Lizards and rodents: an explanation for their relative species

A r c h . B i o l . M e d . E x p e r . 12:179-190, 1979
L i z a r d s and rodents: an explanation for their
relative species diversity in C h i l e
Lagartijas y roedores: una explicación para su
diversidad relativa en Chile
E D U A R D O R. F U E N T E S , F A B I A N M . J A K S I C
Instituto de Ciencias Biológicas, Universidad Católica de Chile.
Casilla 114-D, Santiago de Chile
(Recibido para su publicación el 3 de diciembre de 1977)
F U E N T E S , E . R . , J A K S I Ó , F . M . L i z a r d s and rodents: an explanation for their relative species diversity
in C h i l e . ( L a g a r t i j a s y roedores: una explicación para su diversidad relativa en C h i l e ) . A r c h . B i o l .
M e d . Exper.
It
72.179-190, 1979.
is discussed that the relative richness o f l i z a r d fauna in C h i l e might be related
attributes of this g r o u p ( m a r k e d altitudinal segregation, coarse-grained
vagility associated
w i t h e c t o t h e r m y ) , which w o u l d favor a rapid
to ecological
habitat selection, and l o w
speciation pattern
concomitantly
w i t h Q u a t e r n a r y Glaciations.
L i z a r d s w o u l d d i v e r g e on mountaintops during interglacial periods and w o u l d m e r g e into fewer
forms o r further d i v e r g e on the l o w l a n d s during glacial periods' intermingling. It is shown that
number of subspecies per species in mountaintops is greater than on l o w l a n d s , which is consistent
with the above hypothesis hereafter referred to as " m o u n t a i n speciation m o d e " . H o w e v e r , it is also
documented that lizards might exhibit a " v a l l e y speciation m o d e " , in which case they w o u l d d i v e r g e
in
non-icy valleys during glacial periods, intermingling
w i t h lizards in adjacent
valleys during
interglacials. A s in the previous case, merging or speciating of divergent forms w o u l d depend on
the degree of reproductive isolation attained.
A s a contrast, it is discussed the situation o f the relatively poor Chilean rodent fauna. It is shown
that although
rodents exhibit some altitudinal segregation
they do not
mountaintops than on l o w l a n d s , which is possibly related to their
and greater vagility associated
w i t h endothermy.
O n the other
form m o r e subspecies on
fine-grained
habitat
selection
hand, number of subspecies per
species is positively correlated w i t h the extension of its geographical range, which strongly
suggests
a " v a l l e y speciation m o d e " for rodents in C h i l e .
SPECIATION
THE
BIOGREOGRAPHY
QUATERNARY GLACIATIONS
PROBLEM
depauperated
VERTEBRATES
when
compared
CHILE
with
the
fauna
of an area of similar climate and resources, like
C h i l e has
a geographically isolated position
in
C a l i f o r n i a for e x a m p l e .
South A m e r i c a . T h e high A n d e s on the east, the
barren A t a c a m a
desert on the north, and
M a m m a l s , ants and
bees are about half as
the
diverse in C h i l e than in C a l i f o r n i a ( 2 ) . Birds
Pacific O c e a n on the west, are all strong barriers
and frogs are about the same, but lizard species
to the dispersal
are about one and a half times m o r e numerous
of most o r g a n i s m s ( 1 ) . C o n c o ­
mitantly, the Chilean fauna tends to be relatively
in C h i l e than in California ( 2 ) . In fact, speciation
179
180
F U E N T E S and J A K S I C
in Chilean Liolaemus
species has
been
strong
tend
to exhibit
strong
altitudinal
partitioning.
enough to produce a mosaic of alternative c o m ­
Of
munities in central C h i l e ( 3 ) . O n the other hand,
20 are predominantly found above 1000 meters
endemism in m a m m a l s , ants, and bees also tends
above sea level ( m a s l ) , and only 3 of them
to be high ( 1 , 2, 4 ) .
known
The
question
w e will attempt
is
species known in C h i l e ,
to live above and
this
However,
at
varies.
but complex archipelago with copious speciation
and 27° latitude south by the A t a c a m a
for
there are 8 Liolaemus
m o r e like an island for other
latitudes
Between
are
altitude.
segregation
groups.
different
below
w h y C h i l e seems to be comparable to an isolated
lizards, and
to answer
the 36 Liolaemus
altitudinal
aproximately
18°
desert,
species above 1000 masl
and only 1 below it. Further south, as the valley
Possible explanations
for differences
in
the
gets m o r e mesic, the proportion of species found
number of species between C h i l e and C a l i f o r n i a
below
could be related to the amount of time the dif­
Between 27° and 37° latitude, the ratio of species
ferent groups have had to speciate in C h i l e , o r
above 1000 masl to species below is about
1.6;
to
between 37° and 42° latitude, the ratio is
1.0,
different
resource
availabilities in the
two
1000
masl
increases
monotonically.
