°C/min)
Cooling rate (Air) (°C/min)
Cooling rate (Water) (°C/min)
a)
M. leprosa
T. scripta
Z
P
15.9 ± 0.4
527.49 ± 46.47
0.6 ± 0.04
0.64 ± 0.02
2.35 ± 0.1
0.039 ± 0.003
0.058 ± 0.014
0.194 ± 0.032
15.8 ± 0.2
685.59 ± 30.11
0.52 ± 0.03
0.69 ± 0.02
2.2 ± 0.1
0.029 ± 0.002
0.031 ± 0.005
0.143 ± 0.019
0.94
-2.61
2.61
-2.61
2.19
2.61
2.61
2.40
0.35
0.009
0.009
0.009
0.028
0.009
0.009
0.016
30
Figure 4.1 Body temperature responses of M.
leprosa (——) and T. scripta (-----) to a step
change in ambient temperature during (a)
heating and (b) cooling experiments
Temp (ºC)
25
20
T. scripta
15
0
b)
60
120
180
240
Time (min)
30
Air
Water
Temp (ºC)
25
20
M. leprosa
T. scripta
15
0
60
120
Time (min)
180
240
0
15
30
Time (min)
45
60
CAPÍTULO 4: Diferencias en las tasas de intercambio de calor
M. leprosa
95
Table 4.2 Morphological measures: size, weight, surface-to-volume ratio (SA/V), sphericity index
(SI) and flatness index (FI) for tested turtles, with thermal exchange rates (s) and corresponding
R2 values for the three different treatments
Species
M. leprosa
T. scripta
Turtle
1
1
1
2
2
2
3
3
3
4
4
4
5
5
5
1
1
1
2
2
2
3
3
3
4
4
4
5
5
5
Size
(cm)
Weight SA/V
(g)
(cm-1)
SI
16.1
552.20
0.580
0.65
16.1
586.29
0.545
0.67
15.2
505.13
0.598
0.66
15.9
530.08
0.623
0.63
16.2
463.76
0.634
0.62
15.7
709.79
0.518
0.69
15.8
682.94
0.539
0.68
16.0
680.29
0.528
0.68
15.6
715.38
0.466
0.72
16.1
639.56
0.540
0.67
FI
Treatment
s
R2
(min )
-1
2.33 Heating
Cooling (Air)
Cooling (Water)
2.25 Heating
Cooling (Air)
Cooling (Water)
2.25 Heating
Cooling (Air)
Cooling (Water)
2.44 Heating
Cooling (Air)
Cooling (Water)
2.48 Heating
Cooling (Air)
Cooling (Water)
2.19 Heating
Cooling (Air)
Cooling (Water)
2.13 Heating
Cooling (Air)
Cooling (Water)
2.24 Heating
Cooling (Air)
Cooling (Water)
2.08 Heating
Cooling (Air)
Cooling (Water)
2.33 Heating
Cooling (Air)
Cooling (Water)
0.0394
0.0451
0.1876
0.0352
0.0451
0.1472
0.0393
0.0545
0.2138
0.0362
0.0655
0.2311
0.0430
0.0771
0.1899
0.0276
0.0300
0.1445
0.0274
0.0363
0.1349
0.0287
0.0272
0.1359
0.0328
0.0356
0.1749
0.0302
0.0257
0.1241
0.965
0.986
0.961
0.943
0.986
0.956
0.974
0.989
0.967
0.971
0.990
0.942
0.977
0.984
0.971
0.986
0.991
0.968
0.978
0.992
0.977
0.981
0.989
0.953
0.976
0.993
0.970
0.982
0.991
0.984
thus the surface-to-volume ratio is determinant for bodies of similar length,
differences in shell morphology between the two species of turtles may entail a
faster thermal exchange with air and water in M. leprosa than in T. scripta. In
this regard, shell shape and surface-to-volume ratio have been demonstrated to
similarly influence heating and cooling rates among freshwater turtles (Boyer
1965; Spray and May 1972; Gronke et al. 2006). We also found that males of
both species had flatter shells and higher values of surface-to-volume ratio,
likely as a result of the concavity of the male plastron (which reduces shell
height and volume). These differences between males and females were greater
96
CAPÍTULO 4: Diferencias en las tasas de intercambio de calor
in M. leprosa than in T. scripta, in agreement with the deeper plastral concavity
found in M. leprosa (N. Polo-Cavia, pers. obs.). Although sexual dimorphism
has been observed to influence rates of thermal exchange in reptiles (Pearson et
al. 2003) and it may likely have influence on thermal behavior of both species
of turtles, our results cannot yield the effect of sex on their heating and cooling
rates, nor predict its magnitude, as we used only female individuals in our
experiment. As expected, body size was negatively correlated with surface-tovolume ratio, but no correlation was found between size and sphericity or
flatness indexes. Therefore, when turtles reach greater sizes, their volume
increases more than their surface area, while no significant variation in shape
occurs.
Both cladogenesis and environment may be considered as significant
sources of shape variation in turtles (Claude et al. 2003). While clades mostly
differ in shell contour (emydids being posteriorly wider), and in more localized
differences (as in the relative extension of scutes or bones), environment acts
mostly on shell height and on the architecture of costal plates; aquatic species
having a more flattened shell, terrestrial ones a more rounded shape. The flat
aquatic shell has been thought to enhance hydrodynamics. For example, an
explanation for the flattened shell shape of M. leprosa, compared to the
European pond terrapin, Emys orbicularis, might be the hydrodynamic
morphofunction it could confer in more open waters (Arnold and Ovenden
2002). However, a flattened shell may also entail disadvantages for turtles. An
example is that flat shell turtles are easily caught by avian predators (Janzen et
al. 2000). Nevertheless, M. leprosa may compensate the cost of a flattened shell
by fleeing quickly to safe water when facing a terrestrial predator (Polo-Cavia
et al. 2008). In contrast, a more rounded shell might favor T. scripta in an
original habitat where greatest danger comes from aquatic predators (i.e.,
caimans and crocodiles, Greene 1988) and they are pressured to remain for
longer in land, withdrawn inside the shell, exposed to avian and other
terrestrial predators (Polo-Cavia et al. 2008). On the other hand, submerged and
floating vegetation is usually heavy in T. scripta original habitat (Morreale and
Gibbons 1986; Gibbons 1990). Thus, a specific hydrodynamic functional shell
should be less expected in this species.
Even if the further evolutionary causes determining species-specific shell
shape are unknown, and although we do not know whether other factors such
as thickness of carapace bone or differences in color pattern between the two
species might also influence heating and cooling rates, it is clear from our
results that interspecific differences in shape per se influences surface-tovolume ratio, and thus, rates of thermal exchange with the environment. These
interspecific differences may have consequences for the outcome of competition
processes between turtle species in a scenario where T. scripta has been
97
introduced in the original habitat of native M. leprosa. The trade-off fitted
between thermal exchange rates of M. leprosa and other ecological
requirements such as shape functionality or antipredatory strategies might be
threatened when a new competitor interferes in their thermoregulatory
behavior, taking advantage of its original adaptations. The rounded shape of T.
scripta confers them a low surface-to-volume ratio and a greater thermal
inertia, compared with M. leprosa, what might result advantageous in the
Mediterranean habitats into which T. scripta is introduced.
The advantages of a high thermal inertia appear intuitively reasonable in
larger reptiles (Spotila et al. 1973; Slip and Shine 1988; Spotila et al. 1991). For
example, leatherbacks turtles (Dermochelys coriacea) are able to maintain
elevated body temperatures in cold water and avoid overheating in the tropics
(Paladino et al. 1990), which probably allowed them to exploit an ecological
niche unavailable to other marine turtle species (Wallace et al. 2005). On a
different scale, but in a similar way, slight differences in thermal inertia
between species of small ectotherms might favor introduced species in their
new habitats. In the Iberian Peninsula, sliders have been observed to be active
at lower water temperatures, and therefore, to start earlier than native turtles
their annual cycle (Aceituno 2001). Such adaptation is consistent with the
higher thermal inertia of T. scripta observed in our study. In temperate zones,
mechanisms for conserving body heat could have selective advantages in
aquatic turtles, since individuals that have been basking on land and have
achieved high body temperatures may suddenly be exposed to very cool
conditions when entering the water (Bartholomew 1982). However, a greater
thermal inertia helps to stabilize body temperature, so that rapid changes of
temperature in the environment are slowly reflected in changes in body
temperature. In this way, the lower cooling rates of introduced T. scripta
facilitate body heat retention, thus developing a better performance of activities
such as aquatic foraging (Huey and Slatkin 1976; Dunham et al. 1989), and
favoring competition with native turtles. Also, the risk of overheating while T.
scripta remain withdrawn into the shell for a long period of time, trying to
deter a predator (Polo-Cavia et al. 2008), decreases when surface-to-volume
ratio is greater and thus, the thermal buffering is more effective.
Although a greater thermal inertia also entails an increment in time
necessary to attain optimal temperature, T. scripta may compensate for this cost
by being more competitive for basking resources (Cadi and Joly 2003), or by
increasing the duration of initial basking before locomotor activity in
Mediterranean latitudes (see Spotila et al. 1984, showing that the timing of
basking changes with latitude in T. scripta). Also, observations of basking turtles
in field and captivity show that introduced turtles commonly bask with all
limbs outstretched (contrarily to Spanish terrapins, whose limbs are relaxed in
98
CAPÍTULO 4: Diferencias en las tasas de intercambio de calor
the basking position, N. Polo-Cavia, per. obs.), thus considerably increasing
their surface-to-volume ratio and optimizing basking (Crawford et al. 1983).
Similar behavioral control over the rate of heat transfer by means of changing
postures has been observed in large snakes (Ayers and Shine 1997; Rice et al.
2006) and lizards (Martín et al. 1995).
A greater thermal inertia might allow T. scripta to maintain relatively high
and constant body temperatures after basking in air, mostly through behavioral
thermoregulation in water (aquatic basking and selection of heated areas of
water have been demonstrated in T. scripta, Spotila et al. 1984), while native M.
leprosa turtles would require a more intermittent basking activity due to their
higher rate of thermal exchange with environment. Also, M. leprosa
interruptions of basking may result in a more efficient occupation of basking
sites by T. scripta. Cadi and Joly (2003) suggested that introduced T. scripta
seemed more competitive for the most suitable basking places than native
European pond turtles E. orbicularis, which avoided to climb onto a solarium
that was already occupied by a slider. Similar competition for basking places
between T. scripta and M. leprosa has been confirmed experimentally (PoloCavia et al. in press).
With the introduction of a new competitor species interfering in the
efficiency of performance of basking, the lower thermal buffering of native M.
leprosa turtles may entail a difficulty for heat retention and result in the
achievement of suboptimal body temperatures, which may lead to a detriment
in the efficiency of their physiological functions. Low body temperatures
negatively affect food ingestion and digestion (Gianopulos and Rowe 1999),
which ultimately affects growth rates (Congdon 1989; Avery et al. 1993). The
rate and efficiency of digestion are enhanced at elevated body temperatures
(Parmenter 1981; Zimmerman and Tracy 1989), being food energy incorporated
more rapidly and efficiently. This has especial importance to individuals
inhabiting Mediterranean regions, in which high temperatures are limited year
around (Lysenko and Gillis 1980). A deficiency in basking activity has also
consequences in dermal synthesis of vitamin D (Pritchard and Greenhood 1968;
Avery 1982), avoidance of fungal infections and riddance of parasites of shell
and skin (Cagle 1950; Boyer 1965; Vogt 1979), and may also retard maturation
of ova (Obbard and Brooks 1979; Whittow and Balazs 1982).
In conclusion, the more rounded shell of introduced T. scripta endows them
with a greater surface-to-volume ratio, compared with native M. leprosa. The
Spanish turtle present a more flattened shape; likely due to the hydrodynamic
morphofunction it might confer in the more open waters where this species
occurs (Arnold and Ovenden 2002). These differences in shape morphology
between species are related with differences in thermal exchange rates. Since
mechanism for maximizing body heat retention could confer selective
99
advantages to aquatic turtles, which are exposed to chilling conditions when
entering water (Bartholomew 1982), the greater thermal inertia of T. scripta
might result in a competitive advantage for this introduced species in
Mediterranean habitats. Interactions between T. scripta and native M. leprosa
during basking activity could lead to a detriment in the efficiency of basking
and thermoregulation of native turtles, with lower capabilities of heat
retention. It might finally affect digestion rates and other physiological
functions, thus aggravating the outcomes of competition with introduced
sliders.
Acknowledgements We thank A. Marzal for allowing us to work in his dehesa state (‘‘La
Asesera’’), the ‘‘Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat’’ (GREFA) for
providing exotic turtles, and ‘‘El Ventorrillo’’ MNCN Field Station for use of their facilities.
Helpful suggestions for the analytical model of thermal exchange rates were provided by V. Polo.
Financial support was provided by the MEC project CGL2005-00391/BOS and by a MEC-FPU
grant to N.P.-C. The experiments comply with the current laws of Spain and the Environmental
Agencies of the ‘‘Junta de Extremadura’’ and ‘‘Comunidad de Madrid’’ where they were
performed.
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104
Capítulo
5
Relación entre el estado nutricional y los requerimientos de asoleamiento de galápagos nativos e invasores Nuria Polo Cavia, Pilar López y José Martín
En revisión
RESUMEN
106
El comportamiento termorregulador de los ectotermos se
encuentra fuertemente ligado a su estado nutricional.
Recientemente, se ha sugerido que la existencia de un
compromiso entre el mantenimiento del balance energético y
la eficiencia de la digestión podría afectar al comportamiento
de termorregulación en estos animales. Por otra parte, se ha
confirmado la competencia por lugares de asoleamiento entre
las especies nativas de galápagos y el introducido galápago de
Florida (Trachemys scripta elegans). T. scripta interfiere
negativamente en la actividad de asoleamiento de los
galápagos nativos y posee, además, una mayor capacidad para
retener el calor corporal, lo que en conjunto podría conferir
ventajas termorreguladoras a la especie invasora. En
consecuencia, a partir de un comportamiento de
asoleamiento deficiente podrían derivarse efectos complejos y
diversas alteraciones en las tasas metabólicas de los galápagos
nativos. En este trabajo, comparamos los requerimientos de
asoleamiento de una especie autóctona de la Península
Ibérica protegida, el galápago leproso (Mauremys leprosa),
con los del introducido galápago de Florida, en condiciones
de alimentación ad libitum vs. ayuno. Para ello, se analizó el
límite superior del rango de temperaturas seleccionado por
cada especie (LSR) (definido como la temperatura corporal a
la cual cesa la actividad de asoleamiento). La especie nativa
mostró valores más altos de LSR, y ambas especies redujeron
esta temperatura en respuesta a la privación de alimento. Esta
plasticidad del comportamiento termorregulador de los
galápagos en relación a su estado nutricional sugiere la
existencia de un mecanismo adaptativo en ectotermos que
favorece la depresión metabólica y la conservación de la
energía durante periodos de ayuno. Sin embargo, una
reducción en las tasas metabólicas de M. leprosa inducida por
la competencia con una especie invasora podría derivar en
una prolongada deficiencia de las funciones fisiológicas de los
individuos, incurriendo por tanto en elevados riesgos de salud
y depredación, lo cual podría finalmente favorecer la recesión
de la especie nativa en ambientes mediterráneos ■
FEEDING STATUS AND BASKING REQUIREMENTS OF FRESHWATER
TURTLES IN AN INVASION CONTEXT
Abstract Thermoregulatory behavior and feeding status are strongly related in ectotherms. A
trade-off between maintenance of energy balance and digestion efficiency has been recently
proposed to affect thermoregulation in these animals. On the other hand, competition for basking
sites has been described between Iberian turtles and the introduced red-eared slider (Trachemys
scripta elegans). T. scripta negatively interferes on basking behavior of native turtles and benefits
from a greater capacity to retain body heat, which may likely result in thermoregulatory
advantages for the introduced sliders. Consequently, complex effects and alterations in metabolic
rates of native turtles might derive from a deficient basking behavior. We compared the basking
requirements of the endangered native Spanish terrapin (Mauremys leprosa) and those of the
introduced red-eared slider, analyzing the upper set point temperature (USP) (defined as the body
temperature at which basking ceases) of both native and introduced turtles, under feeding and
fasting conditions. We found higher values of USP in the native species, and a reduction of this
temperature associated with food deprivation in the two turtle species. This adjustment of
thermoregulatory behavior to the nutritional status found in freshwater turtles suggests that
ectotherms benefit from metabolic depression as an adaptive mechanism to preserve energy
during periods of fasting. However, a reduction in metabolic rates induced by competition with
sliders might lead M. leprosa to a prolonged deficiency of their physiological functions, thus
incurring increased predation risk and health costs, and ultimately favoring the recession of this
native species in Mediterranean habitats.
L
ike in most ecthotherms, thermoregulation is especially important in
aquatic turtles, since it affects many of their physiological functions
(Huey 1982). Mainly through aerial basking, aquatic turtles can attain
and maintain fairly precise and constant body temperatures (Tb) that allow
them to optimize the efficiency of their physiological processes (Boyer 1965;
Crawford et al. 1983; Scharzkoplf and Brooks 1985; Meek and Avery 1988). In
particular, Tb plays a major role in maximizing digestive processes in reptiles
(Harlow et al. 1976; Troyer 1987). By attaining optimal Tb, turtles that
adequately bask benefit from a corresponding increase in their metabolic rate
(Jackson 1971; Kepenis and McManus 1974; Dubois et al. 2008), digestion speed
and digestion efficiency (Kepenis and McManus 1974; Parmenter 1981; Avery
et al. 1993; Koper and Brooks 2000; Angilletta 2001; Zhang and Ji 2004).
Many ectotherms change their temperature preferences after feeding. A
thermophilic response resulting in increased Tb has been observed in a wide
range of reptiles, including crocodilians (Lang 1979), snakes (Lysenko and Gillis
1980; Dorcas et al. 1997; Blouin-Demers and Weatherhead 2001a), lizards
(Sievert 1989; Tosini et al. 1994; Brown and Griffin 2005; Brown and Roberts
2008), and turtles (Moll and Legler 1971; Gatten 1974; Hammond et al. 1988;
CAPÍTULO 5: Estado nutricional y requerimientos de asoleamiento
Keywords
Feeding status • Freshwater turtles • Invasive species • Mauremys leprosa •
Thermoregulation • Trachemys scripta
107
Dubois et al. 2008). Most of these experimental studies have analyzed the
thermoregulatory behavior of ectotherms after a food ingestion event, while
less emphasis has been placed on their feeding status. Diet composition has been
reported to influence Tb selected by some reptiles (Geiser et al. 1992; Geiser and
Learmonth 1994, Simandle et al. 2001) but little evidence exists to support
similar effects induced by prolonged fasting conditions. Recently, Brown and
Griffin (2005) described a reduction in the selected Tb of the lizard Anolis
carolinensis after food deprivation, suggesting an energy conservation strategy
during periods of low food availability. A similar effect is found in some
terrapin species (Gatten 1974; Dubois et al. 2008), which suggests that turtles
are able to accurately adjust their metabolic rates according to the food intake
opportunities, and also that their basking requirements increase in order to
attain optimal Tb that allow them to maintain a more active metabolism and an
optimal performance of their digestive functions. Many ectothermic vertebrates
exhibit a physiological flexibility that allows them to adjust their energy
expenditure processes during periods of nutritional bottlenecks (Anderson 1993;
Naya and Bozinovic 2006; Naya et al. 2008). Thus, metabolic rates of turtles
have been found to decrease as fasting conditions prolong (Belkin 1965; Sievert
et al. 1988). Sievert et al. (1988) report drops of 1/3 in oxygen consumption of
juvenile turtles Chrysemys picta after only 19 days of fasting. The reduction in
metabolic rates of reptiles has been claimed to act to conserve energy resources
(Bennett and Dawson 1976).
In the Iberian Peninsula, the red-eared slider (Trachemys scripta) is an
introduced exotic turtle (Vilà et al. 2008) that is competing and displacing the
native Spanish terrapin (Mauremys leprosa), whose populations have
considerably declined during the last decades, being currently considered as an
endangered species (Da Silva 2002). The nature of the interspecific interactions
between sliders and Spanish terrapins remains unclear, but it is possible that
direct competition for food, refuges or basking places occurs (Crucitti et al.
1990). Competition for basking sites has been described between sliders and the
European pond turtle (Emys orbicularis) (Cadi and Joly 2003), and recent
studies suggest that competition is very likely to occur also between sliders and
the Spanish terrapins (Polo-Cavia et al. 2008, 2009a,b). Also, native M. leprosa
forced to share basking resources with sliders have been found to reduce their
basking activity and to avoid basking stacked with the exotic turtles (Polo-Cavia
et al. in press). Sliders can then monopolize the most suitable basking places,
impeding native turtles to adequately bask, which might severely affect the
efficiency of physiological, especially digestive, functions of the native species.
Such negative effects of inefficient basking may explain the loss of weight and
decreased survival rates found in native terrapins after long term competition
with sliders (Cadi and Joly 2004). However, anatomical and physiological
108
CAPÍTULO 5: Estado nutricional y requerimientos de asoleamiento
differences between native and invasive turtle species might confer them
dissimilar thermal requirements in relation with digestive processes.
Interspecific differences in thermal exchange rates related to morphological
differences in carapace size and shape have been found between these two
turtle species (i.e., M. leprosa shows a lower thermal inertia associated with a
greater surface-to-volume ratio compared with those of T. scripta, Polo-Cavia et
al. 2009b). Different body surface-to-volume ratios entail different heat
exchange rates, which might further induce different basking requirements.
