relaciones biogeográficas de cuatro áreas de bosque seco tropical

RELACIONES BIOGEOGRÁFICAS DE CUATRO ÁREAS DE BOSQUE
SECO TROPICAL (COLOMBIA, COSTA RICA Y MÉXICO) UTILIZANDO
COMO GRUPO INDICADOR LOS ESCARABAJOS
COPRONECRÓFAGOS (COLEOPTERA: SCARABAEIDAE:
SCARABAEINAE)
TESIS QUE PRESENTA DORA NANCY PADILLA GIL
PARA OBTENER EL GRADO DE DOCTOR EN CIENCIAS
SISTEMÁTICA
Xalapa, Veracruz, México 2006
1
Aprobación final del documento final de tesis de grado:
Relaciones biogeográficas de cuatro áreas de bosque seco tropical (Colombia, Costa Rica y
México) utilizando como grupo indicador los escarabajos copronecrófagos (Coleoptera:
Scarabaeidae: Scarabaeinae)
Nombre
Firma
Director
Dr. Gonzalo Halffter Salas
Comité Tutorial
Dr. Alejandro Espinosa de los Monteros
Solís
Dr. Juan José Morrone Lupi
Dr. Francisco Cabrero
Jurado
Dr. Pedro Reyes Castillo
Dr. Mario Enrique Favila
Dra. Ellen Andresen
2
DECLARACIÓN
Excepto cuando es explícitamente indicado en el texto, el trabajo de investigación
contenido en esta tesis fue efectuado por Dora Nancy Padilla Gil como estudiante de Doctorado
en Ciencias Sistemática entre agosto de 2002 y agosto del 2006, bajo la supervisión del Dr.
Gonzalo Halffter Salas.
Las investigaciones reportadas en esta tesis no han sido utilizadas anteriormente para
obtener otros grados académicos, ni serán utilizadas para tales fines en el futuro.
Candidato: Dora Nancy Padilla Gil
Director de tesis: Dr. Gonzalo Halffter Salas
3
Con amor dedico este trabajo a mis padres Miguel y Ana Delia, a mis hermanos Myriam y
Wilson y a mi hijo Nicolas
4
AGRADECIMIENTOS
Deseo agradecer al Gonzalo Halffter por la dirección del trabajo de tesis, igualmente a David
Edmonds, Alejandro Espinosa de los Monteros y Juan José Morrone, por la orientación y revisión
del trabajo. A Federico Escobar, Fernando Vaz de Mello, Mario Zunino, Ángel Solís, Francisco
Lorea y Alfonso Díaz, por facilitarme bibliografía y responder mis dudas.
A los jurados de tesis: Ellen Andresen, Francisco Cabrero, Pedro Reyes Castillo, Mario
Enrique Favila.
A Irma Guerrero, Carmen Huerta y Maria Eugenia Rivas por su apoyo. A mis padres Miguel y
Ana, por inculcarme el espíritu de superación y a mis hermanos Myriam y Wilson por su ayuda
incondicional.
Al personal de Postgrado del Instituto de Ecología, por su colaboración y a la Universidad de
Nariño, Pasto (Colombia: Nariño) por otorgarme la Comisión de Estudios.
5
CONTENIDO
Págs.
Presentación
1
CAPITULO 1. Introducción General
3
CAPITULO 2. Biogeography of the areas and Canthonini (Coleoptera: Scarabaeidae) of
dry tropical forests in Mesoamerica and Colombia
7
Abstract
8
Inroduction
11
Materials and Methods
13
Results
19
Discussion
29
Literature cited
33
CAPITULO 3. Mesoamerican and Colombian Dry Tropical Forest and Phanaeine Dung
Beetles (Coleoptera: Scarabaeidae, Scarabaeine): A Cladistic Analysis of Relationships
Abstract
59
Introduction
60
Methods
61
Results
62
Discussion
63
Literature cited
67
CAPITULO 4. Discusión y Conclusiones
Literatura citada
82
95
6
ÍNDICE DE FIGURAS, TABLAS Y APÉNDICES
Págs.
CAPITULO 2
Fig. 1. Study sites
45
Fig. 2. Cladogram of geological areas
46
Fig. 3. Cladogram of the areas of affinity of Canthonini.
47
Table 1. Bibliography consulted for the selection of geomorphological characters
48
Table 2. Geological-geomorphological characters and their states
49
Table 3. Matrix with character states for the cladogram of geomorphological areas
50
Table 4. List of Canthonini species from the study forests
51
Table 5. Data matrix for the cladogram of the Canthonini areas
52
Appendix 1. Scarabaeinae (Canthonini and other tribes) of the forests studied
53
CAPITULO 3
Fig. 1. Study sites
74
Fig. 2. Cladogram of relationships among dry forest sites, using phanaeines as the
indicator group
75
Fig. 3. Cladogram of relationships of dry forest sites using Phanaeus as the
indicator group
76
Appendix 1. Description of study sites
77
Appendix 2. Phanaeini occurring in the study areas
79
Appendix 3. Cladogram data matrix, study site
80
Appendix 4. Phanaeus, Coprophanaeus and Canthon (Glaphyrocanthon) viridis group 81
CAPITULO 4
Cuadro 1. Canthonini, índice de similitud de Jaccard/ distancia
92
Cuadro 2. Phanaeini índice de similitud de Jaccard/ distancia
93
Cuadro 3. Comparación de la diversidad florística de los bsT
94
7
PRESENTACIÓN
Los objetivos de este trabajo son estudiar la biogeografía histórica de los bosques secos
tropicales de Mesoamérica1 y Colombia y establecer la relación entre el origen y la distribución
de los bosques secos tropicales y la biogeografía de los Scarabaeinae (Canthonini y Phanaeini)
presentes en tales bosques secos. Las áreas estudiadas son: en la Costa Pacifica de Mesoamérica,
Chamela (México: Jalisco) y Palo Verde (Costa Rica: Guanacaste); en Colombia en la Región
Caribe, cuatro sitios: Neguanje, Tierra Bomba, Los Colorados y Zambrano; también en
Colombia, en el Valle Superior del Magdalena, el norte del Tolima. Los anteriores bosques secos
conforman el grupo interno, las áreas de bosque húmedo tropical constituyen el grupo externo y
son Los Tuxtlas (Veracruz, México) y Leticia (Amazonas, Colombia).
El capítulo II incluye tanto la biogeografía de las áreas de bosque seco (bsT) como la
biogeografía de los Canthonini; el capitulo III comprende la biogeografía de áreas de bsT
tomando como indicador a los Phanaeini y el análisis comparativo entre las relaciones de los
Canthonini y Phanaeini que comparten los mismos escenarios biogeográficos.
La biogeografía de las áreas de bosque seco se abordó a través de un análisis cladístico basado
en caracteres geológicos y geomorfológicos de los terrenos donde se ubican los enclaves de
bosque seco y su interpretación en el contexto histórico-geográfico, climático y ecológico. Para el
análisis biogeográfico de los Canthonini y de los Phanaeini de los bosques secos se utilizó el
Análisis de Parsimonia de Endemismos (PAE) enraizando el cladograma con el grupo externo
previamente indicado. Para este análisis se tomó en cuenta la información publicada para cada
una de las localidades, los estudios faunísticos, ecológicos, biogeográficos, taxonómicos y
filogenéticos sobre los Canthonini y Phanaeini, las bases de datos SNIB-CONABIO de México e
INBio de Costa Rica. Los resultados revelan la formación de los bosques secos a partir del
Pleistoceno y la fijación de sus condiciones ambientales a partir del Holoceno Medio.
Considerando los Canthonini, los bosques secos más afines son los de Colombia y Chamela
(México). Se plantean tres patrones que explican tanto las relaciones como su presencia en los
bosques secos. Los bosques secos de Chamela y Palo Verde más los del Valle Superior de
Magdalena y la Región Caribe de Colombia, según los Phanaeini presentan mayor afinidad; se
1
Mesoamérica incluye México y los siete países de América Central (Guatemala, Belice,
Honduras, El Salvador, Nicaragua, Costa Rica y Panamá; 7- 18°N y 77- 92°W). Ver distribución
geográfica del bosque seco tropical, fig. 1.
1
plantea un patrón biogeográfico que explica los resultados anteriores. El análisis biogeográfico
comparativo entre los dos grupos establece la convergencia del patrón de especiación in situ y
proporciona elementos para formular varias hipótesis biogeográficas. La biogeografía de los
enclaves de bosque tropical seco de Mesoamérica y Colombia y la coincidencia espacio-temporal
de los Canthonini y Phanaeini en el mismo escenario permitió proponer elementos tanto para
entender el origen y la evolución de los bosques secos como los patrones de distribución de los
dos grupos de Scarabaeinae, así como plantear nuevas hipótesis sobre el probable origen espaciotemporal de los Canthonini y Phanaeini de los bosques neotropicales considerados.
2
CAPÍTULO I
Introducción General
La biogeografía es la disciplina científica consagrada al estudio de los patrones de distribución
espacial de los organismos y las causas o procesos históricos y ecológicos que los determinan. En
esta definición se subrayan las dos aproximaciones esenciales al estudio de distribución de
organismos: la que indaga las causas próximas que operan en el presente (escala ecológica) y la
que estudia las causas pretéritas de gran magnitud espacio-temporal (escala histórica) (MartínPiera & Sanmartín 1999).
Dentro de la biogeografía histórica contemporánea existen tres enfoques para explicar la
distribución de los seres vivos: el dispersalismo, la panbiogeografía y la biogeografía cladística.
El más antiguo es la biogeografía dispersalista, que se originó a partir de las ideas de Darwin y
Wallace a mediados del siglo XIX (Crisci y Morrone 1992). Trabaja con taxones individuales, en
el sentido que son los organismos poblaciones/especies los que se dispersan sobre una geografía
estable. Como reacción a la biogeografía dispersalista, a mediados del siglo XX surge la
panbiogeografia, la cual fue propuesta originalmente por Croizat (1958). Croizat hizo énfasis en
el análisis conjunto de diferentes taxones para buscar patrones comunes de distribución, evitando
analizar un sólo taxón como se hacía tradicionalmente. Supone que organismos con distintas
capacidades de dispersión pueden compartir similitudes en sus distribuciones, ya que cualquier
distribución en plantas de alguna u otra forma tiene su contraparte en los animales (Craw et al.
1999). A partir de la combinación de la biogeografía con la sistemática filogenética, surge la
biogeografía cladística en la década de los setenta (Morrone et al. 1996).
El Análisis Parsimonioso de Endemicidad (PAE) es considerado como una técnica
panbiogeográfíca y ha sido aplicado por diferentes autores (ver Morrone 2004). La
panbiogeografía intenta identificar homologías biogeográficas primarias, las cuales suponen una
historia biogeográfica común. La biogeografía cladística asume la correspondencia entre las
relaciones filogenéticas de los taxones estudiados y las relaciones entre las áreas donde éstos
habitan y trata las homologías biogeográficas secundarias, las cuales representan la prueba
cladística de la homología biogeográfica primaria antes reconocida. La panbiogeografía y la
biogeografía cladística pueden ser combinadas bajo el denominador común de “biogeografía
vicariante”, cuyo principal objetivo es la homología biogeográfica (Ebach & Morrone 2005).
Las relaciones entre áreas geológicas tratan las áreas como unidades funcionales (reales) y
3
plantean hipótesis similares a las presentadas en sistemática filogenética (Wiley 1988). Craw
(1988) implementó esta metodología enraizando el cladograma con base en un área geológica
ancestral hipotética codificada en ceros.
En la biogeografía histórica la reconstrucción de eventos pasados puede ser realizada desde tres
perspectivas diferentes, cada una con objetivos diferentes: 1) reconstrucción de la distribución
histórica de grupos individuales (biogeografía del taxón), 2) reconstrucción de las áreas de
endemismo (búsqueda de relaciones generales de áreas, biogeografía de área) y 3) reconstrucción
de la distribución histórica de biotas (todas las especies que habitan en una región específica y
comparten una historia geográfica). Las dos últimas buscan la homología espacial: elementos
comunes espacio-temporales compartidos de la biogeografía histórica (Crisci et al. 2006).
La base del conocimiento biogeográfico está integrada por los patrones de distribución
geográfica de los organismos, las relaciones (genealógicas) entre ellos y el conocimiento acerca
de la historia del espacio físico en que se distribuyen. Por tanto, la base explicativa de la
biogeografía histórica integra los principios biológicos generales que relacionan espacio y
evolución (Andersson 1996). Los patrones de distribución de los grupos de organismos han sido
determinados por evolución, adaptaciones fisiológicas y etológicas, mecanismos de dispersión e
igualmente por habilidades de dispersión, competencia entre especies, sucesión ecológica,
cambios de clima, cambios en el nivel del mar, movimiento de los continentes y recientemente,
por los impactos directos e indirectos de los seres humanos (Spellerberg & Sawyer 2000). Los
patrones de distribución de los organismos son el resultado de ecología e historia y representan el
objetivo común y último hacia la aproximación de la biogeografía ecológica e histórica (Crisci et
al. 2006).
Los objetivos de este trabajo son estudiar la biogeografía histórica de los bosques secos
tropicales de Mesoamérica y Colombia y establecer la relación entre el origen y la distribución de
los bosques secos tropicales y la biogeografía de los Scarabaeinae (Canthonini y Phanaeini)
presentes en tales bosques secos.
El bosque seco tropical (bsT) o bosque tropical caducifolio o selva caducifolia, se define como
aquella formación vegetal que presenta una cobertura boscosa continua, con condiciones de lluvia
marcadamente estacionales, que se distribuye entre los 0-1000 m de altitud, con temperaturas
superiores a los 24 ºC y precipitaciones entre los 700 y 2000 mm anuales (IAvH 1997). Presenta
especies arbóreas que pierden sus hojas en la época seca del año durante un lapso variable que en
4
general oscila alrededor de seis meses (Rzedowski 1978).
El bsT se encuentra dentro de los ecosistemas más intensamente utilizados, perturbados y
menos conservados del Neotrópico. Tanto el origen como la biogeografía histórica de los bosques
secos neotropicales siguen siendo imprecisas y poco entendidas (ver Sarmiento 1975, Pennington
et al. 2000, Becerra 2005).
De acuerdo con Sarmiento (1975), es probable que las formaciones vegetales secas actuales de
Centro y Suramérica se hayan originado y evolucionado de manera independiente desde hace 1.8
millones de años, a partir de cuatro grandes comunidades florísticas. La primera incluye los
bosques secos tropicales que se extienden desde el sur de México al norte de Sudamérica; la
segunda incluye las formaciones de Caatingas del noreste de Brasil; la tercera, los bosques del
Chaco, y la cuarta, los arbustales y bosques de clima mediterráneo del centro y sur de Chile.
Este trabajo aborda la primera comunidad florística delimitada por Sarmiento (1975). Para tal
efecto se eligieron los siguientes bosques secos tropicales: en la Costa Pacifica de Mesoamérica:
Chamela (México: Jalisco) y Palo Verde (Costa Rica: Guanacaste); en Colombia en la Región
Caribe, cuatro sitios: Neguanje, Tierra Bomba, Los Colorados, Zambrano, y en el Valle Superior
del Magdalena: el Norte del Tolima.
Los grupos de Scarabaeinae seleccionados son dos tribus, los Canthonini (excepto el género
Deltochilum) y los Phanaeini, las cuales presentan distribución neotropical. Estos grupos han sido
incluidos en numerosos estudios faunísticos y ecológicos principalmente relacionados con
diversidad y abundancia, algunos de éstos en los bosques secos tropicales (ver Andresen 2005).
Sin embargo, se desconocen las afinidades de ésta biota en los distintos bsT así como las
relaciones con el origen y distribución de los bsT y el porqué de su distribución geográfica.
Las relaciones biogeográficas de las áreas de bsT, así como la presencia de los Scarabaeinae en
tales áreas se basa en una serie de hipótesis y se explican empleando una perspectiva holística
que tiene en cuenta los eventos histórico-geomorfológicos de los terrenos donde se ubican los
bosques secos, el origen y eventos climáticos, las afinidades taxonómicas y/o filogenéticas y los
factores que influyeron en los procesos de especiación y dispersión de los taxones implicados.
En el segundo capítulo se incluye la biogeografía histórica de las áreas de bosque seco que
pretende inferir y explicar el origen y relaciones histórico-geomorfológicas de tales enclaves. Las
relaciones biogeográficas de los Canthonini y de los Phanaeini (Scarabaeinae) en los bosques
secos de Mesoamérica y Colombia se abordarán en sendos capítulos (II y III), los cuales se
5
orientan bajo los siguientes supuestos:
1) El origen y establecimiento de los bosques secos guarda relación con los procesos de
dispersión y especiación de los Scarabaeinae examinados.
2) Los Scarabaeinae de los bosques secos muestran relaciones taxonómicas y biogeográficas
con los taxones provenientes de Sudamérica.
3) Tanto los Canthonini como los Phanaeini de bsT presentan similaridades en sus patrones
biogeográficos. El análisis de sus relaciones aportará argumentos para plantear nuevas hipótesis
biogeográficas.
El estudio biogeográfico es abordado bajo una concepción histórica y ecológica para permitir
una aproximación al entendimiento del origen y de las relaciones de los bosques secos de
Mesoamérica y Colombia, la identificación de los patrones biogeográficos de los Scarabaeinae
presentes en tales enclaves, y la formulación de hipótesis sobre los procesos que los causan.