regions. H o w e v e r , recent studies ( 2 , 5, 6 ) have
and further
shown
the l o w productivity in the northern valley, the
resource
organisms
is
California. O n
evidence
does
supply
quite
aid
several groups o f
in
Chile
and
the other hand, paleontological
is weak or
not
for
comparable
to
inexistent,
explain
conceivable though
that
the
both
and
therefore
patterns.
of these
It
could be shown to be important.
tive route which w e hope will at least offer
explanation
for
the
relative
a
species
diversity phenomenon. W e will attempt to show
that ecological differences between lizards
other
groups,
manifest
low
average height o f the Andes south of 42°
latitude (see 7 ) .
T h u s , there is strong altitudinal
partitioning
only in the central part of the country, roughly
around Santiago. F i g . 1 shows altitudinal species
In this contribution w e have taken an alterna­
partial
reflects
m o r e mesic climate in the central part, and the
is
factors
south it is 0.0. T h i s trend
themselves in
and
different
speciation patterns. Because available ecological
sequences
on
the
mesic
Roble, L a Campana)
slopes ( L a g u n i l l a s ) .
Coastal
Ranges
(El
and on the drier A n d e s
T h e figure starts only at
about 1000 masl and does not contain the species
b e l o w the level (see 8 ) . Still, it can be seen that
there is species turnover on the three
mountains,
although it is not strictly parallel in all o f them.
It
information about most taxa is scarce, w e w i l l
is important
to emphasize
at this
point
restrict
ourselves mostly to the comparison o f
that in other transects covering a w i d e r altitudinal
lizards
with rodents.
range, some species would probably be added,
T h e r e is no doubt
that
these are " p a r t i c u l a r " groups, but as will be seen
and
later in this paper, their speciation modes could
slope and exposure. T h e important
Fig.
offer clues for future w o r k on other taxa.
First
manner,
w e w i l l document,
in a fairly detailed
the ecological attributes of lizards in
the
will then c o m p a r e these attributes with the
available ecological information on rodents
and
their postulated speciation mode.
1 are the existence of species turnover
lack
of parallelism
in
The
the distribution
biological
leopardinus
lizards,
country.
The
and
of
reasons
for
the
altitudinal
ed, but there are already some e m e r g i n g patterns.
L.
high A n d e s border its east side, and on the west
on
aspects in
S o m e species in F i g . 1, like L. nigroviridis
PARTITIONING
C h i l e is basically a mountainous
depending
species replacement are currently being investigat­
L.
ALTITUDINAL
be dropped,
species on nearby mountains.
relation to their proposed pattern of speciation.
We
perhaps other
are
whereas
schroederi
other
and L.
species further
typically
species like L.
nitidus
and
high-mountain
are
low
south or north ( 8 , and
tenuis,
altitude
personal
observations). Species w o u l d thus be " t r a c k i n g "
coast it is limited by the Coastal R a n g e s , with
in altitude
only a n a r r o w central valley in between. T h i s
can survive and reproduce. H o w e v e r , what
physiography is strongly reflected in the distri­
the restrictions which limit the use o f the w h o l e
bution of the organisms. T h u s , Chilean
altitudinal gradient by the species?
lizards
and
latitude conditions w h e r e they
are
LIZARDS A N D
Fuentes
that
and
density
selective
and
Jaksic
pressure on
open
(in
preparation)
of grasses can
ground
show
impose
a
such
that
lizards,
analogue
species
strong
grass
can
be
181
RODENTS
lemniscatus
( F i g . 1). L. lemniscatus
At
El R o b l e , as grass density
altitude, L.
lemniscatus
decreases
munity,
in each habitat are different, and thus presence
nigrouiridis
or
is absent from the Coastal R a n g e s .
absence of grass acts as a sieve
alternative
communities
(9,
separating
10) in
each
environment.
We
found
with
drops out of the c o m ­
distinguished. O p t i m a l morphologies for survival
true
is a grass-
species which uses ground preferentially ( 5 , 11).
being replaced by the j u v e n i l e s o f
(see 5 ) . In this case L.
L.
leopardinus
O t h e r species seem to be strongly
associated
with the presence or absence of a v e r y particular
this mechanism
to explain
some
environmental
feature.