This might also imply that the feeding status of the turtles may affect differently
to the thermoregulatory behavior of sliders and native terrapins. Moreover, an
individual that is able to maintain its selected Tb for a longer time period should
assimilate more metabolic energy during digestion (Angilletta et al. 2001). Thus,
due to their higher thermal inertia, sliders would take more time to attain an
optimal Tb but they could maintain body heat for longer when entering the
water, favoring the maintenance of elevated metabolic rates and the proper
performance of digestive processes. On the other hand, Spanish terrapins would
attain faster an optimal Tb during basking, but because of their greater tendency
to loss heat when entering water, they might require more frequent basking
episodes in order to increase Tb during feeding periods. Then, in a new
competitive situation in which introduced sliders actively displace native
terrapins from the basking places and impede them to adequately bask, Spanish
turtles might not be able to maintain optimal Tb for appropriate food
assimilation. This could lead to a reduction of their metabolic activity, and thus
to a detriment in the efficiency of food ingestion and digestion, which might
finally affect negatively the outcome of competition between introduced and
native freshwater turtles.
The purpose of this study was to compare the thermal requirements during
basking of native Spanish terrapins M. leprosa and introduced sliders T. scripta,
analyzing the effects of prolonged feeding and fasting conditions on preferred
basking temperatures. We considered the upper set point temperature (USP),
measured as the Tb at which turtles ceased basking and entered into the water,
as a good indicator of thermal requirements related with feeding in aquatic
turtles (Dubois et al. 2008; see methods). Thus, our objectives were to determine
1) whether differences in USP occurred between native and invasive turtle
species, and 2) the effect of food deprivation on the USP of the two turtle
species. Finally, since turtles’ morphology might indirectly affect the
thermophilic response through its influence on thermal exchange rates, we also
analyzed 3) the relation between surface-to-volume ratio and USP of turtles.
109
METHODS
Study animals
We captured with baited funnel traps 18 individuals of native Spanish terrapins
(M. leprosa) (carapace length: mean ± SE = 14.7 ± 0.3 cm, range = 11.5-16.3 cm)
in several ponds and tributary streams of the Guadiana River, located inside
dehesa woodlands with scattered holm oak (Quercus ilex) at Olivenza (Badajoz
Province, southwestern Spain). We also obtained 16 red-eared sliders (T.
scripta) (carapace length: mean ± SE = 14.8 ± 0.6 cm, range = 11.3-17.9 cm),
from a large pond located in Madrid Province (central Spain), where they had
been maintained under seminatural conditions by the conservationist private
organization “EXOTARIUM” (Exotic Animal Rescue Center). These sliders had
been recently extracted from introduced populations in central Spain to avoid
aversive effects on the original ecosystem balance.
All turtles were housed individually at “El Ventorrillo” Field Station
(Navacerrada, Madrid Province), in outdoor aquaria (60 x 40 x 30 cm) filled
with water and containing stones that allowed them to bask. The temperature
and photoperiod were those of the natural surroundings. Turtles were held in
their home-aquaria for at least two weeks before testing, so that they became
familiarized with captivity conditions. To avoid potential confounding effects of
the diet on the results, turtles were fed ad libitum small pieces of commercial
compound feed. All turtles were healthy during the trials and all maintained or
increased their body mass. At the end of experiments, turtles were returned to
the EXOTARIUM’s pond (sliders) or to their exact field capture sites (Spanish
terrapins).
Surface-to-volume ratio
We estimated the surface-to-volume ratio of turtles, basing on biometric
measures. We approached the hemispherical shape of the turtles carapace to a
scalene semiellipsoid of revolution whose axes 2a, 2b, 2c were given by CL
(carapace straight length), CW (carapace straight width, measured at the 6-7
marginal scutes joint) and 2CH (maximum carapace height) respectively.
To assess the surface area of turtles, we adapted Klamkin’s equation (this
expression approximates the true surface area of an arbitrary ellipsoid, Klamkin
1971), for a semiellipsoid:
SA ≈ 2π
110
{( a b
2
2
) }
+ a 2c 2 + b 2c 2 / 3
1/ 2
+ π ab
To asses volume of the turtles body, we used an interpolated equation
which approaches the volume of the turtles from their shell dimensions (CL,
CW and CH) (coefficient values: i = 0.381299, j = 53.3286, k = -2.360010, l = 0.169371):
V ≈ iπ (CL / 2 + j )(CW / 2 + k )(CH / 2 + l )
This method has been validated and used before in assessing the surface-tovolume ratio of both M. leprosa and T. scripta species (see Polo-Cavia et al.
2009b for a detailed description).
According to the thermal coadaptation hypothesis, since performance is
enhanced when Tb approaches a species and specific-process optimal
temperature (To), the preferred –or set point- body temperature (Tset) of a
species should match this thermal optimum for performance (Huey and Bennett
1987; Angilletta et al. 2006). Consequently, Tset is commonly used to estimate
the Tb that maximizes locomotion or physiological performance (Dawson 1975;
Stevenson et al. 1985; Hertz et al. 1993; Brown and Weatherhead 2000; BlouinDemers and Weatherhead 2001b). In estimations of Tb that maximizes digestive
functions, in which energy gain typically increases continuously to To and then
sharply decreases (Lillywhite et al. 1973; Stevenson et al. 1985; Niu et al. 1999),
Tset is more properly defined as the upper set point temperature (USP) selected
by an animal in a thermal gradient (Dubois et al. 2008), rather than as the mean
(Pough and Gans 1982) or a central quartile range (Hertz et al. 1993). Upper and
lower bounds of Tset have to be defined arbitrarily in thermal gradients, but they
can be directly determined as the Tb at which an individual shows heat
avoidance behavior and shifts to cooling and viceversa (Kingsbury 1993, 1999;
Tosini and Avery 1994; Ben-Ezra et al. 2008). Thus, Tb at which aerial basking
ceases can be considered an appropriate measure of USP associated with
maximizing digestive processes in aquatic turtles.
Experimental procedure
We compared USP of native M. leprosa and introduced T. scripta under feeding
and fasting conditions. Each subject turtle was tested in two experimental
treatments (‘feeding vs. fasting’), with the order of application differing
between individuals (random assignment). For the ‘feeding’ treatment, turtles
were fed ad libitum commercial compound feed once a day during seven
CAPÍTULO 5: Estado nutricional y requerimientos de asoleamiento
Set point temperatures
111
consecutive days before testing. All turtles readily ate this type of food, and we
considered that turtles were able to eat enough food until satiation. For the
‘fasting’ treatment, turtles were deprived of food for seven consecutive days
prior to testing. After this time, turtles were considered to be postabsorptive
(i.e., to have digested and absorbed all food in their digestive tract) (Bennet and
Dawson 1976; Gatten 1974). Water was continuously available during the
period of fasting. At the end of trials, animals were fed ad libitum and recovered
their normal nutritional state seven days after trials had finished.
We carried out experiments indoor to maintain experimental conditions
stable (ambient air temperature in the laboratory was kept at 20 ± 1 °C). We
used an aquarium equal to the ones used to house the turtles. The aquarium was
filled with 10 L water at ambient temperature, and a brick (24 x 11.5 x 7 cm)
was placed in the center, emerging 3 cm above the water surface. An infrared
heat reflector (250 W, 250 V) was situated hanging 30 cm over the brick in the
center of the aquarium. In this way, we simulated a basking place located in a
body of water reflecting natural temperature conditions. A similar experimental
device that allowed turtles to shuttle between aerial basking and cold water has
been used before to measure set point temperatures of aquatic turtles (Ben-Ezra
et al. 2008). Each turtle was initially cooled inside a thermostatic chamber that
was maintained at 15 ± 1 °C until Tb stabilized at 15 °C, and then carefully
placed on the plastron over the brick’s surface and left undisturbed for one
hour. From that moment, the turtle was free to dip into the water, although the
lower Tb encouraged the turtle to bask. Turtles were used to handling and they
normally bask as they did in their home aquaria.
We monitored Tb of turtles during the whole tests, using HOBO U-12 data
loggers with HOBOware Pro Software for Windows (Onset Computer
Corporation). A cloacal probe (38 ga copper-constantan thermocouple;
temperature range: -200 to 100 °C; precision: ±1.5 °C; resolution: 0.1 °C) was
inserted into each turtle’s cloaca to approximately a third of the total length of
the plastron (Mrosovsky 1980). Gauge thermocouples into the anal opening of
reptiles are generally well tolerated and spare from disturbing the subject
and/or the experiment. Therefore, it is considered an appropriate method for
measuring Tb in these animals (Kingsbury 1999). To prepare the thermally
sensitive probe, we entwined the leads at one end of the thermocouple, fused
the entwined leads together at the tips, and encapsulated the end in epoxy
resin. We used duct tape to secure the exiting thermocouple wire to the turtle’s
carapace (Do Amaral et al. 2002). Previous studies have shown that cloacal
temperatures of turtles were highly correlated with air and water temperatures
immediately surrounding turtles (Obbard and Brooks 1981; Ernst 1982; Wilson
1994) and with internal Tb (Edwards and Blouin-Demers 2007; Ben-Ezra et al.
2008; Dubois et al. 2008). Therefore, we assumed that cloacal temperature was a
112
reasonably accurate estimate of turtles Tb. Data loggers recorded the changes in
the Tb of each turtle during basking, and its USP right before the turtle dived
into the water, and consequently, the Tb started to decrease to water
temperature (20 °C).
Statistical analyses
We used a two-way repeated measures analyses of variance (ANOVA) to
analyze the differences between M. leprosa and T. scripta in USP across
treatments by the same individual subject turtle. The experimental treatment
(‘feeding’ vs. ‘fasting’) was included as a within subject factor, and the species of
the subject turtle as a between-subjects factor. We used simple linear regression
to analyze the effect of surface-to-volume ratio on the USP of turtles, under
feeding and fasting conditions. Data normality was verified by Shapiro-Wilk’s
test and tests of homogeneity of variances (Levene’s test) showed that variances
were not significantly heterogeneous.
We found significant differences in overall USP between M. leprosa and T.
scripta (two-way repeated measures ANOVA, species: F = 33.05, df = 1,32, P <
0.0001). Native Spanish terrapins showed higher values of USP than invasive
sliders (M. leprosa: mean ± SE = 31.9 ± 0.6 °C; T. scripta: mean ± SE = 26.7 ± 0.7
°C). We also found significant differences between treatments (F = 28.16, df =
1,32, P < 0.0001), with greater values of USP when the turtles had been fed than
in the fasting treatment (Fig. 5.1). The interaction between species and
treatment was non-significant (F = 0.003, df = 1,32, P = 0.95) (Fig. 5.1).
36
Figure 5.1 Set point body temperatures
T. scripta
M. leprosa
34
USP (ºC)
32
30
28
26
24
22
(USPs) (mean ± SE) at which basking ceased
of introduced T. scripta and native M.
leprosa, under feeding and fasting
treatments
Feeding
Fasting
CAPÍTULO 5: Estado nutricional y requerimientos de asoleamiento
RESULTS
113
USP of turtles were positively correlated with their surface-to-volume ratio
under feeding and fasting treatments (Pearson’s correlations, feeding: r = 0.69, F
= 28.53, df = 1,32, P < 0.0001; fasting: r = 0.60, F = 17.93, df = 1,32, P < 0.0002).
Thus, turtles with lower surface-to-volume ratio showed lower USP (Fig. 5.2).
Figure 5.2 Pearson’s correlations
between USP and surface-tovolume ratio of turtles, when they
were under feeding (solid line) and
fasting (dotted line) conditions
DISCUSSION
Our results firstly reveal clear interspecific differences in the Tb at which
basking ceased (i.e., USP) between introduced T.scripta and native M. leprosa
freshwater turtles, with overall USP being on average 5.2 °C higher in M.
leprosa. This result clearly suggests different thermal requirements of sliders
and Spanish terrapins. Behavioral thermoregulation through aerial basking
allows ectotherms to maximize physiological performance by regulating Tb to
approach a species and specific-process optimal temperature (Huey and Slatkin
1976; Huey and Bennett 1987; Angilletta et al. 2002, 2006). Thus, differences in
thermal optima for performance between the two species might likely explain
their differences in USP.
On the other hand, the correlation found between set point temperatures of
turtles and their surface-to-volume ratio points out to a close relation between
interspecific differences in basking requirements and interspecific differences in
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CAPÍTULO 5: Estado nutricional y requerimientos de asoleamiento
carapace morphology. Interspecific differences in thermal exchange rates with
the environment related to different surface-to-volume ratios have been
reported for M. leprosa and T. scripta (Polo-Cavia et al. 2009b). The more
rounded shape of T. scripta confers them a low surface-to-volume ratio and a
greater thermal inertia, compared with M. leprosa, which facilitates body heat
retention. Since freshwater turtles usually lose the heat gained from basking
very rapidly when they re-entry to water (Avery 1982; Bartholomew 1982),
strategies that contribute to maximize heat retention could be selectively
advantageous for aquatic species, especially in Mediterranean habitats in which
high temperatures are limited year around (Lysenko and Gillis 1980). We
suggest that Spanish terrapins, more flattened and with higher surface-tovolume ratios, might compensate their greater heat loss by increasing the USP.
In this way, Spanish terrapins could benefit from a better performance when
entering into water for foraging or other activities. At this regard, a positive
effect of increased Tb on aquatic and terrestrial locomotor performance of
juvenile western painted turtles (Chrysemys picta bellii) has been reported
recently (Elnitsky and Claussen 2006). Also, Ben-Ezra et al. (2008) found that
the optimal temperature for swimming and righting of the northern map turtle
(Graptemys geographica) fell within Tset, very close to the upper bound.
However, because of the wide range of Tset that turtles exhibited, these authors
suggested that coadaptation may not reflect selective pressures for the
convergence of preferred basking temperature and locomotor performance in
this species. Moreover, Ben-Ezra et al. (2008) argued that, in turtles with
pronounced aerial basking behavior, the locomotory potential of elevated Tb
achieved by basking would rapidly be lost in aquatic environments because of
the high thermal conductivity of water. Nevertheless, turtles might be able to
maintain relatively high and constant Tb after basking in air by later selecting
heated areas of water (aquatic thermoregulatory behavior has been
demonstrated in T. scripta, Spotila et al. 1984). Thus, behavioral
thermoregulation may be also linked with locomotory performance in aquatic
turtles, as it is in other reptiles (Bauwens et al. 1995; Angilletta et al. 2002;
Blouin-Demers et al. 2003). Although, behavioral regulation of Tb is considered
to primarily serve to maximize energy gain, rather than locomotory
performance, and it seems to be of particular importance for turtles inhabiting
environments where high temperatures are limited (Dubois et al. 2008).
Since heat transference from air occurs faster in M. leprosa than in T.
scripta (Polo-Cavia et al. 2009b), a higher USP would not imply that Spanish
terrapins need to have longer basking periods than sliders. Thus, the higher USP
of M. leprosa would not necessarily entail a disadvantage in terms of time
budget by itself. However, negative effects may arise from basking interactions
with the introduced competitor, if native turtles find difficulties to compensate
115
their faster body heat loss in water with more frequent episodes of aerial
basking to regain temperature (see Cady and Joly 2003; Polo-Cavia et al. in
press, describing negative impact of sliders introduction on basking behavior of
native turtles).
The results of our experiments also reveal a clear variation in USP of turtles
associated with feeding status. Both M. leprosa and T. scripta showed USP 2.4
°C higher on average when they had been fed than under fasting conditions.
Previous studies on turtles have reported similar effects on thermoregulatory
behavior related to feeding (Moll and Legler 1971; Hammond et al. 1988;
Dubois et al. 2008), with selected Tb even 4.5 °C higher in recently fed T. scripta
(Gatten 1974). Snakes (Lysenko and Gillis 1980; Blouin-Demers and
Weatherhead 2001a), crocodilians (Lang 1979), and lizards (Sievert 1989; Tosini
et al. 1994; Brown and Griffin 2005; Brown and Roberts 2008) also establish
higher Tb after feeding, and a big snake, Boa constrictor, places the portion of its
body containing a bolus of food directly below the heat source (Regal 1966).
Such thermoregulatory behavior of reptiles in response to feeding conditions is
assumed as an adaptive adjustment to the optimal temperatures for some
components of the digestive process (Dorcas et al. 1997), which may require
different thermal optima from those selected for other behaviors and functions
(Huey 1982; Stevenson et al. 1985; Van Damme et al. 1991; Du et al. 2000). The
thermophilic response of freshwater turtles found in our experiments is
consistent with previous results for correlations between basking and feeding in
red-eared sliders (Gatten 1974), and suggests that both M. leprosa and T. scripta
require from an extra body heat contribution to successfully complete digestive
processes. Thermophilic response elicited by feeding varies widely among
reptile species (Sievert 1989), and variability has also found between freshwater
and terrestrial turtles (Gatten 1974). Thus, differences in extra heat contribution
required by introduced and native turtles could be expected in our experiment.
However, the magnitude of the effect of feeding status on the USP of turtles
was similar for introduced and native terrapins, indicating that basking
requirements of both M. leprosa and T. scripta similarly increment with
increased food intake. Since aquatic turtles experiment very contrasting
temperatures when they shift between aerial basking and water immersion to
maintain Tset, thermoregulation seems to be much more challenging for
freshwater turtles than for terrestrial ones (Ben-Ezra et al. 2008). Then, similar
basking habits of M. leprosa and T. scripta, and their association with
freshwater aquatic habitats, in comparison with terrestrial turtles, may explain
the similarities in precision of thermoregulation between the two species.
Increased metabolisable energy intakes could be one of the advantages of
higher Tb selected by ectotherms during digestion (Angilletta 2001), but energy
expenditure increases at elevated Tb, what suggests a trade-off between
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CAPÍTULO 5: Estado nutricional y requerimientos de asoleamiento
maintenance of energy balance and digestive efficiency. Consequently, a
reduction of the Tb could help to improve energy balance during periods of low
food availability by means of energy conservation (Lillywhite et al. 1973; Brown
and Griffin 2005). Similarly, many ectotherms maintain lower Tb during
inactivity (e.g., Hutchison and Spriesterbach 1986; Sievert and Hutchison 1988,
1989; Angilletta and Werner 1998), possibly as an energy saving mechanism
(Huey 1982; Hutchison and Spriesterbach 1986). Therefore, the shift in the USP
of fasted vs. fed turtles that we found might be due to an adaptive mechanism to
moderate the impact of low levels of energy intake during periods of fasting on
other parameters of the energy budget. Under prolonged fasting conditions,
turtles might save energy reducing activity and metabolic rates (Belkin 1965;
Sievert et al. 1988), which would involve accurately adjustment of their
thermoregulatory behavior to their feeding status, by reducing basking and
selecting lower Tb. Even if there is no supporting evidence that energy saving
by decreased Tb could have a substantial impact in wild ectotherms, the shift in
the set point temperatures of freshwater turtles observed here contributes to
support the generality of the finding of decreased selected Tb associated with
periods of food deprivation in ectotherms (Brown and Griffin 2005). Our results
further suggest that ectotherms benefit from adjusting their Tb and metabolic
rates according to the food intake opportunities.
Thus, feeding status and selected Tb of ectotherms seem to influence each
other in a complex bidirectional way. Increased consumption related to
increased Tb has been reported for many reptile species (e.g., Dutton et al. 1975;
Waldschmidt et al. 1986; Van Damme et al. 1991; Angilletta 2001). Constraints
on locomotion and increased gut passage time seem to be responsible for limited
consumption at low temperatures (Angilletta 2001). Even if turtles do not use
rapid locomotion to capture food (Harding and Bloomer 1979; Ernst 2001),
consumption might be constrained by food processing rate, especially at
northern latitudes, where temperature may be more limiting than food
availability (Congdon 1989; Grant and Porter 1992; Koper and Brooks 2000).
Also, many of the processes determining food intake (i.e., prey detection and
capture, handling time, ingestion) are sensitive to Tb (Greenwald 1974; Van
Damme et al. 1991; Ayers and Shine 1997). Since Tb clearly influences the
performance of activities associated with feeding (Bennett 1990), it is very
likely that turtles with low basking opportunities show also a less active
foraging, besides a reduced metabolism, decreased digestion rates, and a general
depression of their physiological functions (Parmenter 1981; Sievert et al. 1988;
Zimmerman and Tracy 1989; Gianopulos and Rowe 1999). With the
introduction of a new competitor species interfering in their basking behavior,
native Spanish terrapins likely find difficulties to properly bask, thus being
unable to reach and maintain optimal Tb, with might negatively affect their
117
food ingestion. Turtles might then experiment a reduction in their selected Tb
in order to compensate their energy balance, which might finally induce a
feedback effect between basking requirements and feeding performance, thus
resulting in a more and more depressed metabolism. Negative effects derived
from a dropped metabolism might be poor food energy incorporation
(Parmenter 1981; Zimmerman and Tracy 1989), lowered blood circulation and
suppressed immune defenses (Cooper et al. 1985), retarded growth rates
(Congdon 1989; Avery et al. 1993) or maturation arrest of ova (Obbard and
Brooks 1979; Whittow and Balazs 1982). In such lethargic conditions, native
turtles might easily incur increased predation risk and health costs, thus
aggravating the competition process with introduced turtles and favoring the
recession of native Spanish terrapins.
In short, our experiments revealed differences in USP of M. leprosa and T.
scripta, which might have different specific thermal optima for performance.
However, differences in morphology and associated thermal exchange rates
may be also responsible for the different basking requirements of M. leprosa and
T. scripta. A similar thermophilic response was elicited by feeding in both
turtles species, which showed higher USP during basking. The reduced basking
requirements related to fasting conditions that we found in freshwater turtles
confirm that ectotherms might benefit from metabolic depression as an adaptive
mechanism to preserve energy during periods of low food intake. Nevertheless,
a reduction in the metabolic rates of native turtles induced by competition with
a new introduced species interfering in their thermoregulatory behavior might
lead to serious consequences for Spanish terrapins.
Acknowledgements We thank A. Marzal for allowing us to do field work in his dehesa state (“La
Asesera”), the Exotic Animal Rescue Center “EXOTARIUM” for providing sliders, and “El
Ventorrillo” MNCN Field Station for use of their facilities. Financial support was provided by the
MEC project CGL2005-00391/BOS and the MCI project CGL2008-02119/BOS, and by an ‘‘El
Ventorrillo’’ CSIC grant and a MEC-FPU grant to N. P.-C.