6
CAPITULO 2
Biogeography of the areas and Canthonini (Coleoptera: Scarabaeidae) of dry tropical forests in
Mesoamerica and Colombia
Acta Zoológica Mexicana, vol. 23, 1 (2007)
7
CAPÍTULO II
BIOGEOGRAPHY OF THE AREAS AND CANTHONINI (COLEOPTERA:
SCARABAEIDAE) OF DRY TROPICAL FORESTS IN MESOAMERICA AND
COLOMBIA
Dora Nancy PADILLA-GIL1 and Gonzalo HALFFTER 1
1
Instituto de Ecología, A.C., Apdo. Postal 63, 91000 Xalapa, Veracruz, MEXICO
[email protected], [email protected]
ABSTRACT
This biogeographical analysis examines the historical, geological, climatic and ecological
processes that have influenced the formation of the dry tropical forests (DTF) of Mesoamerica
and Colombia, areas that are the setting for multiple biogeographical stories that in this case are
illustrated by the patterns and evolutionary processes of Canthonini. In this study we test the
hypothesis that the Canthonini fauna of dry tropical forests has a South American affinity. To this
end, we compare extant species from a tract of dry tropical forest in Mexico, a second enclave in
Costa Rica, four from the Caribbean region of Colombia and finally one from the north of Tolima
in the Upper Magdalena River Valley, Colombia. The geomorphological characteristics of the
enclaves of DTF are also compared, as are the geographical distribution and taxonomic affinities
of each of the species found in these dry tropical forests. The biogeographical, historical and
geological aspects of the enclaves were evaluated using a Parsimony Analysis of Endemicity
(PAE), with two tropical rain forests as the outgroup: Leticia (Amazonas, Colombia) and Los
Tuxtlas (Veracruz, Mexico).
This study reveals the origin and distribution of Neotropical dry forests in the Pleistocene, and
the establishment of its dry conditions during the Holocene. It also reveals apparent similarities
among the Canthonini of the dry tropical forests of Mexico, Costa Rica and Colombia, with three
geographical distribution patterns that correspond to different degrees of expansion towards the
north and the diversification of evolutionary lines, and even species of South American origin.
The comparison of the cladogram generated for species of Canthonini with that of the geological
events that have occurred in the study regions indicates that the distribution of Canthonini in dry
tropical forests began during the Pliocene with the re-establishment of the Panamanian
8
connection, with no evidence of previous geomorphological events having any influence. On the
other hand, there are few species shared with the tropical rain forests used as the outgroup for the
cladograms.
Key words: Scarabaeinae, Canthonini, dry tropical forest, Mexico, Costa Rica, Colombia,
biogeographical patterns
RESUMEN
Este análisis biogeográfico examina los procesos históricos: geológicos, climáticos y ecológicos
que han influido en la formación de los bosques tropicales secos (DTF) de Mesoamérica y
Colombia, bosques que son sitios de múltiples historias biogeográficas como la que ilustran los
Canthonini. Sometemos a prueba la hipótesis que la fauna de Canthonini de los bosques
tropicales secos tiene una afinidad sudamericana. Para este propósito comparamos las especies
que se encuentran en un enclave de bosque tropical seco en México, en un segundo enclave en
Costa Rica, en cuatro de la región Caribe de Colombia y finalmente uno más en el norte de
Tolima en el valle superior del río Magdalena, Colombia. Las características geomorfológicas de
los enclaves son también comparadas, así como la distribución geográfica y las afinidades
taxonómicas de cada una de las especies de Canthonini que se encuentran en estos bosques
tropicales secos. Los aspectos de historia biogeográfica, geológica y ecológica de los enclaves
son evaluados usando un Análisis de Parsimonia de Endemicidad (PAE), utilizando como grupo
externo dos lugares de selva siempre-verde: Leticia (Amazonas, Colombia) y Los Tuxtlas
(Veracruz, México). Este estudio pone de manifiesto que el origen y distribución de los bosques
tropicales secos de la región ocurre durante el Pleistoceno, con una acentuación de las
características de sequía durante el Holoceno. También revela similitudes entre los Canthonini de
los bosques tropicales secos de México, Costa Rica y Colombia, con tres patrones de distribución
que corresponden a diferentes grados de expansión hacia el norte y a la diversificación de líneas
evolutivas, e incluso la presencia de especies sudamericanas.
La comparación entre el cladograma generado por las especies de Canthonini y el de eventos
geológicos, indica que la distribución de los primeros en los bosques tropicales secos comienza
en el Plioceno con el restablecimiento de la conexión panameña, sin evidencias de que eventos
geomorfológicos previos hayan ejercido influencias. Por otra parte, hay muy pocas especies
9
compartidas con la selva siempreverde usadas como grupo externo en los cladogramas.
Palabras clave: Scarabaeinae, Canthonini, bosque tropical seco, México, Costa Rica, Colombia,
patrones biogeográficos.
10
INTRODUCTION
It has been suggested that tribe Canthonini (Scarabaeidae: Scarabaeinae) has an ancient
Gondwanian distribution with high species richness in South America (Halffter 1974). In the
Americas, the genus with the most species is Canthon, with 174 according to Halffter & Martínez
(1977) that are distributed from Argentina to Canada. The origin of Canthon and close genera
appears to be northern South America where it reaches its greatest richness in phyletic lines and
species, with an expansion of lines toward the periphery of Chile where it is barely represented
(Halffter 1974, Rivera-Cervantes & Halffter 1999). From South America, Central and North
America were populated by elements of this tribe during two probable great expansion events
(Halffter 1964, 1974, 1976, Kohlmann & Halffter 1990). The first could have occurred before or
during the Miocene and the second when the connection with South and Central America was reestablished from the Pliocene to the Recent. In the phyletic lines that participated in the first
expansion, although it is possible to identify the South American affinities at the level of genus,
there was a notable speciation in Mexico and the United States of America, followed in some
cases by secondary expansion. For those phyletic lines that participated in the second expansion
event, the affinities with northern South America are much more marked, although there was also
in situ speciation.
The objective of this study is to test this biogeographical hypothesis. To that end, we chose to use
the species of Canthonini that inhabit dry tropical forest (DTF). These were selected because they
are the least studied Scarabaeinae fauna compared to their tropical rain forest (TRF) counterparts
and also because their distribution, now discontinuous, has been much less interrupted in the
recent past.
This hypothesis regarding the biogeographical history of the Canthonini (common for other
groups of Scarabaeinae and, in general, for insects) has been tested in various ways. First, by
establishing the similarity of the Canthonini present in a series of enclaves found in DTF in
Mexico, Costa Rica and Colombia – places for which we have reliable lists of the fauna. Second,
we have analyzed the historical and geological relationships of the regions where these enclaves
are located in order to relate the history of the areas with both the phylogeny and the geographical
distribution of Canthonini. Finally, the two previous points are integrated in order to recreate the
setting of the DTF where the processes of speciation and dispersion of some Canthonini probably
took place, and also to explain their geographic distribution. As proposed by Zunino (2005) we
11
intend to compare the distribution and phylogenetic history of the taxa with the geography and
geomorphological history of the areas to arrive at a comprehensive interpretation of the entire set
of elements.
DTF, also known as tropical deciduous forest or low deciduous forest is defined as that formation
of vegetation with a continuous woody cover distributed from sea level to 1000 m, with mean
temperatures above 24 ºC and precipitation ranging from 700 to 2000 mm per year (Espinal
1985; IAvH 1997a). This vegetation has woody species that lose their leaves during the dry
season over a variable period of time that lasts around six months (Rzedowski 1978).
According to Rzedowski (1978) DTF is particularly characteristic of the Pacific Slope of Mexico,
where it covers extensive areas almost uninterrupted from the south of Sonora and southwest of
Chihuahua to Chiapas, continuing southwards in Central America. It penetrates deep into the
Balsas and the Santiago River basins, as well as those of the tributaries of these rivers. In the
Isthmus of Tehuantepec, DTF passes the watershed and occupies a good part of the Central
Depression of Chiapas. On the Atlantic Slope there are at least three large patches of DTF and it
is also found on the Yucatan Peninsula (see Trejo 2005).
In Mexico, DTF once covered 6 to 14% (270 000 km2) of the area in the country that lies
between sea level and 1500 m. DTF has been reduced to 27% of its original cover (Trejo & Dirzo
2000). In Costa Rica almost all of the Nicoya Peninsula and Chira Island in the northeast of the
country were covered by this type of forest 100 years ago (Kohlmann et al. 2002). In Central
America, DTF once covered 7% (33 600 km2) of the total area between 0 and 1000 m. The
remaining tropical dry forest in Central America probably represents less than 2% of the original
(Sabogal & Valerio 1998). Colombia has three large regions with DTF and the two largest are the
Caribbean Plain, including southern Guajira and the Magdalena River Valley in the Departments
of Tolima, Cundinamarca and Huila (IAvH 1997b). In Colombia the status of DTF is critical. It is
estimated that only 1% of the original 80 000 km2 of dry to subhumid forests remains (Etter
1993). Figure 1 summarizes the distribution of DTF in the study area.
The biogeography of the areas of dry tropical forest is undertaken with cladistic analysis, keeping
in mind the past and present geological and geomorphological characteristics of the area. In order
to understand the biogeographical relationships between the enclaves of DTF and the species of
Canthonini, we used a Parsimony Analysis of Endemicity (PAE) that produces a hierarchical set
of the species represented in the different areas, and associates it with the geological or ecological
12
factors, or a combination thereof. PAE can provide the grounds for explaining: 1) the effects of
geological events on evolution; 2) the effects of ecological factors on evolution; 3) the influence
of geological events on ecological conditions and the evolutionary consequences of these; 4)
distribution patterns, i.e. which sets of species can appear in different areas owing solely to
events in geological history or the association of the latter with ecological conditions (Rosen
1988).
This study has two purposes, the first is to analyze the biogeographical history of the areas of dry
tropical forest in Mesoamerica and Colombia based on their geomorphological characteristics and
their geological origin; the second is to establish the relationships between these forests using the
Canthonini as an indicator group, comparing their distribution with the geomorphological history
of those areas and explaining the presence of Canthonini in dry forest.
First we carry out the biogeographical analysis of the Neotropical dry forests that are the object
of this study, and then the biogeographical analysis of the Canthonini. Some aspects of
Canthonini in dry forest are discussed in light of other floristic, faunal, ecological and
biogeographical elements that are particularly related to the Canthonini and the geographical
limits of some species.
MATERIALS AND METHODS
Study sites
The DTF sites we selected in Mesoamerica and Colombia are enclaves representative of the
current distribution of this type of vegetation (Fig. 1). Chamela (Jalisco, Mexico) and Palo Verde
(Guanacaste, Costa Rica) are located on the Pacific coast. In the Caribbean region of Colombia
we selected four areas: Neguanje, Tierra Bomba, Los Colorados and Zambrano. In the
Magdalena River Valley, we selected the DTF located in the north of the Department of Tolima.
Two of the sites selected in the Caribbean region, Los Colorados and Neguanje, have the highest
floristic richness, basal area and canopy height of the DTF found in the Caribbean and Tolima
region (Mendoza 1999). Another factor which led to the selection of these sites was the
availability of information on the Scarabaeinae fauna. There are publications for each of the sites,
and there are also databases for Costa Rica (INBio) and Mexico (SNIB-CONABIO). The sites are
described below together with the most relevant features associated to geological and
geomorphologic characters (see Tables 1 & 2).
13
Chamela, Jalisco, Mexico. The Chamela-Cuixmala Biosphere Reserve is located on the Pacific
coast (19º 30’ N, 105º 03’ W). The study site is between the San Nicolas River in the north and
the Cuixmala River in the south, centred in the surroundings of the Chamela Biological Station
(Fig. 1). With altitudes lower than 200 m, the climate has no marked seasonality with respect to
temperature. Mean monthly maxima range from 28.8 to 32.2 ºC, and the minima from 15.9 to
22.6 ºC. Mean annual precipitation is 707 mm. The rainy season lasts four months on average,
starting at the beginning of July and ending at the beginning of November (Bullock 1988).
Chamela belongs to the Jalisco Block (JB), which constitutes a tectono-stratigraphic assemblage
from the Late Cretaceous to Early Tertiary (Paleocene), with volcanic and volcaniclastic
deposits and marine sedimentary sequences intruded by granitoid plutons. The plutonic and
volcanic rocks of the JB are part of the magmatic arc, which is found southeastward along the
terrain of the state of Guerrero. On the other hand, Chamela is aseismic and is located on the
North American tectonic plate. It is characterized by an undulating landscape, the presence of
metals, soil with low permeability and organic matter
Palo Verde, Guanacaste, Costa Rica. The Palo Verde Biological Station (Fig. 1) is located in
the Palo Verde National Park (10º 20’ N, 85º 18’ W) on the Pacific slope, in the Province of
Guanacaste and halfway up the basin of the Tempisque River at an altitude of 10 to 50 m. Mean
annual temperature ranges from 24.0 to 27.8 ºC and mean annual precipitation is 1750 mm
(Quigley & Platt 2003), with a 6.5 month long dry season each year (SIEPAC 2003).
It is characterized by an undulating landscape, with slightly developed soils, and the most
abundant minerals are olivine-pyroxene. The local fault is responsible for the seismicity. The
Palo Verde region dates from the Paleocene to Early Eocene. This site is characterized by high
magnetism, and is located on the Caribbean tectonic plate
Colombia, Caribbean Region. The sites selected (Fig. 1) have been described by Mendoza
(1999). Located between 50 and 300 m, their mean temperatures are greater than 24 ºC and they
receive 700 to 2000 mm of precipitation per year. There are two marked dry seasons per year
(IAvH 2000). This region is represented by four sites:
a) Zambrano: Forest Reserve, Monterrey. Located in the Departament of Bolivar, Zambrano
Municipality (9º 37’ 48” N, 74º 54’ 44” W) at 155 m. Mean annual precipitation is 1048 mm.
b) Los Colorados. Located in the Departament of Bolivar, San Juan de Nepomuceno
Municipality (9º 51’ 33” N, 75º 06’ 38”W), at 300 m. Mean annual precipitation is 1189 mm.
14
This remnant of DTF belongs to the Los Colorados Flora and Fauna Sanctuary Conservation
Unit.
c) Tierra Bomba Island. Located in the Department of Bolivar, Cartagena Municipality (10º 21’
36” N, 75º 34’ 11” W), at 50 m. Mean annual precipitation is 789 mm.
d) Neguanje. Located in the Department of Magdalena, in the Santa Marta Municipality (11º
18’05” N, 74º 06’ 11” W) at 300 m. Mean annual precipitation is 1420 mm. Neguanje belongs to
the Tayrona National Park.
The Caribbean Region is located between the Perijá to the east and the Sierra Nevada. On the
surface, fluvial and lacustrine sediments from the Quaternary predominate. It is characterized by
a sequence of sandy, slime and clay and feldspar is the most abundant mineral in the sandy
fraction of the soil. It is aseismic and located on the Caribbean tectonic plate. In geological terms,
Neguanje belongs to the geotectonic province de Santa Marta (land originating in the Mesozoic:
Middle Jurassic to Late Cretaceous) and the other three sites belong to the province of Caribbean
Plain: Zambrano belongs to the San Jorge-Plato geostructure (the land dates from the
Quaternary), Los Colorados to the San Jacinto Belt (the land dates from the Tertiary: Late
Eocene) and Cartagena to the Sinú Belt (Tierra Bomba is from the Quaternary). The Sierra
Nevada is associated with the Santa Marta fault and the Caribbean Plain is associated with the
Romeral fault system in the west.
North Tolima. We selected the study area described by Escobar (1997). It is located on the east
side bank of the Magdalena River (Fig. 1), 130 km from the city of Ibagué in the jurisdiction of
the municipalities of Honda, Armero-Guayabal and Piedras, at (4º 15’ - 5º 10’ N, 74º 45’ - 74º
50’ W) at 250 m. Mean annual precipitation is 1387 mm and the mean annual temperature is 28
ºC, with two well defined dry periods, one from December to March and the other from June to
August.
North Tolima forms part of the Upper Magdalena River Valley, an inter-Andina valley on the
eastern slope of the Cordillera Central. It belongs to the Honda formation dating from the
Tertiary: Miocene. There are faults nearby and it is associated with the Plio-quaternary volcanic
activity of the Cordillera Central, as reflected in its notable seismicity.
Los Tuxtlas, Veracruz, Mexico. The Los Tuxtlas Biological Station is located in the foothills of
the San Martin Volcano, 19 km north of the city of Catemaco in the state of Veracruz (Fig. 1; 18º
34’ - 18º 36’ N, 95º 04’ - 95º 09’W) at 150 to 530 m. Mean annual precipitation is 4560 mm and
15
the mean annual temperature is 23.7 ºC (Morón 1979).
Los Tuxtlas Reserve belongs to the formation La Laja, which dated Oligocene and is located on
the North American tectonic plate. It is characterized by an undulating landscape, igneous rocks
of continental origin, nearby mountains, soils with high permeability and organic material, and
high seismicity.
Leticia, Amazonas, Colombia. The Colombian Amazon has a humid tropical climate. The site is
located at 4º 8’ S, 70º 1’ W, and 96 m (Fig. 1). Mean annual precipitation is 3500 mm, with the
majority of the rain falling between April and June. Mean annual temperature is 26 ºC, with
maximum temperatures in October and November 35 ºC. It is cooler in July with minima from 20
to 25 ºC (Galvis et al. 1979).
It is characterized by an undulating landscape, with highly evolved soils, a limited presence of
minerals and low levels of natural fertility. Quartz dominated more than 90% of the sandy
fraction and potassium was scarce. This geomorph developed over sedimentary rocks with thick
grain. The Quaternary deposits are comprised of sand, possibly of eolic origin, with recent
terraces and alluvial deposits. This is an aseismic region located on the South America plate.
Ingroup and Outgroup
Our decision to use a real outgroup is based on the fact that the rain forest provides ecological
characteristics that contrast with those of dry forest and take into account previous hypotheses
about its probable origin in Neotropical forest. Also, rain forest is supposed to be older than dry
forest (see Sarmiento 1975, Platt et al. 1981, Gentry 1982, Hooghiemstra & van der Hammen
2001, Richardson et al. 2001, Hooghiemstra et al. 2002, Graham 2003). The use of an outgroup
provides both a geographical context and vegetation formations that contrast with the
characteristics of the areas, where Scarabaeinae we are studying are currently found.