Thus,
L.
monticola
is
latitudinal as well as altitudinal habitat partition­
a
ing.
presence of boulders and rocks ( 8 , 11, 12). T h e s e
T h u s , L. nigrouiridis
dweller,
ground
but
can
is preferentially a rock
frequently
if grass density
be found
Both
species
are
leopardinus
as grass density increases.
preferentially
rock
dwellers,
but have the option of hunting on the
and L. leopardinus
L.
the
is l o w . A t L a g u n i l l a s
(east of Santiago) w e found that L.
replaces L. nigrouiridis
on
ground,
The
dweller
features
strongly
associated
tend to be more frequent
with
the
high in
the
mountains, close to tops and ridges, and concomi­
tantly L. monticola
at l o w altitudes.
drops out of the community
Similarly, L.
tenuis
is a tree
dweller ( 5 , 8 ) and its presence is strongly
as­
sociated with the distribution of trees.
is more of a grass-species than
nigrouiridis.
rock
Besides
these
particular
elements,
some
general metabolic difficulties seem to add more
same grass-non grass phenomenon could
be involved in setting an altitudinal
EL
1000
limit on
L.
ROBLE
1200 1400 1600
T
1
constraints on high altitude
hance
zonation.
CAMPANA
1800 2000
1
1
1000
1200
1400
1600
species and to en­
Shortening
of
the
growing
LAGUNILLAS
I8D0 20CO
I0CO
1
1400
1830
2200
1 1 1 1 1 1 1
L_ nigroviridis
L leopardinus
L_ schroederi
L_ tenuis
L. monticola
L nitidus
L. lemniscatus
Lgravenhorsti
L. fuscus
C maculatus
Fig. 1. Altitudinal species replacement of lizard species.
Altitudinal species sequences at the closeby mountains El Roble, Campana, and Lagunillas are compared. Data for El
Roble were obtained from Pinto el al. (43). Data for Campana from Jerez and Ortiz (44). Notice that species sequences
differ on the three mountains. See the text for further explanation and discussion.
182
F U E N T E S and J A K S I C
season with altitude imposes strong
on
some species. Fuentes
and
restrictions
D i Castri ( 1 3 )
noted that high altitude Liolaemus
species are
1. Species which live on mountains and do not
form subspecies. H o w e v e r , this is strictly not
an
exception
but
sustaining evidence, since
forced to be o m n i v o r o u s , incorporating vegetable
these species are known from only one locality
tissues
and therefore give strong evidence for genetic
into
their
diet.
They
interpreted
this
plant consumption as compensation for l o w and
isolation
unpredictable
category are L. signifer,
ments.
insect densities in those e n v i r o n ­
Furthermore,
large Callopistes
its
( 5 ) found
that
eats vegetation at
quardi,
L.
not
paulinae,
(see 8 ) .
of
altitudinal
favorable season
distribution,
but
shortens with altitude,
lizards
mountaintops.
L.
L.
2. M o u n t a i n
Species
L.
buergeri,
constanzae,
species
at
in
L. ornatus,
pantherinus,
lorenzmulleri,
d o w n . A g a i n , it w a s suggested that as
limit
further
Fuentes
maculatus
on
L.
L.
L.
knegi,
and
high
L.
darwxni
latitudes
do
form
pensate the l o w consumption of insects by eating
mountains are very l o w , and distinction
plant material. T h e p r o b l e m is that only large
ween mountain
lizards can
all
use vegetation efficiently,
plants
are
physiological
edible
(13,
difficulties
14).
for
(see 7 ) . A g a i n , this is expected from the h y ­
the
pothesis
lizards
of
fitzingeri
17). T h i s
seasons at
indicates
higher
that
altitudes
be viviparous
shorter
could
favorable
impose alti­
tudinal restrictions to egg development of some
Liolaemus
species. O n the other side, l o w alti­
tudinal limits are likely to be associated
with
particular habitat features ( i . e . rocks and trees),
and diffuse competition ( 9 ) in these m o r e stable
environments.
In
and
does not contradict
it. Species
in this category are L. magellanicus,
altitude
(8,
bet­
and valley becomes arbitrary
not
L.
to
not
latitudes
and
most
also tend
H o w e v e r , at high
Besides
eating l o w caloric plant material ( 1 5 , 1 6 ) , high
Liolaemus
moc-
fitzgeraldi,
have to be less insectivorous and have to c o m ­
subspecies.
this
L.
lineomaculatus,
L.
L.
d'orbignyi,
kingi,
and
L.
(see 8 ) .
T h u s , the pattern of divergence on mountains
but homogeneity at l o w altitudes, confirms the
suggestion
isolation
based
on
of lizard
altitudes.
ecological data
populations
A s w e saw
regarding
living
before, habitat
at
high
selection
(most likely in relation with interspecific c o m ­
petition) can set barriers to movement of lizards
on an altitudinal gradient. It is likely then that
sum, in central C h i l e there is
altitudinal
species turnover of lizards and this pattern seems
to be associated
with alternative
these barriers have a l l o w e d for intraspecific dif­
ferentiation in mountain species (see Fig. 2 ) .
morphologies
and behavior of the species. In general, species
Interestingly,
the
of
nal
parable t o , or greater than differences observed
habitats,
are not
suggesting
equally adapted
the
presence
to
other
of ecological
barriers to lizard movement between
mountains.
populations
differentiation
between
gradient
mountain
degree
with optimal fitness at one point in the altitudi­
has
been c o m ­
between mainland and island populations. T h e r e
are no island species absent from the mainland,
and the existing island forms are o n l y subspecies
of mainland species ( 8 ) .
