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A test of Allen's rule in subterranean mammals: The genus Ctenomys (Caviomorpha, Ctenomyidae)

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We tested the applicability of Allen's rule in 47 species and 32 unnamed forms (populations that are probably good species or undefined taxa within a superspecies or species group) of the South American subterranean Hystricomorph rodents of the genus Ctenomys (tuco-tucos) (Rodentia: Ctenomyidae) by analyzing tail length in relation with head and body length, and body mass. Tail length allometry was analyzed by Reduced Major Axis regression while the possible correlation of relative tail length with temperature, precipitation and evapotranspiration variables was explored through Simultaneous Autoregression to account for spatial autocorrelations. Our results indicate that tuco-tucos do not follow Allen's rule but its converse, tail proportion relative to body mass increasing with latitude while body size decreases in the same direction (the trend is similar for tail length relative to head and body length but not statistically significant). Regarding climatic variables, the main predictors of relative tail length were temperature and evapotranspiration variables with trends confirming the positive (non-Allenian) correlation of relative tail length with latitude. We conclude that tuco-tucos, being almost fully subterranean, thermoregulate behaviorally by maintaining constant temperatures within their burrows independent of geographic location. The former confirms previous results that indicated that Ctenomys follows the converse to Bergmann's rule. Relative tail length variation would be a result of simple allometric growth.
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Mammalia 75 (2011): 311–320 © 2011 by Walter de Gruyter • Berlin • Boston. DOI 10.1515/MAMM.2011.044
A test of Allen s rule in subterranean mammals: the genus
Ctenomys (Caviomorpha, Ctenomyidae)
Claudio J. Bidau 1, a ,* , Dardo A. Mart í 2,4 and
Alonso I. Medina 3,4
1 Instituto Oswaldo Cruz , FIOCRUZ, Rio de Janeiro,
Laborat ó rio de Biologia e Parasitologia de Mam í feros
Silvestres Reservat ó rios, Av. Brasil 4365, Pav. Arthur
Neiva, sala 14, Manguinhos, Rio de Janeiro, RJ-21045-
900 , Brazil, e-mail: bidau47@yahoo.com
2 Laboratorio de Gen é tica Evolutiva , Facultad de Ciencias
Exactas, Qu í micas y Naturales, Universidad Nacional de
Misiones, 3300 Posadas , Argentina
3 Instituto de Biolog í a Marina y Pesquera “ Almirante
Storni ” , 8520 San Antonio Oeste, Rio Negro , Argentina
4 Consejo Nacional de Investigaciones Cient í fi cas y
T é cnicas , Buenos Aires , Argentina
*Corresponding author
Abstract
We tested the applicability of Allen s rule in 47 species and
32 unnamed forms (populations that are probably good spe-
cies or undefi ned taxa within a superspecies or species group)
of the South American subterranean Hystricomorph rodents
of the genus Ctenomys (tuco-tucos) (Rodentia: Ctenomyidae)
by analyzing tail length in relation with head and body
length, and body mass. Tail length allometry was analyzed
by Reduced Major Axis regression while the possible cor-
relation of relative tail length with temperature, precipita-
tion and evapotranspiration variables was explored through
Simultaneous Autoregression to account for spatial autocor-
relations. Our results indicate that tuco-tucos do not follow
Allen s rule but its converse, tail proportion relative to body
mass increasing with latitude while body size decreases in
the same direction (the trend is similar for tail length rela-
tive to head and body length but not statistically signifi cant).
Regarding climatic variables, the main predictors of relative
tail length were temperature and evapotranspiration variables
with trends confi rming the positive (non-Allenian) correla-
tion of relative tail length with latitude. We conclude that
tuco-tucos, being almost fully subterranean, thermoregulate
behaviorally by maintaining constant temperatures within
their burrows independent of geographic location. The for-
mer confi rms previous results that indicated that Ctenomys
follows the converse to Bergmann s rule. Relative tail length
variation would be a result of simple allometric growth.
a Present address: Universidad Nacional de R í o Negro, Sede Alto
Valle, Subsede Villa Regina, Tacuar í 669, 8336 Villa Regina, R í o
Negro, Argentina.
Keywords: allometry; body proportions; climate;
geographic cline; subterranean rodent.
Introduction
Allen ’ s rule (Allen 1877 , 1905 , Mayr 1999 ) is an empirical
geographical pattern according to which, protruding body
parts of endothermic animals, such as tails, limbs, ears, bills,
etc. tend to be relatively shorter in the cooler parts of the
range of a taxon than in its warmer parts. This ecogeographi-
cal rule has been considered traditionally as a complement
to Bergmann s rule (Bergmann 1847 ), but has received less
attention than the former. Nevertheless, a small number of
studies have demonstrated the existence of Allenian clines in
endotherms (birds: Snow 1954 , Meril ä 1977, Raveling and
Warner 1978 , McGillivray 1989 , Bried and Jouventin 1997 ,
Laiolo and Rolando 2001 , Cartar and Morrison 2005 , Yom -
Tov et al. 2006 ; mammals: Mitchell 1971 , Griffi ng 1974 ,
Ramey and Nash 1976 , Stevenson 1986 , Lindsay 1987 ,
Ellison et al. 1993 , Vrba 1996 , Wiggington and Dobson
1999 ) and also ectotherms (Ray 1960 , Salthe and Crump
1977 ). Both rules as originally interpreted, considered that the
increase in body size (Bergmann s rule) and the decrease in
the proportions of protruding body parts towards higher lati-
tudes and altitudes conformed to thermoregulation (i.e., heat
conservation or the avoiding of heat loss). For Bergmann s
rule, a number of alternative explanations other than thermo-
regulation have been proposed (Ashton et al. 2000 , Meiri and
Dayan 2003 , Medina et al. 2007 ) many of which could be
readily related also to Allen s rule. Both rules, which have
been alternatively considered in inter- or intraspecifi c appli-
cations (Blackburn et al. 1999 ), with exceptions in different
animal groups reported.
Classically, natural selection for thermoregulatory adapta-
tion has been invoked as the essential cause of Allen geograph-
ical patterns. Experimental evidence of the former hypothesis
has recently been obtained for humans (Tilkens et al. 2007 ).
The authors demonstrated that shorter limbs help reduce the
metabolic cost of maintaining body temperature, while lon-
ger limbs cause greater heat dissipation independent of the
effect of mass. Nevertheless, other factors could be involved.
Recently, Serrat et al. (2008) demonstrated that in laboratory
mice, appendage outgrowth is also markedly infl uenced by
environmental temperature. Vasomotor changes would con-
trol limb length indirectly through their effects on appendage
temperature. Thus, clinal distributions of limb length follow-
ing the Allen s rule trend, may represent a complex amalgam
of genetic assimilation after generations of selection com-
bined with direct temperature responses in growing cartilage.