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122
Capítulo
6
Efectos de la temperatura corporal en la respuesta de ‘giro’ de galápagos nativos e invasores: consecuencias en la competencia Nuria Polo Cavia, Pilar López y José Martín
En revisión
RESUMEN
124
La coadaptación entre la temperatura preferida de
asoleamiento y la respuesta locomotora de los galápagos es
una cuestión arduamente controvertida, argumentándose que
las temperaturas alcanzadas durante el asoleamiento aéreo
difícilmente podrían favorecer la locomoción de los galápagos
en el agua. Sin embargo, el comportamiento de ‘giro’ de estos
animales podría estar sujeto a presiones de coadaptación,
puesto que tiene lugar fundamentalmente en tierra y puede
determinar críticamente su supervivencia. En este estudio se
analizó el efecto de la temperatura corporal (Tb) en la
respuesta de ‘giro’ de dos especies de galápagos, el autóctono
galápago leproso (Mauremys leprosa) y el introducido
galápago de Florida (Trachemys scripta elegans), una especie
invasora que está desplazando a las poblaciones nativas en la
Península Ibérica. Es posible que la respuesta de ‘giro’ de estas
dos especies pudiera verse afectada diferencialmente por la
Tb. Así mismo, las diferencias interespecíficas potenciales en
el comportamiento de ‘giro’ de los galápagos podrían
contribuir a explicar la mayor capacidad competitiva de T.
scripta. Los resultados mostraron un claro efecto de la Tb en la
repuesta de ‘giro’ tanto de M. leprosa como de T. scripta, la
cual fue favorecida a las temperaturas preferidas de
asoleamiento respectivas de cada especie, sugiriendo la
existencia de coadaptación entre esta temperatura y la
respuesta de ‘giro’ de los galápagos. Por otra parte, M. leprosa
requirió tiempos medios más largos que T. scripta para volver
a la posición prono, lo que indica una mayor eficiencia de la
especie invasora en la respuesta de ‘giro’. Esta ventaja
competitiva podría favorecer la expansión de los galápagos
exóticos en los nuevos ambientes en los que han sido
introducidos, en detrimento de las poblaciones nativas de
galápago leproso ■
EFFECTS OF BODY TEMPERATURE ON RIGHTING PERFORMANCE
OF NATIVE AND INVASIVE FRESHWATER TURTLES:
CONSEQUENCES FOR COMPETITION
Abstract Coadaptation between preferred basking temperature and locomotion of aquatic turtles
remains controversial because aerial basking could hardly improve locomotor performances in
water. However, righting behavior might be subject to coadaptation pressures, given that it is
mainly performed on land and may critically determine survival of turtles. We analyzed the
effect of body temperature (Tb) on righting performance of two species of freshwater turtles, the
endangered native Spanish terrapin (Mauremys leprosa), and the red-eared slider (Trachemys
scripta elegans), an introduced invasive species that is displacing native turtles in the Iberian
Peninsula. We hypothesized that Tb might differently affect righting response of these two turtle
species, and that interspecific behavioral asymmetries in righting performance might contribute
to explain the greater competitive ability of introduced T. scripta. We found a clear effect of Tb on
righting response of both M. leprosa and T. scripta, being the performance enhanced at the
preferred basking temperature of each turtle species. These results suggest that righting might be
coadapted to preferred basking temperature in freshwater turtles. Also, M. leprosa required
longer times to right on average than T. scripta, what denotes a higher efficiency of introduced T.
scripta at righting performance. This might favor the expansion of exotic sliders in the new
environments in which they are introduced, in detriment of native Spanish terrapins.
A
ccording to the thermal coadaptation hypothesis, the preferred
temperature (Tset) of a species should match the thermal optimum (To)
of thermally sensitive processes that influence fitness (Huey and
Bennett 1987; Angilletta et al. 2006). In ectotherms such as reptiles,
temperature is the major limiting factor affecting locomotor performances,
which are determining in critical activities such as foraging, mating, or predator
avoidance (Huey 1982; Irschick and Garland 2001). Thus, coadaptation between
Tset and To for locomotion is present in many reptile species, including lizards
(Bauwens et al. 1995; Angilletta et al. 2002) and snakes (Stevenson et al. 1985;
Blouin-Demers et al. 2003). However, it has been claimed recently that Tset and
To might not be coadapted for locomotor performances in turtles with
pronounced aerial basking behavior, since individuals usually lose the heat
gained from basking very rapidly when entering the water (Ben-Ezra et al.
2008).
A locomotor activity of special interest in turtles is the ability of righting.
Turtles may result overturned in natural environments while climbing or
competing for solaria, during male fights, or as consequence of predatory attacks
(Corti and Zuffi 2003; Stancher et al. 2006). In these cases, the capacity of
turtles to right is critical to survival, as turtles in an upside-down position are
CAPÍTULO 6: Temperatura corporal y respuesta de ‘giro’
Keywords
Freshwater turtles • Invasive species • Mauremys leprosa • Preferred basking
temperature • Righting performance • Trachemys scripta
125
particularly exposed to predators, changes in body temperature (Tb) and
dehydration, and may experience difficulties to breathe (Burger 1976; Finkler
1999; Steyermark and Spotila 2001; Martín et al. 2005). Righting performance
has been shown to be uncorrelated with swimming and other locomotor
performances in turtles (Elnitsky and Claussen 2006), what suggests that
righting might be subject to different coadaptation pressures. Because most
critical righting behavior occurs mainly on land, where turtles can maintain
substantially higher Tbs, it might be possible that selective pressures favor the
convergence between preferred basking temperature and To for righting
performance in aquatic turtles. By regulating Tb to approach To, turtles may
benefit from a positive effect on their lifetime fitness. Thus, a strong thermal
dependence of righting has been observed in a variety of turtle species
(Steyermark and Spotila 2001; Freedberg et al. 2004; Elnitsky and Claussen
2006). More recently, Ben-Ezra et al. (2008) found that Tset encompasses To for
righting in the northern map turtle (Graptemys geographica), an active aerial
basker. However, enough evidence for coadaptation between Tset and To for
righting in aquatic turtles is not yet provided, and the relationship between
behavioral thermoregulation and locomotor performances in turtles with
striking aerial basking remains unclear.
In this study, we analyzed the effect of body temperature on righting
behavior of two species of freshwater turtles which actively bask on air: the
Spanish terrapin (Mauremys leprosa) and the red-eared slider (Trachemys
scripta elegans). The Spanish terrapin is widespread in the south and central
Iberian Peninsula and northwestern Africa (Keller and Busack 2001). However,
this species has suffered a considerable recession during the last decades, being
currently considered as an endangered species (Pleguezuelos et al. 2002).
Besides habitat destruction and human pressure, the remainder populations
endure competition with exotic introduced turtles, mainly American sliders (Da
Silva and Blasco 1995; Pleguezuelos 2002; Vilà et al. 2008). Although the nature
of the interspecific interactions between native and introduced turtles is not
completely clear, recent studies have pointed out to diverse competitive
advantages of sliders over Spanish terrapins, such as a more accurate assessment
of predatory risk in altered habitats, displacement of native turtles mediated by
chemical cues avoidance, or a greater thermal inertia that favors heat retention
(Polo-Cavia et al. 2008, 2009a,b). Both M. leprosa and T. scripta turtles are
predominantly aquatic, but they actively bask on land to attain and maintain Tb
within the intervals necessary for their daily activities (Meek 1983; Gibbons
1990). During basking bouts, turtles are extremely alert and vigilant, as they are
potential prey of birds and mammals (Martín and López 1990; López et al.
2005). In such vulnerable situations, overturning accidentally may have serious
or even lethal consequences for turtles, if they are not efficient at self-righting.
126
CAPÍTULO 6: Temperatura corporal y respuesta de ‘giro’
Righting response of turtles consists of two different stages, the lag time
(time elapsed to response) and the mechanical righting time. The first time
represents the behavioral decision of turtles of when to right, while the second
one depends mainly on physical traits and physiological state of turtles
(Steyermark and Spotila 2001; Elnitsky and Claussen 2006). During the lag
phase, turtles must accurately assess the costs of remaining overturned vs. those
of returning to prone position, and properly determine the optimal time to
initiate righting, basing on this trade-off. Similarly, turtles adjust the time spent
inside refuges or withdrawn within the shell so that the optimal time to emerge
is the time when the costs of staying equal the costs of leaving (Sih 1992, 1997;
Martín et al. 2005; Cooper and Frederick 2007; Polo-Cavia et al. 2008).
Specifically, overturned turtles may suffer increased predation exposure,
overheating or difficulties to breath, but righting response requires from a
particular energy effort related with variables such as health and nutritional
state or temperature, which may also vary over time. In this way, the decision
of when to start righting (i.e., the duration of the lag phase) may be determined
by expectancy of turtles on righting success, which depends on individual
intrinsic variables and external factors that affect their physiological response,
On the other hand, once a turtle decide to right, the righting response basically
relies on its temperature-dependent locomotor performance and physical traits.
Morphological comparisons indicate that factors such as neck-length to
carapace-height ratio, tail length or shell height and width influence the tactic
and efficiency of turtles at mechanical righting (Rivera et al. 2004; Domokos
and Várkonyi 2008). Thus, righting performance should be determined by
accuracy of turtles during the lag time in assessing risk and own capabilities to
return to prone position, and by their specific morphology and physical skills
during the mechanical phase. However, righting might be also influenced by
environmental factors affecting physiological performance, especially
temperature.
Interspecific differences in behavioral responses to predation risk have been
found between Spanish terrapins and introduced sliders (Polo-Cavia et al.
2008), as well as anatomical differences in carapace size and shape, what
suggests that these two turtle species might also differ in efficiency of righting
response. Also, preferred basking temperature and optimal righting
performance might be differently related in Spanish terrapins and sliders. We
hypothesized that righting responses of M. leprosa and T. scripta might be
determined by species specific risk-sensitive decisions and/or morphological
traits. But also, we hypothesized that there might be interspecific differences in
the effects of Tb of turtles on righting performance, which might differentially
affect mechanical aptitudes of turtles to perform righting, and thus, risk
assessment during the lag phase. We compared behavioral and mechanical
127
aspects of righting response of native M. leprosa and introduced T. scripta
turtles, examining their relation with Tb of turtles. Our objectives were to
determine 1) whether interspecific differences in righting response exist, 2)
whether Tb affects differentially the righting performance of native and invasive
turtles, and 3) whether possible behavioral asymmetries in righting response
between the two turtle species might contribute to the greater competitive
ability of introduced T. scripta. Finally, 4) to explain whether possible
differences between M. leprosa and T. scripta were due to dissimilarities in
morphology that might affect mechanical righting, we compared their carapace
height-to-width ratios, sphericity and flatness indexes, and tail-length-to-size
ratios, and analyzed within species the effects of sphericity and flatness indexes
and tail-length-to-size ratio on mechanical righting times of turtles.
METHODS
Study animals
During May 2007, we captured with baited funnel traps 14 individuals of native
Spanish terrapins (M. leprosa) (carapace length: mean ± SE = 14.9 ± 0.3 cm,
range = 12.5-16.3 cm) in several ponds and creeks of the Guadiana River at
Olivenza (Badajoz Province, southwestern Spain). These freshwater habitats,
located inside dehesa woodlands with scattered holm oak (Quercus ilex) held an
important population of Spanish turtles. We also obtained 13 introduced redeared sliders (T. scripta) (carapace length: mean ± SE = 14.3 ± 0.6 cm, range =
11.3-17.4 cm), from a large pond located in Madrid Province (central Spain),
where they had been maintained under seminatural conditions by the
conservationist private organization “EXOTARIUM” (Exotic Animal Rescue
Center). These sliders had been recently extracted from introduced populations
in central Spain to preserve the original ecosystem balance. None of the turtles
presented shell imperfections that might hinder righting success.
Turtles were individually housed at “El Ventorrillo” Field Station
(Navacerrada, Madrid Province), in outdoor aquaria (60 x 40 x 30 cm) that were
filled with water and provided with stones that allowed turtles to bask. Turtles
were maintained under natural temperatures and photoperiods and fed small
pieces of commercial compound feed three times per week. We held turtles in
their home-aquaria for at least two weeks before testing, so that they became
familiarized with captivity conditions. During this time, we minimized contact
with animals to avoid habituation to the experimenter that could affect risk
assessment during trials. At the end of experiments, all turtles had maintained
or increased their body mass, and were returned to the EXOTARIUM’s pond
(sliders) or to their exact field capture sites (Spanish terrapins).
128
Morphological traits
We compared morphological traits of M. leprosa and T. scripta basing on
biometric measures of turtles. Four parameters: CL (carapace straight length),
CW (carapace straight width at the 6-7 marginal scutes joint), CH (maximum
carapace height), and TL (tail length) were measured with a digital caliper
(Mitutoyo) to the nearest mm. Thus, we estimated carapace height-to-width
ratio as CH / CW and tail-length-to-size ratio as TL / CL. Carapace height-towidth ratio approximates shell geometry and has been used to classify turtle
species into equilibrium classes determining the strategy and efficiency of
righting (Domokos and Várkonyi 2008). On the other hand, higher values of
tail-length-to-size ratio might favor mechanical righting (Rivera et al. 2004).
We also estimated sphericity and flatness indexes of both species of turtles,
using Krumbein’s Sphericity Index (SI) (Krumbein 1941) and Cailleux’s Flatness
Index (FI) (Cailleux 1947):
13
⎛ qr ⎞
SI = ⎜⎜ 2 ⎟⎟
⎝p ⎠
FI =
p+q
2r
Experimental procedure
We carried out experiments in outdoor enclosures with a substrate of uniform
low grass. Trials were performed on sunny days, at an ambient temperature of
approximately 25 °C. We tested each subject turtle at three different
temperatures (15 °C, 20 °C and its species-specific Tset). Tsets were estimated as
the upper set point temperature (USP) selected by turtles in a basking device
(see below). The Tb at which turtles cease basking and shift to water represents
properly the upper bound of Tset and can be precisely determined. For this
reason, it can be considered an appropriate measure of Tset associated with
maximizing processes in which performance increases continuously to To and
then sharply decreases (Kingsbury 1993, 1999; Tosini and Avery 1994; Ben-Ezra
et al. 2008; Dubois et al. 2008). Thus, we considered USP of basking as an
appropriate measure of Tset that should maximize righting performance in
turtles under the coadaptation hypothesis.
CAPÍTULO 6: Temperatura corporal y respuesta de ‘giro’
where p, q and r were given by CL, CW and CH, respectively (see Polo-Cavia et
al. 2009b). Higher values of sphericity index and lower values of flatness index
mean a more rounded shell, which entails lower energy barriers between stable
and unstable equilibria (Domokos and Várkonyi 2008).
129
We determined the USPs of M. leprosa and T. scripta as the average USPs of
all experimental individuals of each respective species. To allow turtles to bask
until they attained USP, we used an infrared heat reflector (250 W, 250 V). An
aquarium equal to the ones used to house the turtles was placed indoor
(ambient air temperature in the laboratory was kept at 20 ± 1 °C) and filled with
10 L water at ambient temperature. A brick (24 x 11.5 x 7 cm) was placed in the
center of the aquarium, emerging 3 cm above the water surface and the heat
reflector was situated hanging 30 cm over the brick. In this way, we simulated a
basking place located in a body of water reflecting average temperature
conditions in the natural environment of turtles. Turtles were initially cooled
inside a thermostatic chamber, in order to encourage them to bask. We
monitored Tb of each turtle inside the chamber and during the whole time of
basking using HOBO U-12 data loggers with HOBOware Pro Software for
Windows (Onset Computer Corporation). A cloacal probe (38 ga copperconstantan thermocouple; temperature range: -200 to 100 °C; precision: ± 1.5
°C; resolution: 0.1 °C) was inserted into each turtle’s cloaca (see Polo-Cavia et al.
2009b for a detailed description). Previous studies have shown that cloacal
temperatures of turtles were highly correlated with air and water temperatures
immediately surrounding turtles (Obbard and Brooks 1981; Ernst 1982; Wilson
1994), and with internal Tb (Edwards and Blouin-Demers 2007; Ben-Ezra et al.
2008; Dubois et al. 2008). Therefore, we assumed that cloacal temperature was a
reasonably accurate estimate of turtles Tb. When Tb stabilized at 15 °C, we took
the turtle out of the chamber and carefully placed it on the plastron over the
brick’s surface. Thereafter, we left the turtle undisturbed for one hour in the
aquarium. Turtles were used to handling and they normally basked as they did
in their home aquaria. USP values were recorded by data loggers right before
the turtles dipped into the water, and consequently, the Tb started to decrease to
water temperature (20 °C). Results showed that M. leprosa selected significantly
higher average USP values (mean ± SE = 30.6 ± 1.0 °C) than T. scripta (27.5 ± 0.7
°C) after removing the effect of size (General Linear Model, F = 9.36, df = 1,24,
P = 0.005).
For righting trials, we carried M. leprosa and T. scripta turtles to three
different testing temperatures, placing each turtle inside the thermostatic
chamber, until Tb stabilized at 15 °C, 20 °C, or its species-specific USP. Then, we
took the turtle out of the chamber, rapidly removed the cloacal probe and
placed the turtle upside down in the outdoor enclosure with short grass
substrate to start the test. From the moment that turtles were released upside
down on the grass, they typically spent some time entirely withdrawn in the
shell, after which they put the head partially out and scanned the surroundings.
Then, turtles put the head, neck and legs entirely out from the shell, and started
to right. From a hidden position, we used a stopwatch to record, to the nearest
130
second: (1) the time at the first contact of the head or a limb with the substrate
since the turtle was turned over on its back on the grass (‘latency time’), and (2)
the time for a turtle to right itself since it initiates righting (‘time to right’).
These two different measures have been used before to analyze the two
different components of the righting response of turtles (Steyermark and Spotila
2001; Elnitsky and Claussen 2006; Delmas et al. 2007). While the first time
represents the lag time, the second time informs about mechanical skills and
physiological state of turtles to right. Turtles were given 900 s to start righting
and 900 s in addition to return to prone position.
Tests with different temperatures were performed in a random order and
each turtle participated in only one trial per day to minimize the influence of
stress resulting from one test on the results of subsequent tests. To avoid
confounding effects that may affect risk assessment, all turtles were handled by
the same person, who performed all the experiments in a standardized way.
Times of turtles inside the thermostatic chamber were similar between
individuals and species, so we discarded possible effects of different stress levels
induced by handling on response times of turtles.
We used two-way repeated measures analyses of variance (ANOVAs) to test for
differences in latency time and time to right of the same individual turtle at the
three different testing temperatures. Temperature was included as a withinsubject factor and the turtle species as a between-subject factor. We also
included the interaction in the models to analyze whether the effects of
temperature changed between species. Previous analyses showed that sex did
not influence latency time or time to right and, thus, sex was excluded in final
analyses. Righting response times were not normally distributed, so we
transformed all data using Box-Cox transformation (Sokal and Rohlf 1995). We
verified normality by Shapiro-Wilk’s test and tested for homogeneity of
variances (Levene’s test). Pairwise comparisons were made using Tukey’s
honestly significant difference tests (Sokal and Rohlf 1995).
We compared carapace height-to-width ratio, sphericity and flatness
indexes, and tail-to-length ratio of M. leprosa and T. scripta turtles using oneway ANOVAs. To analyze the effects of sphericity and flatness indexes and tailto-length ratio on time to right of the two turtle species, we used simple linear
regressions.
CAPÍTULO 6: Temperatura corporal y respuesta de ‘giro’
Statistical analyses
131
RESULTS
Latency time
There were no significant differences between M. leprosa and T. scripta in
overall latency time that they remained waiting before the initiation of righting
(two way-repeated measures ANOVA, species: F = 0.66, df = 1,25, P = 0.42).
However, we found a significant effect of Tb on latency time of turtles (F =
18.73, df = 2,50, P < 0.0001), and the interaction between species and turtles’ Tb
was significant (F = 7.70, df = 2,50, P = 0.001). Thus, while latency times were
independent of Tb in T. scripta (Tukey’s tests, P ≥ 0.68 in all cases), in M. leprosa
latency times were significantly greater at 15 °C than at 20 °C (P = 0.0002), and
than at USP of turtles (P = 0.0001) (Fig. 6.1a). However, differences between
latency time of M. leprosa at 20 °C and at USP of turtles were non-significant (P
= 0.89). The two turtle species did not significantly differ in latency time at any
of the testing temperatures (P ≥ 0.63 in all cases).
Time to right
We found significant differences between the two species of turtles in overall
time required to return to prone position since they started to right (two wayrepeated measures ANOVA, species: F = 11.60, df = 1,25, P = 0.002), with lower
time to right in T. scripta (mean ± SE = 78 ± 34 s) than in M. leprosa (151 ± 33 s).
Time to right was significantly influenced by Tb of turtles (F = 23.64, df = 2,50, P
< 0.0001). Thus, time to right was greater at 15 °C than at 20 °C (Tukey’s test, P
= 0.001) or at USP of turtles (P = 0.0001), and greater at 20 °C than at USP (P =
0.007) (Fig. 6.1b). The interaction between species and Tb of turtles was nonsignificant (F = 0.67, df = 2,50, P = 0.52). Therefore, Tb similarly affected the
time to right of both M. leprosa and T. scripta.