H e r e w e refer only to islands connected with
M O V E M E N T S BETWEEN MOUNTAINS
the mainland during the last glaciation, that is
H e l l m i c h ( 1 2 , 18) noted that high altitude species
separated
tend to diverge more than species inhabiting the
meters deep channel
valley. In fact, using the data by H e l l m i c h ( 1 2 )
excludes mainly the Juan Fernández archipelago
and
and some large islands on the southern channels,
D o n o s o - B a r r o s ( 8 ) , w e have been able to
from the continent
by at
(19, 20). T h i s
most
100
restriction
show that species living under 800 masl tend to
both of which are not known to h a v e lizards. It
have fewer
also excludes Easter
subspecies
than
species above that
level (Fischer's exact probability test, P < . 0 0 1 ) .
Typical
Furthermore,
braltstroemi,
species
8 0 0 masl (L. nitidus,
living
above and
L. fuscus,
and L.
below
lemnisca-
major
island
Island, since it is oceanic.
subspecies
L.
pictus
are
L.
chiloensis,
cyanogaster
L.
pictus
on the southern C h i l o é archipelago (43°
tus) do not form subspecies. T h e r e are t w o types
latitude south), L. nigromaculatus
of exceptions to this rule:
nigromaculatus
ater,
and
sieversi at about 30° latitude.
L.
183
LIZARDS A N D RODENTS
Fig. 2. Altitudinal islands in central Chile.
Distribution of heights above 1000 masl (black) or above 600 masl (dashed) are comparable to an altitudinal mainland on
the east, with an archipelago on the west. Glacial snows could have been as low as 900 masl (see 21) and therefore the
density of altitudinal islands is a measure of alternative recolonization opportunities in central Chile during interglacial times. See the text for discussion and more explanations
In sum, adaptations of lizards to their habitats
seems to be fine enough to entail
reproductive
isolation between populations on nearby
moun­
tains.
would
have
formation
isolation
in the European
Alps,
Hell-
mich ( 1 2 ) suggested the Andean races o f
mus
would
develop
on
different
Liolae-
mountains
during interglacial periods and eventually come
into
contact
with
each
on
glaciations,
ranges
Based on research
other
during
glacial
resource
partitioning
By the above mechanism, races and
species
A T W O W A Y SPECIATION MODEL
favored
and
hence n e w forms capable o f coexistence.
would
separate
populations
follow
perhaps
interglacial
mountains.
formerly
w o u l d intermingle and
During
on
different
further
diverge,
or if differences achieved are not strong enough,
they w o u l d m e r g e into one species. A t any rate,
this
is
a
speciation
model
which
in
repeated
glaciation events could generate great diversity.
In central C h i l e there have occurred three to
periods. T h a t is, as snow level approaches l o w e r
four
altitudes,
ranges along the A n d e s , as well as in the Coastal
high
altitude
lizard species and
sub­
glaciations
(21)
and
there
are
separate
closer to
R a n g e s ( 7 ) , thus a l l o w i n g for multiple
species
the valley, with many of them c o m i n g in contact
formation within even a small latitudinal
range.
with each other. If reproductive difference achiev­
The
essential factors in this speciation mode is
ed during the isolation in the interglacial period
that
species
were
and that during interglacial periods, movements
species w o u l d shift their distributions
pronounced
enough,
natural
selection
partition
the
habitat
altitudinally
184
F U E N T E S and JAKSIC
between mountains are restricted and comparable
On
to
by valley speciation
movements
between
on the continental
of
this
mainland
and
islands
shelf. In the remaining part
contribution
we
shall
refer
to
this
speciation mode as " m o u n t a i n speciation".
A
second mode of speciation,
the other
number
side, the same design
of species per cycle. T h e point is that
speciation
rate depends
isolates and amount
not exclusive
operating
would at most double the
directly on number o f
of intermingling. C l e a r l y ,
speciation rate of groups using both
modes
C h i l e . D u r i n g glaciations, pockets of non snowed
speciation rate of groups using only one mode.
been
inferred
to occur
in
the
southern
be
considerably
higher
than
For all the reasons given above, lizards seem
habitats or at least with short g r o w i n g seasons,
have
would
speciation
of the former, is also likely to have operated in
to fall into the mountain
speciation mode. T h e
A n d e s ( 2 1 ) . T h e s e pockets being more or less
evidence given on their altitudinal
isolated from each other, can lead to reproductive
and on the
isolation
inter-
presence of subspecies and even species on some
glacial periods, the formerly isolated populations
mountains during the present interglacial, point
between
populations.
w o u l d intermingle and further
During
differentiate, or
m e r g e into fewer forms. F o r analogous reasons
stratification
isolation between mountains,
in this direction. H o w e v e r , in addition
with
lizards
could have also used the valley speciation mode.
as before, w e will refer to this speciation mode
Unfortunately, since w e are living on interglacial
as " v a l l e y speciation". In valley speciation, the
period at present and therefore during an
essential
features
mingling phase for valley
between
valleys
are
or
restricted
pockets
movements
during
glacial
possible to clearly determine its importance.
periods, and m i x i n g during interglacial periods.