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312 C.J. Bidau et al.: Allen s rule in Ctenomys
Tuco-tucos (genus Ctenomys de Blainville, 1826) constitute
a useful model to test predictions about relationships between
body size and environmental variables. The genus includes at
least 62 species, showing a wide variation in body size and
an enormous geographic distribution spanning across 45 °
of southern latitude from ca. -10 ° in the Peruvian highlands
to almost -55 ° in Tierra del Fuego). Populations are found
between 0 m and 5000 m above sea level from the Pacifi c to
the Atlantic coasts (Contreras and Bidau 1999 , Bidau 2006 ,
2011 ). These rodents are fully subterranean spending more
than 95 % of their lives underground (Nevo 1999 ) and are
morphologically homogeneous, all species showing the same
adaptations for living underground although varying greatly
in size (Medina et al. 2007 ). Furthermore, tuco-tucos inhabit
an enormous variety of habitats and climates and although
localized populations may be subjected to intense environ-
mental selection resulting from differences in soil texture and
depth, available food plants, intensity of predation, etc. their
burrows maintain fairly constant temperature and humidity
independently of geographic location (Reig et al. 1990 , Nevo
1999 , Busch et al. 2000 , Bidau 2006 , Medina et al. 2007 ).
This characteristic probably isolates them quite effectively
from the external environment much more than other subter-
ranean rodents (Medina et al. 2007 ). Finally, it has recently
been demonstrated that tuco-tucos follow the converse to
Bergmann s rule (Medina et al. 2007 ).
Similar to other subterranean mammalian taxa, the
Ctenomyidae exhibit a complex set of adaptations to the
underground milieu that include not only specialized morpho-
logical, physiological and biochemical characteristics (Reig
et al. 1990 , Nevo 1999 , Sedl á cek 2007a,b ) but also special-
ized behaviors regarding burrow construction and mainte-
nance of its internal microclimate (Burda 2007 ). The aim of
this study was to test for Allen s rule across these rodents
wide geographical distribution considering that Ctenomys
species thermoregulate essentially controlling temperature
within their burrows and not by changes in body size.
Materials and methods
Study species and morphometric traits
We based this study on 719 specimens of Ctenomys belonging
to 133 natural populations including 47 named species and 32
unnamed or undescribed forms (the term form is used here
to denote populations that are probably good species or unde-
ned taxa within a superspecies or species group; see Mirol
et al. 2010 ) from Argentina, Bolivia, Chile, Paraguay and
Uruguay sampled by the authors and collaborators (Medina
et al. 2007 ) or obtained from the literature (see Figure 1 and
Appendix 1 in Medina et al. 2007 ). External measurements
of all specimens included Total Body (TL) and Head plus
Body (HB), and Tail (T) lengths. In most individuals, body
mass (BM) was also measured or obtained from the literature.
The proportions of TL relative to HB and BM were calcu-
lated for all individuals and arcsin transformed. Males and
females were analyzed separately since all tuco-tuco species
exhibit male-biased sexual size dimorphism (SSD) which
decreases signifi cantly towards South following the converse
Bergmannian pattern of the genus but conforming Rensch s
rule (Bidau and Medina, submitted).
Independent variables
For each studied locality, latitude (LAT) and longitude (LON)
were recorded and transformed to decimal units. Altitude
was recorded as metres above sea level. However, one-
dimensional analyses have no explanatory power (Hawkins
and Diniz -Filho 2004 ), because size clines may obey to
multiple selection pressures that are not only dependent on
temperature constraints but also on other climatic and biotic
factors that could infl uence body size as explained above
(Jones et al. 2005 ). Therefore we considered other indepen-
dent variables as follows. Environmental variables for each
locality included: mean annual temperature (TMEA), mean
minimal and maximal temperatures (TMIN, TMAX), mean
temperature of the dry season (Tdry), total annual precipi-
tation (PANN), minimal and maximal precipitation (PMIN,
PMAX) and mean rainfall of the dry season (Pdry) (Cramer
and Leemans 2001 ). To estimate seasonality, we calculated
the annual variability of the climatic factors. Annual variabil-
ity of temperature was estimated through the coeffi cient of
variation (CV = SD*100/ x) (CVT; where x in this case, is the
mean annual temperature of each sampled locality, and SD
its standard deviation), and the difference between average
maximum and minimum annual temperatures (TM-m). We
assessed variability of precipitation by the CV of mean annual
precipitation (CVP, calculated from mean monthly precipita-
tion and its SD), and the difference between maximum and
minimum average monthly precipitation (PM-m).
Because body size clines may be correlated with pri-
mary productivity and ambient energy, two correlates of
actual (AET) and potential (PET) evapotranspiration were
considered (Rosenzweig 1968 , Olalla -T á rraga et al. 2006 ,
Rodr í guez et al. 2006 ). Therefore, we obtained for each geo-
graphic point, AET, an estimator of primary productivity
(calculated by the Thornthwaite formula), PET, a measure of
ambient energy (calculated by the Priestley-Taylor equation),
and Water Balance (WB). We used vectors, databases and
maps for AET, PET and WB from Ahn and Tateishi (1994a,b) .
Data analysis was performed with the Geomatica FreeView
V. 10.0 software by PCI Geomatics, Ontario, Canada ( www.
pcigeomatics.com ). All data are in mm/year. Mean annual
AET, PET and WB values were calculated for each sampled
locality. To analyze tail length allometry we used Reduced
Major Axis regression (RMA) to estimate slopes for the rela-
tionship between log
10 (TL) and log
10 (HB or BM) employing
the software of Bohonak and van der Linde (2004) . Clarke s t
statistic with adjusted degrees of freedom was used for testing
the null hypothesis that b
RMA = 1.0 for the linear relationship
TL/HB, and b
RMA = 0.33 for TL/BM (Clarke 1980 ).
Because most environmental variables show a high degree
of colinearity, dimensionality of the predictors was reduced
by means of Principal Component Analyses (PCA). We estab-
lished the number of principal components retained and later
used as predictors in correlation/regression analyses, by the
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C.J. Bidau et al.: Allen s rule in Ctenomys 313
Figure 1 Geographic distribution of Ctenomys populations studied in this paper. See Medina et al. (2007) for references to all localities.
Table 1 RMA regressions of tail length on head and body length, and body mass for population means of males and females of 112 and 114
Ctenomys populations.
Trait 1 Trait 2 Correlation coeffi cient RMA slope RMA intercept
r t df p-Value β (SE) T df1 p-Value 95 % CI a (SE) 95 % CI
Male TL HBL 0.610 8.07 110 < 0.001 0.996 0.09 95.99 ns 0.847, 1.145 -0.374 -0.710
(0.075) (0.169) -0.038
BM 0.948 25.67 74 < 0.001 0.325 0.30 53.74 ns 0.301, 0.349 1.668 1.613
(0.012) (0.028) 1.723
Female TL HBL 0.634 8.50 112 < 0.001 1.220 3.02 96.09 0.0032 1.043, 1.397 -0.865 -0.846
(0.089) (0.199) 0.245
B M 0 . 6 8 6 8 . 2 8 7 7 < 0.001 0.303 0.42 65.13 ns 0.253, 0.353 1.202 1.091
(0.025) (0.056) 1.313
a, RMA intercept; β , RMA slope; BM, body mass (all variables were log-transformed); CI, confi dence interval; df, degrees of freedom; df
1 ,
adjusted degrees of freedom; HB, head and body length; ns, non-signifi cant; p, probability; r, Pearson s correlation coeffi cient; SE, Standard
error; t, Student s t-statistic; T, Clarke s T-statistic; TL, tail length.