Effects of morphological traits
There were no significant differences between M. leprosa and T. scripta in
carapace height-to-width ratio (one-way ANOVA, F = 0.05, df = 1,25, P = 0.82)
(M. leprosa: mean ± SE = 0.51 ± 0.01; T. scripta: 0.51 ± 0.01). Differences
between the two turtle species in sphericity and flatness indexes were
significant (one-way ANOVAs, F = 87.63, df = 1,25, P < 0.0001 and F = 11.85, df
= 1,25, P = 0.002 respectively), being M. leprosa more flattened (sphericity
index: mean ± SE = 0.64 ± 0.004; flatness index: 2.37 ± 0.04) and T. scripta more
rounded (sphericity index: 0.70 ± 0.01; flatness index: 2.19 ± 0.04). However,
interindividual variation in time to right within each species were not
132
a)
Figure 6.1 Mean (± SE) of (a) latency time
T. scripta
M. leprosa
500
Latency time (s)
400
300
200
and (b) time to right of T. scripta and M.
leprosa, representing behavioral and
mechanical components of the righting
response at three different body
temperatures: 15 °C, 20 °C, and the speciesspecific preferred basking temperature (USP)
of turtles
100
0
15
20
USP
Body temperature (ºC)
b)
500
T. scripta
M. leprosa
Time to right (s)
400
300
200
0
15
20
USP
Body temperature (ºC)
significantly correlated with any of the two indexes (Pearson’s correlations,
sphericity index, M. leprosa: r ≤ -0.40, F ≤ 2.24, df = 1,12, P ≥ 0.16 in all cases, T.
scripta: r ≤ -0.40, F ≤ 2.08, df = 1,11, P ≥ 0.18 in all cases; flatness index, M.
leprosa: r ≤ 0.38, F ≤ 2.06, df = 1,12, P ≥ 0.18 in all cases, T. scripta: r ≤ 0.42, F ≤
2.41, df = 1,11, P ≥ 0.15 in all cases).
We also found significant differences between species in tail-length-to-size
ratio (one-way ANOVA, F = 10.46, df = 1,24, P = 0.004), with greater values for
M. leprosa (mean ± SE = 0.46 ± 0.02) than for T. scripta (0.35 ± 0.02). However,
the effect of tail-to-length ratio on times to right of M. leprosa and T. scripta
within each species was not significant at any of the testing temperatures
(Pearson’s correlations, M. leprosa: r ≤ 0.28, F ≤ 0.92, df = 1,12, P ≥ 0.36 in all
cases; T. scripta: r ≤ 0.17, F ≤ 0.34, df = 1,11, P ≥ 0.57 in all cases).
CAPÍTULO 6: Temperatura corporal y respuesta de ‘giro’
100
133
DISCUSSION
Our results revealed clear differences between M. leprosa and T. scripta in
behavioral and mechanical components of the righting response. Although
lengths of latency time that native and introduced turtles remained waiting
before the initiation of righting did not significantly differ, the lag phase was
independent of Tb in T. scripta, but not in M. leprosa, suggesting that risk
assessment during overturning is more influenced by Tb in M. leprosa than in T.
scripta. Also, although mechanical phase of the two turtle species similarly
speeded up with increasing temperatures, M. leprosa required longer times on
average to right than T. scripta, regardless of temperature, which suggests a
higher efficiency of mechanical righting in introduced sliders.
Righting performance entails important costs for turtles, such as revealing
the own presence to possible predators, and in particular, the great energy
expenditure to overcome gravity. However, overturned turtles are especially
exposed to suffer increased predation risk, overheating or rather serious
difficulties at breathing that may lead turtles to critical conditions (Rivera et al.
2004; Stancher et al. 2006). Because both righting performance and overturning
entail costs, turtles must accurately decide when to right, in order to maximize
righting response. Thus, turtles should optimize the decision of when to initiate
righting, by balancing righting energy inputs with costs of remaining
overturned, in a similar way that prey respond to predators by accurately
assessing risk level to decide when to change between alternative antipredatory
tactics that entail different costs (Lima and Dill 1990; Sih 1997). Supporting this,
Martín et al. (2005) observed experimentally that, after a simulated predatory
attack, overturned M. leprosa adjusted their righting decisions basing on
persistence of predators and proximity to water. In consequence, lag phase of
righting is determined by environmental factors such as level of predatory
threat, overheating and/or dehydration risks. But also, latency time is
influenced by expectancy of turtles on their own mechanical righting response,
which depends on intrinsic variables (i.e., morphology and physical skills), and
physiological performance of turtles that may vary over time with health and
nutritional state, or more unpredictably, with Tb of turtles.
Overall latency times of M. leprosa and T. scripta were similar, what might
initially suggest that confidence of native and introduced turtles in their own
capacities to perform righting was similar (as environmental variables affecting
risk assessment were constant in our experiment). However, times to right of
M. leprosa were almost two times longer on average than those of T. scripta,
what indicates that sliders are more efficient at mechanical righting than
Spanish terrapins. Therefore, one would expect that T. scripta turtles showed
lower latency times in comparison with those of M. leprosa terrapins, according
134
CAPÍTULO 6: Temperatura corporal y respuesta de ‘giro’
with an accurate perception of turtles of their own capabilities to perform
righting. Similarities in lengths of lag phase between the two turtle species
might then be explained by asymmetries in risk assessment between Spanish
terrapins and sliders that might compensate the higher confidence in righting
success of introduced T. scripta. For example, predation threat while
overturning might differ between M. leprosa and T. scripta, which have evolved
within dissimilar predatory-systems in their original assemblages (i.e., predation
threat is mainly posed by terrestrial mammals and birds in the Iberian
Peninsula, while a great variety of aquatic predators are present in the original
habitats of sliders). In agreement with the hypothesis of divergences in risk
assessment between the two turtle species, we observed in a previous study
that, after a simulated predatory attack on land, T. scripta exceeded M. leprosa
in length of time that turtles spent withdrawn into the shell before emerging
and escaping, likely waiting for the predator to abandon the surroundings and
thus, avoiding potential encounters with more dangerous aquatic predators
(Polo-Cavia et al. 2008). On the other hand, overheating risk perceived while
overturned by sliders might be lower than that perceived by native terrapins, as
introduced T. scripta presents greater thermal inertia, and therefore, heat gain is
slowed down in this species (Polo-Cavia et al. 2009b). This might also explain
that sliders waited for longer than we expected before starting to right. Finally,
we cannot discard that other interspecific differences, such as a more protecting
shell of T. scripta, or a more constrained physiology of M. leprosa in an upsidedown position, might also explain the lack of significant differences in latency
times of native and invasive turtles, even when they greatly differed in
efficiency of mechanical righting.
Testing temperature did not significantly affect latency times of T. scripta,
what suggests that risk assessment during overturning in T. scripta is less
dependent on turtles’ Tb. In contrast, lag phase of M. leprosa was greater at 15
°C than at 20 °C or at preferred basking temperature of the species, but lag time
was not significantly greater at 20 °C than at the preferred basking temperature.
It might be possible that extremely low Tbs discourage M. leprosa from turning
right-side up, since in such motionless conditions, the highly increased costs of
performing righting might induce turtles to remain for longer onto their
carapaces. However, the elevated costs of remaining overturned, and
consequently, the strong selective pressure for turtles to right might minimize
differences between motivation of turtles to perform righting at 20 °C and at
preferred basking temperature, despite the fact that a non-optimal Tb could lead
turtles to wait for a longer time in an upside-down position before starting to
right. Therefore, only when M. leprosa turtles are extremely cold, the costs of
righting seem to incline turtles to remain for longer onto their carapaces.
Likewise, the absence of relation between latency times and Tb of turtles in T.
135
scripta might rely on the short times that they employed to perform righting,
compared with those of M. leprosa. A high efficiency of mechanical righting
might likely reduce the effect of temperature on risk assessment, explaining that
none of the testing temperatures was low enough to incline sliders to assume
overturning costs for longer times. Although, it is also possible that the lower
preferred basking temperature of T. scripta, which implied less variability
between the three testing temperatures, contributes to explain the absence of
differences between latency times found in this species.
Interspecific differences in mechanical righting times between the two
turtle species must rely on dissimilar specific morphologies and mechanical
skills. Recently, Domokos and Várkonyi (2008) established equilibrium classes
of turtles and their relation to righting behavior, basing on geometric measures
of the shell. They concluded that righting strategy of turtles was basically
determined by carapace height-to-width ratio, since this parameter was enough
to approximate shell geometry. According with Domokos and Várkonyi’s (2008)
models, both M. leprosa and T. scripta turtles from our experiment fell within
‘flat turtles’ class, which present two stable equilibria (one on the plastron and
one opposite, on the carapace), and a high energy barrier between stable and
unstable equilibria. Since flat turtles with high energy barriers use primarily
their necks for righting (Rivera et al. 2004; Domokos and Várkonyi 2008), neck
length should be considered the main factor of available biomechanical energy
to right in both M. leprosa and T. scripta. However, our geometric models of
turtles, based on sphericity and flatness indexes of the shell, have yielded
morphological shape differences between M. leprosa and T. scripta (i.e., Spanish
turtles being more flattened, sliders more rounded, Polo-Cavia et al. 2009b; this
study), which might also play a role in determining the physical skills of the
two turtle species to right, jointly with interspecific asymmetries in neck
length. Thus, although both M. leprosa and T. scripta turtles from our
experiment were considered ‘flat turtles’, Spanish terrapins are more flattened
than sliders, which show a more rounded shell that likely endows them with a
lower energy barrier between stable and unstable equilibria, thus requiring less
time to right. However, mechanical righting times of M. leprosa and T. scripta
were not significantly correlated within each species with sphericity or flatness
indexes of turtles at any of the testing temperatures, likely due to the effect of
individual differences in more determining variables such as neck length. Tail
length has also been claimed to influence mechanical phase of righting (Rivera
et al. 2004). However, although M. leprosa showed clearly greater tail-lengthto-size ratios than T. scripta, M. leprosa took more time to right than T. scripta.
Also, tail-length-to-size ratio was not correlated within each species with times
to right of turtles. This suggests, in agreement with previous studies, that tail
length is not a primary factor determining righting in flat turtles.
136
CAPÍTULO 6: Temperatura corporal y respuesta de ‘giro’
Mechanical righting performance of both M. leprosa and T. scripta were
similarly affected by Tb. Turtles took less time to return to prone position as Tb
approached their species-specific preferred basking temperature. Because
physiological performances in ectotherms typically increase with Tb up to a
species and process specific To, after which it steeply decreases (Huey 1982),
reptiles are expected to select Tbs that maximize locomotion. However, aquatic
turtles with pronounced aerial basking have been claimed to be an exception,
since the elevated Tb achieved on land could hardly improve locomotor
performances during the vital activities that they normally develop in water
(e.g., foraging or mating) (Ben-Ezra et al. 2008). Nevertheless, several studies
have reported a sharp thermal dependence of righting, among other locomotor
performances, in aquatic turtles (Steyermark and Spotila 2001; Freedberg et al.
2004; Elnitsky and Claussen 2006). In agreement with them, our results indicate
that righting behavior of M. leprosa and T. scripta is enhanced at their specific
preferred basking temperatures, further suggesting that selected Tbs might be
related to locomotion, or at least, to righting performance, in freshwater turtles.
Recently, Elnitsky and Claussen (2006) showed that righting response of
juvenile western painted turtles (Chrysemys picta bellii) was uncorrelated with
other terrestrial and aquatic locomotor performances. This suggests that
righting might represent a different locomotor trait following different adaptive
forces. Righting constitutes a risky manoeuvre in which a great effort is
required to overcome the energy barrier of the unstable equilibrium at the
turtle’s side. However, there is a strong selective pressure for turtles to right, as
while overturned, they are specially exposed and vulnerable. For these two
reasons, maximizing righting performance by regulating Tb seems to be an
ability of considerable adaptive value, even for aquatic turtles.
In addition, righting performance is considered an indicator of fitness in
freshwater turtles (Delmas et al. 2007). Since efficiency of righting varies
significantly with Tb in M. leprosa and T. scripta turtles, individuals that attain
and maintain Tbs that approach To will benefit from a positive increment in
fitness. Thus, considering that righting performance of the two turtle species is
speeded up at their respective species-specific preferred basking temperatures,
the higher thermal inertia of exotic T. scripta turtles might confer them a
competitive advantage over Spanish terrapins (Polo-Cavia et al. 2009b). Due to
their greater capacity to retain heat, sliders might maintain preferred
temperatures after basking for longer times than native turtles, whose higher
tendency to loss body heat would make them more dependent on basking to
maintain selected Tbs (Polo-Cavia et al. 2009b). Then, in a competitive situation
in which introduced turtles actively displace native terrapins from the basking
places and impede them to adequately bask (Polo-Cavia et al. in press), Spanish
turtles might not be able to maintain the elevated Tbs that optimize righting.
137
Also, T. scripta requires shorter times to turn right-side up than M. leprosa,
likely due to their more rounded shell and specific anatomy of its neck, which
might facilitate mechanical righting. In this way, introduced sliders could avoid
the long exposure to potential predators and overheating risk while overturning
that Spanish terrapins might have to endure. In addition, M. leprosa turtles are
more prone to suffer a successful predatory attack during the time that they
remain overturned, as more flattened turtles are more easily caught by snapping
jaws or avian predators (Pritchard 1979; Janzen et al. 2000). Also, more rounded
shells confer higher thermal inertias that protect turtles from desiccation and
improve thermoregulation (Carr 1952; Wyneken et al. 2008; Polo-Cavia et al.
2009b). Thus, the lower thermal inertia of native turtles, compared with that of
exotic ones, entails an increased risk of overheating if turtles become exposed to
intense sun rays before they can return to their normal position and shift to a
sheltered place. On the other hand, under extremely low temperatures, M.
leprosa experiences a considerable increment in lengths of lag phase and
mechanical stage of righting performance, which might exceedingly prolong
the time overturned, thus compromising the survival of turtles. In contrast, T.
scripta might minimize the risks of overturning by means of a more rounded
shape that deters predators and facilitates righting, and a greater thermal inertia
that protects turtles from overheating and favors the maintenance of selected
Tbs that allow a highly efficient righting performance. Hence we can conclude
that behavioral asymmetries in righting response between native and invasive
turtle species might contribute to the greater competitive ability of T. scripta,
thus favoring the expansion of sliders and aggravating the conservation state of
populations of Spanish terrapins in environments in which exotic turtles are
introduced.
Acknowledgements We thank A. Marzal for allowing field work in his dehesa state (“La
Asesera”), the Exotic Animal Rescue Center “EXOTARIUM” for providing red-eared sliders, and
“El Ventorrillo” MNCN Field Station for use of facilities. V. Polo helped with useful comments on
data transformations. Financial support was provided by a MCI project CGL2008-02119/421 BOS,
and by a MEC-FPU grant to N. P.-C. The experiments enforced all current laws of Spain and of
the Environmental Organisms of the “Junta de Extremadura” and “Comunidad de Madrid” where
they were performed.
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Capítulo
7
Las diferencias interespecíficas en las respuestas al riesgo de depredación pueden conferir ventajas competitivas a las especies invasoras de galápagos Nuria Polo Cavia, Pilar López y José Martín
Ethology 114 (2008) 115-123
RESUMEN
142
La naturaleza de las interacciones competitivas entre especies
nativas e introducidas no está clara. En la Península Ibérica,
el galápago de Florida (Trachemys scripta elegans) se
encuentra introducido como especie invasora, compitiendo y
desplazando al galápago leproso (Mauremys leprosa). Es
posible que diferencias potenciales en el comportamiento
antidepredatorio de las dos especies puedan conferir ventajas
competitivas al introducido T. scripta. En este estudio,
examinamos si las diferencias interespecíficas en las
respuestas al riesgo de depredación afectan al tiempo que los
galápagos permanecen refugiados en el interior del caparazón
antes de escapar activamente hacia el agua. Ambas especies
de galápagos ajustaron el tiempo que pasaron escondidos en el
caparazón en función del nivel de amenaza depredatoria, el
microhábitat y los costes de mantenerse escondidos. Sin
embargo, los introducidos T. scripta pasaron escondidos más
tiempo que los nativos M. leprosa, los cuales, en contraste,
escaparon rápidamente hacia aguas más profundas. Estas
diferencias interespecíficas podrían deberse a los distintos
tipos de depredadores (terrestres vs. acuáticos) que amenazan
a los galápagos nativos e introducidos en sus respectivos
hábitats originales. Sin embargo, en hábitats alterados
antropogénicamente donde la presencia de depredadores se
ha reducido considerablemente, T. scripta podría evitar los
costes potenciales de repetidas e innecesarias huidas hacia el
agua (e.g., la interrupción de actividades como el
asoleamiento). Estas asimetrías en el comportamiento
antidepredatorio entre las dos especies de galápagos podrían
en parte explicar la mayor capacidad competitiva del
introducido T. scripta en ambientes con modificaciones
antropogénicas ■
INTERSPECIFIC DIFFERENCES IN RESPONSES TO PREDATION RISK
MAY CONFER COMPETITIVE ADVANTAGES TO INVASIVE
FRESHWATER TURTLE SPECIES
Abstract The nature of competitive interactions between native and introduced invasive species
is unclear. In the Iberian Peninsula, the introduced red-eared slider (Trachemys scripta elegans) is
an invasive species that is competing and displacing the endangered native Spanish terrapin
(Mauremys leprosa). We hypothesized that interspecific differences in antipredatory behavior
might confer competitive advantages to introduced T. scripta. We examined whether interspecific
differences in responses to predation risk affect the time that turtles remained hidden in the shell
before using an active escape to water. Both turtle species adjusted hiding times by balancing
predation threat, microhabitat conditions and the costs of remaining hidden. However,
introduced T. scripta showed longer hiding times before escaping than native M. leprosa, which,
in contrast, switched from waiting hidden in the shell to escape to deep water as soon as possible.
These interspecific differences might result from the risk of facing different types of predators in
different microhabitats (land vs. water) in their original habitats. However, in anthropogenically
altered habitats where predators have been greatly reduced, T. scripta may avoid potential costs of
unnecessary repeated escape responses to water (e.g., interruption of basking). These behavioral
asymmetries could contribute to the greater competitive ability of introduced T. scripta within
anthropogenically disturbed environments
Keywords Freshwater turtles • Invasive species • Mauremys leprosa • Microhabitat • Predatory
threat • Trachemys scripta
CAPÍTULO 7: Comportamiento antidepredatorio
T
he introduction of alien species outside their natural geographic range
area represents the second greatest threat to biodiversity after habitat
destruction (Devine 1998; IUCN 2000; Mack et al. 2000). Alien species
may displace native species from their ecological niches by means or processes
such as predation, hybridization, introduction of pathogens, or competition for
resources (Dodd and Seigel 1991; Williamson 1996; Butterfield et al. 1997;
Manchester and Bullock 2000). The outcome of competition processes depends
on the ability of alien species to adapt to strange habitats, as well as on the
ability of native species to resist invasion (Williamson 1996; Joly 2000). Alien
invasive species are often those with wide ecological valence, high reproductive
output, or that tolerate or benefit from human presence (Sax and Brown 2000;
Kolar and Lodge 2001). Invasive species often come from areas with a high
diversity of predators, which may favor these species that are better suited for
evading predators than native species. Even if a species is introduced in a new
habitat with fewer predators, a species subjected to past selection for
antipredatory behavior will retain this behavior (i.e., ‘ghost of predators past’
hypothesis; Peckarsky and Penton 1988; Blumstein 2006). On the other hand,
native species that occupy geographically isolated habitats, which have been
anthropogenically modified and lack predators of alien species, are more prone
to suffer invasions (Fox and Fox 1986; Ewell 1999; Sax and Brown 2000).
143
The American red-eared slider (Trachemys scripta elegans) is currently
introduced as a breeding species in many countries of Africa, Asia and Europe,
especially in Mediterranean countries (Luiselli et al. 1997; Chen and Lue 1998;
Pleguezuelos 2002). In the Iberian Peninsula, T. scripta have been released in
diverse aquatic habitats after having been imported and sold as pets (Pleguezuelos
2002). Many observations indicate that introduced T. scripta are competing
with the two native Iberian freshwater turtle species; the European pond
terrapin (Emys orbicularis) and the Spanish terrapin (Mauremys leprosa). These
native terrapins are considered as endangered species because their populations
have considerably declined (Pleguezuelos 2002). However, the nature of the
interspecific competitive interactions is unclear. Competition for food, refuges
or basking places are likely to occur (Crucitti et al. 1990; Cadi and Joly 2003).
The advantages of T. scripta as an invasive species over native freshwater turtles
might be larger adult body size, more diverse diet, higher fecundity, earlier
sexual maturity, adaptation to lower water temperatures, and a greater tolerance
to pollution and human presence (Gibbons 1990; Pleguezuelos 2002). Also, the
absence of Spanish terrapins in areas with high predation risk occupied by T.
scripta (Pleguezuelos 2002) suggests that the native species is more sensitive to
predation pressure. Although these freshwater turtles are predominately
aquatic, they have to come to land for basking, where they are potential prey of
birds and mammals (Greene 1988; Martín and López 1990). For this reason,
they are very cautious, being extremely alert and vigilant, and diving quickly
when disturbed. However, this seems to be especially true for native terrapins
in Iberian habitats (López et al. 2005; N. Polo-Cavia, unpubl. data).
Turtles usually escape to a safe refuge such as water or thick vegetation
when they detect danger. However, if a predator approaches close enough,
turtles will withdraw and hide the legs, tail and head inside the shell, trying to
deter the attack (Greene 1988; Hugie 2003). Most predators would leave turtles
alone if they do not come out of the shell. However, some predators are able to
break the shell or to access the soft parts of the turtle’s body (Greene 1988;
Martín and López 1990; see also Mima et al. 2003 for a similar situation in
hermit crabs). Turtles must choose between two alternative antipredatory
tactics (passive hiding or active escape), but both may imply costs. Escaping to
water may be safer in some habitats, but, apart from the energy lost in the
escape sequence (Martín and López 1999a), it supposes an interruption of
basking with a subsequent decrease in the efficiency of digestion under the low
temperatures of water (Parmenter 1981; Huey 1982). Also, in some habitats
entering the water soon after predator detection may expose turtles to aquatic
predators. On the other hand, hiding in the shell allows turtles to continue
basking, but it may decrease time available for mating or foraging (Sih et al.
1990; Koivula et al. 1995; Dill and Fraser 1997; Martín et al. 2003a,b), and this
144
METHODS
Study Animals
During May 2005, we captured 20 adult T. scripta (9 males and 11 females;
carapace straight length: mean ± SE = 15.1 ± 1.5 cm, range = 12.7-17.7 cm) from
CAPÍTULO 7: Comportamiento antidepredatorio
strategy may greatly increase the risk of being damaged at land (Mima et al.