Fig. 3 shows the t w o speciation modes in a
Possible
lizards
examples
could
patterns
of L.
t w o valleys, as shown in F i g . 3, each cycle o f
L.
platei
mountain
26°
diagram.
number
Note
that
speciation
for three
mountains
would at most triple
and
the
of species (species 1 and 2 in Fig. 3 ) .
BEGINNING
INTERGLACIAL
END OF
INTERGLACIAL
inter­
speciation, it is not
platei
and
be
of
the
platei
valley
speciation
geographical
and
L.
nigromaculatus.
is roughly distributed
32° latitude
south, whereas
known subspecies L. platei
GLACIAL
in
subspecies
curicensis
between
its only
is restrict-
INTERGLACIAL
MOUNTAIN / 1
SPECIATION,
DIFFERENTIATION
DIFFERENTIATIONS OF
POPULATIONS
OF POPULATIONS
VALLEY
SPECIATION
DIFFERENTIATION
OF POPULATIONS
Fig. 3. Speciation modes.
Mountain and valley speciation are asynchronous with regard to the phases of differentiation and of mixing of differentiat­
ed populations. In mountain speciation, differentiation occurs during interglacial periods and mixing in valleys
during glaciations. T h e opposite is true of valley speciation, where differentiation occurs in isolated habitat pockets or
val leys during gl acial periods. See th e text for further discussion.
185
LIZARDS A N D RODENTS
ed to a few valleys of
C u r i c o , at 35°
C o d y et at.
latitude
( 2 ) used
beta-diversity, that is
(see 2 2 ) . Both D o n o s o - B a r r o s ( 8 ) and M u l l e r
species turnover over comparable habitat tran­
and H e l l m i c h ( 2 2 ) insist on the subspecies level
sitions, to describe species turnover of m a m m a l s
of
differentiation, although
for
the
L. platei
the
argument.
this is not
It is reasonable
to
crucial
assume
and lizards in California and C h i l e . T h e y found
that
beta-diversity
altitudinal
is
in
central C h i l e . T h i s means not only that lizards
the
continuous
32° and
last
35° latitude
glaciation,
the
south.
previously
distribution of L. platei
could have
and
mammals
rodents
lizards
between
gap
for
transects
quite
During
comparable
on
once had a wider distribution, covering
change
with
and
altitude,
but
that
in central C h i l e — at least around the latitude of
been fragmented. L a t e r , during the interglacial,
Santiago — they seem to change at about
L. platei
same rate.
w o u l d have persisted only in its known
distribution,
35°
with extinctions between 32° and
latitude.
Lwlaemus
Here,
competition
with
other
species could have been very important,
T h e biological compromises involved
altitudinal
segregation
by
rodents
are
the
in
the
not
as
clear as in lizards. In N o r t h A m e r i c a , structural
since they reach high species densities in that
habitat ( 2 7 , 28, 2 9 ) and productivity ( 3 0 , 3 1 )
latitudinal
have been
range
preparation)
L.
platei
( 8 ) . Fuentes
offer
evidence
and Jaksic (in
suggesting
that
— a non grassy species ae is in fact
replaced by L. lemniscatus
the permanence of L. platei
last
glaciation
is not
curicensis
clearly
since the
understood,
but
could be related to the local physiography.
The
second
evidence for
valley
in
lizards is the
kreiss of L.
L.
nigromaculatus
and its numerous
W h a t e v e r the reasons are which explain the
altitudinal
partitioning phenomenon in rodents,
o n e requirement of mountain
nigromaculatus.
subspecies,
evidence for isolation of lizards is the
race
formation
between
between
localities in
a
we
data by O s g o o d
manifestation
lemniscatus
of
the
secondary
discussed
L.
contact
platei
(12).
—
L.
transition occurs at about this same
tend to be relatively
isolated, the same is not true for rodents.
form a latitudinal cline ( 2 , 12), suggested to be
Interestingly,
speciation is not
met by these vertebrates. W h e r e a s lizards living
on different mountaintops
speciation
par­
there
is no published information.