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314 C.J. Bidau et al.: Allen s rule in Ctenomys
140
120
100
80
60
arcsin tail length/body massarcsin tail length/body mass
arcsin TL/BM=-0.282+0.028*LAT
R2=0.394; p<0.001
arcsin TL/BF=0.146*(1.036LAT)
R2=0.224; p<0.001
40
20
0
120
100
80
60
40
20
0
10 20 30
Latitude
40 50
10 20 30
Latitude
40 50
A
B
Figure 2 Regressions between the proportion of tail length to
body mass (expressed as arcsin *100) and latitude in males (A) and
females (B) of Ctenomys . For males, the best regression model was
linear while for females, exponential.
of Ctenomys although progress is being made in this sense by
CJB and colleagues.
Results
The static allometric scaling of TL in relation with HBL
and BM of both sexes was investigated by means of RMA
regresssion. Results of the analyses are shown in Table 1
and
seem to indicate an isometric scaling of tail length with body
size with the exception of the relationship between female
TL and HBL where β RMA > 1.0 suggesting positive allometry.
However, since ontogenetic allometry was not studied due to
the lack of enough juvenile individuals (which are usually not
captured) it is not possible to know if tail growth is isometric
or allometric in either direction.
Raw tail length has a negative correlation with latitude ( r =
-0.374, df = 131, p < 0.001) as expected because of the converse
Bergmann s rule followed by this rodents. We regressed the
arcsin -transformed proportion of TL respect to body mass
against latitude of the sampled localities. In both sexes, the
proportion showed a highly signifi cant positive correlation
with latitude; that is tuco-tucos show relatively longer tails as
latitude increases (Figure 2 ). No signifi cant correlations were
observed between TL/HBL and latitude (females, p = 0.822,
df = 112; males, p = 0.629, df = 110). Also, no signifi cant altitudi-
nal clines were obtained for either of the analyzed variables.
In order to test the possible relationship of relative tail length
to climatic factors we considered 14 temperature, precipita-
tion and evapotranspiration variables as represented by the
two fi rst principal components that include almost 75 % of the
Table 2 Principal components analyses of climatic data for species
and populations of Ctenomys .
Climatic variables Principal components (broken stick)
Male data Female data
PC1 PC2 PC1 PC2
AET 0.907* -0.018 0.918* -0.003
PET 0.696* -0.318 0.675* -0.347
TMEA 0.879* -0.076 0.899* -0.102
Tdry 0.812* -0.102 0.850* -0.093
TMIN 0.929* 0.116 0.937* -0.114
TMAX 0.761* 0.092 0.781 -0.058
CVT -0.810* 0.255 -0.827* 0.226
TM-m -0.362 -0.388 -0.430 0.341
PANN 0.877* 0.270 0.872* 0.303
Pdry 0.737* -0.605* 0.739* 0.605*
PMIN 0.571* -0.735* 0.553* 0.747*
PMAX 0.778* -0.276 0.777* -0.271
CVP -0.257 0.916* -0.259 0.923*
PM-m 0.508* 0.681* 0.508* -0.690*
% Total variance
explained
53.9 0 19.50 55.30 19.60
Factors were extracted and rotated with the VARIMAX procedure
with Kaiser Normalization for 15 environmental variables (see
Materials and methods for nomenclature of variables). Values cor-
respond to correlation coeffi cients between variables and factors.
Relatively high loadings ( | r | > 0.5) are marked with an asterisk.
broken-stick criterion (Legendre and Legendre 1998 ). To
improve interpretation of the principal components, they were
rotated to simple structure using VARIMAX criterion (Kline
1994 ). After identifi cation of the best PCA predictors, the best
model (combination of variables with high loadings in that
PCA) was identifi ed using Akaike s Information Criterion
(Burnham and Anderson 2002 ).
Most biogeographic and macroecological data are spatially
autocorrelated (Legendre 1993 , Diniz -Filho et al. 2003 , Rangel
et al. 2006 ) thus, special statistical procedures are required
for hypothesis testing, such as Simultaneous Autoregression
(SAR) with preset coordinate variables (LON, LAT). In this
paper, we performed all spatial analyses in SAM v.3 (Spatial
Analysis in Macroecology) (Rangel et al. 2006 ). Finally, inde-
pendent contrasts (although desirable) were not used because
until now, there is not a published comprehensive phylogeny
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C.J. Bidau et al.: Allen s rule in Ctenomys 315
Table 3 Standardized partial regression coeffi cients ( b ) and their respective t -values for the two principal components (PC1, PC2) derived
from 13 environmental variables predicting patterns of tail length proportion distribution in males (M) and females (F) of Ctenomys , from a
simultaneous autoregressive (SAR) model.
Sex Trait Predictor b t R2
full R2
pred
ρ AIC
M TL/HB PC1 -0.086 -0.82 0.035 0.022 0.28 -568.1
PC2 -0.049 -0.46
TL/BM PC1 -0.311 -2.49* 0.182 0.166 0.47 -215.3
PC2 -0.059 0.48
F TL/HB PC1 -0.212 -2.00* 0.152 0.133 0.51 -626.4
PC2 -0.127 -1.16
TL/BM PC1 -0.332 -2.74* 0.330 0.293 0.64 -228.5
PC2 0.226 1.93
AIC, is the value of Akaike s Information Criterion; ρ, is the autoregressive coeffi cient of the SAR model; R
2 full , is the total coeffi cient of
determination of the model (predictors + spatially structured error term); R
2 pred , refers to the effects of the predictors independently of spatial
structure. *Signifi cant at the 0.05% level.
Table 4 Standardized partial regression coeffi cients ( b ) and their respective t-values for the best univariate models derived from 13
environmental variables predicting patterns of tail length/body mass distribution in males (M) and females (F) of Ctenomys , from a simultaneous
autoregressive (SAR) model.
Sex Trait Predictor b t R2
full R2
pred ρ AIC
M PET -0.277 -2.399* 0.148 0.134 0.467 -429.216
TL/BM Tdry -0.280 -2.452* 0.166 0.144 0.467 -430.116
TM-m 0.457 4.019** 0.229 0.216 0.467 -440.137
F AE T -0.314 -2.581* 0.2 83 0.187 0.6 43 - 4 4 6.918
TL/BM Tdry -0.311 -2.799* 0.168 0.141 0.643 -448.900
TM-m 0.443 4.012** 0.292 0.248 0.643 -448.179
AIC, is the value of Akaike s Information Criterion; ρ, is the autoregressive coeffi cient of the SAR model; R 2
full
, is the total coeffi cient of deter-
mination of the model (predictors + spatially structured error term); R 2
pred
, refers to the effects of the predictors independently of spatial structure.