2003).
Prey should adjust time spent inside refuges so that the optimal time to
emerge is the time when the costs of staying exceed the costs of leaving (Sih
1992, 1997; Dill and Fraser 1997; Martín and López 1999b). Also, when using
non-secure refuges, animals should estimate predation threat to decide whether
and when to employ alternative defensive tactics if a predator persists in the
attack (Martín and López 2003). Similarly, in turtles, the decision of when to
emerge from their shells should be a trade-off between the perceived predation
threat and the probability of reaching safe habitat and encountering a novel
predator vs. the costs of remaining within the shell (Sih et al. 1998; Martín et al.
2005). This would require turtles to accurately assess predation threat and
flexibly employ different antipredatory tactics as risk level changes. In the
Iberian Peninsula, we have observed that a simulated terrestrial predator may
approach closer to introduced T. scripta than to native M. leprosa while they
are basking before they plunge in the water (N. Polo-Cavia, unpubl. data). This
suggests that risk perception while basking might be different in native or
invasive turtles, which might be due to the different types of predators in their
original habitats. In this paper, we analyzed whether there were interspecific
differences in responses to predation threat between introduced T. scripta and
native M. leprosa in Iberian habitats. We specifically asked whether differences
in risk assessment may affect the decision of using diverse antipredatory tactics
that have different potential costs. We simulated attacks of different
characteristics (different combinations of several factors of risk posed by the
predator) and under different conditions of proximity to water refuges, which
would contribute to the total estimation of risk. Particularly, we examined how
perceived predation threat affected the time that turtles remained hidden in the
shell before using an active escape strategy. We hypothesized that T. scripta
will remain withdrawn into the shell for longer, trying to deter the predator,
before incurring costs of an active escape. In contrast, M. leprosa will initiate, as
soon as possible, an active flee to deep water. Thus, in habitats where current
human pressure had greatly reduced the numbers of predators, the costs derived
from interruption of basking and repeated unnecessary flees to water (Dill and
Fraser 1997; Sih 1997; Martín and López 1999a) might suppose a disadvantage
for native turtles when competing with introduced ones.
145
a large seminatural outdoor pond where they had been maintained by the
conservationist organization “Grupo de Rehabilitación de la Fauna Autóctona y
su Hábitat” (GREFA). These turtles had been extracted from introduced
populations in central Spain to avoid their negative effects on populations of
native terrapins. We also captured, during May, with funnel traps 16 adult M.
leprosa (9 females and 7 males; carapace straight length: mean ± SE = 15.2 ± 0.5
cm, range = 14.6-19.3 cm) in several ponds and tributary streams of the
Guadiana river, located inside dehesa woodlands with scattered holm oak
(Quercus ilex) at Olivenza and Alconchel (Badajoz Province, southwestern
Spain). In this area, we verified the presence of many known potential
predators of this turtle, including birds such as white storks (Ciconia ciconia),
grey herons (Ardea cinerea), Egyptian vultures (Neophron percnopterus) and
black kites (Milvus migrans), and mammals, such as wild boars (Sus scrofa), and
foxes (Vulpes vulpes) (Martín and López 1990; Andreu and López-Jurado 1998).
All turtles were individually housed at “El Ventorrillo” Field Station
(Navacerrada, Madrid Province), in outdoor aquaria (60 x 40 x 30 cm) with
water and stones that allowed them to bask. The temperature and photoperiod
were the same as the natural surroundings. Turtles were fed mince beef,
earthworms and slugs three times a week. Turtles were held in captivity for at
least two weeks before experiments, to allow turtles to habituate to captivity
conditions. At the end of experiments, all turtles had maintained their body
mass, and were returned to the GREFA ponds (T. scripta) or to their exact field
capture sites (M. leprosa).
Experimental Procedure
We simulated predatory attacks toward individual turtles in an outdoor
transparent plastic container (70 x 60 x 15 cm) with either a substrate of low
grass (‘land’ treatment) or filled with 4 cm deep clean water (‘water’ treatment).
This container was used as a mean to keep water or grass within a controlled
standardized area, but turtles could see all the surroundings and easily go out
from the container, so that their behavior was not restricted by the container
walls. Thus, we simulated two different microhabitat conditions: the turtle was
attacked on land, away from a water pool, or in a shallow water area similar to
river banks, presumably close to deeper water areas (Martín et al. 2005). To
simulate different levels of predation threat, we took one turtle from its
aquarium and after handling it gently for 2 s, we released it in the middle of the
experimental container (‘low predation threat’ treatment). Alternatively, we
handled the turtle for 5 s, left it in the experimental container, and we
continued simulating the attack by handling and tapping the shell with the
hand during 20 s before definitively releasing it (‘high predation threat’
146
Data Analyses
We used repeated measures analyses of variance (ANOVAs) to test for
differences in appearance and waiting times of the same individual turtle in
each condition of microhabitat (land vs. water), perceived predation threat (low
vs. high) and predator persistence (close vs. far), all of them within factors. The
turtle species was included as a between-subjects factor. Data were logtransformed to ensure normality (verified by Shapiro-Wilk’s test) and we tested
for homogeneity of variances (Levene’s test). Pairwise comparisons were made
using Tukey’s honestly significant difference tests (Sokal and Rohlf 1995).
CAPÍTULO 7: Comportamiento antidepredatorio
treatment). Thereafter, and without further handling, the experimenter
simulated either a persistent waiting predator by remaining immobile at a point
close to the container (<1 m; ‘close’ treatment), or a predator that left the area to
a hidden position at a distance of 8 m (‘far’ treatment). To avoid confusing
effects that may affect risk perception, all experiments were performed by the
same person, in a similar way and wearing the same clothes (Burger and
Gochfeld 1993).
We tested each individual turtle under all the eight possible combinations
of treatments, and order of presentation of treatments was randomized. Each
turtle participated in only one trial per day to minimize the influence of stress
resulting from one test on the results of subsequent tests. Before the trials,
turtles were allowed to bask for at least 2 h in their home aquaria, so that they
could attain optimal body temperatures (Andreu and López-Jurado 1998). We
ensured that ambient temperature was similar during all tests.
After the attacks, and as a result of handling, turtles usually remained
withdrawn into the shell (head, legs and tail were not visible from above the
carapace). After some time spent entirely withdrawn in the shell, turtles
typically put the head partially out from the shell until the eyes could be used
to scan the surroundings. Then, turtles waited for a while, and finally put the
head, neck and legs entirely out from the shell, and started to walk. We used a
stopwatch to record, to the nearest second, the time that turtles spent
withdrawn inside their shell after release into the container until the head
emerged and the eyes were out of the carapace (appearance time). We then
measured the time from appearance until the head and legs emerged completely
and the turtle started walking (waiting time). These two hiding times were
considered because turtles entirely withdrawn into the shell had no visual
information of the predator or the surroundings until the ‘appearance time’.
Thus, ‘waiting time’ represented the time during which the turtle could visually
scan the environment, and decide whether and when to switch to active escape
toward safer refuges (Martín and López 1999b; Martín et al. 2005).
147
RESULTS
Appearance Time
The two turtle species differed significantly in the length of time they remained
entirely hidden inside their shells after a staged predatory encounter (repeated
measures ANOVA, F = 7.92, df = 1,32, P = 0.008), with T. scripta having longer
overall appearance times (mean ± SE = 19 ± 5 s) than M. leprosa (5 ± 6 s). There
were no significant differences between sexes in appearance time for either
turtle species (sex: F = 0.01, df = 1,32, P = 0.96; sex x species: F = 0.02, df = 1,32,
P = 0.88). Thus, sex was not considered in further analyses.
Despite the magnitude of differences in appearance times between species,
the effects of microhabitat and perceived predation threat were similar for both
turtle species (i.e., no interaction with species). Appearance times were
significantly longer on land than in water, and significantly longer when
perceived predation threat was high than when it was low (Fig. 7.1; Table 7.1).
However, there was a significant interaction between microhabitat and
perceived predation threat. Both turtle species appeared from their shells more
quickly following a low predation threat attack than a high predation threat
attack when they were on land (Tukey’s test, P = 0.0002), but there was no
significant difference in their response to low vs. high predation threat in water
(P = 0.97).
The effect of predator persistence differed significantly between the two
turtle species (interaction: persistence x species; Table 7.1). However, post hoc
Tukey’s tests did not provide any significant result for these differences (P >
0.46 in all cases). The rest of effects and interactions were non-significant
(Table 7.1).
Waiting Time
The two turtle species differed significantly in the length of time they remained
waiting with their heads partially out of the shell until they started walking
(repeated measures ANOVA, F = 34.98, df = 1,32, P < 0.001), with overall
waiting times of T. scripta (174 ± 27 s) being significantly longer than those of
M. leprosa (93 ± 30 s). Waiting time did not significantly differ between sexes in
any turtle species (sex: F = 0.69, df = 1,32, P = 0.41; sex x species: F = 0.10, df =
1,32, P = 0.75). Thus, sex was not considered in further analyses.
Microhabitat and predator persistence affected waiting times of both turtle
species. Thus, overall waiting times were significantly longer on land than in
water, and significantly longer when the predator remained close to the turtle
148
Figure 7.1 Mean (± SE) appearance times
from their shells of (a) introduced T.
scripta and (b) native M. leprosa after an
attack. Six conditions of attacks were
simulated: two different perceived
predation threat levels (‘low’ vs. ‘high’),
two different microhabitats (‘land’ vs.
‘water’) and the experimenter either
remained close to the turtle (‘close’) or
retreated to a distant hidden position
(‘far’)
Table 7.1 Results from three-way repeated measures ANOVAs examining the effects of turtle
Appearance time
Effect
Species
Microhabitat
Microhabitat x species
Predation threat
Predation threat x species
Persistence
Persistence x species
Microhabitat x predation threat
Microhabitat x predation threat x species
Microhabitat x persistence
Microhabitat x persistence x species
Predation threat x persistence
Predation threat x persistence x species
Waiting time
F
P
F
P
8.53
23.16
0.07
11.69
0.35
0.25
6.95
20.29
1.76
2.11
1.43
0.34
1.87
0.006
< 0.0001
0.80
0.0016
0.56
0.62
0.012
< 0.0001
0.19
0.16
0.24
0.56
0.18
35.58
38.16
2.93
1.11
0.25
38.71
2.04
17.30
7.52
15.58
27.41
2.65
0.54
< 0.0001
< 0.0001
0.10
0.30
0.62
< 0.0001
0.16
0.0002
< 0.01
0.0004
< 0.0001
0.11
0.47
CAPÍTULO 7: Comportamiento antidepredatorio
species, microhabitat, perceived predation threat and predator persistence on appearance and
waiting times of turtles (df = 1,34 in all cases)
149
Figure 7.2 Mean (± SE) waiting times of
(a) introduced T. scripta and (b) native M.
leprosa after an attack. Six conditions of
attacks were simulated: two different
perceived predation threat levels (‘low’ vs.
‘high’), two different microhabitats (‘land’
vs. ‘water’) and the experimenter either
remained close to the turtle (close) or
retreated to a distant hidden position (far)
after the attack. However, the effects of predation threat level and predator
persistence depended of microhabitat and differed between turtle species (Fig.
7.2; Table 7.1). Thus, with respect to the interaction ‘microhabitat x predation
threat x species’, predation threat level did not significantly influence waiting
times of T. scripta in either microhabitat (Tukey’s test, P = 0.99 in both cases),
whereas waiting times of M. leprosa were not affected by predation threat level
on land (P = 0.64) but were significantly shorter under high predation threat in
water (P = 0.0007). With respect to the interaction ‘microhabitat x persistence x
species’, waiting times of T. scripta were not affected by predator persistence in
any microhabitat (Tukey’s tests, water: P = 0.14; land: P = 0.64), whereas in M.
leprosa predator persistence was not important in water (P = 0.99), but on land
waiting times were significantly longer when the predator remained close (P =
0.0001). The rest of interactions were non-significant (Table 7.1).
150
Our results revealed that T. scripta and M. leprosa differed in the magnitude of
their hiding responses after a predatory attack. The invasive T. scripta spent
longer times withdrawn into the shell before emerging and switching to an
active escape response. However, despite the magnitude of differences in hiding
times, both turtle species also adjusted the time spent withdrawn into their own
shell by assessing predation threat, and microhabitat conditions.
In response to predators, basking turtles may choose between withdrawing
into their shells and actively escaping to a water source (Martín et al. 2005).
Predators typically would abandon immobile hidden prey (Martín and López
1999a,b; Hugie 2003). However, time spent within the shell implies costs such
as the risk of overheating on land, or the loss of time available for foraging or
mate searching (Martín et al. 2003a,b). But initiating active escape entails other
more important costs for turtles, such as alerting the predator in case it has not
noticed the prey, the energy spending in the dash for flee, and especially the
interruption of basking. Basking is a crucial activity for turtles and other
ectotherms (Huey 1982; Crawford et al. 1983) because increasing body
temperature activates metabolism and digestive turnover rates (Kepenis and
McManus 1974; Parmenter 1981). Therefore, to decide when to change
between these two antipredatory tactics (i.e., duration of hiding times), turtles
must be able to balance all the costs associated to both tactics, the risk of
emerging from the shell before the predator has left (Sih 1992; Hugie 2003), the
possibility of reaching a safer refuge in different microhabitats (Martín et al.
2005), and also the potential risk of predation in water by other types of
predators (Sih et al. 1998). Similar modification of hiding times occurs in sessile
animals hidden inside their defensive structures (Dill and Gillett 1991;
Johansson and Englund 1995; Dill and Fraser 1997), and in mobile animals
hidden in external refuges (Cooper 1998; Martín and López 1999a,b).
Interestingly, our results indicate that the combined effects of these factors
also differed between turtle species. Thus, on land both turtle species appeared
sooner if the risk was low than if it was high, but, in the water, they appeared
quickly from the shell under both predation threat levels as the possibility of
escaping successfully toward safer deep waters is greater than the one of
dissuading the terrestrial predator by remaining hidden. However, T. scripta did
not alter waiting time in response to predation threat, but had shorter waiting
times in the water than on land, whereas M. leprosa did alter their waiting
times in response to predation threat and microhabitat, having shorter waiting
times under high threat compared with low threat in the water, but not on
land.
CAPÍTULO 7: Comportamiento antidepredatorio
DISCUSSION
151
Predator persistence did not affect appearance from shell in any species,
suggesting that when the turtles are withdrawn inside the shell, they could not
visually determine whether a predator was still present (Martín et al. 2005).
Only when turtles had their eyes outside the shell, they can acquire more visual
information on the predator. However, waiting times were not affected by
predator persistence in T. scripta, whereas in M. leprosa, predator persistence
influenced waiting times only when turtles were on land and there were no
other alternative refuges, but not when they could escape toward a safer refuge
in water even if the predator was close.
These interspecific differences in responses to predation risk might be
explained because predators of adult M. leprosa are terrestrial mammals and
birds (Martín and López 1990), and, thus, this turtle species is safer in deep
water, where no predators occur. In contrast, T. scripta elegans comes from an
original habitat with terrestrial predators that prey mainly on young and eggs
(e.g., raccoons, skunks, foxes, raptors and storks), but where the greatest danger
comes from aquatic predators (i.e., caimans and crocodiles), which also attack
adults (Greene 1988). Prey exposed to multiple types of predators can
experience two conflicts; if enhanced survival to one predator simultaneously
increases vulnerability to another predator, or if prey have limitations to
produce only one type of defensive response at a time (Sih et al. 1998; DeWitt et
al. 2000). If prey have a conflict with specific defensive tactics to multiple
predators, and one predator type is more dangerous than the other, then prey
should tend to ignore the less dangerous predator (Lima 1992; McIntosh and
Peckarsky 1999; Bouwma and Hazlett 2001). Thus, in their original habitat,
basking T. scripta should remain hidden inside the shell for longer before
initiating active escape toward the water, since entering quickly in water can
face sliders with other more dangerous aquatic predators. In contrast, basking
M. leprosa should favor the strategy of escaping toward the safety of deep water
whenever possible and immediately after any smallest alarm signal on land
(López et al. 2005). This latter species would use the shell as a refuge only when
it was on land far from water and predator’s harassment was extreme. In
agreement with this prediction, preliminary field observations in Iberian
habitats suggested that a terrestrial predator might approach closer to basking T.
scripta than to basking M. leprosa before they dived in water (N. Polo-Cavia
unpubl. data).
In their original habitat, T. scripta would be able to face potential attacks by
little dangerous terrestrial predators, by just remaining immobile on basking
places, while avoiding exposure to more dangerous, aquatic predators. Also, the
antipredatory behavior of native M. leprosa could decrease predation by their
main terrestrial predators in their natural habitats. However, in circumstances
in which human pressure on the ecosystems increases and terrestrial predators
152
Acknowledgements We thank two anonymous reviewers for helpful comments, the “Grupo de
Rehabilitación de la Fauna Autóctona y su Hábitat” (GREFA) for providing sliders, A. Marzal, D.
Martín, and A. Pintado for allowing field work in their dehesa states, and “El Ventorrillo” MNCN
Field Station for use of their facilities. Financial support was provided by the project MECCGL2005-00391 ⁄ BOS, and by an “El Ventorrillo” CSIC grant and a MEC-FPU grant to N. P.-C.
The experiments enforced all the present Spanish laws and of the Environmental Organisms of
the Extremadura and Madrid Communities where they were carried out.
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155
156
Capítulo
8
La incapacidad de los renacuajos para reconocer depredadores introducidos puede conferir ventajas competitivas a los galápagos invasores Nuria Polo Cavia, Adega Gonzalo, Pilar López y José Martín
En revisión
RESUMEN
158
El impacto que los depredadores exóticos ejercen sobre las
poblaciones de presas nativas es de sobra conocido en biología
de la conservación. Sin embargo, se ha prestado escasa
atención a los efectos negativos que la introducción de
depredadores exóticos puede ocasionar sobre los
depredadores nativos a través de la competencia por los
recursos tróficos. En la Península Ibérica, el galápago de
Florida (Trachemys scripta elegans) se encuentra introducido
junto con otras especies exóticas de galápagos. Estos galápagos
se comportan como especies invasoras, compitiendo y
desplazando a los galápagos nativos (el galápago europeo,
Emys orbicularis, y el galápago leproso, Mauremys leprosa).
Aunque no está claro cómo se producen las interacciones
competitivas, es posible que exista competencia directa por la
alimentación. Tanto los galápagos nativos como los exóticos
depredan habitualmente sobre renacuajos de anfibios. Los
renacuajos son capaces de reconocer y responder de forma
innata a las señales químicas de los depredadores locales, pero
a menudo se muestran incapaces de reconocer especies
nuevas de depredadores potenciales con los que no han
compartido una larga historia evolutiva. Examinamos la
capacidad de cuatro especies de renacuajos de anuros ibéricos
para reconocer y responder a estímulos químicos de galápagos
nativos y exóticos invasores. Tres de las cuatro especies de
renacuajos redujeron su actividad natatoria frente a estímulos
químicos de galápagos nativos presentes en el agua, pero
ninguna de ellas modificó su nivel de actividad frente a
estímulos químicos de galápagos exóticos. Sugerimos que esta
incapacidad de las presas para discriminar y responder de
forma innata a las sustancias químicas de depredadores
introducidos podría conferir ventajas competitivas a las
especies invasoras. Esta podría ser una de las causas que
expliquen el desplazamiento de las poblaciones nativas de
galápagos ibéricos por los galápagos exóticos invasores, y
podría también contribuir a clarificar la paradoja de por qué
los depredadores exóticos a menudo prosperan mejor en sus
nuevos hábitats que los depredadores nativos localmente
adaptados ■
Abstract The impact of alien predators on prey populations is well known by conservation
biologists, but little attention has been paid to the negative effects that the introduction of exotic
predators may have over native predators through competition for food. In the Iberian Peninsula,
the red-eared slider (Trachemys scripta elegans) and other exotic freshwater turtles have been
introduced. These exotic turtles behave as invasive species that compete and displace the
populations of native endangered terrapins (the European pond turtle, Emys orbicularis, and the
Spanish terrapin, Mauremys leprosa). Although the nature of competitive interactions is not clear,
direct competition for food is likely to occur. Both native and invasive freshwater turtles are
common predators of amphibian tadpoles. Naïve amphibian tadpoles may be able to recognize
and respond to local predators with no prior experience, but tadpoles might not recognize new
potential predatory species, since they have not shared a long evolutionary history with them.
We examined the ability of four species of Iberian anuran tadpoles to recognize and respond to
chemical cues from invasive and native freshwater predatory turtles. Three of the four tadpole
species tested reduced their swimming activity when chemical cues from native turtles were
present in water, but activity levels remained invariable when cues belonged to exotic turtles. We
suggest that this inability of tadpole prey to innately discriminate and respond to chemicals from
introduced predatory turtles might confer a competitive advantage to invasive turtles over native
terrapins. This may be one of the causes that explains the displacement of native populations of
Iberian terrapins by invasive exotic turtles, and may contribute to clarify the paradox of why
alien predators sometimes prosper better in new habitats than locally adapted predators.
Keywords
Alien predators • Amphibian tadpoles • Chemoreception • Freshwater turtles •
Invasions • Predation risk
T
he introduction of alien predators outside their natural geographic
range area can create novel ecological contexts in which the adaptive
antipredatory responses of native prey may not be successful (Callaway
and Aschehoug 2000; Shea and Chesson 2002). Decision making rules or
‘Darwinian algorithms’ (Cosmides and Tooby 1987) are expected to be adaptive
in the environment in which species evolved, because they rely on cues that,
over evolutionary time, promote survival and reproductive success in such
environments (Williams and Nichols 1984). Thus, adaptive evolutionary
responses of prey to predation risk adequately work in their specific habitats,
but organisms may not be innately equipped to cope with suddenly introduced
new predators (Schlaepfer et al. 2002). Prey are often naïve to the hunting
tactics of novel introduced species or unable to detect these alien predators,
which result more harmful to prey populations than native predators (Salo et al.