Geomorphological cladogram
Historical and geomorphological relationships were analyzed following Craw (1988). The seven
dry forests make up the ingroup, however our analysis differs because for the outgroup we have
used real sites of tropical rain forest, instead of coding for the outgroup with zeros. The rain
forests selected carrying out the analysis using this outgroup allows the cladogram to be polarized
and hence produces a more parsimonious solution than one that uses zeros.
In order to select characters and assign character states for each of the sites, more than fifty
references were consulted. The list of the main studies consulted is presented by country in table
16
1.
The geologic-geomorphological characters provide evidence from different sources of characters:
geomorphostructural, geophysical and of edaphic. The geomorphostructural characteristics of the
terrain are defined by its geological and morphostructural history (origin and evolution) and by
the lithological composition of the materials. Geophysical characters include the geotectonic,
magnetic and gravimetric anomalies of the physiographical regions. On the other hand, the origin
of the soil is influenced by the relative material, relief, climate and the organisms that are present.
Eighteen characters and their states were selected (Tables 2 & 3). Ambiguous characters were
discarded as were those for which there is insufficient information for more than two sites. All
the characters were given equal weight, with three ordered characters: 8, 9 and 16. These
characters were taken as ordered because they are related to chronological sequences of events
associated to the scale of geological time.
Cladogram of the areas of affinity for the Canthonini
The relationships of DTF were analyzed using Parsimony Analysis of Endemicity (PAE), where
the taxa are analogous to the sites and the characters to the species. In contrast to the
methodology proposed by Rosen (1988) where the cladogram is rooted in a hypothetical ancestral
area coded in zeros, here we use an external group, the outgroup, of real sites. The ingroup and
outgroup are the same as mentioned for the previous analysis.
We chose PAE because it allows for the use of an outgroup in the analysis, the polarization of
the cladogram, the addition of taxonomic hierarchies and it has a small data matrix.
A cladogram of the areas was generated using lists of the species (Table 4) present in each forest,
indicating presence (1) or absence (0) according to the matrix (Table 5). Given that 24 of the 28
species belong to the genus Canthon, the subgenera of this taxon were included. The PAUP
4.0b10 (Swofford 2002) program with Acctran optimization and exhaustive search was used. The
results were analyzed based on the majority consensus tree as it offered the greatest resolution.
Canthonini Species
All the genera of Canthonini present in the forests studied are included in the analysis, with the
exception of Deltochilum for which there is insufficient taxonomic and biogeographical
information.
In order to compile the lists for Palo Verde and the Mexican site, in addition to a review of the
publications mentioned below, the following data bases were used: INBio (Costa Rica) and
17
SNIB-CONABIO (Mexico). The following publications were consulted: Chamela - Morón et al.
(1988), Andresen (2005); Palo Verde - Kohlmann & Wilkinson (2003); North Tolima - Escobar
(1997), Bustos-Gómez & Lopera-Toro (2003); Caribbean Region of Colombia - Escobar (1998,
2000a); species lists for these Colombian sites were also provided by F. Escobar; Leticia – list
compiled by Bruce Gill, 12, I, 1997 with material collected by Howden & Nealis (1975), Escobar
(2000a), Medina et al. (2001); Los Tuxtlas - Morón (1979), Halffter et al. (1992), Favila & Díaz
(1997), Deloya & Morón (1998), Díaz (1998, 2003).
Canthon deyrollei was described by Harold in 1868, with the type locality unknown. It has been
included for Colombia, without any other data in numerous publications (Vulcano & Pereira
1964, Howden & Young 1981, Solis & Kohlmann 2002). In the publications that we consulted
for Colombia this species is either not recorded or is not assigned a locality. Hence, the record for
Colombia was not included.
Canthon cyanellus and C. indigaceus are included in the analysis with their respective
subspecies according to Halffter (1961).
Geographical distribution of Canthonini
There are many studies that include the geographical distribution of Canthonini in Mexico. Some
of those that we consulted for this study are: Halffter 1961, 1964, 1976; Martínez et al.1964;
Halffter & Matthews 1966; Barrera 1969; Martínez & Halffter 1972; Morón & Terrón 1984;
Morón et al. 1985, 1986; Deloya et al. 1987; Delgado 1989; Kohlmann & Halffter 1990;
Palacios-Ríos et al. 1990; Arellano 1992, 2002; Deloya 1992; Capistrán 1992; Estrada et al.
1993; Deloya & Morón 1994; García-Real 1995; Halffter et al. 1995. The most recent and
relevant publications on Canthon in Mexico are Rivera-Cervantes & Halffter (1999) and Halffter
(1961, 2003). Solis & Kohlmann (2002) review Canthon for Costa Rica, as do Howden & Young
(1981) for Panama. In Colombia there are several local revisions (Amézquita et al.1999, Escobar
2000b, Escobar & Chacón de Ulloa 2000, Neita et al. 2003, Pulido et al. 2003). The catalogue
prepared by Medina et al. (2001) lists the species for Colombia. Information about the
geographic distribution of Canthonini in America is given in Bates (1886-1890), Blackwelder
(1944), Vulcano & Pereira (1964), Halffter & Martínez (1966, 1977), as well as in the previously
cited articles.
18
RESULTS
Geomorphological cladogram
The 50% majority consensus tree of four equally parsimonious trees is shown in Figure 2.
The cladogram has 43 steps, a consistency index (CI) of 0.60 and a retention index (RI) of 0.56.
The Colombia and Palo Verde (Costa Rica) sites are sister groups and these two, in turn are sister
group to Chamela (Mexico). Los Tuxtlas (Mexico) represents the first clade banching out, being
the sister group to the other sites included in the analysis.
There are two well supported clades, the first includes Leticia, Tierra Bomba and Zambrano
which have both the era and geological period in common: Quaternary: Pleistocene, Holocene.
They are also free of tectonic faults. The second well supported clade grouped all the DTF of
Colombia and Leticia. All of the sites in Colombia (except Neguanje) have sedimentary rock,
though it originates from different processes. In Leticia, the rock results from dendritic
accumulations, terraces and alluvial deposits from the margins of the Amazon River. At Tierra
Bomba, it originates in marine deposits. In Zambrano, it results from the fluvial-deltaic action of
the Magdalena River, at Los Colorados it comes from rocks corresponding to carbonate facies
and in the Upper Magdalena River Valley, it is comprised of carbonacious and clay sediments
that are both sandy and conglomerate. The soils of the sites are highly developed and have low
concentrations of organic material.
Palo Verde and the majority of the sites in Colombia (except Leticia) are characterized by high
magnetism and are located on the Caribbean tectonic plate (except Leticia and N. Tolima).
Chamela is a sister group to Palo Verde and Colombia, where the soils have optimum
concentrations of potassium (except Leticia).
On the other hand the forests studied in the Caribbean Region (except Neguanje) and Leticia (the
Amazon) are on sites of very recent geological origin (Quaternary) compared to the DTF of
North Tolima (C), Costa Rica (Palo Verde) and Mexico (Los Tuxtlas and Chamela) which are of
Tertiary origin.
The assemblage of the Caribbean Region, Colombia
The areas where Los Colorados and Neguanje are found, are part of a mosaic of blocks that later
came together to form the Caribbean Region. Los Colorados belongs to the San Jacinto Fold Belt
which is the result of the interaction between the oceanic crust of the southwestern Caribbean and
the continental crust of northern South America. Forces of tension and compression alternated
19
along the platform’s margin, especially during the pre-Andina period of orogeny (Middle
Eocene) which lifted, folded and shaped this belt. The geomorphological features of the Santa
Marta Massif (from which the Neguanje is derived) are the result of its location during the
Mesozoic-Tertiary at the intersection of faults on the northeastern corner of South America
(González et al. 1988). According to Ujueta (2003) this Massif should be considered a northern
extension of the Cordillera Central and its relief is a result of mostly vertical tectonic movement
accompanied by moderate horizontal movement.
The tectonic history of San Jacinto, the location of the Sierra Nevada of Santa Marta and the
sedimentation of the Plato and San Jorge basins, is correlated in space and time from the Late
Miocene to the Pliocene (Caro & Spratt 2003). The assemblage and the sedimentation of the
Caribbean Region of Colombia ended in the Quaternary. It is likely that the climatic and
ecological changes were shared by all the sites of the Caribbean Coast of Colombia and so reflect
in one way or another the affinities of the biota present in the DTF. The Caribbean Region,
together with the north of Venezuela make up the phytogeographic region of Northern South
America (Gentry 1995).
Geomorphological relationships of the study sites and their relationship to the origin of
DTF
Three events have exerted a great effect on the evolution of Neotropical flora: the rise of the
Andes, the exchange of biota with North America after the formation of the Central American
Isthmus and the climatic fluctuations of the Pleistocene (Guariguata & Katan 2002). This, in
addition to the culmination of the majority of orogenic processes that occurred on the continental
land of Mexico toward the end of the Pliocene (see Challenger 1998) and the sedimentation of
some parts of the mid- and lower Balsas River basin in the Pleistocene. The convergence of the
DTF studied can be attributed to the climatic and ecological events of recent geological time,
probably since the Pleistocene. This confirms the observations of Gentry (1982) who suggests
that the high number of species in the dry tropical area of Mexico is probably the result of an
active evolutionary diversification in response to the increase in dry climate regimes during the
Pliocene and the Pleistocene. This is in accordance with the higher rate of speciation of the genus
Bursera (toward the Pliocene) and its concentration in areas of intermediate and low altitudes of
the Pacific Slope of Mexico, and in particular the Balsas River Basin (see Becerra 2005,
Rzedowski et al. 2005).
20
One can think about a general process of south-north expansion since, as Rzedowski (1978) has
said, the dry tropical forests of Mexico are characterized by a strong predominance of
Neotropical elements, and the scarcity or absence of holarctic elements. Although dry forests
have their origin in the Pleistocene, it is likely that their current, dry conditions were set during
the Middle Holocene in the Caribbean Region of Colombia, as well as on the Pacific coast of
Mexico and Costa Rica. During the Middle Holocene, about 5000 to 7000 years B.P. (Steig
1999), the dominant climate system was ITCZ (Intertropical Convergence Zone), given that the
ENSO (El Niño-Southern Oscillation) was absent or weak (Fontugne et al. 1999, Cole 2001,
Tudhope et al. 2001, Riedinger et al. 2002). Haugh et al. (2001) propose that the driest climatic
phase of the Holocene results from the change in the ITCZ to its current position.
Cladogram of the areas of affinity of Canthonini
The cladogram of the areas of affinity of the Canthonini, with 28 taxa and three subgenera of
Canthon (Figure 3) is the result of the majority consensus of three trees, with 40 steps, and CI of
0.77 and an RI of 0.64. The cladogram groups the Colombian DTF as follows: the first group is
comprised of the forests of Tierra Bomba, Zambrano and Neguanje (Caribbean Region); the
second is North Tolima alone, and the third group is comprised of Los Colorados, also of the
Caribbean Region. In the first group the subgenus Glaphyrocanthon is not represented by a single
species; in the other two groups this subgenus is represented by C. (Gl.) subhyalinus.
The Canthonini of the dry tropical forest of Chamela and Palo Verde are related to those of the
forests of Colombia. Those of Palo Verde show an affinity to both those of Chamela and those of
Colombia. The canthonines of the two tropical rain forests are totally different from each other
and do not share any species.
There are three species that characterize the relationships between the dry forests of Colombia:
Canthon juvencus, C. cyanellus sallei and C. lituratus (except in Los Colorados). The Amazon
(Leticia) only shares C. aequinoctialis with the dry forests of North Tolima and Los Colorados
Caribbean Region, Colombia).
Chamela has the most exclusive species (Canthon corporali, C. humectus and C. pacificus), and
is followed by Palo Verde (Costa Rica): Canthon deyrollei and C. meridionalis, and North
Tolima (Colombia) with C. acutus.
Eighty-six percent of the species included in the analysis belong to the genus Canthon. To
21
explain these results and explore why such species are found in the forests studied, their
distribution patterns are analyzed below (see Table 4 and Appendix 1).
Analysis of the distribution of Canthonini in the dry forests studied
The cladogram of the species of Canthon for North America (including Mexico) proposed by
Kohlmann & Halffter (1990) shows the spread of this genus from South America in two big
expansion events: the first towards the Miocene and the second towards the Plio-Pleistocene and
continuing to the Recent (see also Halffter 1964, 1976). The phyletic lines that correspond to the
first expansion were not influenced by the events that affected the integration and distribution of
the dry forests which came afterwards. Their presence in these forests (Chamela) are a result of
later colonization. In contrast, the species of the second expansion exhibit a correspondence to
the historical and biogeographical conditions that influenced the distribution of DTF: orography
that was broadly similar to the current situation, the reestablishment of the connection and
exchange of biota between South and North America, and an expansion of the dry conditions in
the Holocene.
In order to explain the presence of Canthonini species in the enclaves of DTF we have studied
both the distribution patterns proposed by Halffter (see Halffter 1964, 1976; Kohlmann &
Halffter 1990) and the phyletic lines proposed for taxa of the genus Canthon according to the
taxonomic affinities recognized by Halffter & Martínez (1977), and propose a pattern of
speciation in situ.
Pattern 1
This pattern is observed for species belonging to the phyletic lines that expanded through
Mexico, most likely before the Miocene (the High Plains Distribution Pattern of Halffter). These
were the earliest species of Neotropical affinity to penetrate the Mexican Transition Zone (MTZ)
(Halffter 1976, 1978). Canthon (C.) humectus belongs to this pattern, and represents a
phyletically isolated line within the subgenus Canthon according to Halffter & Martínez (1977).
Of the eight subspecies (Halffter & Halffter 2003) distributed throughout the High Plains of
Mexico, Oaxaca, Chiapas and Guatemala, only C. humectus riverai Halffter & Halffter is found
in Chamela, a new record not indicated by Andresen (2005), perhaps because it is outside of the
area she studied. This species occurs at the lowest altitude for both the species and Canthonini
found on the High Plains. It was previously collected in the lower part of the Manantlán
Mountain Range (Jalisco) in DTF at altitudes from 700 to 1000 m. Its presence in Chamela can
22
be considered a result of secondary expansion. In a study of the entire Scarabaeoidea superfamily
in Chamela, Morón et al. (1988) found some species with the ancient MTZ dispersal patterns,
though the majority have the Neotropical Pattern that developed from the Pliocene onwards (see
below).
Pattern 2
These species participated in the expansion that probably began in the Pliocene with the
reestablishment of the Panamanian connection, and have different degrees of northwards
expansion in North and Central America, to the United States of America (and thus together
result in the Typical Neotropical Distribution Pattern of Halffter). The affinities of these species
with the South American fauna are much better defined than is the case for Pattern 1 (see
affinities under each species). The penetration of these species into the MTZ (Pliocene onwards)
coul have occurred in distinct stages, depending on the species’ antiquity. The most ancient
species have undergone processes of subspeciation in the MTZ. We will examine the distribution
of these species, from the oldest (and with the widest distribution) to the most recent.
a) Species with a wide distribution that reaches the United States of America.
C. (C.) indigaceus LeConte ranges from Panama to Texas and Arizona in the United States. In
Mexico it is found in tropical landscapes on the Gulf slope, the Pacific slope and the Yucatan
Peninsula. It is comprised of three subspecies that are found under different ecological
conditions: Canthon i. chiapas in TRF; C. i. chevrolati in places with greater insolation, with less
or no woody vegetation; and C. i. indigaceus in DTF or more xerophyllous vegetation. In
Chamela we found C. i. indigaceus; in Guanacaste, C. i. chevrolati; and in the TRF of Los
Tuxtlas, C. i. chiapas. Overall, C. i. indigaceus is a good example of a species exhibiting the
Typical Neotropical Pattern with a wide distribution in the MTZ. As in the previous case
(Canthon humectus), this species constitutes a phyletic line within the subgenus Canthon
(Halffter & Martínez 1977) that has only one species.
C. (C.) cyanellus LeConte has a similar geographic history and distribution, although the latter is
broader. It is found from Peru and Brazil to the southern United States and under a wide variety
of ecological conditions though it is usually associated with tropical forests or treed sites along an
altitudinal range from sea level to 2600 m. This species is found at all the DTF sites we studied
and in Los Tuxtlas, but not in Leticia.
In Mexico it is found all along the Pacific coast, from Chiapas to Jalisco and on the Atlantic slope
23
it is found on the Yucatan Peninsula and along the Gulf Coast of Mexico up to Tamaulipas and
Nuevo León. In the interior of Mexico it is found in the states of Puebla, Morelos, Hidalgo and
San Luis Potosí. In Central America, it is found on both the Pacific and the Atlantic slopes; in
northern Panama it is found near the Caribbean Sea (Bocas del Toro) and to the south on the
border with Colombia in the Darien region on the Pacific coast. In Colombia, according to our
findings this species is found throughout the Caribbean Region and the high valley of the
Magdalena River, as well as in the Department of Meta (Amézquita et al. 1999, Medina et al.
2001). In Venezuela this species occurs in Táriba, San Cristóbal, as well as in Arima, Trinidad
and in Uaupés, Brazil (the Amazon) according to the records of Solís & Kohlmann (2002).
Canthon cyanellus belongs to a phyletic line (the bispinus line) with many species in South
America (Halffter & Martínez 1977).