*Signifi cant at the 0.05% level; **signifi cant at the 0.001 level.
total variance explained in both samples as shown in Table 2
in which correlations between loadings and the variables
are shown. SARs were performed separately for males and
females and both tail length proportions. Except for TL/HB of
males, the other proportions were signifi cantly correlated with
PC1 (Table 3
). All regression slopes were negative (Table 3 ).
However, PC1 includes most of the climatic variables consid-
ered (Table 2 ) many of which are colinear and signifi cantly
correlated (Appendices 1 and 2) thus, the analyses have not
great explanatory power. To explore more thoroughly the
relationship between tail proportions and environmental fac-
tors, we performed SARs between tail proportions and differ-
ent combinations climatic variables having the highest and
lowest Eigenvector loadings in random combinations of 1, 2,
3 and 4 variables using the Akaike Information Criterion to
select the best models that predict variation in tail proportion
with respect to body mass in both sexes. The best models are
shown in Table 4
. In the case of males, PET, Tdry and TM-m
were the best univariate models with coeffi cients for the lat-
ter two being the most statistically signifi cant (Table 4 ). No
multivariate model showed higher AIC values. Similarly in
females, TL/BM was best explained by three univariate mod-
els (Table 4 ) also including Tdry and TM-m, although AET
and not PET was signifi cantly correlated with tail proportion.
The four climatic variables are highly signifi cantly correlated
with latitude (see Appendices 1 and 2).
Discussion
Variation in body size and other morphological traits of ani-
mals along geographical gradients is one of the most interest-
ing and least understood patterns in nature (Lomolino et al.
2006a ). A number of these trends have been identifi ed and
are usually referred to as ecogeographical rules (Ashton
2001 , Lomolino et al. 2006b , Millien et al. 2006 , Gaston et al.
2008 ). Of these, Bergmann ’ s and Allen ’ s rules refer specifi -
cally to body size and body proportions of protruding append-
ages, respectively (Bergmann 1847 , Allen 1877 , 1905). We
chose to analyze variation in relative tail length for reasons
discussed below.
Although Bergmann s rule has received much attention
from researchers during more than 160 years and a wealth
of information on Bergmannian patterns in endotherms and
ectotherms is available (Blackburn et al. 1999 , Ashton et al.
2000 , Freckleton et al. 2003 , Meiri and Dayan 2003 , Medina
et al. 2007 ), Allen s rule has been rather neglected despite the
fact that the proposed mechanism for explaining the trend to
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316 C.J. Bidau et al.: Allen s rule in Ctenomys
shorter appendages toward higher latitudes is essentially the
same for Bergmann s rule, i.e., conservation or dissipation of
heat (Allen 1877, Lomolino et al. 2006a ).
Another problem regarding Allen s rule as well as
Bergmann s and other ecogeographical rules is whether they
apply to inter- or intraspecifi c variation (Blackburn et al. 1999 )
and if this is the case, whether mechanisms responsible for the
trends are similar or different. In this sense, Watt et al. (2010)
have discussed that Bergmann s rule is probably a concept
cluster (Peet 1974 , see also Lawton 1999 ) since it has been
applied at different taxonomic levels and many underlying
mechanisms have been proposed. This may well be applied
to Allen s rule too. Most of the published accounts of Allen
trends have been intraspecifi c, tracing relative proportions of
protruding body parts across the latitudinal or altitudinal dis-
tribution of a species, with few exceptions (e.g., Cartar and
Morrison 2005 ). By far, the most thorough interspecifi c study
of Allen s rule is that of Nudds and Oswald (2007) in gulls
and terns. The authors conclude that the mechanism explain-
ing Allen s rule, is the reduction of thermoregulatory cost dur-
ing the coldest part of the breeding season of these species. It
is interesting to note that variation occurred in the exposed
leg bone elements and not in the feathered elements, reinforc-
ing the thermoregulatory interpretation (Nudds and Oswald
2007 ).
In rodents, the more important structure involved in ther-
moregulatory function is the tail, which serves as a heat-
loss organ (Thorington 1966 , Hickman 1979 , Young and
Dawson 1981 , Dawson and Keber 2007 ). For example, the
Sciurognath Geomys pocket gophers facilitate heat loss dur-
ing heat stress by increasing blood circulation in their naked
tails through which they can lose up to 30 % of their heat pro-
duction (McNab 1966 ). Geographic variation in heat loading
has produced reduction of body size or increase in tail length
in these subterranean rodents (McNab 1966 ). Tuco-tucos
(Hystricognathi) share with pocket gophers many adapta-
tions to the subterranean lifestyle (Nevo 1999 ) although less
is known about thermoregulatory mechanisms in this genus.
Tuco-tucos tail which has sensory functions, is almost hair-
less and, if it is used in thermoregulation, is a good candidate
to show variation in length according to Allen s rule.
The case of tuco-tucos reported here is signifi cant in
more than one aspect. First, the observed trend for relative
tail length is inverted with respect to Allen s rule expecta-
tions. Our fi rst hypothesis was that, being fully subterranean
thus being much less affected by surface climatic conditions
than cursorial species, Allen s rule should not operate in this
genus, and that was the case. However, instead of lacking a
geographical trend, tuco-tucos tend to have relatively longer
tails at higher latitudes. Tuco-tucos as other subterranean
mammals, maintain fairly constant microclimatic conditions
of their burrows, within which they spent > 95 % of the time
(Reig et al. 1990 ) through specialized behaviors (Nevo 1999 ,
Burda 2007 ). The degree of exposure to external environmen-
tal conditions is minimal.
Although only three species have been adequately stud-
ied in this respect their comparison is revealing. Ctenomys
torquatus and C. talarum were distributed between 25 ° – 35 °
and 35 ° – 40 ° , respectively (0 200 m), and inhabited widely
different environments. They maintain constant burrow
temperatures of 20° – 22 ° C throughout the year (Medina
et al. 2007 ). More notorious is the case of C. fulvus , which
inhabits the Chilean Puna (20 ° – 26 ° S) in isolated oases up to
4000 m elevation; this species maintains burrow temperatures
between 19 ° C and 25 ° C, when the above-ground temperature
varies from less than 4 ° C to more than 45 ° C with a mean ther-
mal amplitude of ca. 38 ° C during the day and independently
of season (Cort é s et al. 2000 ). Tuco-tuco burrows maintain
more constant temperatures than those of other studied sub-
terranean species, such as African bathyergids (Reichman and
Smith 1990 , Roper et al. 2001 , Sumbera et al. 2004 , Burda
2007 ). It is thus possible that all species maintain similar tem-
perature conditions within their burrows independently of lati-
tude and altitude (Reig et al. 1990 ). It has also been reported
for Ctenomys talarum that seasonal changes in fur length may
help thermal stability (Cutrera and Antinuchi 2004 ).