2007). In this context, alien predators are considered to be one of the most
important causes of decline and extinction of prey species (Vitousek et al. 1997).
Impact of alien predators on prey populations is well documented (Dickman
1996; Kinnear et al. 2002), but less attention has been paid to the competitive
CAPÍTULO 8: Reconocimiento de galápagos introducidos por renacuajos presa
FAILED PREDATOR-RECOGNITION BY TADPOLE PREY MAY CONFER
COMPETITIVE ADVANTAGES TO INVASIVE TURTLE PREDATORS
159
advantages of alien predatory species over endangered native ones. When
invasive predators alter environments in such a way that normal antipredatory
strategies of native prey are no longer adaptive, they may benefit from
evolutionary releases (Schlaepfer et al. 2005). The advantage of an evolutionary
release may explain the paradox of why invasive species sometimes enjoy a
competitive advantage over locally adapted species (Blossey and Notzold 1995;
Shea and Chesson 2002; Allendorf and Lundquist 2003). For example, several
studies have demonstrated that larval amphibians from populations that have
co-occurred during long time with predatory fish or bullfrogs are able to
recognize and respond to these predators without any prior experience (Kats et
al. 1988; Sih and Kats 1994; Kiesecker and Blaustein 1997). In contrast, naïve
larval amphibian often cannot recognize introduced species such as bullfrogs
(Kiesecker and Blaustein 1997) or crawfish (Marquis et al. 2004) as potential
predators, since these prey have not shared a long evolutionary history with
these novel predators. As a result, alien predators are released from some of the
difficulties of finding larval amphibian prey, which keep working for native
predators (Lawler et al. 1999; Kiesecker et al. 2001; Baber and Babbitt 2003).
Nevertheless, there are a few documented cases of native prey able to learn or
evolve the ability to avoid invasive species (Chivers and Smith 1995; Kiesecker
and Blaustein 1997; Chivers et al. 2001).
In the Iberian Peninsula, the two native freshwater turtles, Emys orbicularis
and Mauremys leprosa, are common predators of amphibian tadpoles (Arnold
and Ovenden 2002; Gomez-Mestre and Keller 2003). Both turtle species are
similar in body size and may be locally abundant in permanent and temporary
ponds, posing a threat to tadpole populations, especially in spring, when peak
densities of many tadpole species coincide with the main activity season of
turtles (Díaz-Paniagua 1988; Keller 1997). Both turtle species consume mainly
animal matter, although M. leprosa also feeds on plants, whereas E. orbicularis
is an almost strict carnivore and insectivore (Keller and Busack 2001). Both
terrapins are considered as endangered species due to the considerable decline
of their populations since the last decades (Pleguezuelos et al. 2002). Although
habitat destruction and human pressure are major causes for this recession,
competition with introduced exotic turtle species might be worsening the
conservation state of native Iberian turtles (Da Silva and Blasco 1995;
Pleguezuelos et al. 2002). Red-eared sliders (Trachemys scripta elegans) and
other exotic freshwater turtle species are nowadays introduced as breeding
species in diverse aquatic habitats of many Mediterranean countries (Luiselli et
al. 1997; Pleguezuelos 2002). The introduction of these turtles was due to
uncontrolled releases after having been imported into Europe and sold as pet
animals. Many observations indicate that introduced turtles are competing with
the native Iberian turtle species. However, how the interactions are taking
160
METHODS
Study animals
During May 2007, we collected by netting larval tadpoles of four anuran
species. We collected tadpoles of common tree frogs (Hyla arborea) in several
ponds located inside dehesa woodlands with scattered holm oak (Quercus ilex)
at Olivenza (Badajoz Province, southwestern Spain) where native turtles were
common but exotic ones did not occur. Tadpoles of Iberian green frogs
(Pelophylax perezi), natterjack toads (Bufo calamita) and western spadefoot
(Pelobates cultripes) were collected in several temporary small ponds in Collado
CAPÍTULO 8: Reconocimiento de galápagos introducidos por renacuajos presa
place is not clear. Competition has been described between sliders and the
European pond turtle (Emys orbicularis) (Cadi and Joly 2003), and recent
studies suggest that competition is very likely to occur also between sliders and
the Spanish terrapins (Polo-Cavia et al. 2008, 2009a,b). A greater tolerance to
pollution and human presence (Pleguezuelos 2002), combined with larger adult
body sizes and higher fecundity (Gibbons 1990), seem to be the main
advantages of introduced turtles in the Iberian habitats. Although sliders are
more phytophagous than the two native terrapins (Díaz-Paniagua et al. 2002),
direct competition for food is very likely to occur in wild, because invasive
freshwater turtles also feed on animal matter (frequently native amphibians), as
native turtles do (Pleguezuelos 2002). Feeding competition between sliders and
native terrapins has been confirmed in laboratory, as well as predatory events
over amphibian tadpoles by both native and invasive turtles (N. Polo-Cavia,
unpubl. data). In this context, we hypothesized that the ability of larval
amphibian prey to innately detect predation risk posed by native turtle
predators, but not risk posed by invasive ones, might confer an initial
competitive advantage to alien freshwater turtle species over native ones (at
least until learned predator-avoidance behavior propagates through a naïve
tadpole population), thus favoring the expansion of invasive turtle species.
It has been widely tested that tadpoles (among other aquatic prey) strongly
respond to the presence of chemical cues from potential predators by reducing
their activity levels as an antipredatory strategy (e.g., Stauffer and Semlitsch
1993; Wilson and Lefcort 1993; Holomutzki 1995; Kiesecker et al. 1996; see Kats
and Dill 1998 for a review). In this study, we experimentally tested the ability
of different species of native anuran larvae to recognize in water chemical cues
from native and exotic freshwater turtle species, and consequently to display
antipredatory responses. We used naïve tadpoles that had no previous contact
with invasive turtles to avoid conditioning the response by learned recognition
of the introduced predators.
161
Mediano (Madrid, central Spain), where native and exotic turtles were absent.
Tadpoles were transported to “El Ventorrillo” Field Station (Navacerrada,
Madrid Province) and housed individually in plastic inner aquaria (18 x 25 x 10
cm) with water at ambient temperature and under a natural photoperiod. They
were fed every two days with commercial fish flakes. No contact with the scent
and visual stimuli of turtles was allowed before tadpoles were tested.
We also captured with baited funnel traps some individuals of native and
invasive freshwater turtle species that are common potential predators of
tadpoles to be used as predator scent donors. Native Spanish terrapins (M.
leprosa) and European pond terrapins (E. orbicularis) were collected in ponds
and tributary streams of the Guadiana River at Olivenza (Badajoz Province,
southwestern Spain). Introduced red-eared sliders (T. scripta) and false map
turtles (Graptemys pseudogeografica) were obtained from a large seminatural
outdoor pond where they had been maintained by the conservationist
organization “Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat”
(GREFA). These turtles had been extracted from introduced populations in
central Spain, with the purpose of preserving the original ecosystem balance.
Turtles were housed individually at “El Ventorrillo” Field Station in outdoor
aquaria (60 x 40 x 30 cm) with water and stones that allowed them to bask. The
temperature and day-length cycle of light were the same as the natural
surroundings. To avoid potential confounding effects of the diet on the results,
all turtles were fed small pieces of commercial compound feed, which did not
contain tadpoles, during two weeks before collecting their chemical stimuli.
We obtained from a commercial dealer non-predatory zebra danio fish
(Brachyodanio rerio) to be used as source of neutral scent. Before and after the
experiment finished, fishes were maintained in a large filtered aquarium and
regularly fed with commercial fish flakes.
All the animals were healthy during the trials, all maintained or increased
their original body mass, and all tadpoles metamorphosed into subadult
anurans. At the end of the tests, all these frogs and toads and the turtles were
returned to their exact field capture sites or to the GREFA ponds.
Chemical stimuli
Each turtle aquaria was filled with 5 L of clean water and left overnight to
prepare the turtle scents. Then, we extracted and mixed the water of two
conspecific turtles, and froze it in 10 mL portions until use. Clean water was
collected from a nearby high mountain spring that did not house frogs nor
fishes nor turtles.
The neutral stimulus was prepared by placing zebra danio fishes in groups
of three into a 3 L aquarium with clean water for three days. These aquaria
162
were aerated but not filtered. Fishes were not fed during this short period to
avoid contaminating water with food odor. Thereafter, water was drawn from
the aquaria and frozen in 10 mL portions until its use in experiments. Fishes
were returned and fed in their home large aquaria. We prepared control water
in an identical manner but without placing fishes or turtles in the aquaria
(Woody and Mathis 1998; Gonzalo et al. 2007).
To determine whether larval anuran tadpoles assess predation risk of native and
exotic turtles differently, we designed an experiment to analyze the levels of
basal activity of tadpoles in pools filled with water with chemical stimuli from
different species of turtles. We tested separately 15 individual tadpoles of each
anuran species in six different treatments (‘clean water’ vs. ‘E. orbicularis scent’
vs. ‘M. leprosa scent’ vs. ‘T. scripta scent’ vs. ‘G. pseudogeographica scent’ vs.
‘non-predatory fish scent’) in a random sequence. We allowed tadpoles to rest
for one day between trials to avoid stress. ‘Clean water’ treatment was included
to determine the basal activity level of tadpoles in a predator-free environment,
and to use it as a control for the effect of the different turtle predators and the
fish. The ‘non-predatory fish scent’ treatment was used to test for a possible
alteration of activity levels due to any strange odor present in the water. The six
treatments were carried out in parallel, and observations were carried out blind.
Tadpoles were tested individually in grey, U-shaped, gutters (101 x 11.4 x
6.4 cm) sealed at both ends with plastic caps. We marked the internal part of
the gutters with four crossing lines that created five subdivisions of equal
surface. We filled each gutter with 3 L of clean water from a mountain spring at
20 °C and 20 mL test solutions (two ice aliquots) of clean water or turtle or fish
scent. We assigned test solutions to one end of each trough (right or left) by
stratified randomization (see Rohr and Madison 2001; Gonzalo et al. 2007).
We placed a single tadpole covered with a release cage (made of clear
plastic; 21 x 7.6 x 6.4 cm) in the middle of the central subdivisions of each
gutter, and waited 5 min for acclimation. Then we deposited the test solution
ice aliquots and we began trials by slowly lifting the cages above each tadpole 5
min after we deposited the test solution ices aliquots (i.e., after the ices aliquots
had entirely thawed). We used the instantaneous scan sampling method to
monitor each tadpole during 30 min, scanning as motionless as possible from a
hidden position and recording at 1 min intervals the quadrant that each tadpole
occupied (30 scans per tadpole in total). We calculated levels of activity from
the number of lines crossed by each tadpole during the observation period
(Rohr and Madison 2001; Gonzalo et al. 2007). Diffusion of chemicals in still
water may be a slow process. However, all individual tadpoles used in the
CAPÍTULO 8: Reconocimiento de galápagos introducidos por renacuajos presa
Experimental procedure
163
experiment were observed at least once in all of the subdivisions of the gutter,
so we were confident that all tadpoles were really exposed to the chemical
stimuli. Moreover, tadpoles often showed episodes of fast swimming which
should contribute to diffuse chemicals in water.
Statistical analyses
We used separate one-way repeated measures analyses of variance (ANOVAs)
for each tadpole species to analyze the differences in basal activity levels of the
same individual tadpole across the six treatments with water containing
different chemical cues (within subject factor; ‘clean water’ vs. ‘non-predatory
fish’ vs. ‘E. orbicularis’ vs. ‘M. leprosa’ vs. ‘T. scripta’ vs. ‘G.
pseudogeographica’). Levels of activity (number of lines crossed by tadpoles)
were log-transformed to ensure normality (verified by Shapiro-Wilk’s test) and
tests of homogeneity of variances (Levene’s test) showed that variances were
not significantly heterogeneous. Pairwise comparisons were made using Tukey’s
honestly significant difference tests (Sokal and Rohlf 1995).
RESULTS
We found significant differences between predator cue treatments in overall
activity levels of three of the four species of anuran tadpoles that we tested (Fig.
8.1). Tadpoles of H. arborea, P. perezi and P. cultripes showed significantly
different levels of activity between treatments (one-way repeated measures
ANOVAs, H. arborea: F = 6.97, df = 5,70, P < 0.0001; P. perezi: F = 15.02, df =
5,70, P < 0.0001; P. cultripes: F = 7.20, df = 5,70, P < 0.0001). However, there
were no significant differences in overall activity levels of B. calamita tadpoles
between treatments (F = 0.26, df = 5,70, P = 0.93).
Baseline activity levels of H. arborea tadpoles in clean water were not
significantly different of those in the non-predatory fish treatment (Tukey’s
tests, P > 0.99) and in both exotic turtle treatments (T. scripta: P = 0.94; G.
pseudogeographica: P = 0.58). However, H. arborea tadpoles significantly
responded to chemical cues from native turtle species by reducing their activity
levels with respect to their baseline activity in clean water (E. orbicularis: P =
0.002; M. leprosa: P = 0.0008). Activity levels of H. arborea tadpoles in water
with non-predatory fish stimulus did not significantly differ from those in
water with both T. scripta and G. pseudogeographica cues (P > 0.80 in both
cases), but activity levels were significantly lower in water with chemical cues
from both native turtles than in water with non-predatory fish stimulus (E.
orbicularis: P = 0.007; M. leprosa: P = 0.003). Responses to both E. orbicularis
and M. leprosa stimuli significantly differed from responses to T. scripta
164
a)
Hyla arborea
40
30
20
10
0
Water
b)
Fish
Emys
Mauremys
Trachemys
Graptemys
Pelophylax perezi
Activity level
50
40
30
20
Graptemys
pseudogeographica) 10
0
Water
c)
Fish
Emys
Mauremys
Trachemys
Graptemys
Trachemys
Graptemys
Trachemys
Graptemys
Pelobates cultripes
Activity level
50
40
30
20
10
0
Water
Fish
d)
Emys
Mauremys
Bufo calamita
50
Activity level
Figure 8.1 Activity
levels (mean ± SE
number of lines crossed
during 30 min) of four
species of anuran
tadpoles: (a) H. arborea,
(b) P. perezi, (c) P.
cultripes and (d) B.
calamita, in trials with
clean water, water with
chemical cues from a
non-predatory fish and
water with chemical
cues from two native
predatory turtle species
(Emys orbicularis and
Mauremys leprosa), and
two exotic predatory
turtle species
(Trachemys scripta and
40
30
20
10
0
Water
Fish
Emys
Mauremys
CAPÍTULO 8: Reconocimiento de galápagos introducidos por renacuajos presa
Activity level
50
165
stimulus (P = 0.03 and P = 0.01 respectively), but they did not differ
significantly from responses to G. pseudogeographica stimulus (P = 0.17 and P =
0.09 respectively). Responses to chemical cues from the two native turtles were
not significantly different (P > 0.99), and neither were responses to chemical
cues from the two exotic turtles (P = 0.98).
Tadpoles of P. perezi showed no significant differences between activity
levels in clean water and those in water with chemical cues from the nonpredatory fish, or from both exotic predatory turtles (Tukey’s tests, P > 0.99 in
all cases). However, P. perezi tadpoles reduced their activity in water with
chemical cues from both native predatory turtles (E. orbicularis: P = 0.0001; M.
leprosa: P = 0.002). Responses to the non-predatory fish stimulus did not
significantly differ from responses to both exotic turtle stimuli (P > 0.99 in both
cases), but responses to fish were significantly different from responses to both
native turtle stimuli (E. orbicularis: P = 0.0001; M. leprosa: P = 0.005). Responses
to both exotic turtles differed significantly from responses to both native turtles
(P < 0.003 in all cases). There were no significant differences between responses
to E. orbicularis and M. leprosa stimuli (P = 0.17) and neither there were
between responses to T. scripta and G. pseudogeographica (P > 0.99).
Tadpoles of P. cultripes significantly reduced their activity levels in water
with chemical cues from the native turtle E. orbicularis in comparison with
their basal activity in clean water (P = 0.004), but there were non-significant
differences in activity between clean water and the rest of experimental
treatments (non-predatory fish: P = 0.80; M. leprosa: P = 0.12; both exotic
turtles: P > 0.99). Differences between responses to non-predatory fish stimulus
and both exotic turtles stimuli were non-significant (P > 0.60 in both cases), but
differences between responses to non-predatory fish stimulus and both native
turtles stimuli were significant (E. orbicularis: P = 0.0002; M. leprosa: P = 0.004).
Activity levels of P. cultripes tadpoles in water with chemical cues from native
E. orbicularis were significantly different from those in water with chemical
cues from both exotic turtles (T. scripta: P = 0.004; G. pseudogeographica: P =
0.01), but they did not differ from those in water with chemical cues from
native M. leprosa (P = 0.80). However, activity levels in water with M. leprosa
cues were not significantly different from those in water with chemical cues
from exotic turtles (T. scripta: P = 0.14; G. pseudogeographica: P = 0.24). There
were no significant differences between responses to the two exotic turtles’
stimuli (P > 0.99).
DISCUSSION
Our results confirm that antipredatory responses in amphibian larvae are
mediated by water-borne chemical cues, and particularly show that different
166
CAPÍTULO 8: Reconocimiento de galápagos introducidos por renacuajos presa
species of native Iberian anuran tadpoles can use chemoreception to assess
predation risk. We observed substantial variation in the activity levels of H.
arborea, P. perezi and P. cultripes tadpoles when they perceived dissimilar
degrees of predatory threat through chemical cues present in water, thus
indicating that these tadpole species are able to discriminate predator-specific
scents and consequently respond to the predation risk assessed.
In contrast, B. calamita tadpoles seemed unable to discriminate chemical
cues released by predators in water, or, at least, the presence of such cues did
not affect their predation risk assessment, as tadpoles did not show any
significant variation in their swimming activity between treatments. However,
several studies have shown that Bufo species reduce activity when they are
exposed to predators that were fed with conspecifics (Skelly and Werner 1990;
Semlitsch and Gavasso1992; Anholt et al. 1996; Kiesecker et al. 1996; Summey
and Mathis 1998). It is possible that the simple presence of predator scents may
have a less important role in the chemical detection of predators by bufonid
tadpoles compared with the presence of additional cues provided by predators
that have eaten conspecifics tadpoles. In this regard, Marquis et al. (2004) found
a slight but non-significant reduction in swimming behavior of the common
toad (Bufo bufo) in presence of chemical cues from starved sympatric predators,
while swimming activity of these tadpoles significantly decreased in response to
chemical cues released by crushed conspecifics. Thus, the absence of responses
that we found in B. calamita might be due to that none of the experimental
subjects we used to provide chemical stimuli (neither the turtles nor the nonpredatory fishes) were fed with anuran tadpoles.
On the other hand, several studies have reported unpalatability of Bufo
embryos and tadpoles to vertebrate predators (Heyer et al. 1975; Denton and
Beebee 1991; Azevedo-Ramos and Magnusson 1999). It might be also possible
that antipredatory strategies of B. calamita tadpoles mainly rely on the
defensive value of producing substances aimed at distastefulness. Also, GomezMestre and Keller (2003) suggested that Iberian turtles are generally keener on
large tadpoles (as for example P. cultripes), which are easier to see when they
move, and represent a higher energy reward per unit of effort. In this way,
small B. calamita tadpoles might have experienced a slighter selective pressure
in the development of mechanisms to detect specific turtle cues, what might
also contribute to explain the absence of specific antipredatory responses found
in our experiment.
Our results further suggest that native Iberian anuran tadpoles of H.
arborea, P. perezi and P. cultripes are capable to discriminate semiochemicals
released in water by native predatory turtles, but they are not able to detect
chemical cues released by exotic turtle predators when no previous contact has
taken place. Tadpoles of these three species significantly reduced their
167
swimming activity when chemical stimuli from native turtles were present in
water. In contrast, their activity levels remained invariable when chemical cues
belonged to exotic turtles, suggesting that these tadpole species are capable of
facing potential predatory events posed by native predatory turtles, by
responding with accurate antipredatory tactics, but they are not able to
appropriately respond to introduced turtle predators. Moreover, the presence of
a neutral chemical cue (from the non-predatory fish) neither elicited an
antipredatory response in any of the tadpole species, thus indicating that
reduction of activity only occurred when tadpoles perceived a predatory threat.
Such situation was solely induced by the native turtle scents. As a consequence,
the failed ability of naïve tadpoles to discriminate chemical cues from unknown
turtle predators might represent a competitive advantage for introduced turtles
over native ones in the Iberian Peninsula. Once released from being
chemosensory detected by prey anuran tadpoles, alien turtles may easily
capture and incorporate tadpoles to their diet, in detriment of native turtles,
which must still face an effortful hunting. Thus, the interaction between native
prey anuran tadpoles and introduced predatory turtles, which do not share an
evolutionary history, could result in a positive outcome for the alien predators.
A few studies report similar results for interactions between native amphibian
prey and introduced predators that benefit from evolutionary releases. For
example, naïve red-legged frog, Rana aurora, tadpoles cannot recognize
introduced American bullfrog, Rana catesbeiana, as a potential predator, which
benefits from prey innocence (Kiesecker and Blaustein 1997). Also, chemical
cues from starved crawfish Astacus leptodactylus, a recently introduced
predator, produce no change at all in behavior of B. bufo tadpoles (Marquis et
al. 2004).
However, the initial competitive advantage that naïve native tadpoles may
confer to introduced predatory turtles might vanish if native tadpole species,
given enough time, learn or evolve mechanisms to cope with their introduced
predators. There are some documented cases on this subject. Chivers and Smith
(1995) describe how predator-avoidance behavior propagated through a naïve
population of fish in less than two weeks after the introduction of a novel
predator. In amphibians, Kiesecker and Blaustein (1997) state that R. aurora
individuals are able to acquire the ability to recognize chemical cues of their
new predator R. catesbeiana and exhibit predator avoidance behavior. Also,
juvenile Pacific treefrogs (Hyla regilla) from a syntopic population with
introduced R. catesbeiana showed a strong avoidance of chemical cues from this
novel predator (Chivers et al. 2001). Recently, Bosch et al. (2006) found that
Rana iberica tadpoles reacted to chemical cues from both native and exotic
trout species by decreasing their activity, although the response toward native
predators was stronger than the response toward exotic trout. Learned predator
168
CAPÍTULO 8: Reconocimiento de galápagos introducidos por renacuajos presa
recognition can also occur in P. perezi tadpoles, when naïve tadpole individuals
are exposed to chemical cues from exotic turtle predators jointly with alarm
cues released by injured conspecifics tadpoles (A. Gonzalo, unpubl. data).