— a grassy species —
at about 32° latitude south. O n the other hand,
invoked in relation to habitat
titioning, but about the Chilean situation
used
Rottmann
to
be
( 3 2 ) , and
statistically
mountaintops
the valley.
found
For
( 1 ) and
Our
greater
than
rodents,
Miller
and
this difference not
significant
(Fischer's
exact
latitude ( 3 2 ° ) and shows clear signs of h y b r i d i z ­
probability test, P > . 3 4 ) . T h a t is, species restric­
ation and secondary contact (Fuentes and Jaksic,
ted to l o w altitudes tend to form as many sub­
in p r e p a r a t i o n ) . ' It is very likely therefore, that
species ( o r to be as isolated) as species living
there w a s a glacial barrier to dispersal at about
on mountaintops.
that latitude. N o w a d a y s w e w o u l d be o b s e r v i n g
the
merging
and
differentiation
of
The
formerly
isolated populations. M o r e evidence on areas o f
secondary contact, and k n o w l e d g e o f which valleys
w e r e glaciated (see 21) are needed before w e
can postulate a set of barriers to dispersal in the
above result
is particularly
important
for our speciation model, since the three m a m malogically better known islands off the coast
of C h i l e ( T i e r r a del Fuego, C h i l o e and M o c h a )
w e r e all connected to the mainland during the
last glaciation ( 2 1 ) , and n o w a d a y s they exhibit
past.
subspecies of mainland forms. T i e r r a del Fuego
Rodents present a clearly contrasting situation
in comparison to lizards. Rodents exhibit alti-
has
three
subspecies,
C h i l o e four, and
Mocha
three (see 1, 3 2 ) .
tudinal habitat partitioning (see 2 3 , 24, 25, 2 6 )
T h e evidence suggests then, there has
but, as w i l l be seen, also m o r e movement between
time for rodent subspeciation on mountains,
mountains.
well as intermingling of populations during the
dinal
F i g . 4 shows the patterns of altitu-
segregation at
about
18° latitude
south,
and M a l l e c o ( 3 9 ° latitude). It can be seen that
in
both
to
mountain
down.
situations
tops,
there
and
are
species
species
present
further
as
interglacial, and hence the lack of dif­
ferentiation.
restricted
living
been
This
difference in mobility between
lizards
and rodents is likely to be related to their mode
of
thermoregulation,
and energy
requirements.
186
F U E N T E S and J A K S I C
T A R A F » C A ( I 8 * - 2 0 " L A T SUR)
M A L L E C 0 ( 3 8 ' - 3 9 ° L A T SUR )
1000 2000 3000 4030 5000
T
~r
A cirwco
1500 2000
0. glifoidas
P oaqoodi
A. botiviaww
A sublimit
E typu»
L- viicqcio
Ch. tahomqe
A. «don
Ch. brevicouda
N. ebriwus
C. lepidus
Fig. 4. Altitudinal species replacement of rodents .'pedes.
Altitudinal species sequences in central Chile (Malleco) and northern Chile (Tarapacâ). Data for Malleco were obtained
from Greer (24). Data for Tarapacâ were taken from Miller and Rottmann (25), Spotorno (26), and records of Museo
Nacional de Historia Natural (Chile). See the text for discussion.
Rodents
are
endotherms
and
do not have
the
of geographical distribution
measured in degrees
capability to hybernate, at least in C h i l e ( 1 , 2 4 ) ,
(r = .82, P < . 0 0 0 1 ) . T h a t is, species
so
over long latitudinal stretches tend to have m o r e
they
their
are
more
altitudinal
likely
range
to
periodically
and
diet.
In
shift
contrast,
lizards are temporal opportunists, have relatively
l o w e r energetic requirements,
and restrict
activity to the season of m a x i m u m
not
shifting
in altitude.
their
productivity,
use one environmental
whereas
type
preferentially,
rodents w o u l d be more finely
grained
than
isolation
during
In
towards
speciation m o d e for rodents.
compensate
than
In
sum,
of their
high
for
do
not
mountain
comply
speciation
mobility during
the
valley
mode.
Number
is
true
w o u l d thus have
for
the
more
been
diverse
for
than
able to
centers
of
other
with
the
because
of subspecies
with
opposite
moun­
interglacials.
rodents is significantly correlated
the
origin of t h e ' C a l i f o r n i a fauna. R o d e n t s , on the
On
the other hand, rodents seem to have speciated
in
latter, and
hand,
speciation
rode
whereas
moun­
tain lizards.
requirements
In agreement w i t h
T h e former w o u l d speciate faster
the
tains, and hence less subspeciation
our
this is the fact that C h i l e has m o r e lizards than
being less specialized than lizards, w o u l d have
between
secondary
a valley
exhibited more between-year i n t e r m i n g l i n g
probabilities
is
valley
evidence points
rodents.
transition
This
for
glacial periods, and
conclusion,
California,
greater
ones.
conclusive)
a t w o - m o d e speciation for lizards, but
to the p r o p o r t i o n o f their occurrence.
and
not
contacts during interglacials.
tending to use more environmental types, related
Rodents,
m o r e restricted
(certainly
In the sense described
by L e v i n s ( 3 3 ) , lizards w o u l d be coarsely grained
and
subspecies
evidence
distributed
of
breadth
depending
conditions,
on
more
w o u l d have
stringent
speciated
at
a slower rate and w o u l d therefore not have been
able to compensate
for the diversity of centers
of origin in the Californian rodent fauna.