This almost independence of external conditions suggests
that classical ecogeographic rules based on thermoregulatory
mechanisms, such as Allen s, do not need to operate in tuco-
tucos but in fact do occur. Furthermore, body size of Ctenomys
species decreases signifi cantly toward higher latitudes and
lower temperatures, opposing Bergmann s rule (Medina
et al. 2007 ). Medina et al. (2007) explained this inverse pattern
by temperature-independent mechanisms, such as geographic
variation in resources, seasonality and intensity of predation.
Because the relative tail length trend observed in tuco-tucos
also inverts Allen s rule, it is tempting to attribute the pattern
as a consequence of the converse Bergmannian pattern. As
shown in results, predictors of relative tail length were Tdry,
AET, PET (negative) and TM-m (positive). Tail is relatively
longer at lower temperatures, lower primary productivity and
less ambient energy (two correlates of AET and PET), and high
thermal amplitude. This combination of factors indicates pro-
gressively higher seasonality, one of the factors suggested to
produce the inverse Bergmann s cline (Medina et al. 2007 ). It is
thus proposed that the inversion of Allen s rule in Ctenomys is
a consequence of negative allometric growth of the tail, and
is probably independent of external ambient conditions. As
shown in the results, raw tail length is not correlated with lati-
tude while body length and body mass are strongly negatively
correlated with latitude thus, while body size decreases pro-
gressively towards south, tail length does not, indirectly sug-
gesting that negative ontogenetic allometry (species attaining
larger sizes having a slower tail growth) could be the subjacent
cause of the converse Allenian pattern which in turn, would
result from the inversion of Bergmann s rule.
Acknowledgements
We are grateful to all students and colleagues that helped during
eld work. Financial support from CNPq, FAPERJ, FIOCRUZ and
FONCyT through grants to CJB is especially acknowledged. Rocio
Hassan read a previous draft of this manuscript and her important
contributions were incorporated to the fi nal version. The comments
of the Associate Editor and two anonymous reviewers improved the
manuscript substantially.
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C.J. Bidau et al.: Allen s rule in Ctenomys 317
Appendix
Appendix 1 Correlation matrix of all geographic, climatic and morphometric variables considered for males.
Variables Morphometric variables Geographic variables Climatic variables
logHB logWt Arcsin
T/HB
Arcsin
T/Wt
LAT LON ALT TMEA TMAX TMIN CVT TM-m Tdry PANN PMAX PMIN CVP PM-m Pdry AET PET
LogHb 0.931 -0.458 ns ns 0.376 0.334 0.408 -0.449 -0.384 0.322 0.408 ns 0.233 0.387 ns 0.316 0.370 0.356
LogWt 0.943 -0.448 -0.246 ns 0.444 0.399 0.450 -0.502 -0.405 0.420 0.377 ns 0.252 0.371 ns 0.311 0.385 0.397
ArcsinT/HB 0.335nsnsnsnsns nsnsns nsnsnsnsnsnsnsnsns
ArcsinT/Wt 0.442 0.466 ns ns -0.438 -0.385 -0.449 0.510 0.429 -0.411 -0.363 -0.373 ns ns -0.329 -0.231 -0.378 -0.394
LAT -0.430 -0.433 ns 0.377 -0.582 -0.475 -0.635 0.781 0.651 -0.474 -0.346 -0.635 ns -0.506 -0.733 ns -0.574 -0.679
LON ns -0.228 ns 0.241 -0.541 -0.480 -0.590 0.449 ns -0.452 -0.695 -0.301 -0.841 0.704 ns -0.826 -0.549 -0.404
ALT ns ns ns ns -0.215 -0.223 -0.250 ns ns -0.243 -0.398 ns -0.784 0.798 0.408 -0.640 -0.233 ns
TMEA 0.354 0.399 ns -0.333 -0.564 -0.681 -0.419 0.958 0.974 -0.876 -0.378 0.877 0.716 0.650 0.352 ns 0.476 0.521 0.825 0.516
TMAX 0.245 0.274 ns -0.212 -0.330 -0.697 -0.606 0.944 0.908 -0.767 0.221 0.821 0.649 0.540 0.307 ns 0.289 0.482 0.758 0.358
TMIN 0.394 0.430 ns -0.377 -0.665 -0.686 -0.303 0.973 0.856 -0.941 -0.495 0.886 0.756 0.693 0.396 ns 0.495 0.554 0.851 0.592
CVT -0.350 -0.360 ns 0.321 0.778 0.645 ns -0.851 -0.692 -0.908 0.667 -0.828 -0.693 -0.697 -0.294 ns -0.540 -0.458 -0.820 -0.680
TM-m -0.297 -0.340 ns 0.357 0.654 ns -0.535 ns 0.212 -0.324 0.449 -0.442 0.492 -0.554 -0.223 ns -0.389 -0.300 -0.501 -0.562
Tdry 0.397 0.450 ns -0.398 -0.454 -0.500 -0.404 0.849 0.726 0.874 -0.688 -0.322 0.637 0.600 0.304 ns 0.492 0.415 0.726 0.451
PANN 0.320 0.326 ns -0.345 -0.380 -0.686 -0.354 0.604 0.531 0.670 -0.504 0.294 0.571 0.783 0.760 -0.398 0.386 0.874 0.860 0 . 4 8 9
PMAX ns ns ns -0.355 -0.608 -0.398 ns 0.515 0.382 0.587 -0.470 -0.410 0.524 0.797 0.303 ns 0.827 0.476 0.814 0.608
PMIN 0.188 0.251 ns -0.259 ns -0.764 -0.480 0.309 0.315 0.359 -0.235 ns 0.288 0.786 0.351 -0.851 ns 0.944 0.481 0.209
CVP 0.278 0.307 ns ns -0.477 0.624 0.710 ns -0.265 ns ns -0.214 ns -0.437 ns -0.782 0.562 -0.726 ns ns
PM-m ns ns ns -0.254 -0.685 ns 0.211 0.374 0.231 0.423 -0.367 -0.376 0.396 0.411 0.861 ns 0.488 ns 0.580 0.515
Pdry 0.276 0.257 ns -0.293 ns -0.795 -0.476 0.482 0.460 0.536 -0.354 ns 0.443 0.904 0.514 0.955 -0.710 ns 0.659 0.310
AET 0.304 0.339 ns -0.357 -0.590 -0.600 -0.222 0.709 0.608 0.764 -0.653 -0.332 0.617 0.867 0.796 0.523 -0.214 0.559 0.698 0.601
PET 0.370 0.395 ns -0.380 -0.662 -0.455 ns 0.533 0.381 0.601 -0.668 -0.439 0.460 0.514 0.606 0.267 ns 0.493 0.364 0.660
Spearman correlation coeffi cients are represented above the diagonal; Pearson s r s, below. All shown coeffi cients are statistically signifi cant. ns, non-statistically signifi cant correlation.
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318 C.J. Bidau et al.: Allen s rule in Ctenomys
Appendix 2 Correlation matrix of all geographic, climatic and morphometric variables considered for females.