Malagoniella (M.) astyanax (Harold). The genus Malagoniella is distributed throughout the
Neotropical region, except in Chile and the Antilles. It is richest in species in Argentina,
Uruguay, Paraguay and southern Brasil (Halffter & Martínez 1966). The subgenus Malagoniella
has a similar distribution. It includes the only taxon found in the north, M. (M.) astyanax
yucateca (Harold), that is found in Central America, Neotropical areas of Mexico and at a point
on the border of the United States of America. The other subspecies that make up M. astyanax are
South American. Citations for Colombia possibly refer to M. (M.) astyanax columbica (Harold), a
subspecies for which the distristubion is limited to Colombia (Halffter & Martínez 1966), where
it is found in the DTF of Zambrano and North Tolima, as well as in the Departments of Chocó
and Magdalena (Medina et al. 2001). This species appears to have a preference for DTF and has
not been recorded in Leticia (the Amazon).
M. (M.) astyanax yucateca (Harold) has a very wide distribution in Mexico and Central
America, but has been found at isolated points that are often separated by great distances. In this
case, it is difficult to attribute this to capture inefficiency (at least for many of the places where it
has not been found), given that this is a large and very striking species. It has been collected in
Brownsville, Texas, on the border with Mexico, and also at Tamazunchale (San Luis Potosí),
Quintana Roo, Escárcega (Campeche), Puerto Ángel (Oaxaca), Cacahoatan, Tapachula and
Rosario Izapa (Chiapas), Yucatan (Bates 1886-1890; Halffter & Martínez 1966; SNIBCONABIO database), Guatemala, in the west of Nicaragua and Costa Rica. The Chiapas and
Central American sites are on the Pacific slope. In Costa Rica it is restricted to the Guanacaste
24
region, to the northwest of the Pacific coast, over an altitudinal range of 10 to 400 m. In the
present study, it is recorded for Palo Verde. Except for the capture in Brownsville (Texas), the
rest were captured in tropical forest. M. astyanax yucateca appears to be most often associated
with seasonal forests (i.e. those that have a dry season). It has not been found in TRF (Los
Tuxtlas, Veracruz or Selva Lacandona, Chiapas) within its distribution perimeter.
The distribution of M. astyanax appears to reflect an ancient expansion from South America, one
that is currently quite fragmented.
Pseudocanthon perplexus (LeConte). The genus Pseudocanthon Bates is comprised of eight
species, and two of these are found in Mexico. Of the Mexican species, one is found in the
Antilles where there are also five endemic species. The other species is South American.
Pseudocanthon perplexus is found in Mexico in both TRF and DTF. It is captured sporadically in
sites that are distant from each other. Its distribution extends from the United States of America
down to South America. It was found in Chamela and Palo Verde of the DTF we studied.
In Mexico it is distributed along the coast of the Gulf of Mexico up to the eastern United States,
and on the Pacific coast to Sonora. In Costa Rica, it has been recorded in Guanacaste Province
and in Alajuela on the Cordillera Central, over an altitudinal range of 10 to 540 m (INBio
database). In Panama, it has been found in Balboa in the Canal Zone (Pacific coast).
b) Species with limited penetration into Mexico.
Canthon (C.) morsei Howden is distributed from Ecuador to the warm areas of Mexico, where it
extends along the Pacific slope from Chiapas (Halffter et al. 1992) to Jalisco (García-Real 1995).
Along the Atlantic slope it ranges northwards up to Tamaulipas. In Costa Rica it is found in the
northeast on the Pacific coast (Solis & Kohlmann 2002). In Colombia, it is found in the Upper
Magdalena River Valley (Tolima). This species is associated with DTF and TRF. In the DTF
studied, it was recorded in Palo Verde and in Colombia only in North Tolima. In Mexico, it was
not found in the DTF of Chamela, although it is has been recorded in deciduous and
semideciduous tropical forests in the state of Jalisco relatively close to Chamela.
According to Halffter & Martínez (1977) C. morsei belongs to a phyletic line of the subgenus
Canthon that includes other South American species.
C. (Gl.) subhyalinus Harold is distributed from Bolivia to Mexico and is associated with TRF,
especially those sites with monkeys (Halffter 1991, Estrada et al, 1993, Rivera-Cervantes &
Halffter, 1999). This species was not found in the DTF of Chamela or Costa Rica. In Colombia it
25
is associated with DTF in Tolima and in Los Colorados (Bolívar); other records for Colombia
include the Departments of Antioquia and Cundinamarca (Medina et al. 2001). In Panama,
Howden & Young (1981) have recorded it for Darien, Santa Fe, and on the Pacific coast and in
the Caribbean on Barro Colorado and in the Canal Zone. In Costa Rica it is found in the foothills
of premontane wet forest. In Mexico it is only found in the south in the states of Chiapas,
Quintana Roo and Veracruz. Canthon subhyalinus is a beetle associated with TRF (RiveraCervantes & Halffter 1999), and so it is probable that the neighbouring vegetation between TRF
and DTF facilitates the dispersal of this species toward DTF. This explains the presence of C.
subhyalinus in Los Colorados, where the DTF includes a patch of TRF, a lone remnant in the
Caribbean Region of Colombia (Gentry 1995). It is also found in the DTF of North Tolima,
which is between two mountain ranges and in the foothills of the mountain where wet montane
forest predominates.
The northern distribution limit for C. subhyalinus coincides with that of the howler monkey,
Alouatta palliata. It is probable that the dispersal of these species coincide from South America
up to Los Tuxtlas. This is supported by field observations of the arboreal behavior of these
beetles and their attraction to the dung of these monkeys (Howden & Young 1981, Halffter 1991,
Estrada et al. 1993, Rivera-Cervantes & Halffter 1999). There is additional support in the origin
of these monkeys, Late Miocene to the Pliocene, and their dispersal during the Pleistocene
(Cortés-Ortiz et al. 2003), as well as the biogeographic pattern proposed in this study for C.
subhyalinus.
C. (Gl.) euryscelis Bates belongs to the same group of species of the subgenus Glaphyrocanthon
as C. (Gl.) subhyalinus (see Rivera-Cervantes & Halffter 1999). It is distributed in TRF from
Mexico to Panama. In the DTF we studied, it was collected at Palo Verde (Guanacaste). Solis &
Kohlmann (2002) indicate that it has a broad tolerance of climate, and is found from sites with
marked seasonality (altitude < 800 m in the Province of Guanacaste) to very humid ones. In
Mexico it has been recorded in the TRF of Los Tuxtlas.
Agamopus lampros Bates belongs to a genus (currently under revision by Fernando Vaz de
Mello) with four South American species, of which A. lampros extends to Central America and
the tropical areas of Mexico. We recorded this species in the DTF of Chamela, Palo Verde
(Guanacaste) and Los Colorados (Colombia).
26
c) The species mentioned below belong to South American phyletic lines whose northern
geographic distribution only extends to Central America.
Canthon (C.) mutabilis Harold, within the subgenus Canthon, belongs to the bispinus line that,
as mentioned in the section on C. cyanellus, is comprised of many South American species. Its
distribution extends from Argentina to Costa Rica. It was found in Palo Verde (Guanacaste) and
in North Tolima (Colombia). Solis & Kohlmann (2002) indicate that in Costa Rica it is found
from sites that are very humid to those with marked seasonality and a dry season as long as six
months. In Colombia, Medina et al. (2001) have recorded it for the Departments of Bolívar and
Meta, associated with dry conditions. Canthon juvencus, C. mutabilis and C. meridionalis are
abundant in the driest forests of some of the smallest islands in Lake Gatun and Gamboa
(Caribbean region) near the continent (Gill 1991).
Canthon (C.) lituratus (Germar) is also widely dispersed from Argentina to Costa Rica. It
belongs to a phyletic line within the subgenus Canthon that includes another South American
species (Halffter & Martínez 1977). In Colombia it is found in Tolima and in the Caribbean
Region in all the DTF studied, except for Los Colorados. In Colombia, Medina et al. (2001) have
recorded it for the Departament of Valle. In Costa Rica it is only found to the southwest of the
Pacific coast, in the savannahs bordering the Térraba River (Solis & Kohlmann 2002). Its
distribution extends southwards from the Pacific, and it has also been recorded for the provinces
of Chiriqui and Cocle in Panama at altitudes above 800 m (Howden & Young 1981).
Canthon (C.) juvencus Harold is found from Brazil to Costa Rica. In Colombia it is found in the
DTF of the Caribbean Region and in the Upper Magdalena River Valley (Tolima) as well as in
other Departments in Colombia: Guainia, Guaviare, and Meta (Amézquita et al. 1999, Medina et
al. 2001, Escobar 2000 b). In Costa Rica it is restricted to the southern Pacific in TRF located
below 500 m (Solis & Kohlmann 2002). It is found in Panama in the pronvinces of Panamá,
Colón and the Canal zone (Howden & Young 1981).
Canthon septemmaculatus (Latreille) has a broad distribution range from Argentina to Costa
Rica. In the DTF studied, it was only recorded in Zambrano Caribbean Region, Colombia).
Medina et al. (2001) have recorded it for the Colombian Departments of Bolívar, Chocó, Meta,
Caquetá and Nariño. In Panama it has been recorded in the provinces of Los Santos, Coclé,
Panamá and the Canal Zone. In Costa Rica it is only found to the southwest of the Pacific coast,
in the savannas surrounding the Térraba River (Solis & Kohlmann 2002).
27
Canthon (C.) aequinoctialis Harold occurs from Brazil to Belize. According to Halffter &
Martínez (1977) it belongs to a South American phyletic line of the genus Canthon. In Colombia
it is found in both the DTF of the Upper Magdalena River Valley (Tolima), in Los Colorados
(Caribbean Region) and in the TRF of Leticia (the Amazon). It has also been found in the
Departments of Antioquia, Caquetá, Choco, Guainia, Guaviare, Meta, Nariño, Valle, and Cauca
(Escobar 2000 a, Medina et al. 2001, Neita et al. 2003, Pulido et al. 2003). In Panama it is found
to the north, on the Pacific coast and in the Canal Zone on the Caribbean. In Costa Rica it is
spread out along the Caribbean and to the north of the country, but it was not recorded in Palo
Verde (Guanacaste). On the Pacific coast, it has been cited for two sectors: to the south on the
Osa Peninsula and in the basin of the River Tárcoles, with a marked preference for TRF (Solis &
Kohlmann 2002).
Pattern 3
These taxa likely reflect the processes of speciation in situ in the DTF of Mexico, Costa Rica and
Colombia.
Glaphyrocanthon, a subgenus of Canthon with many South American species, has two phyletic
lines in Mexico with a clear origin in the north of South America. We have already referred to
one of these lines, that of C. (Gl.) subhyalinus. The second line is comprised of an isolated
species with South American affinities. In addition there is the viridis group with strong
speciation in Mexico and which clearly belongs to the subgenus Glaphyrocanthon although it has
no evident relationship to South American species.
The viridis group is comprised of 15 species, of which only C. (Gl.) meridionalis Martínez,
Halffter & Halffter has a distribution that expands towards Central America, opposite to the
dominant direction for the distribution of the Canthonini studied. Several of the species of this
group are associated with TRF, many others are found in DTF.
Canthon (Glaphyrocanthon) pacificus Rivera & Halffter and C. (Gl.) corporali Balthasar belong
to this group and both form part of a set of species that are distributed in Mexico along the Pacific
slope, from the state of Nayarit to the state of Oaxaca. Canthon (Gl.) corporali is widely
distributed in association with DTF, including the Balsas River Basin and the coast of the Pacific
on both sides of its outlet. Canthon (Gl.) pacificus is found in dry deciduous and semideciduous
forests of the Pacific coast, from the state of Jalisco to the state of Oaxaca.
From the same viridis group in Guanacaste the lone species C. (Gl.) meridionalis Martínez,
28
Halffter & Halffter is found and extends to Central America: Guatemala, El Salvador, Nicaragua,
and Costa Rica (Solis & Kohlmann 2002). In Costa Rica it has a wide distribution, on both the
Pacific and the Atlantic sides (Solis & Kohlmann 2002).
Canthon (C.) deyrollei Harold has a geographic distribution from Guatemala to Costa Rica. It is
the only species in its phyletic line (Halffter & Martínez 1977). In Costa Rica it is restricted to the
area with the greatest climatic seasonality, i.e. land below 600 m in the province of Guanacaste,
in the northwest of Costa Rica (Solis & Kohlmann 2002).
Canthon (Gl.) acutus Harold was collected in North Tolima. It has also been found in other
Departments in Colombia: Bolívar, Guainia and Meta at elevations of 300 m (Medina et al.
2001).
DISCUSSION
1) The geological (Fig. 2) and Canthonini species composition (Fig. 3) cladograms only coincide
in their general features. The dry tropical forests from Mexico to Colombia arose during a
relatively recent geological stage. Hence, historical geological events prior to the Pliocene do not
appear to have affected the distribution of this vegetation type. Its distribution is determined by a
combination of temperature and rainfall conditions, particularly by a prolonged and marked dry
season (see Rzedowski 1978).
2) The flora of dry tropical forests is almost exclusively comprised of species with Neotropical
affinities (Rzedowski 1978). The Canthonini fauna has the same affinities. As shown by Trejo
(2005), there is a high degree of plant species exchange between different dry tropical forest sites.
It is not surprising that the same phenomenon occurs in the Canthonini.
The cladograms of the dry tropical forests and the Canthonini exhibit the same affinities found by
Gentry (1995) for flora; i.e. a similarity between the dry forests of northern Colombia and
Venezuela with that of Chamela, with 15 shared genera, while Chamela and Guanacaste (Costa
Rica) only share six genera.
3) The Canthonini species found in the dry tropical forests studied show a clear gradient of
affinity associated with the different degrees of expansion of the Canthonini from South America.
In spite of the great distance and the ecological barriers that exist between Colombia and
Chamela, the affinities are marked and appear to indicate a certain degree of continuity among
the dry forests studied.
There is little doubt that the expansion of the distribution area of South American Canthonini,
29
and that of many other Scarabaeinae with the same biogeographical history was greatly facilitated
by the presence of mammalian megafauna that has since disappeared (see Janzen & Martin
1982). Nevertheless, there are differences among the enclaves of dry tropical forest. In Chamela,
the only pre-Pliocene expansion species was collected (Canthon humectus), along with several
species of ancient expansion within the Neotropical Pattern, and several species whose
distribution in Mexico is more recent, including two belonging to a group (Canthon
(Glaphyrocanthon) viridis group) which speciated in Mexico. Palo Verde has a mix of PlioPleistocene and recent expansion species. In Colombia, species with a South American
distribution dominate, although it shares species with Palo Verde and Chamela.
The biogeographical hypothesis proposed in the Introduction about the origin of Canthonini and
their northwards expansion at different times and with different degrees of penetration is
supported. The relationships between distinct phyletic lines and even species, with South
American fauna clearly demonstrates these biogeographical phenomena.
4) Several of the species found in Colombia, but not in Palo Verde or Chamela, have the northern
limit of their distribution in the Térraba River basin in the extreme south of Costa Rica on the
Pacific coast. This is the case for C. lituratus, C. juvencus and C. septemmaculatus (see Solis &
Kohlmann 2002). As these species do not reach Palo Verde the differences of this site with those
of Colombia are accentuated. This northern limit in the distribution of South American species to
the extreme south of Costa Rica is interesting. The lowlands of Nicaragua to the north of Lake
Nicaragua were proposed by Halffter (1976) as the southern limit of the Mexican Transition
Zone. The present study shows the South American affinity of the Canthonini of Costa Rica for
dry tropical forest (they share 40% of the species with the DTF of North Tolima), and this seems
to apply in general to those species found in other types of vegetation (see Solis & Kohlmann
2002).
5) A good number of the species found in the sites we studied are characteristic of dry tropical
forest, and even exclusive to this vegetation type. However, some species are shared with tropical
rain forest. The proportion of shared species is much lower in Chamela, moderate in Palo Verde
and greatest in the sites of Colombia. The latter is also reflected in the greater affinity of the
Canthonini of Colombian DTF with those of Leticia (TRF), than with those of the DTF of
Chamela (Fig. 3). Palo Verde shares 30% of its species with Los Tuxtlas, a forest where the DTF
and the TRF species of Mesoamerica meet.
30
6) As regards in situ speciation, the most notable example is that of the viridis group, which has
no direct relationship with the South American fauna of Canthon (Glaphyrocanthon). This group
underwent much diversification in Mexico that appears to be recent and influenced by the process
of drying out during the Holocene (many of its species are adapted to dry forest).
7) The enclaves of dry tropical forest in Colombia, in both the Caribbean Region and the Upper
Magdalena Valley, are close to tropical rain forest. In the first case, Neguanje is part of the
Province of the Sierra Nevada of Santa Marta where the vegetation changes with increasing
altitude and in Los Colorados there is still a remanent of rain forest. The Upper Magdalena River
Valley is surrounded by rain forest on the skirts of the Cordillera Central and the Cordillera
Oriental, and to the north by the Middle Magdalena Valley. This allows them to share species
with adjacent ecosystems.
8) The Canthonini fauna of the tropical rain forests (Los Tuxtlas and Leticia) that were used as
the outgroup, is very different between these two rain forests and also different from the fauna of
the dry tropical forests. Considering all Scarabaeoidea, the similarity in species between Chamela
and Los Tuxtlas is only 13 (Sørensen’s QS index), while between Chamela and other dry tropical
forest in Mexico the value is 41 (Morón et al. 1988).
9) The quality of the species list is the main limitation of the biogeographical analysis presented
here. We have gathered all of the published information as well as that recorded in the databases
of CONABIO and INBIO. Even so, these collections cannot be considered exhaustive, especially
for Colombia.
10) The predominance of roller species (Canthonini) in dry tropical forest is well defined. On
average 33.45% of the Scarabaeinae species found are Canthonini, a value that rises to 35.45% if
we exclude Neguanje as the least representative site. In contrast, in the tropical rain forests
studied, on average only 28% are rollers. The affinity of the rollers for sunny conditions is even
greater in sites that are drier and have very open vegetation.