T h e by n o w well k n o w n radiation of altiplano
rodents ( 2 3 , 26, 3 4 ) w o u l d thus be linked to the
existence of numerous v a l l e y s and
surrounding
187
LIZARDS A N D RODENTS
mountains,
which w o u l d h a v e provided during
glacial times the reproductive isolation
needed
for speciation. T h e geographical and ecological
proximity
of
these
valleys during
the
inter-
south
and
southwest
deserts),
the
relatively
low. For
speciation
(Sonoran
Chilean
in
the
and
immigration
several
country
Mexican
has
faunistical
has
been
copious.
glacials, their isolation from each other by the
A m o n g these,
high mountains, and the vaster areas associated
an excelent e x a m p l e o f adaptive radiation. T h e i r
with
the
altiplano,
would have
conditions for greater
provided
the
speciation of rodents
in
lizards (Liolaemus)
been
groups,
seem to be
speciation has been explained as a result of the
greater
speciation
rate
as
compared
to
other
the northern region than in the more extended
groups, particularly rodents. T h e basic difference
southern A n d e s .
between these t w o types of vertebrates seems to
Other groups besides rodents and lizards are
more difficult to explain, and
the
required
information
w e do not have
to
examine
tlieir
reside
in
their
different
mobilities,
ultimately
related to their endothermy or ectothermy. A s
a consequence of this difference, lizards w o u l d
speciation patterns. H o w e v e r , it is possible that
speciate during and between glaciations, whereas
both birds and frogs also have valley speciation
rodents would do so only during glacial periods.
patterns.
Birds
have
high
mobilities and
are
not expected to show the large phenotypic dif-
It is possible the speciation of birds and frogs
could be explained by the same scheme.
ferences between mountains as lizards d o . C o d y
( 3 5 , 3 6 ) has shown Chilean birds tend to segregate
more
Speciation
by
regions than
in
these
by habitat
animals
would
operate not only between valleys, but
distant
and
postulated
isolated
ones.
types.
between
Vuilleumier
that the Nothofagus
RESUMEN
probably
bird fauna
(37)
as-
C h i l e es un país relativamente rico en lagartijas,
pero
pobre
en
roedores, en
comparación
lugares que exhiben características
con
similares de
sociated with forest speciated phyletically, which
clima y recursos. En este trabajo se intenta res-
strongly suggests that long distances are requir-
ponder por qué nuestro país ha sido análogo a
un archipiélago para las lagartijas (alta diferen-
ed for genetic isolation in these animals.
Birds
would
thus
be
expected
to
exhibit
ciación
específica
e intraespecífica), pero
relatively lower endemism than lizards or rodents.
bien como una
The
diversidad y diferenciación intraespecífica).
similarity
of C a l i f o r n i a
and
Chile
bird
faunas remains to be explained, but it is probably
a compound phenomenon
and
relatively more
with local speciation
immigration
from
Se muestra
isla
para los roedores
que las
lagartijas
más
(menor
exhiben
una
fuerte segregación altitudinal, que es particular-
distant
mente patente en la zona central de C h i l e (véase
Frogs might have speciated locally ( 3 8 ) and
nal de especies estaría relacionado con la selec-
localities.
F i g . 1). L a razón para este r e e m p l a z o altitudi-
could exhibit valley and perhaps some mountain
ción
speciation. F r o g s seem to c o m p l y with the l o w
parte de las lagartijas, que les proporcionarían
mobility requirement,
condiciones óptimas para su sobrevivencia y re-
but to our
is not k n o w n h o w much altitudinal
k n o w l e d g e it
stratification
they exhibit. It is suggestive though that total
species counts
for C a l i f o r n i a and
de ciertas
características
del habitat
producción. En el texto se analizan
por
numerosos
casos en que esta situación es evidente.
C h i l e frogs
Intimamente ligados a la selección del habitat
are about the same (see 39, 4 0 ) . M o r e research
se encontrarían
on this point is necessary.
miento de las
las morfologías y el comportalagartijas,
por lo que
fenotipos
óptimos en un cierto lugar no lo serían en o t r o ,
CONCLUSIONS
en donde podrían ser reemplazados por fenotipos
(especies)
It
has
been
assumed
—
and
there
are
diferentes.