Variables Morphometric variables Geographic variables Climatic variables
LogHB LogWt ArcsinT/HB ArcsinT/Wt LAT LON ALT TMEA TMAX TMIN CVT TM-m Tdry PANN PMAX PMIN CVP PM-m Pdry AET PET
LogHb 0.912 -0.554 ns ns 0.426 0.383 0.451 -0.462 -0.334 0.376 0.390 ns 0.372 ns ns ns 0.370 0.356
LogWt 0.899 -0.496 ns ns ns ns ns -0.370 -0.415 ns ns 0.354 ns ns 0.389 ns ns 0.474
ArcsinT/HB 0.562 0.008 0.294 0.233 ns ns ns ns ns ns ns ns -0.255 0.224 ns -0.196 ns ns
ArcsinT/Wt 0.554 0.516 ns -0.051 -0.361 -0.241 -0.389 0.471 0.450 -0.322 -0.364 -0.439 ns ns -0.565 -0.183 -0.365 -0.467
LAT -0.541 -0.493 ns 0.629 -0.413 -0.236 -0.488 0.604 0.706 -0.382 ns -0.494 0.283 -0.490 -0.680 ns 0.303 -0.708
LON ns ns 0.258 0.230 -0.732 -0.757 -0.735 0.659 0.285 -0.655 -0.808 -0.431 -0.781 0.650 ns -0.816 -0.802 -0.346
ALT ns ns ns ns -0.496 -0.627 -0.491 0.390 ns -0.490 -0.637 -0.269 -0.794 0.801 ns -0.760 -0.637 -0.089
TMEA 0.379 ns ns -0.322 -0.544 -0.743 -0.451 0.947 0.977 -0.917 -0.426 0.837 0.754 0.697 0.341 ns 0.514 0.553 0.870 0.542
TMAX 0.342 ns ns ns -0.223 -0.721 -0.583 0.940 0.909 -0.808 -0.262 0.821 0.707 0.595 0.325 ns 0.481 0.537 0.826 0.362
TMIN 0.401 ns ns -0.399 -0.625 -0.750 -0.400 0.979 0.872 -0.987 -0.517 0.899 0.779 0.726 0.390 ns 0.512 0.572 0.881 0.605
CVT -0.388 0.320 ns 0.441 0.751 0.677 ns -0.896 -0.757 -0.922 0.659 -0.877 -0.705 -0.718 -0.281 ns -0.531 -0.466 -0.836 -0.666
TM-m -0.278 0.370 0.245 0.501 0.697 ns -0.223 -0.235 ns -0.404 0.460 -0.480 -0.479 -0.544 -0.229 ns -0.356 -0.306 -0.470 -0.606
Tdry 0.336 ns ns -0.277 -0.425 -0.627 -0.458 0.857 0.732 0.888 -0.736 -0.439 0.690 0.666 0.310 ns 0.488 0.461 0.791 0.482
PANN 0.348 ns ns -0.427 -0.297 -0.793 -0.487 0.632 0.574 0.680 -0.510 -0.311 0.628 0.771 0.752 -0.394 0.376 0.865 0.846 0.498
PMAX ns 0.361 ns -0.561 -0.569 -0.491 ns 0.554 0.430 0.599 -0.471 -0.416 0.579 0.780 0.273 ns 0.827 0.456 0.802 0.655
PMIN 0.332 ns -0.272 -0.223 ns -0.707 -0.486 0.294 0.297 0.348 -0.246 ns 0.304 0.790 0.336 -0.852 -0.235 0.929 0.451 0.195
CVP ns ns 0.200 ns -0.420 0.622 0.752 ns -0.283 ns ns -0.209 -0.206 -0.460 ns -0.786 0.577 -0.721 ns ns
PM-m ns 0.347 ns -0.504 -0.675 ns ns 0.416 0.285 0.434 -0.356 -0.349 0.437 0.380 0.858 -0.196 0.493 ns 0.569 0.527
Pdry ns ns -0.208 -0.288 ns -0.795 -0.533 0.502 0.478 0.556 -0.409 -0.239 0.503 0.903 0.503 0.941 -0.707 ns 0.641 0.313
AET 0.331 ns ns -0.455 0.470 -0.770 -0.439 0.771 0.695 0.800 -0.661 -0.328 0.703 0.851 0.781 0.501 -0.220 0.540 0.699 0.615
PET 0.319 0.410 -0.196 -0.556 -0.752 -0.382 ns 0.530 0.365 0.591 -0.664 -0.520 0.436 0.488 0.607 0.247 0.184 0.498 0.350 0.648 –
Spearman correlation coeffi cients are represented above the diagonal; Pearson s r s, below. All shown coeffi cients are statistically signifi cant. ns, non-statistically signifi cant correlation.
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... To date, only a few macroecological investigations of species' range and/or body size distribution patterns have been focused on tuco-tucos. Among them, found that tuco-tuco body size follows the converse of Bergmann's rule, Bidau et al. (2011) found increases in relative tail length with increases in latitude (the converse of Allen's Rule), and explored the overlap of species range maps with protected areas. ...
Book
This book examines the biology of tuco-tucos (Ctenomys) from an evolutionary perspective. Historically, these subterranean rodents have long attracted the attention of scientists due to its remarkable chromosomes variability and rapid diversification. A wealth of knowledge on physiology, ecology, genetics, morphology, paleontology, and taxonomy has been documented in the last 70 years through numerous single publications. In this volume, expert investigators review and frame these essays with the breadth of current understanding. The collection of chapters are presented into the major topics: i) Evolution of Ctenomys, ii) Geographic Patterns, iii) Organismal Biology, and iv) Environmental Relationships. Given its scope, the book will be of interest to both students and researchers and may stimulate further research with this exciting model on a wide range of evolutionary topics.
... To date, only a few macroecological investigations of species' range and/or body size distribution patterns have been focused on tuco-tucos. Among them, found that tuco-tuco body size follows the converse of Bergmann's rule, Bidau et al. (2011) found increases in relative tail length with increases in latitude (the converse of Allen's Rule), and explored the overlap of species range maps with protected areas. ...
Chapter
Subterranean rodents are widely recognized as ecological engineers. The habitat requirements and ecological characteristics of animals that live underground influence numerous aspects of their biology, including where they live and how they behave. Regional distributions of Ctenomys species vary substantially with soil and vegetation characteristics and resource availability, and it is apparent that tuco-tucos can also increase local environmental heterogeneity at the landscape level. However, obtaining sufficient ecological information about tuco-tucos is challenging due to the majority of life activities taking place underground. In this chapter, we discuss spatial habitat use patterns, general ecological characteristics, species interactions, and social structure in tuco-tucos, as well as their impacts on the local environment and implications for conservation. Despite many previous studies of tuco-tucos having estimated ecological data using various approaches, it remains difficult to corroborate those data with ecological parameters at broad scales.
... To date, only a few macroecological investigations of species' range and/or body size distribution patterns have been focused on tuco-tucos. Among them, found that tuco-tuco body size follows the converse of Bergmann's rule, Bidau et al. (2011) found increases in relative tail length with increases in latitude (the converse of Allen's Rule), and explored the overlap of species range maps with protected areas. ...