11) There have been several studies of the changes in the abundance of Scarabaeinae species
from the dry season to the rainy season in dry tropical forest: Chamela (Andresen 2005), North
Tolima (Escobar 1997), Guanacaste, Costa Rica (Janzen 1983) have produced similar results and
emphasize the severity of the dry season. Soil humidity and ambient temperature control the
activity and life cycle of Scarabaeinae (Halffter 1991, Martínez & Montes de Oca 1994, BustosGómez & Lopera-Toro 2003, Andresen 2005). On the other hand, the Scarabaeinae of dry
31
tropical forests show a marked tendency for a generalist diet (copro-necrophagous). In Chamela
70% of Scarabaeinae (Andresen 2005) and in the north of Tolima 71% (Bustos-Gómez &
Lopera-Toro 2003) have this type of diet.
Closing Remarks
The biogeographical analysis of areas of dry tropical forest in Mesoamerica and Colombia has
provided and integrated geological, geomorphological, climatic and ecological elements that have
brought us closer to understanding the creation and relationships of Neotropical dry forests.
The use of an outgroup polarized the cladograms, adding a new dimension to the study by
establishing an axis for comparison that stood out in all analyses. The analises carried out, along
with previous knowledge of the group allowed for an explanation of the spatio-temporal
dynamics exhibited by the Canthonini in dry tropical forests.
Dry tropical forest represents a setting where the processes of vicariance and dispersal
occur. This study reveals Canthonini’s routes of dispersal via the dry forests while the speciation
processes of some Canthon, appearing to be synchronous with the establishment of the dry
forests of Mesoamerica and Colombia, also indicate the affinities of Canthonini to dry tropical
forest, very similar to that of the flora of said ecosystem.
Biogeographical and ecological elements were brought together and these allowed us to explain
both their presence in and the preference of some Canthonini for dry forest, and/or their exclusive
distribution in some dry forests of Colombia and their absence from those of Mesoamerica, as
was the case for C. (Gl.) subhyalinus, so clearly demonstrated by the PAE.
ACKNOWLEDGEMENTS
The first author is grateful to A. Espinosa de los Monteros and J. J. Morrone for their comments
on the manuscript; to F. Escobar, M. Zunino, A. Solís, F. Vaz de Mello and A. Díaz, for
providing bibliography; to C. Álvarez for providing access to the SNIB-CONABIO data base
projects E7, K5, P134, G19, H125, Mexico City and the data base of the National Biodiversity
Institute,
Costa
Rica,
Atta:
Information
System
on
Costa
Rican
Biodiversity
(http://www.inbio.ac.cr/atta/index.htm). Thanks also to the Universidad de Nariño, Pasto
(Colombia: Nariño) for the award of a Commission to Study.
We thank two anonymous reviewers for their very useful comments. We are also are grateful to
B. Delfosse for translating the manuscript into English. This study represents part of the project
32
“Analysis of the relationships between alpha, beta and gamma diversity on different spatial
scales: the historical and ecological processes involved”, Stage V (CONABIO-Mexico).
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44
Fig.1 Study sites,DTF (1-7 dry forest sites): 1 = Chamela, 2 = Palo Verde, 3 = Neguanje, 4 = Tierra Bomba, 5 = Los
Colorados, 6 = Zambrano, 7 = Norte del Tolima; TRF (8-9): 8 = Los Tuxtlas, 9 = Leticia (Amazonas). The dotted
area corresponds to the distribution of DFT, based on Gómez (1982), IAvH (1997 b), CONABIO (1990) and Trejo &
Dirzo (2002).
45
1(0)
2(0)
10(0)
75/57
4(1)
16(0)
Leticia
5(2)
13(0)
14(0)
100/81
T. Bomba
7(1)
8(2)
9(3)
75/54
18(1)
Zambrano
12(1)
Colombia
100/57
1(2),
14(0)
6(1)
18(1)
Los Colorados
16(1)
100/70
3(0)
11(0)
15(0)
4(3)
8(0)
9(0)
11(2)
Neguanje
5(0)
10(1)
1(1)
5 (2)
9(2)
17(1)
2(1),
14(0)
N. Tolima
P. Verde
3(1)
4(2)
16(1)
14(0)
Central
America
Chamela
6(1)
17(1)
Mexico
13(0)
3(1)
4(2)
7(1)
Los Tuxtlas
Fig. 2. Cladogram of geological areas. The numbers above the nodes indicate 50% majority consensus tree frequency
/ Jackknife frequency with 20% deletion, 500 replicas. In each clade the appearance of derived = and reversed =
characters is indicated.
46
T. Bomba
100/85
Zambrano
67/54
Neguanje
100/75
N. Tolima
100/81
Los Colorados
100/67
Leticia
Chamela
P. Verde
Los Tuxtlas
Fig. 3. Cladogram of the areas of affinity of Canthonini. The numbers above the nodes indicate
50% majority consensus tree frequency / Jackknife frequency with 20% deletion, 500 replicas.
47
Table 1. Bibliography consulted for the selection of geomorphological characters.
Mexico
López-Ramos 1980, Bullock 1988, Bandy et al. 1999, Ferrari et al. 1999, Ferrari
& Rosas-Elguera 1999, Rutz 2002, Campo-Alves 2003, Hernández-Quintero
2003, Sommer-Cervantes et al. 2003.
Costa
Schmidt-Effing 1980, Rich & Rich 1983, Vásquez 1983, Alvarado et al. 1986,
Rica
Chiesa et al. 1994, Henríquez et al. 1994, Meschede et al. 2000, Nelson &
Nietzen 2000, Alfaro et al. 2001, Jaccard et al. 2001, Montero 2001, Cuevas et
al. 2003.
Colombia
Taborda 1950, Rubio et al. 1977, Galvis et al. 1979, Aucott 1983, González et
al. 1988, Malagón 1988, Sánchez et al. 1998, Sánchez-Valbuena 1992, París &
Romero 1994, Giunta et al. 1996, Molina 1996, Herrera et al. 2001, Ramón et al.
2001, Caro & Spratt 2003.
48
Table 2. Geological-geomorphological characters and their states
1. Land profile. undulating (0), valley (1), flat (2)
2. Potassium. low (0), optimal (1)
3. Organic material in the soil. high (1), low (0)
4. Most abundant minerals in the sandy fraction of the soils. feldspar (0), quartz (1), olivinepyroxene (2), amphiboles (3)
5. Tectonic plate. Caribe (0), North America (1), South America (2)
6. Seismicity. high (0), low-absent (1)
7. Faults. present (0), absent (1)
8. Geological era. Mesozoic (0), Tertiary (1), Quaternary (2)
9. Geological period. Middle Jurassic – Late Cretaceous (0), Eogene [Oligocene, Eocene,
Paleocene] (1), Neogene [Pliocene, Miocene] (2), Pleistocene, Holocene (3)
10. Magnetism. low (0), high (1)
11. Type of rock. sedimentary (0), igneous (1), metamorphic (2)
12. Nearby volcanic range. present (0), absent (1)
13. Soil permeability. high to moderate (0), low (1)
14. Origin of rock. marine (0), continental (1)
15. Evolution of the soil profile. zoned (highly evolved) (0), not zoned (young or slightly
developed) (1)
16. Origin of the plate. Paleozoic (0), Mesozoic (1)
17. Metals. Ag, Pt, Au, Fe. absent (0), presente (1)
18. Bouguer’s anomalies (gravimetric anomalies). positive (0), negative (1)
49
Table 3. Matrix with character states for the cladogram of geomorphological areas.
123456789012345678
Leticia ( C )
000121123001010000
Neguanje ( C )
210301000120110100
Zambrano ( C )
210001123101110101
Los Colorados ( C ) 210001011101100101
T. Bomba ( C )
210001123101000100
N. Tolima ( C )
110020012100100010
Chamela ( M )
010011011010111010
Los Tuxtlas ( M )
001210111010011000
P. Verde (CR)
011200011110101100
50
Table 4. List of Canthonini species from the study forests. Numbers are those used in the matrix
of Table 2. The subgenera of the genus Canthon are Glaphyrocanthon (Gl.), Canthon (C.),
Goniocanthon (G.).
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
Canthon (C.) aequinoctialis Harold
C. (Gl.) acutus Harold
C. (Gl.) corporali Balthasar
C. (C.) cyanellus cyanellus LeConte
C. (C.) cyanellus sallei Harold
C. (C.) deyrollei Harold
C. (Gl.) euryscelis Bates
C. (Gl.) femoralis (Chevrolat)
C. (G.) fulgidus Redtenbacher
C. (C.) humectus riverai Halffter & Halffter
C. (C.) indigaceus indigaceus LeConte
C. (C.) indigaceus chiapas Robinson
C. (C.) indigaceus chevrolati Harold
C. (C.) juvencus Harold
C. (C.) lituratus (Germar)
C. (Gl.) luteicollis Erichson
C. (Gl.) meridionalis (Martínez, Halffter & Halffter)
C. (C.) morsei Howden
C. (C.) mutabilis Harold
C. (Gl.) pacificus Rivera & Halffter
C. (Gl.) semiopacus Harold
C. septemmaculatus (Latreille) Insertae sedis
C. (Gl.) subhyalinus Harold
C. (Gl.) vazquezae (Martínez, Halffter & Halffter)
Cryptocanthon peckorum Howden
Pseudocanthon perplexus (LeConte)
Agamopus lampros Bates
Malagoniella astyanax (Harold)
51
Table 5. Data matrix for the cladogram of the Canthonini areas
12345678901234567890123456789012
Chamela ( M )
00110000011000000001000001101001
Los Tuxtlas ( M )
00010011000100000100001101001001
P. Verde (CR )
00001110000010001100000001111001
N. Tolima ( C )
11001000000001100110001000011001
Zambrano ( C )
00001000000001100000010000011010
Los Colorados ( C ) 10001000000001000000001000101001
T. Bomba ( C )
00001000000001100000000000001000
Neguanje ( C )
00001000000001100000000000001000
Leticia ( C )
10000000100000010000100010001101
52
Appendix 1. Scarabaeinae (Canthonini and other tribes) of the forests studied
MEXICO, CHAMELA
Agamopus lampros Bates
Canthon corporali Balthasar
Canthon pacificus Rivera & Halffter
Canthon cyanellus cyanellus LeConte
Canthon humectus riverai Halffter & Halffter
Canthon indigaceus LeConte
Pseudocanthon perplexus (LeConte)
Deltochilum timidum Howden
Deltochilum gibbosum (Fabricius)
Phanaeus demon Laporte
Phanaeus furiosus Bates
Coprophanaeus pluto Harold
Digitonthophagus gazella (Fabricius)
Onthophagus landolti Harold
Onthophagus igualensis Bates
Onthophagus hoepfneri Harold
Canthidium sp.
Dichotomius colonicus (Say)
Dichotomius amplicollis (Harold)
Ateuchus rodriguezi (Borre)
Uroxys sp.
Copris lugubris Boheman
PALO VERDE,COSTA RICA
Agamopus lampros Bates
Canthon cyanellus sallei Harold
Canthon deyrollei Harold
Canthon euryscelis Bates
Canthon indigaceus chevrolati Harold
Canthon meridionalis (Martinez, Halffter & Halffter)
Canthon morsei Howden
Canthon mutabilis Harold
Pseudocanthon perplexus (LeConte)
Deltochilum lobipes Bates
Malagoniella astyanax (Harold)
Phanaeus wagneri Harold
Phanaeus demon Laporte
Phanaeus eximius Bates
Coprophanaeus telamon (Erichson)
Coprophanaeus pluto (Harold)
Onthophagus acuminatus Harold
Onthophagus championi Bates
53
Onthophagus landolti Harold
Onthophagus hoepfneri Harold
Onthophagus marginicollis Harold
Onthophagus batesi Howden & Cartwright
Canthidium laetum Harold
Canthidium guanacaste Howden & Gill
Dichotomius yucatanus (Bates)
Dichotomius centralis (Harold)
Dichotomius annae Kohlmann & Solis
Ateuchus rodriguezi (Borre)
Copris lugubris Boheman
COLOMBIA, CARIBE REGION
Zambrano
Canthon cyanellus sallei Harold
Canthon juvencus Harold
Canthon lituratus (Germar)
Canthon septemmacutatus (Latreille)
Malagoniella astyanax (Harold)
Coprophanaeus jasius (Olivier)
Canthidium sp.
Dichotomius belus (Harold)
Onthophagus marginicollis Harold
Onthophagus lebasi Boucomont
Uroxys sp.
Eurysternus impressicollis Laporte
Los Colorados
Agamopus lampros Bates
Canthon aequinoctalis Harold
Canthon cyanellus sallei Harold
Canthon juvencus Harold
Canthon subhyallinus Harold
Coprophanaeus jasius (Olivier)
Diabroctis cadmus Harold
Phanaeus hermes Harold
Canthidium sp.
Dichotomius belus (Harold)
Onthophagus marginicollis Harold
Onthophagus lebasi Boucomont
Onthophagus sp.
Uroxys sp.
Tierra Bomba
Canthon cyanellus sallei Harold
Canthon juvencus Harold
54
Canthon lituratus (Germar)
Diabroctis cadmus Harold
Canthidium sp.
Dichotomius belus (Harold)
Onthophagus marginicollis Harold
Onthophagus lebasi Boucomont
Onthophagus landolti Harold
Uroxys sp.
Eurysternus impressicollis Laporte
Neguanje
Canthon cyanellus sallei Harold
Canthon juvencus Harold
Canthon lituratus (Germar)
Phanaeus prasinus Harold
Canthidium sp.
Dichotomius belus (Harold)
Dichotomius sp.
Dichotomius sp.
Onthophagus marginicollis Harold
Onthophagus lebasi Boucomont
Onthophagus landolti Harold
Eurysternus impressicollis Laporte
Eurysternus caribaeus (Herbst)
COLOMBIA, NORTH TOLIMA
Canthon acutus Harold
Canthon aequinoctialis Harold
Canthon cyanellus sallei Harold
Canthon juvencus Harold
Canthon lituratus (Germar)
Canthon morsei Howden
Canthon mutabilis Harold
Canthon subhyalinus Harold
Malagoniella astyanax (Harold)
Phanaeus hermes Harold
Dichotomius belus (Harold)
Dichotomius sp. 1
Dichotomius sp. 2
Onthophagus landolti (Harold)
Onthophagus lebasi (Boucomont)
Onthophagus marginicollis (Harold)
Onthophagus rubrescens (Blanchard)
Canthidium sp.
Ateuchus sp.
55
Uroxys sp.
Canthidium sp.
Eurysternus plebejus (Harold)
MEXICO, LOS TUXTLAS (for rainforest, M. Favila pers. com.)
Canthon euryscelis Bates
Canthon femoralis (Chevrolat)
Canthon morsei Howden
Canthon vazquezae (Martinez, Halffter & Halffter)
Canthon subhyalinus Harold
Canthon edmondsi Rivera & Halffter
Deltochilum scabriusculum Bates
Deltochilum pseudoparile Paulian
Delthochilum gibbosum sublaeve Bates
Phanaeus endymion Harold
Sulcophanaeus chryseicollis (Harold)
Onthophagus nasicornis Harold
Onthophagus rhinolophus Harold
Canthidium aff. ardens Bates
Canthidium centrale Boucomont
Canthidium aff. perceptibile Howden & Young
Scatimus ovatus Harold
Uroxys boneti Pereira & Halffter
Uroxys bidentis Howden & Young
Uroxys transversifrons Howden & Gill
Ontherus mexicanus Harold
Bdelyropsis newtoni Howden
Dichotomius satanas (Harold)
Copris laeviceps Harold
Eurysternus angustulus (Harold)
Eurysternus caribaeus (Herbst)
Eurysternus velutinus Bates
COLOMBIA, LETICIA
Canthon aequinoctialis Harold
Canthon fulgidus Redtenbacher
Canthon luteicollis Erichson
Canthon semiopacus Harold
Cryptocanthon peckrorum Howden
Canthonella n. sp.
Scybalocanthon sp.
Deltochilum amazonicum Bates
Deltochilum carinatum Westwood
Deltochilum sp. 1
Deltochilum sp. 2
56
Deltochilum sp. 3
Coprophanaeus telamon (Erichson)
Coprophanaeus n. sp.
Oxysternon conspicillatum (Weber)
Oxysternon silenus Laporte
Phanaeus bispinus Bates
Phanaeus cambeforti Arnaud
Phanaeus chalcomelas (Perty)
Phanaeus meleagris Blanchard
Onthophagus haematopus Harold
Onthophagus sp. 1
Onthophagus sp. 2
Onthophagus sp. 3
Ontherus pubens Génier
Ontherus diabolicus Génier
Uroxys sp. 1
Uroxys sp. 2
Dichotomius boreus (Oliver)
Dichotomius mamillatus (Felsche)
Dichotomius ohausi (Luederwalt)
Dichotomius podalirius (Felsche)
Dichotomius sp. 1
Dichotomius sp. 2
Dichotomius sp. 3
Dichotomius sp. 4
Canthidium bicolor Bouc.
Canthidium gerstaeckeri Harold
Canthidium sp. 1
Canthidium sp. 2
Canthidium sp. 3
Canthidium sp. 4
Canthidium sp. 5
Bdelyrus sp.