Some authors have suggested that prey might innately respond to chemical
cues released by novel predators that remind them to those released by native
ones (Ferrari et al. 2007). Although this strategy may work in other species, the
results of our study suggest that Iberian anuran tadpoles are incapable of
relating scents from native turtle predators with those from introduced ones,
and thus, innately respond to the latter. Nevertheless, H. arborea tadpoles
showed a minor tendency to reduce their swimming activity when chemical
cues from the exotic turtle G. pseudogeographica were present in water. This
behavior might be due to a vague resemblance between exotic and native
predators’ cues. However, most of the studies aimed to test generalization of
predator recognition in aquatic vertebrates have obtained unsuccessful results
(Chivers and Smith 1994; Darwish et al. 2005), and it points out that
generalization behavior broadly fails with distantly related predators. Although
the native E. orbicularis and the two introduced turtles, T. scripta and G.
pseudogeographica, all belong to the family Emydidae, it might seem a too long
genetic distance to allow effective chemical generalization of predator
recognition by Iberian tadpoles.
Additionally, the results of our study indicate that P. perezi and P. cultripes
tadpoles innately respond to the scent of the two native predatory turtle species
E. orbicularis and M. leprosa, as no previous contact occurred between prey
tadpoles and predators’ cues before the experiment. In contrast, our study can
not clarify whether H. arborea responses to chemical cues from native turtles
come from innate or learned predator recognition, as H. arborea tadpoles came
from a syntopic population with the two native turtle predators. On the other
hand, although there were no significant differences in swimming behavior of
H. arborea, P. perezi and P. cultripes tadpoles when the scents present in water
belonged to E. orbicularis or M. leprosa, we observed a slight tendency of P.
perezi and P. cultripes tadpoles to reduce more their activity in presence of
chemical cues from E. orbicularis than from M. leprosa. This tendency was
more striking for P. cultripes tadpoles, which did not show a significant
response to M. leprosa cues. It might be possible that, for native Iberian
tadpoles, assessment of predation risk posed by the predatory turtle E.
orbicularis was greater than the one posed by M. leprosa, as tadpole
consumption rates are significantly higher for the mainly carnivorous E.
orbicularis than for M. leprosa (Gomez-Mestre and Keller 2003).
In conclusion, the evolved or learned chemical recognition of native
predatory turtles that native anuran tadpoles of H. arborea, P. perezi and P.
cultripes species show, and their failure in innate discrimination of chemicals
169
from introduced turtle predators, may represent a competitive advantage for
invasive turtles over native ones in the Iberian Peninsula. However, the
magnitude of the negative outcome that this interaction between naïve prey
and novel competitive predators may have on native populations of Iberian
turtles, E. orbicularis and M. leprosa, remains uncertain, as abilities of
amphibian prey to develop learned recognition of novel predators are widely
known. Nevertheless, invasive predatory turtle species will still benefiting from
inaccurate antipredatory behavior of naïve tadpoles prey, in detriment of native
turtles. Thus, the advantage of competitive alien predators may explain why
invasive species sometimes prosper in their new habitats better than native
adapted species. Our study yield interesting data and points out new
perspectives for conservation research in the framework of biological invasions.
Future investigations on competitive predation may reveal why certain species
are more likely to successfully invade than others.
Acknowledgements We thank A. Marzal for allowing us to work in his dehesa state (“La
Asesera”), the “Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat” (GREFA) for
providing exotic turtles, and “El Ventorrillo” MNCN Field Station for use of their facilities.
Financial support was provided by the MEC project CGL2005-00391/BOS and by MEC-FPU
grants to N.P.-C. and A.G. The experiments comply with the current laws of Spain and the
Environmental Agencies of the “Junta de Extremadura” and “Comunidad de Madrid” where they
were performed.
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— SÍNTESIS DE
RESULTADOS Y DISCUSIÓN
—
Capítulo 1
RECONOCIMIENTO QUÍMICO
1Las
tablas y figuras se muestran en el apartado de resultados en cada uno de los capítulos
SÍNTESIS DE RESULTADOS Y DISCUSIÓN
S
e encontraron diferencias significativas entre los periodos reproductivo y
no reproductivo en el porcentaje de tiempo que Trachemys scripta ocupó
acuarios con estímulos químicos propios y de coespecíficos vs. acuarios
con agua limpia (Fig. 1.1)1. Durante el periodo reproductivo, T. scripta
permaneció durante un porcentaje de tiempo menor en acuarios que contenían
estímulos químicos (media ± EE = 38 ± 3 %) que durante el periodo no
reproductivo (49 ± 3 %), lo que sugiere que esta especie es capaz de reconocer
sustancias químicas de coespecíficos disueltas en el agua. Los galápagos
americanos podrían evitar así potenciales encuentros agresivos con otros
individuos de su especie durante la época reproductiva. Sin embargo, al
contrario que los galápagos leprosos (Muñoz 2004), los galápagos de Florida no
discriminaron claramente entre sus propias secreciones y las pertenecientes a
machos y hembras coespecíficos (Fig. 1.1), lo que parece indicar que los
galápagos exóticos son menos dependientes de la comunicación química que los
galápagos nativos. Así mismo, T. scripta no prefirió ni evitó los acuarios con
estímulos químicos secretados por Mauremys leprosa (Fig. 1.2; Tabla 1.1). Esta
ausencia de respuesta podría deberse a la incapacidad para detectar sustancias
químicas de individuos heteroespecíficos, o simplemente a que estas sustancias,
aunque puedan ser reconocidas, no suponen una amenaza para la especie
invasora. En contraste, M. leprosa prefirió agua con secreciones de coespecíficos
y evitó los acuarios con estímulos secretados por T. scripta (Fig. 1.2), lo que
sugiere que estas señales químicas podrían ser usadas por los galápagos nativos
para evitar áreas ocupadas por los galápagos exóticos.
En muchas especies de animales, la habilidad para reconocer olores de
individuos heteroespecíficos contribuye a evitar depredadores o a reducir los
costes de las interacciones agresivas con especies competidoras (Dodson et al.
1994; Kats y Dill 1998). Por otra parte, numerosas especies son capaces de
aprender a reconocer olores nuevos como peligrosos cuando éstos son
173
detectados simultáneamente con indicadores de riesgo conocidos, como por
ejemplo el comportamiento antidepredatorio, o la presencia en el medio de
sustancias químicas de alarma, de coespecíficos (e.g., Magurran 1989; Mathis et
al. 1996; Chivers y Smith 1998). De forma similar, las especies nativas podrían
aprender a evitar olores de especies invasoras que hayan sido previamente
asociados con un comportamiento agonístico o con un aprovechamiento
ineficiente de los recursos. Así, en una situación de desventaja competitiva por
los lugares de asoleamiento o el alimento (Cadi y Joly 2003; Polo-Cavia et al. en
prensa; capítulo 2), la aversión de M. leprosa por los estímulos químicos
secretados por T. scripta podría constituir un mecanismo para evitar encuentros
agresivos con la especie introducida, lo que favorecería la expansión del
galápago de Florida.
Capítulo 2
INTERACCIONES AGRESIVAS DURANTE LA ALIMENTACIÓN
L
os resultados de este trabajo muestran diferencias significativas entre el
galápago de Florida y el galápago leproso en la ingesta de alimento en
condiciones de competencia intra e interespecífica. La cantidad de
alimento ingerida por M. leprosa y T. scripta fue similar cuando compitieron
con coespecíficos, pero cuando estas dos especies compitieron entre sí, el acceso
de M. leprosa al alimento fue restringido por T. scripta, que ingirió un
porcentaje significativamente mayor de la comida suministrada (Fig. 2.1). Estos
resultados indican que la competencia por el alimento entre estas dos especies
de galápagos es asimétrica.
Las habilidades competitivas difieren habitualmente entre individuos en la
naturaleza (Holmgren 1995; Moody y Houston 1995; Spencer et al. 1995). En
consecuencia, algunos individuos son capaces de excluir a otros menos
competitivos utilizando la agresividad (Schoener 1983). De las 27 agresiones
observadas durante la competencia por el acceso a la comida, tan sólo 5 fueron
cometidas por M. leprosa, 2 de ellas sobre individuos coespecíficos y 3 sobre
galápagos americanos. T. scripta, en cambio, agredió en 5 ocasiones a individuos
coespecíficos y 19 veces a galápagos leprosos. Estos resultados indican que T.
scripta es una especie más agresiva que M. leprosa y que las interacciones
agresivas se producen con mayor frecuencia entre individuos heteroespecíficos
(Tabla 2.2). Además, se observó una correlación positiva entre el porcentaje de
alimento ingerido por los galápagos nativos en condiciones de competencia
interespecífica y el nivel de agresividad recibido, lo que sugiere la existencia
de una relación de compromiso entre la eficiencia alimenticia de M. leprosa y
174
los costes de la competencia agresiva con los galápagos exóticos. En las
poblaciones simpátridas naturales, la mayor agresividad y dominancia de T.
scripta podrían traducirse en el desplazamiento de M. leprosa hacia áreas
subóptimas de alimentación. Esta exclusión de los galápagos leprosos de los
recursos tróficos preferidos podría finalmente afectar negativamente a sus
tasas de crecimiento y reproducción (Moll 1976; Bury 1979; Gibbons et al
1979; Vogt y Guzman 1988), contribuyendo a la recesión actual que sufre la
especie.
Capítulo 3
COMPETENCIA DURANTE EL ASOLEAMIENTO
SÍNTESIS DE RESULTADOS Y DISCUSIÓN
E
n condiciones de competencia ocasional, el porcentaje de tiempo que los
galápagos leprosos dedicaron a asolearse fue significativamente menor
cuando el competidor fue un galápago de Florida que cuando fue un
coespecífico (Fig. 3.1a). Cuando la competencia fue a largo plazo, se encontraron
diferencias significativas entre la especie nativa y la invasora, dependiendo del
tipo de competencia (i.e., intra vs. interespecífica), en el tiempo total de
asoleamiento y en la duración media de los periodos dedicados a esta actividad.
El tiempo total de asoleamiento fue similar entre las dos especies en condiciones
de competencia intraespecífica (Fig. 3.1b), y también la duración media de los
periodos de asoleamiento (M. leprosa: 71 ± 15 min; T. scripta: media ± EE = 76 ±
14 min), pero en condiciones de competencia interespecífica, tanto el tiempo
total de asoleamiento (Fig. 3.1b) como la duración media de los periodos
dedicados a esta actividad (M. leprosa: 45 ± 14 min; T. scripta: 121 ± 19 min)
fueron significativamente mayores en el caso de la especie invasora. Los
resultados anteriores indican que, cuando las dos especies compiten entre sí por
los lugares de asoleamiento, el galápago de Florida es más eficiente en la
ocupación de los recursos que el galápago leproso, lo que sugiere la dominancia
de la especie invasora sobre la nativa. Factores tales como un mayor tamaño
corporal o un hábitat original con niveles elevados de competencia (i.e., T.
scripta coexiste con un gran número de especies competidoras de galápagos en
su hábitat natural, en comparación con M. leprosa) podrían favorecer la mayor
habilidad competitiva del galápago de Florida.
Por otra parte, los galápagos leprosos evitaron compartir los recursos de
asoleamiento con galápagos americanos, pero no con individuos coespecíficos
(Fig. 3.5). Este comportamiento de M. leprosa coincide con el descrito para el
galápago europeo (Emys orbicularis). En sus experimentos, Cadi y Joly (2003)
observaron que E. orbicularis evitaba los solarios ocupados por el introducido T.
175
scripta, siendo desplazado hacia lugares subóptimos para el asoleamiento (i.e.,
orillas y aguas someras con mayor riesgo de depredación, López et al. 2005;
Polo-Cavia et al. 2008). De forma similar, es posible que los galápagos
leprosos en libertad se desplacen hacia las áreas menos preferidas para
evitar ser extorsionados durante el asoleamiento por los galápagos
exóticos. Esta ocupación deficiente de los recursos de asoleamiento
por parte de M. leprosa podría suponer una pérdida de eficiencia en su
comportamiento termorregulador, y el subsiguiente detrimento de las funciones
fisiológicas dependientes de la termorregulación (Cagle 1950; Vogt 1979;
Parmenter 1981; Avery 1982; Gianopulos y Rowe 1999; Rollinson y Brooks
2007).
Capítulo 4
DIFERENCIAS EN LAS TASAS DE INTERCAMBIO DE CALOR
E
l análisis de las medidas biométricas de M. leprosa y T. scripta mostró,
tras corregir por las diferencias entre especies en el tamaño corporal,
que la relación superficie-volumen del galápago leproso es
significativamente mayor que la del galápago de Florida. Ambas especies de
galápagos difieren también en los índices de esfericidad y de aplanamiento,
siendo la forma de los galápagos nativos más aplanada y la de los galápagos
exóticos más esférica. Un análisis posterior no paramétrico mostró además
diferencias significativas entre especies en las tasas de calentamiento y de
enfriamiento (Tablas 4.1 y 4.2; Fig. 4.1), siendo la inercia térmica del galápago
de Florida mayor que la del leproso, tanto en el agua como en el aire. Todas las
tasas de intercambio de calor de los galápagos correlacionaron positiva y
significativamente con su relación superficie-volumen.
La forma del caparazón y la relación superficie-volumen han sido
previamente consideradas como factores influyentes en las tasas de
calentamiento y de enfriamiento de varias especies de galápagos (Boyer 1965;
Spray y May 1972; Gronke et al. 2006). Si bien no es posible descartar que
determinados mecanismos fisiológicos puedan estar relacionados con las
diferencias observadas en las tasas de intercambio de calor de M. leprosa y T.
scripta, los resultados de este trabajo indican que las diferencias morfológicas
observadas entre estas dos especies, producto de la adaptación a distintos
ambientes, determinan también la existencia de diferencias interespecíficas en
sus tasas de intercambio de calor. En un escenario en el que el galápago de
Florida ha sido introducido en el hábitat original del galápago leproso, estas
diferencias podrían influir en el resultado de la competencia entre ambas
176
especies de galápagos. La mayor inercia térmica de T. scripta podría conferir
ventajas competitivas a los galápagos introducidos en las regiones templadas, al
facilitar la retención de calor corporal y permitir un mejor desarrollo de sus
actividades (Huey y Slatkin 1976; Dunham et al. 1989).
Capítulo 5
ESTADO NUTRICIONAL Y REQUERIMIENTOS DE ASOLEAMIENTO
SÍNTESIS DE RESULTADOS Y DISCUSIÓN
L
os resultados de este experimento indican que M. leprosa y T. scripta
difieren en sus requerimientos térmicos. La temperatura preferida de
asoleamiento fue significativamente mayor en la especie nativa que en la
invasora (M. leprosa: media ± EE = 31,9 ± 0,6 °C; T. scripta: 26,7 ± 0,7 °C). Esta
temperatura fue mayor en ambas especies en condiciones de alimentación ad
líbitum que en condiciones de ayuno prolongado (Fig. 5.1), y correlacionó
positivamente con la relación superficie-volumen de los galápagos en ambos
estados nutricionales. Así, los individuos con valores de relación superficievolumen más altos mostraron también temperaturas preferidas de asoleamiento
más elevadas (Fig. 5.2).
El comportamiento termorregulador permite a los ectotermos maximizar sus
funciones fisiológicas, al aproximar su temperatura corporal a un óptimo
térmico específico de cada especie y proceso (Huey y Slatkin 1976; Huey y
Bennett 1987; Angilletta et al. 2002, 2006). Así, las diferencias potenciales en los
óptimos térmicos de M. leprosa y T. scripta podrían explicar las diferencias
interespecíficas observadas en las temperaturas de asoleamiento seleccionadas.
Por otra parte, la correlación observada entre las temperaturas preferidas de
asoleamiento de los galápagos y su relación superficie-volumen sugiere la
existencia de una correspondencia entre los requerimientos térmicos de cada
especie y su morfología específica. La forma esférica de T. scripta, en
comparación con el perfil más aplanado de M. leprosa, confiere a la especie
introducida una menor relación superficie-volumen y una mayor inercia
térmica (Polo-Cavia et al. 2009), facilitando la conservación del calor corporal y
el desarrollo de actividades tales como la búsqueda de alimento o la digestión. Es
posible que los galápagos leprosos, con una mayor relación superficie-volumen,
compensen su mayor tendencia a perder calor seleccionando temperaturas de
asoleamiento superiores a las de los galápagos exóticos. Sin embargo, a
consecuencia de la competencia por los recursos de asoleamiento con el
galápago de Florida, los galápagos nativos pueden encontrar dificultades para
asolearse (Polo-Cavia et al. en prensa), lo que podría dar lugar a efectos
negativos en las tasas de ingestión y en las funciones digestivas de M. leprosa.
177
Los resultados de este trabajo revelan también un claro efecto del estado
nutricional en el comportamiento termorregulador de los galápagos. Ambas
especies respondieron a la privación de alimento seleccionando temperaturas
de asoleamiento inferiores, lo que sugiere la existencia de un mecanismo
adaptativo que permita el ajuste de la temperatura corporal y del metabolismo
en función de la disponibilidad de alimento (Lillywhite et al. 1973; Brown y
Griffin 2005). Sin embargo, la introducción de un nuevo competidor
interfiriendo en el comportamiento termorregulador de M. leprosa podría
empujar a los galápagos nativos hacia una creciente depresión metabólica
impulsada por los efectos retroalimentados de una actividad de asoleamiento
reducida y un estado nutricional deficiente, favoreciendo así la recesión de la
especie nativa.
Capítulo 6
TEMPERATURA CORPORAL Y RESPUESTA DE ‘GIRO’
L
os resultados de este estudio revelaron claras diferencias entre M. leprosa
y T. scripta en los componentes comportamental y mecánico de la
respuesta de ‘giro’. A pesar de que la duración media de la fase de
latencia (medida desde el momento en que los galápagos son depositados en el
suelo con el plastrón hacia arriba hasta que inician el movimiento de ‘giro’) no
difirió significativamente entre galápagos leprosos y americanos, esta fase fue
independiente de la temperatura corporal en el caso de T. scripta, pero no en el
caso de M. leprosa (Fig. 6.1a). Así, los galápagos leprosos experimentaron un
considerable incremento en la duración de sus fases de latencia a 15 °C con
respecto a 20 °C y a la temperatura preferida de asoleamiento de la especie, lo
que sugiere que la percepción del riesgo durante el tiempo en que los galápagos
se encuentran tendidos boca arriba se encuentra más influida por la temperatura
corporal en la especie nativa que en la invasora. La duración de la fase mecánica
(desde el momento en que los galápagos inician el movimiento de ‘giro’ hasta
que recuperan su posición natural) se redujo de forma similar en las dos especies
al incrementar la temperatura corporal de los galápagos (Fig. 6.1b), siendo
significativamente menor a las temperaturas preferidas de asoleamiento
respectivas de cada especie que a 15 y a 20 °C. Esto sugiere la existencia de
coadaptación entre esta temperatura y la respuesta de ‘giro’ de los galápagos. Por
otra parte, M. leprosa necesitó tiempos más largos que T. scripta para volver a su
posición natural con independencia de la temperatura (media ± EE = 151 ± 33 s
vs. 78 ± 34 s) (Fig. 6.1b), lo que indica una mayor eficiencia de los galápagos
exóticos en la fase mecánica de la respuesta de ‘giro’. La forma más esférica que
178
presenta T. scripta en comparación con M. leprosa (Polo-Cavia et al. 2009)
podría facilitar la respuesta de ‘giro’ de los galápagos exóticos. Sin embargo, la
duración de las fases mecánicas de M. leprosa y T. scripta no correlacionó
significativamente con los índices de esfericidad o aplanamiento de cada una de
las especies a ninguna de las temperaturas experimentales, probablemente
debido al efecto de las diferencias individuales en variables que podrían ser
más influyentes en la respuesta de ‘giro’ de estas dos especies de galápagos,
como por ejemplo la longitud del cuello (Rivera et al. 2004; Domokos y
Várkonyi 2008).
La capacidad de los galápagos para recuperar su posición natural tras
resultar volteados accidentalmente, o al ser atacados por un depredador,
puede determinar críticamente su supervivencia (Burger 1976; Finkler
1999; Steyermark y Spotila 2001; Martín et al. 2005). En consecuencia,
el incremento de tiempo que M. leprosa experimenta a bajas temperaturas
en la duración de las fases de latencia y mecánica de su respuesta de
‘giro’ podría comprometer la supervivencia de los galápagos nativos. En
contraste, T. scripta posee una respuesta mecánica más eficiente, a la vez que
su mayor competitividad por los recursos de asoleamiento (Polo-Cavia et al.
en prensa) y su mayor inercia térmica (Polo-Cavia et al. 2009) facilitan
el mantenimiento de temperaturas corporales favorables a la respuesta
de ‘giro’, lo que en suma podría contribuir a la expansión de los galápagos
exóticos.