Chapter
The genus Ctenomys is comprised of more than 70 valid living species. It is the largest collection of fossorial mammals that occupy underground habitats, mainly in the grasslands of South America. We investigated different aspects of morphological evolution in the genus Ctenomys, with special attention to the skull. We analyzed 1359 craniums and 830 mandibles of 49 species of Ctenomys. We used geometric morphometric approaches to quantify this morphological diversity across its range. We found geographical structuring in skull shape among the eight clades of Ctenomys structured along east-west and north-south morphological gradients. We observed that many species from the extreme north of the distribution had a robust skull shape, whereas the southern ones had a gracile skull shape. Such structural differences may be following an environmental gradient. The mandible is less variable in shape than the cranium. We found high morphological variation within each of the eight clades and a geographical structuring. The subterranean niche is not homogeneous across space, and morphological adaptation of subterranean species occurs following this spatial gradient.
... Allen's rule (1877) is an extension of Bergmann's rule, predicting that appendage size in endotherms, including limbs, tails and ears, become larger in warm climates for similar thermoregulatory reasons. Studies have found that this pattern is valid for some mammals (Yom-Tov and Yom-Tov 2005;Betti et al. 2015) and birds (Laiolo and Rolando 2001;VanderWerf 2012), but not in some cases (Wiedenfeld 1991;Bidau et al. 2011;Du et al. 2017). One of the most representative examples of Allen's rule is bill size, which has been demonstrated to serve as an efficient radiator in birds (Scott et al. 2008;Tattersall et al. 2009;Campbell-Tennant et al. 2015). ...
Article
Full-text available
Background Animals that live at higher latitudes/elevations would have a larger body size (Bergmann’s rule) and a smaller appendage size (Allen’s rule) for thermoregulatory reasons. According to the heat conservation hypothesis, large body size and small appendage size help animals retain heat in the cold, while small body size and large appendage size help them dissipate heat in the warm. For animals living in seasonal climates, the need for conserving heat in the winter may tradeoff with the need for dissipating heat in the summer. In this study, we tested Bergmann’s rule and Allen’s rule in two widely-distributed passerine birds, the Oriental Magpie ( Pica serica ) and the Oriental Tit ( Parus minor ), across geographic and climatic gradients in China. Methods We measured body size (body mass and wing length) and appendage size (bill length and tarsus length) of 165 Oriental Magpie and 410 Oriental Tit individuals collected from Chinese mainland. We used linear mixed-effect models to assess variation patterns of body size and appendage size along geographic and climatic gradients. Results Oriental Magpies have a larger appendage size and Oriental Tits have a smaller body size in warmer environments. Appendage size in Oriental Magpies and body size in Oriental Tits of both sexes were more closely related to the climates in winter than in summer. Minimum temperature of coldest month is the most important factor related to bill length and tarsus length of male Oriental Magpies, and wing length of male and female Oriental Tits. Bill length and tarsus length in female Oriental Magpies were related to the annual mean temperature and mean temperature of coldest quarter, respectively. Conclusions In this study, Oriental Magpies and Oriental Tits followed Allen’s rule and Bergmann’ rule respectively. Temperatures in the winter, rather than temperatures in the summer, drove morphological measurements in Oriental Magpies and Oriental Tits in Chinese mainland, demonstrating that the morphological measurements reflect selection for heat conservation rather than for heat dissipation.
Article
The genus Desmodillus is monospecific, consisting of only the Cape short-eared gerbil ( Desmodillus auricularis ). Despite being widely distributed across southern Africa, previous studies did not find evidence of intraspecific phenotypic geographic differentiation. The objectives of this study is to use geometric morphometrics to investigate if and how the skull of D. auricularis varies spatially. It examines the covariation of skull morphology with broad spatial (latitude and longitude) and climatic variables, based on a sample of 580 specimens from southern Africa (Botswana, Namibia, and South Africa). The results did not support the differentiation of D. auricularis populations into distinct geographically isolated phenotypic groups. However, there is strong evidence for clinal variation in skull morphology; the most prominent pattern being a decrease in size from the west (closest to the South Atlantic coast) to the east (towards the continent’s interior). Shape variation was not localized in any skull region and seem to be driven mostly by size (allometry), although it also covaried significantly with latitude and longitude. Statistically significant skull shape sexual dimorphism was also detected, with males having larger crania than females. Spatial clinal variation in skull morphology was mostly associated with differences in the aridity of the habitats relative to their distance from the coast as evidenced by precipitation-related bioclimatic variables—annual precipitation (BIO12), precipitation of driest month (BIO14), and precipitation of driest quarter (BIO17)—covarying the most with skull morphology. This could be driven by either the climate influencing local resources available to populations or by the climate directly instigating phenotypic climatic adaptations.
Article
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Bergmann’s and Allen’s rules were defined to describe macroecological patterns across latitudinal gradients. Bergmann observed a positive association between body size and latitude for endothermic species while Allen described shorter appendages as latitude increases. Almost two centuries later, there is still ongoing discussion about these patterns. Temperature, the common variable in these two rules, varies predictably across both latitude and elevation. Although these rules have been assessed extensively in mammals across latitude, particularly in regions with strong seasonality, studies on tropical montane mammals are scarce. We here test for these patterns and assess the variation of several other locomotory, diet-associated, body condition, and thermoregulatory traits across elevation in the Mountain Treeshrew (Tupaia montana) on tropical mountains in Borneo. Based on morphological measurements from both the field and scientific collections, we found a complex pattern: Bergmann’s rule was not supported in our tropical mountain system, since skull length, body size, and weight decreased from the lowest elevations (
Chapter
Tuco-tucos (Ctenomys sp.) are the most speciose genus of octodontoid rodent and are widely distributed in the southern half of South America. Despite their diversity, species of tuco-tucos rarely co-occur in syntopy and most adjacent species pairs are thought to be contiguously allopatric. Greater understanding of their geographic patterns of species diversity, range size, and body size distribution may provide insights on Ctenomys biogeography. In this chapter, we explored spatial patterns of species richness, geographic range size, and body size of tuco-tucos. We recovered a center of geographic range overlap in northern Argentina, and verified that tuco-tucos have a small range size when compared to other caviomorph families. However, we investigated range exclusivity – the proportion of a species range that is not shared with its congeners – and found that the exclusivity of Ctenomys ranges is comparable to that in other species-rich genera of caviomorphs. This finding challenges the idea that tuco-tuco species have a higher degree of allopatry than other genera. The body size distribution of tuco-tucos is right-skewed, as in other mammal groups, and negatively correlated with latitude, as previously documented. Relationships between richness, range size, and body size with geographical variables were presented and briefly discussed.