Ateuchus murrayi (Harold)
Ateuchus sp. 1
Ateuchus sp. 2
Eurysternus caribaeus Herbst
Eurysternus cayennensis Laporte
Eurysternus confusus Jessop
Eurysternus foedus Guérin
Eurysternus hirtellus Dalman
Eurysternus inflexus (Germar)
Eurysternus velutinus Bates
57
CAPITULO 3
Mesoamerican and Colombian Dry Tropical Forest and Phanaeine Dung Beetles (Coleoptera:
Scarabaeidae, Scarabaeine): A Cladistic Analysis of Relationships
(Enviado a Biotropica)
58
CAPÍTULO III
Mesoamerican and Colombian Dry Tropical Forests and Phanaeini Dung Beetles
(Coleoptera: Scarabaeidae, Scarabaeinae): A Cladistic Analysis of Relationships
D. N. Padilla-Gil and D. Edmonds
ABSTRACT
The purpose of this paper is to examine the historical geographical relationship among enclaves
of tropical dry forest in Mexico, Costa Rica and Colombia using the phanaeine dung beetles as
the indicator taxon, and to compare the results with those of a parallel study of the cantonini
dung beetles. Focal dry forest enclaves studied are Chamela (southwestern Mexico), Palo Verde
(Costa Rica) and five localities in upper Rio Magdalena valley and Caribbean regions of
Colombia. For the cladistic analysis two humid tropical tropical forest served as outgroups: Los
Tuxtlas (Mexico) and Leticia (Colombia). Dry forest area relationships were analized with a
Parsimony Analysis of Endemicity (PAE) with species of Phanaeus and related phanaeines as
characters. Area cladograms obtained indicate closest relationships between dry forest enclaves
of Chamela and Palo Verde, and between those Tolima and Los Colorados in the Caribbean
region of Colombia. The Mesoamerican diversification of Phanaeini seems to coincide spatiotemporally with the presumed origin of tropical dry forest of the study areas and has resulted in
several endemic communities. The history of dry forest phanaeine and cantonini dung beetles
coincide in general aspects. In both cases the endemic dry forest taxa are presumed to have
arisen in situ.
Key words: dry tropical forest, Phanaeini, Canthonini, Mexico, Costa Rica, Colombia, area
cladistic.
59
INTRODUCTION
Tropical dry forest (deciduous tropical forest) is characterized as that tropical plant formation
presenting the following suite of features: a) a continuous woody coverage of species that loose
their leaves during a dry season of variable length; b) an average annual temperature above 24ºC;
c) seasonal rains of 700 to 2000 mm alternating with a marked dry season; d) an altitudinal range
from 0 to 1000 m (Espinal, 1985; IavH, 1997a; Rzedowski, 1978). According to Rzedowski
(1978), this formation is especially characteristic of the Pacific slopes of Mexico, where it covers
large areas practically uninterrupted from southern Sonora and southwestern Chihuahua through
Chiapas into Central America (Fig. 1). It penetrates deeply inland along the Santiago and Balsas
Rivers and their tributaries in southern Mexico and the central valleys of Chiapas and several
areas along the Gulf coast into Yucatan. Tropical dry forest at one time covered about 270,000
km2 (6-14%) of Mexican territory below 1500 m; in modern times coverage by intact forest has
been reduced to about 27% of that original area (Trejo and Dirzo, 2000). In Costa Rica about 100
years ago, tropical dry forest covered almost the entire peninsula of Nicoya and the island of
Chira (Kohlmann et al. 2002). While at one time dry deciduous forest covered as much as 7%
(33,600 km2) of the landmass of Central America below 1000 m, its present day coverage is
probably less than 2% of this original area (Sabogal and Valerio, 1998). There are three large
areas of dry tropical forest in Colombia. The two largest of these occur in the Caribbean plains
(including the southern portion of the Department of Guajira) and the valley of the Magdalena
River in the departments of Tolima, Cundinamarca and Huila (IavH, 1997b). These forests are
severely threatened in Colombia, occupying roughly 1% of their original area of approximately
80,000 km2 (Etter, 1993). Dry tropical forests originated in the Pleistocene and, in middle
Holocene, became entrenched in the caribbean region of Colombia as well as the Pacific coast of
Mexico and Costa Rica (Padilla-Gil and Halffter, 2007).
The relationships among dry tropical forests of Mesoamerica and Colombia and the tribe
Canthonini has been considered by Padilla-Gil and Halffter (2007). This parallel study of
Colombian and Mesoamerican dry forests is based on an analysis of the dung beetle tribe
Phanaeini, a New World group comprising about 150 species. Twelve genera are currently
included in the tribe, of which five are known to occur in dry tropical forest habitats in the study
areas (Phanaeus, Coprophanaeus, Sulcophanaeus, Oxysternon and Diabroctis. Remaining
genera are Dendropaemon, Homalotarsus, Tetrameira, Megatharsis, Gromphas, Oruscatus and
60
Bolbites). Several works treat the taxonomy and distribution of the tribe, among them Olsoufieff
(1924), Edmonds (1972), and Arnaud (2002). Philips et al. (2004) presents the only recent view
of the phylogeny of the tribe. Three genera are the subjects of recent revisions, Phanaeus
(Edmonds, 1994), Sulcophanaeus (Edmonds, 2000) and Oxysternon (Edmonds and Zidek, 2004);
and a revision of Coprophanaeus is a work in preparation by Edmonds and Zidek (pers. comm.).
The objectives of this study are as follows: a) to compare the fauna of phanaeines in several
enclaves of Mesoamerican and Colombian dry forests; b) to relate faunal composition of these
areas to the historico-geomorphological characteristics of the regions in which the enclaves
occur; c) to consider other factors that might explain the modern distributions of dry forest
phanaeines; d) to develop a global hypothesis to explain the biogeography of the phanaeines in
Mesoamerican and Colombian dry forests; and e) to integrate, insofar as possible, biogeographic
hypotheses concerning the tribes Phanaeini and Canthonini.
METHODS
Study Sites: The study sites utilized in this study (Fig. 1) are the same representative enclaves of
dry forest habitat used in the analysis of Canthonini by Padilla-Gil and Halffter (2007). Chamela
(Mexico, Jalisco) and Palo Verde (Guanacaste, Costa Rica) lie in the Pacific coastal belt of
Mesoamerica. Four sites (Neguanje, Tierra Bomba, Los Colorados and Zambrano) lie in the
Caribbean region of Colombia; the fifth Colombian site, the northern portion of Tolima, occupies
the upper valley of the Magdalena River. The ecogeographical characters of the study sites are
detailed in the Appendix 1. In addition to faunal lists and other publications that treat phanaeine
distribution, geographical data were extracted from the databases maintained by INBio (Costa
Rica) and SNIB-CONABIO (Mexico).
Area Cladogram: The area relationships were analyzed using Parsimony Analysis of Endemicity
(PAE) as modified by Padilla-Gil and Halffter (2007), where taxa are analogs of localities and
characters analogs of species using an outgroup. The ingroup is defined as the collection of seven
study sites; the outgroup is two enclaves of tropical humid forest (Los Tuxtlas in Veracruz,
Mexico, and Leticia in Amazonas, Colombia). The outgroup provides an important point of view
where contrasting ecological and taxonomic elements can be brought to bear on the current
discussion. Species lists used for the analysis comprise Appendix 2 (see below); Appendix 3 is a
61
data matrix where presence (1) or absence (0) of a given taxon is noted by study and by outgroup
sites. Analysis utilized PAUP 4.0b10 (Swofford, 2002) with Acctran optimization and exhaustive
search.
Species Distribution: In addition to the databases of InBio and SNIB-CONABIO, the species
distribution comprising Appendix 2 were derived from the following literature: Morón et al.,
1988 and Andresen, 2005 (Chamela); Escobar, 1997; Bustos-Gómez and Lopera-Toro, 2003
(northern Tolima); Escobar, 1998, 2000a (caribbean Colombia); Howden and Nealis, 1975
(Leticia); Morón, 1979; Halffter etal., 1992; Favila and Díaz, 1997; Deloya and Morón, 1998 and
Díaz, 1998, 2003 (Los Tuxtlas). In addition, unpublished data were provided by Federico Escobar
(Caribbean Colombia) and Bruce Gill (Leticia).
Geographic Distribution: Distributional data were compiled from the following sources (in
addition to those listed above): Edmonds (1994, 2000, 2003); Morón and Terrón, 1984; Morón et
al., 1985; Morón et al., 1986; Deloya et al., 1987; Deloya, 1992; Halffter et al., 1992; Estrada et
al., 1993; Deloya and Morón, 1994; Garcia-Real, 1995; Halffter et al., 1995; Medina et al,. 2001;
Amézquita et al., 1999; Escobar 2000a, 2000b; Neita et al., 2003; Pulido et al., 2003; Howden
and Young, 1981; Martinez and Clavijo, 1990; and Gámez, 2004; Bates 1887; Blackwelder, 1944
and Barrera, 1969.
RESULTS
Two area cladograms were generated: one based on all phanaeines from all sites, based on the
majority consensus tree as it offered the greatest resolution; another based only on species of
Phanaeus, the largest phanaeine genus, from all sites except Zambrano and Tierra Bomba, where
the genus is not known to occur.
Cladogram of the areas of affinity of Phanaeini (Fig. 2): The most closely related dry tropical
forests considering all 23 phanaeine species are Chamela (Mexico) and Palo Verde (Costa Rica).
Shared species unique to these sites are Coprophanaeus pluto and Phanaeus demon. Species
unique to a single site are as follows: Chamela: Phanaeus furiosus Bates; Palo Verde: P. eximius
Bates, P. wagneri Harold. Species unique to outgroup sites are: Los Tuxtlas: Coprophanaeus gilli
Arnaud, Phanaeus endymion Harold, P. mexicanus Harold, P. sallei Harold, P. tridens Laporte y
62
Sulcophanaeus chryseicollis (Harold); Leticia: P. meleagris Blanchard, P. chalcomelas (Perty),
P. cambeforti Arnaud, P. bispinus Bates, Oxysternon silenus Laporte, O. conspicillatum Weber
and Coprophanaeus parvulus (Olsoufieff).
Cladogram of the areas of affinity of Phanaeus (Fig. 3): The most closely related dry tropical
forests considering only those 14 species of Phanaeus is a tie between Chamela and Palo Verde
on one hand, and Tolima and Los Colorados on the other. In the first case, the shared species is
Phanaeus demon; in the second, P. hermes.
DISCUSSION
Biogeographic Setting of Dry Tropical Forests: The geomorphological cladogram based on the
tribe Canthonini produced by Padilla-Gil and Halffter (2007) links as sister groups the forest
enclaves of Colombia ((((((Leticia, T. Bomba) Zambrano) Los Colorados) Neguanje) Tolima)
Palo Verde, Chamela), while that resulting from this study groups Palo Verde and Chamela
(Mexico). The geologic cladogram and that based on phanaeine taxonomy agree only in general
terms. The dry tropical forests of Mexico and Colombia are of relatively recent origin such that
pre-Pliocene events seem to have had negligible influence on dry forest phanaeine distribution.
The appropriate geological setting to examine phanaeine evolution in dry forests is Pleistocene
(see Padilla-Gil and Halffter, 2007).
Biogeographic Patterns of Tropical Dry Forest Phanaeines: Philips et al. (2004) postulate that
the tribe Phanaeini is a monophyletic group within which Phanaeus and Oxysternon are sister
groups (with Sulcophanaeus nearest outgroup) with co-origin in South America. Edmonds (1972,
1994) concludes that the origin and initial diversification of Phanaeus, sen. str, are
Mesoamerican and occurred at a much earlier date than the relatively recent penetration of
Sulcophanaeus, Coprophanaeus and Oxysternon into that area. The diversification of all four
genera in Mesoamerica seems to coincide spatio-temporally with the presumed origin of
Mesoamerican tropical dry forests. In situ speciation is dry forest enclaves has resulted in the
following endemic phanaeine communities.
Dry forests endemics of the Pacific region of Mexico (Coprophanaeus pluto nogueirai;
Phanaeus demon demon; P. furiosus; P. nimrod; P. zapotecus): The known distribution of
Coprophanaeus pluto nogueirai extends from Chamela northward along the Pacific plains into
63
southern Arizona, and southward along the Pacific seaboard to Colima. Phanaeus demon extends
north from Chamela into Sinaloa and southward to Costa Rica (as P. demon excelsus); P. furiosus
is restricted to the dry forests of southwest Mexico as far north as Sonora; P. nimrod is endemic
to the Valley of Oaxaca, and P. zapotecus occurs in the dry forests of the Sierra Madre del Sur in
southern Oaxaca. The Pacific Coastal Region of Mexico, especially Chamela and the Balsas
River valley, is a speciation center for the phanerogam plants (see Becerra, 2005; Gentry, 1995;
Rzedowski, 1991; and Rzedowiski et al. 2005). Likewise, the dry forests of Oaxaca possess a
high rate of plant endemism (Salas-Morales et al. 2003; Gallardo-Cruz et al. 2005).
Dry forests endemics of Central America (Phanaeus eximius; P. demon excelsus Bates; P.
wagneri wagneri): P. eximius occurs in the Pacific dry forests of Guanacaste northward along the
coast to southern Guatemala; it also occurs in a restricted area near the Caribbean coast of
Honduras. Phanaeus demon excelsus is restricted to Costa Rica Pacific dry forests. P. wagneri
ranges from the dry forests of Costa Rica to the central valley of Chiapas, and from Honduras
northward into the Yucatan Peninsula.
Dry forests endemics of Colombia (Phanaeus hermes; P. prasinus): P. hermes occurs in northern
Tolima, the Colombian Caribbean and Norte de Santander. It has also successfully adapted to the
premontane humid forests on the slopes of the Sierra del Perijá, as well as in Panama and Costa
Rica. Phanaeus prasinus occurs in the Colombian Caribbean in Neguanje and Norte de
Santander. In Venezuela it occurs in the arid region of Falcon, the Maracaibo depression and the
Cordillera de Merida. These species are closely related, the only two members of the P. hermes
group (Edmonds, 1994); both also enter the sub Andean selva. Diabroctis cadmus (probably
endemic) occurs in the dry forest of Tierra Bomba and Colorados (Colombian caribean) and
northern Venezuela. Several other phanaeines also occur in the Colombian Caribbean and
northern Venezuela but are absent from the forest enclaves under study here: Sulcophanaeus
steinheili (an endemic) and Coprophanaeus gamezi (probably endemic).
Other dry forest phanaeines: most widely distributed phanaeine genera are Phanaeus and
Coprophanaeus, each with species as far south as Argentina and as far north as Texas. Except for
limited penetration and Mesoamerican diversification of Sulcophanaeus, and Oxysternon,
phanaeines remain a largely South American group. In the case of Phanaeus, the subgenus
64
Notiophanaeus is South American with limited penetration into Mesoamerica, while Phanaeus,
sen. str., originated and diversified almost exclusively in Mesoamerica. Only the genera
Phanaeus, Coprophanaeus, Sulcophanaeus and Diabroctis include dry tropical forest species,
only the first two in Mesoamerica. In South America, S. steinheili occurs north Colombian and
Venezuelan dry forest habitats; its closest relative, S. imperator, inhabits dry forests of northern
Argentina and Paraguay (Chacoan regions). Other South American dry forest Phanaeus include
P. achilles in Ecuador and Peru, and the species pair P. palaeno – P. kirbyi in the cerrados and
similar formations of central portion of the continent. Most (if not all) members of the subgenera
Megaphanaeus and Metallophanaeus of Coprophanaeus inhabit thorn and other dry forests from
Brazil to Argentina.
Biogeography of the Genus Phanaeus: If we consider dry forest species of Phanaeus in the
context of the biogeography of the genus as a whole, the follow observations emerge: 1) Pacific
dry forests are areas of high endemism; in the case of Chamela, no species is shared with other
dry forests of the Mexican Gulf Region (Halffter and Arellano, 2002; Halffter et al., 1995; see
also the case of plant endemism reported by Rzedowski, 1978); the same is true for 2) no species
occurs both in the dry forests and in humid forests examined; in each case, resident species are
highly stenotopic; 3) in Mesoamerica, several species have broad eco-geographic ranges that
include xeric habitats, among them P. amithaon, P. tridens, P. daphnis, P. mexicanus (Edmonds,
1994; García-Real, 1995; Halffter et al., 1995; Halffter and Arellano, 2002).
Comparative Biogeography of the tribes Phanaeini and Canthonini: 1) The north-south
distributional limit for dry forest species (and perhaps other species) in both tribes lies in Costa
Rica (southern limit for Coprophanaeus p. pluto, Phanaeus demon excelsus, P. eximius and P. w.
wagneri; northern limit for P. hermes). The principal physical barrier appears to be the Cordillera
de Talamanca, which was uplifted in late Miocene-early Pliocene (8-5 mya) during closing of the
Panamanian portal (Coates & Obando, 1996) and the Rio Grande de Térraba. In the case of
Canthonini (Padilla-Gil and Halffter, 2007), the Talamanca zone is the northern limit for the dry
forest taxa Canthon lituratus (Germar), C. juvencus Harold y C. septemmaculatus (Latreille). The
interplay of the climatological effects of the Pacific current and physiographic complexity of the
region has made the southern Pacific coast of Costa Rica and Panama, which is wetter than
coastal areas to the north, is an important barrier to other groups as well (see Kohlmann et al.,
65
2002, for a discussion of climatic differences between these areas). 2) Our best guess is that the
diversification of both Phanaeini and Canthonini in Mesoamerica and northern ColombiaVenezuela began in the Pleistocene (see Padilla-Gil and Halffter, 2007). 3) Dry forest
canthonines clearly demonstrate a wave of diversification from South America. Chamela is home
to species that have followed all three distribution patterns recognized by Padilla-Gil and Halffter
(2007); while the other dry forest sites examined in Costa Rica and South America have species
only of one pattern, recent invaders/endemics. In contrast, the phanaeine faunas of these areas are
endemics resulting from in situ speciation. 4) The Mexican Pacific coast fauna of both groups has
colonized adjacent dry forests to the north, for example, the Jojutla District of Morelos, where
half the species of Phanaeini and Canthon are shared with Chamela (see Deloya and Moron,
1994). The Jojutla district of the state of Morelos separates two major physiogeographic regions,
the Balsas Depression and the Transverse Volcanic Axis; and the fauna of the two dung beetle
groups reflects this transition. 5) The Canthon (Glaphyrocanthon) viridis species group (RiveraCervantes and Halffter, 1999) and the genus Phanaeus (see Edmonds, 1994) share two
Mesoamerican speciation centers; viz., Mexican Transition Zone mountain systems (below 2000
m for the viridis group, 2700 m for Phanaeus) and the Pacific region dry forests. The
diversification of both groups in both centers was undoubtedly synchronous and association with
the later stages of the Pliocene-Pleistocene orogenic development of the Mexican Transition
Zone (see Appendix 4). 6) In the case of Canthon, the evolutionary scenario developed on the
basis of the interrelationships among the dry forest faunas and their relationships with humid
forest faunas confirm previous hypotheses of a South American origin and diversification. It does
not exhibit, as does Phanaeus, two major centers of extensive radiation, Mesoamerica and South
America.