Capítulo 7
L
os resultados de este experimento indican que ambas especies de
galápagos son capaces de ajustar el tiempo que permanecen refugiadas en
el caparazón tras el ataque de un depredador, decidiendo el momento
más oportuno para escapar activamente en función de la intensidad del ataque,
la persistencia del depredador, el microhábitat y los costes de mantenerse
escondidos en el interior del caparazón. Sin embargo, los galápagos nativos y los
exóticos respondieron de forma diferente al efecto combinado de estos factores
de riesgo. El tiempo medio de aparición (medido desde que los galápagos son
depositados en el suelo tras la simulación del ataque hasta que la cabeza y los
ojos emergen del caparazón) y de espera (desde que los galápagos emergen del
caparazón hasta que inician el movimiento y el escape activo) fueron más largos
en el caso de T. scripta (tiempo de aparición: media ± EE = 19 ± 5 s; tiempo de
espera: 174 ± 27 s) que en el caso de M. leprosa (tiempo de aparición: 5 ± 6 s;
SÍNTESIS DE RESULTADOS Y DISCUSIÓN
COMPORTAMIENTO ANTIDEPREDATORIO
179
tiempo de espera: 93 ± 30 s). Cuando se encontraban en tierra, ambas especies de
galápagos emergieron antes del caparazón cuando el ataque del depredador fue
de menor intensidad, y por tanto, menor el nivel de riesgo percibido por los
galápagos, pero en el agua, tanto M. leprosa como T. scripta emergieron
rápidamente con independencia del nivel de riesgo (Fig. 7.1; Tabla 7.1). Es
posible que los galápagos decidan escapar hacia aguas más profundas y seguras
cuando son atacados en aguas someras, en lugar de tratar de disuadir al
depredador permaneciendo más tiempo escondidos en el interior del caparazón.
Los tiempos de espera de T. scripta no se vieron afectados por el nivel de riesgo
percibido, pero sí por el microhábitat, siendo más largos en tierra que en agua
(Fig. 7.2; Tabla 7.1). En contraste, la duración de los tiempos de espera de M.
leprosa fue independiente del nivel de riesgo percibido en tierra, pero en el agua
los galápagos nativos iniciaron antes la huida cuando la intensidad del ataque
fue mayor. La persistencia del depredador no afectó significativamente a los
tiempos de aparición de ninguna de las dos especies (Fig. 7.1; Tabla 7.1), lo que
sugiere que los galápagos no tienen información de la posición del depredador
mientras se encuentran escondidos en el interior del caparazón (Martín et al.
2005). La persistencia tampoco influyó en los tiempos de espera de los galápagos
introducidos, con independencia del microhábitat. Sin embargo, los tiempos de
espera de M. leprosa en tierra fueron significativamente más largos cuando el
“depredador” permaneció junto a los galápagos, pero el efecto de este factor no
fue significativo en el agua, cuando los galápagos podían escapar hacia un
refugio seguro.
Estas diferencias interespecíficas podrían deberse a los distintos tipos de
depredadores (terrestres vs. acuáticos) que M. leprosa y T. scripta enfrentan en
sus hábitats originales. Mientras que los galápagos leprosos tenderían a escapar
rápidamente hacia el agua ante la amenaza de un depredador (López et al. 2005),
un galápago de Florida que se estuviera asoleando en tierra en su hábitat original
permanecería refugiado en el interior de su caparazón por más tiempo antes de
iniciar la huida hacia el agua, donde podría encontrarse con depredadores más
peligrosos, como caimanes o cocodrilos (Lima 1992; McIntosh y Peckarsky 1999;
Bouwma y Hazlett 2001). Sin embargo, la funcionalidad de las estrategias
antidepredatorias de M. leprosa y T. scripta, adaptadas a sus respectivos hábitats
naturales, podría verse alterada en hábitats modificados antropogénicamente,
donde la presencia de depredadores es reducida. En estos ambientes, T. scripta
podría evitar los costes potenciales de repetidas e innecesarias huidas hacia el
agua (e.g., la interrupción de actividades como el asoleamiento) provocados por
la presencia humana (la cual representa un riesgo bajo de depredación), lo que
podría conferir una ventaja competitiva a los galápagos exóticos sobre los
nativos. Así pues, las diferencias interespecíficas en el comportamiento
antidepredatorio de M. leprosa y T. scripta podrían en parte explicar la mayor
180
habilidad competitiva del galápago de Florida en hábitats con alteraciones
antrópicas. Estos resultados proporcionan un interesante marco para próximos
estudios que investiguen el impacto de la conservación de los ecosistemas en el
éxito de las invasiones.
Capítulo 8
RECONOCIMIENTO DE GALÁPAGOS INTRODUCIDOS POR RENACUAJOS PRESA
SÍNTESIS DE RESULTADOS Y DISCUSIÓN
T
res de las cuatro especies de larvas de anuros estudiadas (Hyla arborea,
Pelophylax perezi y Pelobates cultripes) respondieron a los estímulos
químicos de galápagos depredadores disueltos en el agua modificando
sus niveles de actividad natatoria (Fig. 8.1a, b y c). Los niveles de actividad de
los renacuajos de Bufo calamita, en cambio, permanecieron invariables entre
tratamientos con agua limpia y con los diferentes estímulos químicos (Fig. 8.1d),
lo que sugiere que esta especie es incapaz de discriminar las sustancias químicas
de potenciales depredadores, o al menos, que la presencia de estas sustancias en
el agua no influye en la percepción de riesgo de los renacuajos de esta especie.
Estudios previos han demostrado que diversas especies de Bufo requieren de la
presencia en el agua de sustancias de alarma de coespecíficos, o de estímulos
químicos pertenecientes a depredadores previamente alimentados con
individuos coespecíficos, para desencadenar una respuesta antidepredatoria
(Semlitsch y Gavasso1992; Summey y Mathis 1998; Marquis et al. 2004).
Los renacuajos de H. arborea, P. perezi y P. cultripes redujeron su actividad,
con respecto a la que mostraron en agua limpia, en agua con secreciones de
galápagos nativos, pero no en agua con secreciones de galápagos exóticos (Fig.
8.1a, b y c). La presencia de un estímulo químico neutro (perteneciente a un pez
exótico no depredador) tampoco desencadenó una respuesta antidepredatoria en
ninguna de estas tres especies de anuros, confirmando que la reducción
observada experimentalmente en la actividad natatoria de los renacuajos
responde a la percepción de una amenaza depredatoria. Estos resultados indican
que los renacuajos de estas tres especies de anfibios ibéricos son capaces de
responder a los estímulos químicos de galápagos depredadores nativos
empleando estrategias antidepredatorias adecuadas, pero que no son capaces de
reconocer olores de galápagos depredadores introducidos con los que no
comparten una historia evolutiva ni han tenido un contacto previo. En
consecuencia, los galápagos exóticos podrían capturar más fácilmente renacuajos
nativos e incluirlos en su dieta, en detrimento de los galápagos ibéricos. Esta
trampa evolutiva (Schlaepfer et al. 2005) podría contribuir al desplazamiento de
las poblaciones de galápagos nativos por los galápagos exóticos invasores. No
181
obstante, los renacuajos ibéricos podrían adquirir mecanismos, por evolución o
aprendizaje, que les permitieran reconocer a los nuevos depredadores (Chivers y
Smith 1995; Kiesecker y Blaustein 1997; Bosch et al. 2006), reduciendo así el
impacto de la interacción entre las presas nativas y los galápagos depredadores
introducidos sobre las especies nativas de galápagos.
* * *
Los resultados de los experimentos planteados en esta tesis sugieren la
mayor habilidad competitiva del introducido galápago de Florida, Trachemys
scripta, en la competencia por los recursos con el galápago leproso, Mauremys
leprosa. Los galápagos nativos utilizan presumiblemente las señales químicas
disueltas en el agua para discriminar entre individuos coespecíficos y
heteroespecíficos y evitar así los costes de las interacciones con los galápagos
exóticos, abandonando recursos o desplazándose hacia áreas alternativas menos
favorables. La expansión del galápago de Florida podría además verse favorecida
por la ausencia de respuestas quimiosensoriales hacia los galápagos nativos. Esta
alteración en el uso del espacio por M. leprosa en presencia de T. scripta parece
responder al efecto negativo de la competencia directa con la especie invasora
por el aprovechamiento de recursos fundamentales como el alimento o los
lugares de asoleamiento. Los resultados sugieren que la mayor agresividad de los
galápagos exóticos y su dominancia sobre los nativos suponen el desplazamiento
de M. leprosa hacia recursos subóptimos, y por consiguiente, un detrimento en
el estado nutricional y en el comportamiento termorregulador de los galápagos
autóctonos.
Además, las características propias de cada especie, resultantes de la
adaptación a diferentes ambientes, podrían conferir ventajas competitivas a los
galápagos exóticos en los nuevos hábitats en los que han sido introducidos,
favoreciendo a la especie invasora en el proceso de competencia con los
galápagos nativos. Así, por ejemplo, la forma más esférica de T. scripta le
confiere una menor relación superficie-volumen y una mayor inercia térmica
que facilita la retención de calor corporal y favorece el desarrollo de actividades
y funciones fisiológicas tales como la búsqueda de alimento o la digestión. En
contraste, la mayor tendencia a perder calor de M. leprosa, sumada a la
introducción de un competidor que interfiere en su comportamiento de
termorregulación, podría ocasionar una reducción en la actividad locomotora,
en las tasas de ingestión y/o en la eficacia de la digestión de los galápagos
nativos. Puesto que un estado nutricional deficiente conlleva temperaturas
182
SÍNTESIS DE RESULTADOS Y DISCUSIÓN
preferidas de asoleamiento más bajas en ambas especies de galápagos, las
interferencias de T. scripta en la alimentación y en el comportamiento de
asoleamiento de M. leprosa podrían dar lugar a complicados feed-backs y
alteraciones negativas en el metabolismo de los galápagos nativos. Por otra
parte, la eficiencia en el comportamiento de ‘giro’ de ambas especies de
galápagos se encuentra también fuertemente influida por la temperatura. Este
comportamiento puede ser crítico para la supervivencia de los galápagos, ya que
cuando éstos se encuentran tendidos con el plastrón hacia arriba pueden
experimentar diferentes tipos de riesgo (i.e., deshidratación, depredación,
dificultades respiratorias, etc.). En consecuencia, aquellos individuos que sean
capaces de alcanzar y mantener temperaturas corporales óptimas incrementarán
sus posibilidades de supervivencia. De este modo, la mayor inercia térmica de T.
scripta y su mayor competitividad por los lugares de asoleamiento podrían
también favorecer su supervivencia, en tanto que facilitan su respuesta de ‘giro’,
ya de por sí más eficiente que la de los galápagos nativos. La mayor inercia
térmica del galápago de Florida reduce además el riesgo de sobrecalentamiento
en condiciones en las que los galápagos no pueden controlar su temperatura por
medio de la termorregulación (por ejemplo, si son atacados por un depredador).
Tanto el galápago leproso como el de Florida tienden a refugiarse en el
interior del caparazón tras el ataque de un depredador, ajustando el tiempo que
pasan escondidos en función de factores de riesgo tales como el grado de
amenaza, la persistencia del depredador, las posibilidades de escape hacia un
refugio más seguro y los costes de mantenerse escondidos en el interior del
caparazón (e.g., riesgo de deshidratación, interrupción de actividades como el
asoleamiento, la búsqueda de alimento o potenciales parejas, etc.). En estos
casos, la forma más esférica de T. scripta reduce el riesgo de depredación, pues
dificulta la captura de los galápagos por mamíferos o aves. Por otra parte, los
galápagos introducidos tienden a esperar escondidos más tiempo dentro el
caparazón mientras que los leprosos intentan escapar rápidamente hacia el agua
(probablemente debido a las distintas presiones depredatorias que soportan M.
leprosa y T. scripta en sus hábitats originales). Estas diferencias interespecíficas
en el comportamiento antidepredatorio de los galápagos podrían conferir
ventajas competitivas a la especie introducida en ambientes con modificaciones
antrópicas donde el riesgo de depredación es escaso, y los galápagos nativos
podrían sufrir los costes de repetidas e innecesarias huidas provocadas por la
presencia humana. La alteración del hábitat puede ocasionar desajustes en las
estrategias antidepredatorias de los galápagos, pero puede también afectar a la
propia depredación de los galápagos nativos, al introducir una especie
competidora que constituya una trampa evolutiva para sus presas. Éste es el caso
de varias especies de renacuajos de anuros ibéricos, incapaces de reconocer de
forma innata a los depredadores introducidos con los que no han coexistido en
183
el pasado. En consecuencia, las especies exóticas de galápagos poseen una
ventaja sobre las nativas, en tanto que pueden capturar renacuajos ibéricos con
mayor facilidad.
En síntesis, las diferencias interespecíficas observadas en los distintos
aspectos estudiados de la morfología, ecología y comportamiento del galápago
leproso y del galápago de Florida, apoyan la existencia de una mayor habilidad
competitiva por parte de la especie introducida. Esta asimetría, producto de la
adaptación de M. leprosa y T. scripta a sus respectivos hábitats naturales, parece
conferir ventajas a los galápagos exóticos en la competencia por los recursos con
los galápagos nativos, favoreciendo el desplazamiento de M. leprosa hacia áreas
subóptimas y facilitando así la expansión del galápago de Florida en los nuevos
ambientes en los que ha sido introducido, en detrimento de las poblaciones
nativas de galápago leproso.
— ‚ƒ‚ —
184
Ilustración | Dos galápagos leprosos aprovechan las primeras horas de luz sobre unas rocas
— CONCLUSIONES —
1. El galápago leproso podría utilizar las señales químicas del galápago de
Florida para evitar los costes de las interacciones agresivas durante la
competencia por los recursos con esta especie introducida, lo que conduciría
al progresivo desplazamiento de los galápagos nativos hacia áreas
subóptimas ■
2. La mayor agresividad del galápago de Florida y su dominancia sobre el
galápago leproso durante la competencia por los recursos tróficos podrían
dar lugar a la exclusión competitiva de los galápagos autóctonos y al
consiguiente detrimento en su estado nutricional ■
3. La pérdida de eficiencia observada en la actividad de asoleamiento del
galápago leproso en condiciones de competencia con el galápago de Florida
sugiere la existencia de superimposición y desplazamiento de los galápagos
nativos de los lugares óptimos para el asoleamiento en presencia de los
galápagos exóticos ■
4. La forma más esférica que presenta el galápago de Florida en comparación
con el galápago leproso, su menor relación superficie-volumen y su mayor
inercia térmica, facilitan la retención de calor corporal, pudiendo
conferir ventajas competitivas a la especie introducida en los ecosistemas
templados ■
6. La relación entre el comportamiento termorregulador de los galápagos y su
estado nutricional podría ser la base de complejos efectos negativos
inducidos en el metabolismo de los galápagos leprosos a consecuencia de la
competencia con el galápago de Florida por el alimento y los recursos de
asoleamiento ■
CONCLUSIONES
5. Las interferencias del galápago de Florida en la actividad de asoleamiento de
los galápagos leprosos y su mayor capacidad para retener el calor corporal
podrían en conjunto conferir ventajas termorreguladoras a la especie
invasora ■
185
7. La mayor capacidad de los galápagos exóticos para recuperar su posición
natural tras resultar volteados minimiza el tiempo que permanecen
expuestos a diversos peligros (e.g., deshidratación o depredación),
favoreciendo su supervivencia. Además, la mayor inercia térmica del
galápago de Florida y su mayor competitividad por los lugares de
asoleamiento incrementan la eficiencia de la respuesta de ‘giro’ de los
galápagos introducidos ■
8. Tanto los galápagos nativos como los exóticos ajustan el tiempo que
permanecen escondidos en el interior del caparazón tras el ataque de un
depredador, en función de factores de riesgo tales como la intensidad del
ataque, la persistencia del depredador, las posibilidades de escape hacia un
refugio más seguro y los costes de mantenerse escondidos en el caparazón ■
9. En ambientes con modificaciones antrópicas en los que la presencia de
depredadores es escasa, la estrategia antidepredatoria del galápago leproso de
escapar rápidamente hacia el agua ante la menor señal de peligro podría dar
lugar a la interrupción de actividades como el asoleamiento o la búsqueda
del alimento, facilitando al galápago de Florida la monopolización de los
recursos ■
10. La incapacidad de algunas especies de renacuajos de anuros ibéricos para
detectar y responder de forma innata a los estímulos químicos de los
galápagos depredadores introducidos confiere ventajas depredatorias a estas
especies invasoras de galápagos, al menos hasta que los renacuajos adquieren
mecanismos, por evolución o aprendizaje, que les permiten reconocer a los
nuevos depredadores ■
11. Las asimetrías observadas en la morfología, ecología y comportamiento de
los galápagos nativos y exóticos, consecuencia de la adaptación a sus
diferentes hábitats naturales, parecen favorecer la expansión del galápago de
Florida en los nuevos ambientes en los que ha sido introducido,
contribuyendo a la recesión del galápago leproso ■
— ‚ƒ‚ —
186
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— ‚ƒ‚ —
198
— ANEXO —
LISTADO DE LAS 100 ESPECIES INVASORAS MÁS DAÑINAS DE EUROPA
Fuente: DAISIE-project, disponible online en: www.europe-aliens.org/speciesTheWorst.do
MARINAS
Ficopomatus enigmaticus
Alexandrium catenella
Fistularia commersonii
Dinophyta
Osteichthyes
Balanus improvisus
Halophila stipulacea
Crustacea
Magnoliophyta
Bonnemaisonia hamifera
Marenzelleria neglecta
Rhodophyta
Annelida
Brachidontes pharaonis
Marsupenaeus japonicus
Mollusca
Crustacea
Caulerpa racemosa
Musculista senhousia
Chlorophyta
Mollusca
Caulerpa taxifolia
Odontella sinensis
Chlorophyta
Other algae
Chattonella cf.
Paralithodes camtschaticus
Other algae
Crustacea
Codium fragile
Percnon gibbesi
Chlorophyta
Crustacea
Coscinodiscus wailesii
Pinctada radiata
Other algae
Mollusca
Crassostrea gigas
Portunus pelagicus
Mollusca
Crustacea
Crepidula fornicata
Rapana venosa
Mollusca
Mollusca
Ensis americanus
Rhopilema nomadica
Mollusca
Cnidaria
ANEXO: Listado de las 100 especies invasoras más dañinas de Europa
Annelida
199
Saurida undosquamis
Eriocheir sinensis
Osteichthyes
Crustacea
Siganus rivulatus
Gyrodactylus salaris
Osteichthyes
Platyhelminthes
Spartina anglica
Mnemiopsis leidyi
Magnoliophyta
Ectoprocta
Styela clava
Neogobius melanostomus
Tunicata
Osteichthyes
Teredo navalis
Procambarus clarkii
Mollusca
Crustacea
Tricellaria inopinata
Pseudorasbora parva
Ectoprocta
Osteichthyes
Undaria pinnatifida
Salvelinus fontinalis
Chromista
Osteichthyes
DULCEACUÍCOLAS
HONGOS TERRESTRES
Anguillicola crassus
Ophiostoma novo-ulmi
Nematoda
Fungi
Aphanomyces astaci
Phytophthora cinnamomi
Chromista
Chromista
Cercopagis pengoi
Seiridium cardinale
Crustacea
Fungi
Corbicula fluminea
200
Mollusca
INVERTEBRADOS TERRESTRES
Cordylophora caspia
Aedes albopictus
Cnidaria
Insecta
Crassula helmsii
Anoplophora chinensis
Magnoliophyta
Insecta
Dikerogammarus villosus
Anoplophora glabripennis
Crustacea
Insecta
Dreissena polymorpha
Aphis gossypii
Mollusca
Insecta
Elodea canadensis
Arion vulgaris
Magnoliophyta
Mollusca
Cortaderia selloana
Insecta
Magnoliophyta
Bursaphelenchus xylophilus
Echinocystis lobata
Nematoda
Magnoliophyta
Cameraria ohridella
Fallopia japonica
Insecta
Magnoliophyta
Ceratitis capitata
Hedychium gardnerianum
Insecta
Magnoliophyta
Diabrotica virgifera
Heracleum mantegazzianum
Insecta
Magnoliophyta
Frankliniella occidentalis
Impatiens glandulifera
Insecta
Magnoliophyta
Harmonia axyridis
Opuntia ficus-indica
Insecta
Magnoliophyta
Leptinotarsa decemlineata
Oxalis pes-caprae
Insecta
Magnoliophyta
Linepithema humile
Paspalum paspaloides
Insecta
Magnoliophyta
Liriomyza huidobrensis
Prunus serotina
Insecta
Magnoliophyta
Spodoptera littoralis
Rhododendron ponticum
Insecta
Magnoliophyta
PLANTAS TERRESTRES
Acacia dealbata
Magnoliophyta
Ailanthus altissima
Magnoliophyta
Robinia pseudoacacia
Magnoliophyta
Rosa rugosa
Magnoliophyta
VERTEBRADOS TERRESTRES
Ambrosia artemisiifolia
Branta canadensis
Magnoliophyta
Aves
Campylopus introflexus
Cervus nippon
Bryophyta
Mammalia
Carpobrotus edulis
Lithobates catesbeianus
Magnoliophyta
Amphibia
ANEXO: Listado de las 100 especies invasoras más dañinas de Europa
Bemisia tabaci
201
202
Mustela vison
Psittacula krameri
Mammalia
Aves
Myocastor coypus
Rattus norvegicus
Mammalia
Mammalia
Nyctereutes procyonoides
Sciurus carolinensis
Mammalia
Mammalia
Ondatra zibethicus
Tamias sibiricus
Mammalia
Mammalia
Oxyura jamaicensis
Threskiornis aethiopicus
Aves
Aves
Procyon lotor
Trachemys scripta
Mammalia
Reptilia
L
a introducción de seres vivos fuera de su área de
distribución natural se produce cada vez con
mayor intensidad, dando lugar a fenómenos de
invasión, competencia y desplazamiento de los organismos
nativos de sus nichos ecológicos. En la presente tesis se
abordan diversos aspectos de la biología, ecología y
comportamiento del galápago ibérico Mauremys leprosa,
y del introducido galápago de Florida, Trachemys
scripta, que puedan aportar información acerca de cómo
se están produciendo las interacciones competitivas
entre la especie nativa y la invasora.
Departamento de Ecología Evolutiva
Museo Nacional de Ciencias Naturales
Consejo Superior de Investigaciones Científicas
Departamento de Biología
Facultad de Ciencias
Universidad Autónoma de Madrid