L a estrecha relación
que
good
existiría entre fenotipo y ambiente seleccionado,
reasons for it — that C h i l e and C a l i f o r n i a offer
determinaría la partición altitudinal del gradien-
resources for comparable faunas ( 4 1 , 4 2 ) . H o w -
te
ever, whereas C a l i f o r n i a has received immigration
el flujo de individuos desde ciertas porciones del
of species from centers in the north ( G r e a t B a s i n ) ,
gradiente (en las cuales constituyen el fenotipo
de habitats
en las montañas,
restringiendo
188
F U E N T E S and JAKSIC
óptimo)
a estratos similares en
montañas
cer-
citan
posibles
ejemplos
de
especiación
"de
v a l l e " . L a suma de estos dos m o d o s de especia-
canas.
Este r a z o n a m i e n t o
basado
en
datos
ecológi-
ción,
actuando
durante sucesivos ciclos glacia-
cos, se ajusta al hecho que las lagartijas que están
les,
restringidas
a
lagartijas presentes en C h i l e .
divergencia
(mayor
q u e aquellas
las
montañas
muestran
cantidad
que viven
en
de
mayor
El m a y o r
la
gran
diversidad
dores chilenos, que son bastante menos diversos
aislamiento de las cumbres habría entonces per-
q u e las lagartijas. Se discute que, aun
mitido
los
la
mayor
diferenciación
intraespecífica
de
C o m o contraste se presenta el caso de los roe-
subespecies)
el valle.
explicaría entonces
roedores
exhiben
las
un
m a y o r m o v i l i d a d entre ellas. A m o d o de a p o y o
conjunto de islas en las cuales se puede producir
a esta proposición, se muestra que los roedores
divergencia
de
intraespecífica,
asemejarían
a
debido a la
restric-
ción del flujo de individuos entre aislados conti-
montaña
no forman
4),
también
en
que se observa en las montañas. En este sentido,
se
Fig.
cuando
altitudinal
montañas
regiones montañosas
(véase
partición
presentan
significativamente más
subespecies que los de valle. Esto, junto a otras
evidencias, sugiere que los roedores especiarían
nentales (véase F i g . 2 ) .
al modo " d e v a l l e " .
A n t e r i o r m e n t e se ha sugerido que las
de
Lwlaemus
se
desarrollarían
en
razas
montañas
En conclusión, los autores
proponen
que la
diferencia en diversidad de lagartijas y roedores
durante los períodos interglaciales, entrando en
podría deberse a sus distintos modos de especia-
contacto
ción: " d e m o n t a ñ a " y " d e v a l l e " para el primer
con
otras
razas
similares
cuando
el
descenso de la nieve (durante los períodos glaciales) las empujara
a bajar
al valle.
g r u p o , pero sólo " d e v a l l e " para el segundo
En esta
situación, o se refuerzan los mecanismos de aislamiento reproductivo, o las especies incipientes
se refunden
en una
sola. En C h i l e han
tres o cuatro glaciaciones, de manera que el m e canismo de especiación propuesto podría generar
gran
diversidad
en
de las montañas.
sucesivas
recolonizaciones
L o s factores esenciales en este
modelo d e especiación requieren d e la partición
altitudinal del habitat en las montañas, y la restricción
del m o v i m i e n t o de poblaciones que v i -
ven
distintas
en
montañas
durante
ACKNOWLEDGMENTS
habido
los
inter-
Johanna Filp and Patricio Sánchez made useful suggestions
on the manuscript. W e are also grateful to Angel Spotorno
for his advice on altitudinal distribution of Chilean rodents,
and to José Yáñez, curator at the Museo Nacional de Historia Natural (Chile), for allowing us to use localities information on mammals under his care. Research reported in
this contribution has been generously supported by L'niversidad Católica de Chile through grant DIUC 113/76 to
Eduardo R. Fuentes.
glaciales. A este modo de especiación, los autores
llaman "especiación en montañas".
Un
podría
de
segundo
modo
también
ocurrir
períodos glaciales
través
que
de
divergencia
durante
e
"bolsones"
quedarían
de
REFERENCES
la
filética
alternancia
interglaciales,
pero
a
o valles libres de hielo
aislados
unos de otros, p e r m i -
tiendo así la diferenciación de las poblaciones.
A
este tipo de especiación, los autores
"especiación
en
interglaciales,
aisladas
podrían
valles".
las
Durante
poblaciones
reunirse
llaman
los períodos
previamente
y divergir aún
más,
o refundirse en una sola especie. L o s dos tipos de
especiación
figura
propuestos
se
ejemplifican
en
la
3.
En base a las premisas de estos dos modos de
especiación, y a la ecología de las lagartijas, se
postula q u e éstas especiarían en C h i l e a la m a nera
"de
montaña",
aunque
también
se
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