The tropical dry forests of Mesoamerica and Colombia are important centers of diversification for
not only plants and other animals but also for dung beetles. In both the case of the canthonines
(Padilla-Gil and Halffter, 2007) and that of phanaeines analysis of available data permit the
establishment of primary biogeographic hypotheses (sensu Morrone, 2004). These in turn will
permit future comparative studies based on other Scarabaeinae groups and, perhaps a global
hypothesis that explains the current distribution and evolution of this remarkable group of
beetles.
66
ACKNOWLEDGEMENTS
Our sincerest thanks to Gonzalo Halffter, A. Espinosa de los Monteros and J.J. Morrone for their
careful review of the manuscript; to F. Escobar and F. Vaz de Mello for assistance with
bibliography; and to C. Álvarez for permission to access the SNIB-CONABIO database (Projects
E7, K5, P 134, G 19, H125); and to the Universidad de Nariño, Pasto (Colombia) for awarding
NP-G a “Comisión de Estudios.”
67
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Fig.1 Study sites,DTF (1-7 dry forest sites): 1 = Chamela, 2 = Palo Verde, 3 = Neguanje, 4 = Tierra Bomba, 5 = Los
Colorados, 6 = Zambrano, 7 = Norte del Tolima; (8-9 humid forest sites): 8 = Los Tuxtlas, 9 = Leticia (Amazonas).
The dotted area indicates the distribution of dry tropical forest (alter Padilla & Halffter, 2007)
74
100/83
Chamela
P. Verde
N. Tolima
67/49
Zambrano
67/49
Los Colorados
T. Bomba
Neguanje
Leticia
LosTuxtlas
Fig. 2. Cladogram of relationships among dry forest sites, using phanaeines as the indicator
group. Tree length = 26, CI= 0.88 y RI= 0.57. Numbers above nodes indicated frequencies in the
majority rule consensus tree (of 27 trees)/ Jackknife frequency 20% deletion, 500 replicas.
75
62
Chamela
P. Verde
63
N. Tolima
Los Colorados
Neguanje
Leticia
Los Tuxtlas
Fig.3. Cladogram of relationships of dry forest sites using Phanaeus as the indicator group Single
tree length 14, CI= 1.0 y RI= 1.0. Indicated values are Bootstrap, with 500 replicas.
76
APPENDIX 1. Description of study sites (see Fig. 1 and Padilla & Halffter, 2007; 1 – 4 dry
tropical forest sites; 5 – 6 wet tropical forest sites)
1) Chamela, México, Jalisco. Biosphere Reserve Chamela-Cuixmala (19º 30’ N and 105º 03’ W)
on the SW Pacific coast of Mexico between the Río San Nicolás to the north and the Río
Cuitzmala to the south and in the vicinity of Chamela Biological Station; altitude below 200 m,
average maximum monthly temperatures 28.8 to 32.2 ºC, minima 15.9 to 22.6 ºC; pronounced
rainy season July – November, average precipitation 700 mm.
2) Palo Verde, Costa Rica, Guanacaste. Palo Verde Biological Station is located with the Palo
Verde National Park (10º 20’ N and 85º 18’ W) on the Pacific coast in the valley of Río
Tempisque; altitude 10 to 50 m; average annual temperature 24.0 to 27.8 ºC; average annual
precipitation 1750 mm with a pronounced 6.5 month dry season (December-May).
3) Colombia, Caribbean Region.
a) Zambrano: Finca Forestal Monterrey. Department of Bolívar, Municipality of
Zambrano, 9º 37’ 48” N, 74º 54’ 44”W, 155 m altitude, annual average precipitation 1048
mm.
b) Los Colorados. Department of Bolívar, Municipality of San Juan de Nepomuceno, 9º
51’ 33” N, 75º 06’ 38”W, 300 m altitude, average annual precipitation 1189 mm. This
remnant of dry forest lies in the Santuario de Flora y Fauna Los Colorados.
c) Isla de Tierra Bomba. Department of Bolívar, Municipality of Cartagena, 10º 21’ 36”
N, 75º 34’ 11”W, altitude 50 m, average annual precipitation 789 mm.
d) Neguanje. Department of Magdalena, Municipality of Santa Marta, within Parque
Nacional Tayrona, 11º 18’05” N and 74º 06’ 11” W’, altitude 300 m, annual average
precipitation 1420 m
4) Norte del Tolima. A region along the Río Magdalena 130 km north of Ibagué, municipalities
of Honda, Armero-Guayabal and Piedras, 4º 15’ - 5º 10’ N and 74º 45’ - 74º 50’ W; altitude 250
m, average annual temperature 28 ºC, annual precipitation 1387 mm with two well defined dry
seasons (December-March and June-August).
77
5) Los Tuxtlas, Veracruz, México. Tropical Biology Station “Los Tuxtlas” on the slopes of
Volcán de San Martín, 18 km north of Catemaco, Veracruz, 18º 34’ - 18º 36’ N and 95º 04’ - 95º
09’W, altitude 150 to 530 m, average annual precipitation 4560 mm, average annual temperature
23,7 ºC.
6) Leticia, Amazonas, Colombia. City on the Colombian-Brazilian border, 4º 8’ S 70º 1’ W,
altitude 96 m. Average annual precipitation 3500 mm, with heaviest rain from April to June;
average annual temperature 26 ºC.
78
APPENDIX 2. Phanaeini occurring in the study areas; numbering is the same as used in
Appendix 3.
1. Coprophanaeus jasius (Olivier)
2. C. gilli Arnaud
3. C. parvulus (Olsoufieff)
4. C. pluto (Harold) (including P. p. pluto and P. pluto noguerai)
5. C. telamon (Erichson)
6. Oxysternon silenus Laporte
7. O. conspicillatum Weber
8. Diabroctis cadmus (Harold)
9. Phanaeus bispinus Bates
10. P. cambeforti Arnaud
11. P. chalcomelas (Perty)
12. P. demon Laporte (including P. d. demon and P. demon excelsus)
13. P. endymion Harold
14. P. eximius Bates
15. P. furiosus Bates
16. P. hermes Harold
17. P. meleagris Blanchard
18. P. mexicanus Harold
19. P. prasinus Harold
20. P. sallei Harold
21. P. tridens Laporte
22. P. wagneri Harold
23. Sulcophanaeus chryseicollis (Harold)
79
APPENDIX 3. Cladogram data matrix, study site X taxon (M = Mesoamerica; CR = Costa Rica;
C = Colombia)
1
2
123456789 0123456789 0123
Chamela ( M )
000100000 0010010000 0000
Tuxtlas ( M )
010010000 0001000010 1101
P. Verde (CR )
000110000 0010100000 0010
N. Tolima ( C )
000000000 0000001000 0000
Zambrano ( C )
100000000 0000000000 0000
Los Colorados ( C ) 100000010 0000001000 0000
T. Bomba ( C )
000000010 0000000000 0000
Neguanje ( C )
000000000 0000000001 0000
Leticia ( C )
001011101 1100000100 0000
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APPENDIX 4. Phanaeus, Coprophanaeus and Canthon (Glaphyrocanthon) viridis group
confined to (a) the mountainous area of the Mexican Transition Zone and (b) the Pacific coastal
dry forests, respectively:
Phanaeus, Coprophanaeus: (a) P. daphnis Harold, P. tridens Laporte, P. endymion
Harold, P. halffterorum Edmonds, P. adonis Harold, P. scutifer Bates, P. flohri Nevinson,
P. mexicanus Harold, P. amithaon Harold, P. palliatus Sturm, P. quadridens (Say) y P.
damocles Harold; (b) Coprophanaeus nogueirai Arnaud, OR C. pluto (Harold), Phanaeus
demon Laporte, P. furiosus Bates, P. nimrod Harold, P. zapotecus Edmonds
Canthon (Gl.) viridis group: (a) C. circulatus Harold, C. leechi (Martínez, Halffter &
Halffter), C. vazquezae (Martínez, Halffter & Halffter), C. viridis (Palisot de Beauvois),
C. antoniomartinezi Rivera-Cervantes & Halffter, C. montanus Rivera-Cervantes &
Halffter, C. manantlanensis Rivera-Cervantes & Halffter; (b) C. corporali Balthasar, C.
delgadoi Rivera-Cervantes & Halffter, C. pacificus Rivera-Cervantes & Halffter, C.
deloyai Rivera-Cervantes & Halffter.
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CAPÍTULO IV
Discusión y Conclusiones
Metodología utilizada
El grupo externo se elige tomando en cuenta un grupo real o un taxón hipotético que el
investigador considera como primitivo. Sin embargo, en los análisis del PAE y del cladograma
geológico, tradicionalmente se ha venido empleando como grupo externo una localidad hipotética
que no tiene taxa, ante la imposibilidad de definir un área como “área primitiva” (ver Rosen
1988). En este trabajo se eligió un grupo externo que corresponde a una comunidad con
características ecológicas contrastantes con el bosque tropical seco: el bosque tropical húmedo.
Se cuenta con hipótesis previas sobre el posible origen de los bosques neotropicales objeto de
estudio: Sarmiento (1975) propone la evolución independiente de las formaciones vegetales secas
de Sudamérica en el Cuaternario. Hooghiemstra & van der Hammen (2001) plantean el desarrollo
del bosque húmedo tropical sudamericano desde el Mioceno hasta el Cuaternario. Respecto a la
región de los Tuxtlas, tanto el vulcanismo Plio-Cuaternario, como los registros palinológicos de
Paraje Solo de Veracruz, sugieren que la selva alta perennifolia tiene un origen Plio-Pleistoceno
(ver Ferrari et al. 2002, Graham 2003). Presuponemos que éstos bosques húmedos son más
antiguos que los bsT. Por otra parte los bosques neotropicales elegidos hacen parte del contexto
geográfico y ecológico donde se distribuyen los grupos indicadores (Canthonini y Phanaeini).
Los análisis utilizando el grupo externo permitieron la polarización de los cladogramas, la
adición de caracteres y particularmente en el cladograma geomorfológico, una dimensión
espacio-temporal con el ordenamiento de algunos caracteres, logrando así una solución más
parsimoniosa que la que se hubiera obtenido enraizando con un área hipotética codificada en
ceros. En suma, el grupo externo permitió establecer un eje comparativo que trascendió en todo el
trabajo.
En el PAE se adicionaron jerarquías taxonómicas (vg. subgéneros), que en el caso de Phanaeini
no afectaron la estructura del árbol y en los Canthonini aportaron nuevos elementos al análisis.
Los resultados del trabajo se ven apoyados al observar la similitud faunística de los Canthonini
y Phanaeini entre las diferentes localidades a través del índice de Jaccard (Cuadros 1 y 2). Sin
embargo, los dendrogramas obtenidos utilizando el índice anterior, muestran grupos formados
por ausencia de taxones, sin significado en términos biogeográficos.
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El origen del bsT de México
Según Becerra (2005) el origen del bsT de México ocurrió sincrónicamente con la
diversificación del género Bursera hace 20 a 30 Ma (millones de años). Lo cual es discutible, al
reinterpretar las gráficas presentadas por Becerra, considerar otros trabajos florísticos (vg.
Rzedowski et al., 2005) y confrontarlos con los análisis obtenidos en este trabajo.
Los resultados obtenidos por Becerra nos cuentan una historia de extinción y diversificación de
las distintas especies del género, al parecer sincrónicos, con varios eventos geológicos y
climáticos iniciados probablemente a fines del Cretácico (~ 70 Ma) y que dejaron su huella en los
fósiles que datan del Terciario temprano en Colorado-Wyoming (USA). En el Mioceno, las
gráficas indican dos procesos, uno probablemente de extinción (~ 15 Ma), sincrónico con la etapa
final del levantamiento de la Sierra Madre Occidental y otro de diversificación situado
geográficamente en los estados de Nayarit y Sinaloa. En el Plioceno se presentan las más altas
tasas de diversificación, cuya área corresponde a la propuesta por Rzedowski et al. (2005) en
altitudes medias y bajas de la vertiente pacífica de México (Jalisco a Michoacán). En el
Pleistoceno a Reciente en los bsT de Oaxaca continúan su proceso de diversificación. Estos
últimos coinciden con el área de bsT objeto de estudio y por tanto son tomados como apoyo a la
propuesta planteada por Padilla-Gil & Halffter (2007) sobre el origen de los bsT en el Pleistoceno
una vez que ocurrieron los eventos orogénicos que culminaron a finales del Plioceno: el ensamble
geológico de parte de la cuenca del río Balsas (en el Pleistoceno) y el probable establecimiento de
éstas y otras especies vegetales en tal paisaje.
Rzedowski et al. (2005) confirma la existencia de Bursera en todos los estados de México, con
excepción de Tlaxcala; igualmente indican el estado de Guerrero como el territorio más rico en
componentes de Bursera, seguido por Michoacán, Oaxaca y a mayor distancia Jalisco y Puebla.
En el estado de Guerrero se encuentra la parte baja de la cuenca del río Balsas, la cual presenta
las más altas tasas de diversificación del género. La evolución más reciente y máxima
diversificación en la cuenca oeste del río Balsas se presenta en el límite oeste de los estados de
Guerrero y Michoacán.
Las especies de Bursera en Sudamérica están limitadas a bosque seco espinoso principalmente
del sur de Ecuador y Perú. Este género no es característico ni de los bosques secos de Colombia
ni de Las Caatingas en Brasil (ver Sarmiento 1975, Gentry 1995, Pennington et al. 2000,
Mendoza 1999, Albesiano & Rangel-Ch 2003).
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Los puntos anteriores indican que las especies del género Bursera han sido testigo de los
cambios histórico-geológico y climáticos acontecidos desde el Cretácico hasta el presente en los
ecosistemas secos (bosque espinoso, matorral xerófilo, bsT) en el subtrópico y trópico de
Mesoamérica. Sin embargo, la probable biogeografía histórica de un sólo género de plantas no es
suficiente para explicar el origen de este ecosistema en México.
Se plantea el origen de todo el conjunto de los bosques secos de Mesoamérica y Colombia,
tomando en cuenta las características de los bosques secos de México y sus afinidades florísticas:
1) composición florística donde predominan las familias Fabaceae, Euphorbiaceae, Burseraceae
(Trejo 2005); 2) Endemismo de las especies de los géneros Bursera, Acacia, Euphorbia e Ipomea
(Rzedowski 1991); 3) clima, con condiciones de lluvia marcadamente estacionales; 4) la vertiente
pacifica con un clima más cálido que el del Golfo de México debido tanto a su ubicación
latitudinal como al levantamiento de los sistemas montañosos Eje Volcánico Transversal y Sierra
Madre del Sur (ver Challenger 1998); 5) las afinidades florísticas del bosque seco de Chamela
con los de la región fitogeográfica del norte de Colombia y Venezuela (Gentry 1995).
Origen de los bsT de Mesoamérica y Colombia
El origen de los bosques secos neotropicales de los enclaves estudiados es consecuencia de
varios eventos geográficos y geomorfológicos que confluyen espacio-temporalmente hacia fines
del Plioceno y Pleistoceno, como: la ubicación latitudinal y la influencia de la formación del
Istmo de Panamá; el ensamble geológico de tales sitios: ensamble de la región Caribe de
Colombia y el ensamble de los terrenos en la cuenca del río Balsas (Pleistoceno) y los procesos
orogénicos de México continental hacia finales del Plioceno.
Por otra parte la característica más sobresaliente del bsT es la estacionalidad, relacionada con
la desigual distribución de la precipitación a lo largo del año. El principal generador de lluvias en
el trópico es la ZCIT: Zona de Convergencia Intertropical (ver para México, Challenger 1998;
Costa Rica, Kohlmann et al. 2002; región Caribe de Colombia, Molina 1996). La ZCIT se ubica
al sur del ecuador terrestre. El norte de Sudamérica y el mar Caribe reciben relativamente poca
precipitación, en comparación con la que reciben la Amazonia central y sur (Hooghiemstra et al.
2002). Otro factor que modifica el clima tropical, especialmente en la vertiente del pacífico es La
Oscilación del Sur o del Niño (ENSO), trayendo como consecuencia perturbación atmosférica y
redistribución de las lluvias. Al parecer la posición actual de la ZCIT se produjo durante el
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Holoceno y el ENSO fue ausente o débil durante este mismo período. Con base en estos
argumentos Padilla & Halffter (2007) proponen que las actuales condiciones secas se fijaron
durante el Holoceno Medio en la Región Caribe de Colombia, así como en la Costa Pacifica de
México y Costa Rica.
El análisis geomorfológico de los enclaves de bsT de Mesoamérica y Colombia pone en
evidencia la evolución espacio-temporal de los bosques secos desde el Pleistoceno, así mismo
indica la influencia de los factores climáticos en el origen y evolución de esta comunidad. Esta
hipótesis está de acuerdo con: 1) la similaridad en la composición y estructura florística de los
bosques secos estudiados (ver Cuadro 3). En todos predominan las Fabaceae, Bignoniaceae y los
géneros más diversos en cada bosque son: en Chamela Ipomea, en Guanacaste Cassia y en los
bsT de Colombia Capparis (ver Gentry 1995, Mendoza 1999, Quigley & Platt 2003); 2) con la
escasez de elementos neárticos en la flora de los bsT (Rzedowski 1978, Quigley & Platt 2003); 3)
con las ideas de Sarmiento (1975), quien a partir del análisis de símilitud de géneros de plantas de
formaciones vegetales secas de Sudamérica hipotétiza sobre la posible conformación de la
comunidad de bsT del sur de México hasta el norte de Sudamérica, con posible origen en el
Pleistoceno; 4) con el proceso de especiación de Bursera desde el Plioceno al Reciente (ver
primer punto de la discusión); 5) con las afinidades florísticas y de Canthonini y Phanaeini
presentes en los bsT de Mesoamérica y Colombia.