Article
Saltation is movement by means of hopping on two legs, or jumping on four. This locomotory mode is common in various taxa, including desert rodents, that inhabit open, arid environments and is associated with the elongation of hind feet and tails. Many adaptive hypotheses have been proposed to explain why saltation is common in open habitats, including considering it as a strategy for antipredation and/or energy conservation. Yet, the association between saltation ability (i.e., leap distance) and habitat openness has not been demonstrated statistically within any taxonomic group. Here, I use phylogenetic generalized least squares analyses (PGLS) to statistically test the association between indices of saltation, with those of habitat openness, in gerbils. I find that habitat openness is significantly (positively) correlated with relative hind foot length (RHFL), but not with relative tail length (RTL), indicating that gerbil species living in more open environments, have proportionately greater RHFL (and by inference greater leap distance). This supports the hypothesis that increased saltatorial ability is adaptive to more open habitats. The association between RHFL, RTL, in addition to relative ear length (REL) with indices of habitat temperature, was also tested. Temperature was found to be significantly (positively) correlated with RTL, in accordance with Allen’s rule (indicating that gerbils from warmer habitats have proportionately greater RTL), but not with RHFL or REL. These results indicate that, in gerbils, different appendages may be responding to different environmental adaptive pressures (i.e., saltatorial ability vs. thermoregulation).
Article
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Aim: We test whether geographic variation in length of rodent species’ appendages follows predictions of Allen’s rule—a positive relationship between appendage length and temperature—at a broad taxonomic scale (order Rodentia). We also test if the applicability of this rule varies based on the unit of analysis (species or assemblage), examined appendage (tail, hind foot, ear), body size, occupied habitat, geographic range size, life mode, and saltation ability. Location: Worldwide. Time period: Current. Major taxa studied: Rodents (order Rodentia). Methods: We assembled data on morphology, ecology, and phylogeny for up to 2,212 rodent species—representing ~86% of all the described rodent species and ~95% of the described genera. We tested the predicted Allen’s rule associations among size-corrected appendage lengths and both latitude and climatic variables (temperature and precipitation). We applied a cross-species approach based on phylogenetic regressions and a cross-assemblage approach based on spatial regressions in equal-area 1.5-degree grid cells. Results: Support for Allen’s rule was greatest for the tail and was stronger across assemblages than across species. We detected a negative relationship between tail length and (absolute) latitude, which was accounted for by a positive association between tail length and temperature of the coldest month. This association was greatest in desert species. In addition, we observed a negative relationship between ear length and precipitation. Main conclusions: In rodents, Allen’s rule is confirmed only for tails, and this association seems to be driven by adaptation to the cold, rather than warm temperatures. Habitat type seems to influence conformity to this rule. Conformity to Allen’s rule is likely the result of complex evolutionary trade-offs between temperature regulation and other essential species’ traits.
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Anthropogenic habitat change can have varied impacts on primates, including both negative and positive outcomes. Even when behavioural shifts are seen, they may reflect decreased health, or simply behavioural flexibility; understanding this distinction is important for conservation efforts. This study examines habitat-related variation in adult and immature morphometrics among diademed sifakas (Propithecus diadema). We collected morphometric data from sifakas at Tsinjoarivo, Madagascar (19 years, 188 captures, 113 individuals). Captures spanned 12 groups, five within continuous forest (“CONT”), and seven in degraded fragments (“FRAG”) where sifakas have lower nutritional intakes. Few consistent differences were found between CONT and FRAG groups. However, using home range quality as a covariate rather than a CONT/FRAG dichotomy revealed a threshold: the two FRAG groups in the lowest-quality habitat showed low adult mass and condition (wasting), and low immature mass and length (stunting). Though less-disturbed fragments apparently provide viable habitat, we suggest the sifakas in the most challenging habitats cannot evolve fast enough to keep up with such rapid habitat change. We suggest other long-lived organisms will show similar morphometric “warning signs” (wasting in adults, stunting in immatures); selected morphometric variables can thus be useful at gauging vulnerability of populations in the face of anthropogenic change.
Article
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The Black-faced Sheathbill (Chionis minor) is a sedentary and polytypic species. Four allopatric subspecies are known, each breeding on one archipelago in the Southern Indian Ocean. To evaluate the degree of isolation of these four subspecies, morphometrics and vocalizations of adult birds of Iles Kerguelen and Crozet were compared with those of the other localities (Prince Edward and Heard Islands). Two groups were distinguished (Prince Edward-Crozet and Kerguelen-Heard) on geographic and morphological criteria. In the eastern group (Kerguelen-Heard), corresponding to higher latitudes, sheathbills were larger and heavier, following Bergmann's Rule. The sheathbills from Iles Kerguelen also had a lower-pitched voice than those from Iles Crozet, consistent with their larger body size. Moreover, the birds from the southernmost locality (Heard Island) had a shorter culmen, consistent with Allen's Rule, but longer tarsi and deeper sheaths. Within the western group (Prince Edward-Crozet), and at Iles Kerguelen, there also was variability on a microgeographical scale. Differences between subspecies of Black-faced Sheathbill therefore could be due not only to environmental correlates of latitude, but also to possible genetic drift. The four subspecies are allopatric and do not differ in their breeding schedule or in their general behavior and diet, suggesting that differentiation may be recent and mainly due to geographical isolation.
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Article
The Late Neogene African records of climatic change at the start of the modern ice age, and of turnover in some mammalian groups including Hominidae, support the turnover pulse prediction. Many of the new species that appear 2.9-2.5 myr (millions of years) ago show similar suites of integrated character complexes, including larger bodies (consistent with Bergmann's Rule) and relative reduction in some body parts (Allen's Rule in the case of bodily extremities), together with enlargement of others including brains. I explore further the hypothesis (Vrba 1994) that the same evolutionary event of growth prolongation, or time hypermorphosis, as it acts on characters with different ancestral growth profiles in the same body plan, can result in a major reorganization - or "shuffling" - of body proportions such that some characters become larger and others smaller, some hyperadult and others more juvenilized. I suggest that this hypothesis applies to major features of hominid evolution including hominine encephalization.
Article
In this work, the changes in fur density and length in the subterranean rodent Ctenomys talarum were evaluated as a possible compensatory mechanism during seasonal temperature changes in their burrow environment and during pregnancy in females, both situations being thermoregulatory challenging in this species. The ventral fur was shorter and less dense than the dorsal fur in the three groups (males, non-pregnant females and pregnant females) and in the two seasons evaluated. Ventral and dorsal furs were significantly shorter during the warm seasons in the three groups. In the warm season, pregnant females had a ventral fur significantly shorter than that of males and non-pregnant females. The possible thermal advantages that the observed fur changes might represent for the species are discussed, with emphasis on the constraints imposed by the subterranean environment on available ways of dissipating body heat.
Article
Allen's rule states that endothermic animals living in colder climates have relatively shorter appendages than do closely related species in warmer climates. The traditional explanation is that smaller appendages conserve heat (Mayr, 1963). I examined Allen's rule with respect to three appendages (ear, tail, and hind foot), each expressed as a proportion of basilar skull length in rabbits (Sylvilagus) and hares (Lepus). Length of ear and tail in Lepus correlated positively with air temperature, supporting Allen's rule. However, these appendages of Sylvilagus do not follow Allen's rule. Moreover, relative hind foot length was negatively related to temperature in both genera. Allen's rule has limited applicability in North American rabbits and hares.