Relación entre la distancia de los bosques y la similitud faunística
Las distancias entre los enclaves de los bosques escogidos influyen ligeramente en la similitud
faunística de los Canthonini y los Phanaeini. La correlación (p < 0,05) es negativa, pero
estadísticamente no es significativa (ver Cuadro 1 y 2). En los Canthonini, el 30% y en los
Phanaeini el 10 %, de la variación de la distancia entre los bosques se relaciona con la variación
en la similitud de los taxones. Las afinidades faunísticas de cada uno de los grupos con los
bosques están relacionadas con los procesos evolutivos y biogeográficos considerados en este
trabajo.
Biogeografía de los Canthonini y Phanaeini de los bosques neotropicales estudiados
Las relaciones de los Canthonini y en especial del género Canthon en los bosques secos de
Mesoamérica y Colombia se explican mediante tres patrones biogeográficos, lo que evidencia la
85
dinámica espacio/temporal de este grupo en los bosques secos. Por otra parte, se confirma tanto el
origen como la dispersión de la mayor parte de las especies a partir de Sudamérica.
Las especies de Canthon (Gl.) grupo viridis presentan una explosión de especiación en México.
Los escenarios en que ocurre el fenómeno corresponden a zonas de altitud baja y media en las
montañas de la ZTM y a los bosques tropicales de baja altitud. Las especies de los bsT son más
numerosas que las de los bhT. La diversificación se inicia desde finales del Plioceno al Reciente.
Lo cual coincide tanto con el fin de los procesos orogénicos de México continental, como con la
formación de los bosques secos de México.
De acuerdo con los resultados de este trabajo es probable que las especies de C. (Gl.) grupo
viridis de los bosques secos de la vertiente pacífica de México, así como las especies de Canthon
de especiación in situ de Costa Rica y de Colombia se hayan especiado en cada uno de estos
bosques, desde el Pleistoceno, concomitante con la evolución y desarrollo de la comunidad de
bosque seco tropical.
Los Phanaeini de los bsT de México y Costa Rica presentan mayor afinidad como los de los
bosques secos de la región Caribe y de los valles interandinos de Colombia. Tanto por las
afinidades taxonómicas como geográficas, los Phanaeini de los bosques secos estudiados
constituyen comunidades endémicas que probablemente evolucionaron sincrónicamente con los
bsT desde el Pleistoceno.
El estudio comparativo de los patrones de distribución de Canthonini y de Phanaeini en los
bsT, revela la especiación mucho más reciente de los Phanaeini y evidencia la posible
diversificación sincrónica espacio/temporal del género Phanaeus y del subgénero Canthon
(Glaphyrocanthon) grupo viridis en México. Los Phanaeini y los Canthon de los bsT de la
vertiente Pacífica de México presentan una composición característica que los diferencia tanto de
los bsT de la vertiente del Golfo de México, como de las especies que se distribuyen en las
montañas de la ZTM.
Los bsT de Mesoamérica y los del norte de Sudamérica están constituidos principalmente por
elementos neotropicales y presentan afinidades florísticas entre sí como lo señaló Gentry (1995)
el bsT de Chamela comparte 15 géneros con la región fitogeográfica del norte de Colombia y
Venezuela. Son reconocidas las especies provenientes tanto de Centroamérica como de
Sudamérica en los bosques secos de Oaxaca (Salas-Morales et al. 2003). Este trabajo muestra que
los Canthonini presentan las mismas afinidades en los bsT de Mesoamérica y Colombia
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(evidencia apoyada por el índice de Jaccard, Cuadro 1) y al igual que ocurre con las plantas tanto
los Canthonini como los Phanaeini en la vertiente pacífica de México presentan las tasas más
altas de especiación in situ.
Sin duda, numerosas plantas y animales como los Canthonini y Phanaeini, existieron antes de
integrarse a la comunidad de bsT. La comunidad que conocemos hoy como bsT probablemente
inicio su evolución a partir del Plioceno y se integra como conjunto a partir del Pleistoceno
cuando ocurrieron todos los procesos geomorfológicos descritos anteriormente en cada uno de los
bsT, así como los procesos de dispersión y especiación tanto florísticos como faunísticos.
Los bosques secos de Mesoamérica y Colombia constituyen un escenario interesante para los
procesos evolutivos y de dispersión de múltiples especies tanto de la flora fanerogámica como de
la entomofauna. Es destacable la vertiente seca del Pacífico y la cuenca del río Balsas en México,
como centro de especiación de algunos Canthon y de Phanaeus, así como el corredor formado
por los bosques secos desde el sur de México hasta Costa Rica, ámbito de distribución de parte de
las especies de Canthonini y Phanaeini.
Los bsT de la vertiente pacífica de México son heterogéneos. Los bosques secos de Jalisco a
Michoacán y los de Oaxaca, particularmente presentan las tasas más altas tanto de diversidad
como de endemismo. Esto se ve reflejado por la especiación diferencial espacio/temporal de las
especies de Bursera (véase primer punto de la discusión); por la alta riqueza florística de los bsT
de Michoacán (Caleta e Infiernillo) equiparable con la de los bosques de Oaxaca (Copalita) y la
alta diversidad beta (ver Trejo 2005); por la estructura y composición característica de los
bosques secos de Oaxaca (Salas-Morales et al. 2003, Gallardo-Cruz et al. 2005) y por las
especies de Phanaeus y de Canthon circunscritas a los bosques secos de Oaxaca son P. nimrod,
P. zapotecus y C. (Gl.) delgadoi. Las otras especies se encuentran ampliamente distribuidas en la
vertiente pacífica de México.
Análisis de los Canthonini y Phanaeini de los bsT y bhT
La mitad de las especies de Canthon presentes en la selva de Los Tuxtlas (ver capitulo 2,
apéndice 1) mantienen su rango de distribución geográfico hasta Sudamérica. C. (Gl.)
subhyalinus, C. (C.) morsei y C. (Gl.) edmondsi; están asociadas a bhT y probablemente han
colonizado de forma secundaria algunos lugares de bsT: C. morsei se encuentra en los bosques
secos del norte de Tolima y en Palo Verde; C. subhyalinus en algunos bosques secos de la región
87
Caribe de Colombia y en norte del Tolima. Es interesante anotar que ninguna de estas tres
especies fue registrada en Leticia.
Es muy probable que tanto los Canthonini incluidos en el segundo patrón de distribución de los
bsT, así como las especies citadas anteriormente de la selva de los Tuxtlas, se hayan diversificado
en el norte de Sudamérica, una vez finalizó el levantamiento del norte de los Andes (Mioceno
Medio) y se establecieron las cuencas actuales de los ríos Magdalena, Orinoco y Amazonas. Esta
explicación esta de acuerdo con: 1) la afinidad taxonómica de las especies planteadas en este
patrón de distribución, 2) su asociación a los bosques neotropicales (secos y húmedos de baja
altitud), 3) la afinidad neotropical de los Canthonini de los bosques tropicales de tierras bajas y
bosques tropicales subandinos de los Andes del norte de Sudamérica, 4) la disimilitud con los
bsT del este de Bolivia y otras formaciones vegetales de ambiente seco del sur de Sudamérica
(Cerrado y Chaco), 5) la época de cierre del Istmo de Panamá, 6) la ausencia de estas especies en
las Antillas, 7) los diferentes rangos de distribución alcanzados por las especies, en sentido SurNorte, 8) la hipótesis también está de acuerdo con la probable expansión posterior desde la mitad
más austral de Sudamérica de algunas especies como Canthon lituratus, Canthon mutabilis,
Canthon septemmaculatus.
Ninguna especie de Canthonini de Leticia es compartida ni por los bsT de Palo Verde y
Chamela ni por Los Tuxtlas (ver Cuadro 1). Por otra parte C. aequinoctialis presente en Leticia
probablemente ha colonizado los bosques secos del norte del Tolima y los Colorados en la región
Caribe de Colombia.
La Amazonía parece ser el escenario para las especies que evolucionaron según la hipótesis
antes propuesta. Esto esta de acuerdo con la expansión hacia el norte de C. aequinoctialis que
llega hasta Belice y con C. angustatus, presente en Leticia pero ausente en los otros bosques
estudiados. Esta especie asociada a bhT, se distribuye hasta el sur de México, Selva Lacandona
(Halffter com. pers.), así como de especies con especiación in situ, más recientes y con rango
geográfico restringido a la Amazonía.
Los Canthonini tanto de los bsT como de los bhT analizados comparten probablemente la
misma historia biogeográfica. Sin embargo el número mayor de especies asociadas a los bsT, así
como la mayor especiación en este ecosistema permiten reconocer a los Canthonini como
característicos de los bosques secos neotropicales.
Por otra parte el origen y diversificación de los primates neotropicales y especialmente del
88
género Alouatta (ver Schneider, 2000; Cortés-Ortiz et al., 2003) coincide espacio-temporalmente
con el posible origen de los Canthonini planteado en la hipótesis anterior. Esto en parte explicaría
la asociación de algunas de estas especies de Canthon (vg. C. subhyalinus) con A. palliata y
posiblemente su distribución geográfica (ver Padilla-Gil & Halffter 2007).
En la selva de Los Tuxtlas, Phanaeus endymion y Sulcophanaeus chryseicollis están asociadas
a ecosistemas de bhT y muestran rango geográfico restringido a Mesoamérica la primera y al
sureste de México la segunda. Las especies de Phanaeus presentes en Leticia están circunscritas a
la región de la Amazonia (ver Cuadro 2); las de Oxysternon presentan rango geográfico hasta
Centroamérica siempre asociadas a bhT.
La asociación de algunas especies de Phanaeini a ecosistemas secos tanto de Mesoamérica
como de Sudamérica es interesante desde el punto de vista ecológico y geográfico; al parecer
evolucionaron sincrónicamente con la aparición de dichos ecosistemas y presentan rangos
geográficos restringidos. Las especies de Phanaeini de los bhT Los Tuxtlas y de Leticia presentan
la misma tendencia biogeográfica, especiación in situ, probablemente a partir del Pleistoceno.
Al igual que en las plantas, la integración de los escarabajos estudiados al bsT es un
fenómeno geológicamente reciente, como lo evidencia la dinámica espacio temporal de los
Canthonini y la especiación de los Phanaeini. Sin lugar a dudas, tanto los Canthonini como
muchas plantas de origen sudamericano han experimentado procesos similares espaciotemporalmente desde el Plioceno para llegar integrar la comunidad que hoy forma el bsT de
Mesoamérica y Colombia.
Gradiente de distribución en Costa Rica
De acuerdo con la pluviosidad el oeste de Costa Rica queda dividido: al norte predomina el
bsT y el promedio anual de lluvias es menor a 2000 mm (provincia de Guanacaste). Al sur con
predominio del bhT, con promedio de lluvia mayor a 2000 mm anuales, delimitada al norte por el
río Grande de Tárcoles y al sur por el río Grande de Térraba y las cordilleras Central y de
Talamanca.
Debido a este contraste climático y de vegetación la dispersión de algunas especies en ambas
direcciones norte-sur se ve restringido. Algunos Phanaeini con afinidad por los bsT de México
penetran hasta Guanacaste y algunas especies de Canthon de Sudamérica no llegan a Guanacaste,
alcanzando en ambos casos diferentes grados de penetración. Al parecer hay otras especies tanto
89
de animales como de vegetales que presentan también sus límites geográficos en esta área.
Consideraciones finales
Es la primera vez que se analiza la biogeografía de los Canthonini y Phanaeini considerando
las especies de Colombia y Mesoamérica así como su asociación a un tipo de vegetación, en
este caso, al bosque tropical seco. El trabajo revela el predominio de los Canthonini como un
fenómeno biogeográfico característico de los bosques secos y la integración espacio-temporal
de estos Scarabaeinae en la reconstrucción de la biogeografía histórica del bsT.
El análisis geomorfológico de los enclaves de bosque seco y la convergencia de los elementos
que regulan el clima en la zona neotropical y su posible localización y acción en tiempo
geológico reciente permitieron integrar, sintetizar y plantear la hipótesis sobre el origen de los
bosques secos de Mesoamérica y Colombia.
Se proporcionan varios elementos que contribuyen a la reconstrucción de la biogeografía
histórica de la comunidad de bosque seco de Mesoamérica y Colombia, tales como el análisis
geomorfológico de los enclaves de bsT, el planteamiento de la hipótesis sobre su origen, la
comparación tanto con las hipótesis previas sobre su origen como de afinidades de los bsT
basados en la vegetación y los patrones de distribución de Canthonini y Phanaeini.
Las plantas, los Canthonini y los Phanaeini de bsT han experimentado un proceso de evolución
para llegar a integrar la comunidad que es el bsT. Las plantas y los Canthonini estudiados
coinciden en presentar un componente sudamericano de afinidad tropical y las plantas junto con
los Canthonini y Phanaeini una alta evolución in situ, principalmente en los bsT de la vertiente
pacífica de México.
Se contribuye al conocimiento de la biogeografía de los Canthonini y Phanaeini con base en
la reunión e integración de varios elementos tales como: el rango geográfico de las especies; las
relaciones de afinidad de los grupos taxonómicos en los bsT y/o la conformación de
comunidades endémicas de bsT; las relaciones filogenéticas y/o taxonómicas de cada grupo; el
origen de los bosques secos (escenario donde se presentan). La integración de los anteriores
elementos permitieron el planteamiento de los patrones de distribución y ubicarlos espaciotemporalmente, así como la comparación entre los géneros Canthon y Phanaeus circunscritos a
patrón de especiación in situ en Mesoamérica.
Algunas especies de Bursera, de Canthon (vg. especies de C. (Gl.) grupo viridis) y los
90
Phanaeini de bsT, al parecer se encuentran en procesos de especiación y es posible que el
mismo proceso este ocurriendo en los bhT Los Tuxtlas y Leticia. El proceso de expansión de las
especies de Canthon desde Sudamérica hacia Mesoamérica continúa y es posible que futuras
investigaciones refuercen este patrón de distribución.
La generalización del segundo patrón de distribución de los Canthonini con relación a las
especies de los bhT, teniendo en cuenta las afinidades taxonómicas y el contexto biogeográfico
de las especies de este grupo en Sudamérica permitieron formular la hipótesis sobre el posible
origen espacio-temporal de las especies que integran este patrón de distribución.
La realización de estudios similares con otros grupos de insectos u otros organismos en los bsT
de Mesoamérica y Colombia permitirán la adición de más elementos en la reconstrucción de la
biogeografía histórica del bosque seco.
91
Cuadro 1. Canthonini, índice de similitud de Jaccard/ distancia (km) aproximada de los bosques tropicales objeto de estudio.
Chamela
Chamela
Los Tuxtlas
Palo Verde
Tolima
Zambrano
Los Colorados
Tierra Bomba
Neguanje
Tuxtlas
0.25/1177
PVerde
Tolima
Zamb
LCol
TBom
Neguanje
Leticia
0.29/2544
0.32/4214
0.32/4088
0.18/4080
0.18/4082
0.11/4230
0.11/5218
0.15/1418
0.14/3017
0/2930
0/2910
0.09/2972
0/3151
0/4111
0.21/1598
0.13/1540
0/1508
0.08/1515
0/1705
0/2680
0.2/578
0.17/655
0.17/701
0.09/767
0.09/1111
0.4/103
0.4/166
0.33/217
0.33/1593
0.6/163
0.6/1722
0.25/101
0.33/171
0.33/1778
1/1785
Leticia
92
Cuadro 2. Phanaeini, índice de similitud de Jaccard/ distancia (km) aproximada de los bosques tropicales objeto de estudio.
Chamela
Chamela
Los Tuxtlas
Palo Verde
Tolima
Zambrano
Los Colorados
Tierra Bomba
Neguanje
Tuxtlas
0.3/1177
PVerde
Tolima
Zamb
LCol
TBom
0.3/2544
0.22/4214
0.04/4088
0.04/4080
0.13/4082
0.04/4230
0.04/5218
0/1418
0.33/3017
0/2930
0/2910
0/2972
0/3151
0/4111
0.09/1598
0/1540
0/1508
0/1515
0/1705
0/2680
0/578
0/655
0/701
0/767
0/1111
0/103
0.33/166
0/217
0/1593
0.33/101
Neguanje
Leticia
0/163
0/1722
0.33/171
0/1778
0/1785
Leticia
93
Cuadro 3. Comparación de la diversidad florística de los bsT , muestreos de 0.1 ha (DAP 2.5cm) (Gentry 1995, Mendoza 1999,
Quigley & Platt 2003)
Localidad
individuos
Precip.
Temperatura
meses
Área basal
Alt. del dosel
N. de familias
N. de especies
N. de
mm/año
°C
secos
m2/0.1 ha
m
Zambrano
Los Colorados
Tierra Bomba
Neguanje
Norte del Tolima
Chamela (Tierras altas 1)
Chamela (Tierras altas2)
Chamela (Arroyo)
Guanacaste
1048
1189
789
1420
1387
748
748
748
24
28
28
27
28
25
25
25
6-7
6-7
6-7
11.4
7
6-8
6-8
6-8
2.31
6.15
2.77
3.68
3.94
2.63
2.18
5.10
7-9
22-25
7-9
22-25
10-18
15
24
41
26
31
31
37
34
46
55
121
56
67
62
91
89
103
471
534
556
337
515
399
506
453
(bosque de galería)
1600
25
6
4.16
20
35
63
95
individuos
94
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