Behavioral Ecology Vol. 12 No. 2: 227-236
© 2001 International Society for Behavioral Ecology
On the evolution of group-living in the New World cursorial hystricognath rodents
Departamento de Ecología, P. Universidad Católica de Chile, Santiago, Chile
Address correspondence to L.A. Ebensperger. E-mail: lebenspe{at}genes.bio.puc.cl .
Received 19 August 1999; revised 28 August 2000; accepted 8 September 2000.
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ABSTRACT |
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We used the comparative method to examine the evolutionary causes of group-living in the New World cursorial hystricognath rodents. To do so, we used the available literature to collect information on behavioral (group size, burrow digging), ecological (amount of plant cover in the habitat), and life history (body mass, time to sexual maturity) variables, along with phylogenetic relationships of these rodents. We analyzed these variables in the context of three major hypotheses. A first explanation poses that rodents live in groups to reduce the energy needed in the construction of their burrows. A second hypothesis suggests that grouped rodents increase their ability to detect and escape from predators. A third possibility states that group-living is adopted by rodents to provide extra parental care to their offspring. Our comparative analysis revealed that across species variation of group size is, to some extent, influenced by body size, and by the habit of burrow digging. Thus, large sized rodent species that actively dig their own burrows form larger group sizes than small sized species that do not dig burrows. In contrast, across species variation of group size was not influenced by differences in the amount of plant cover in the habitat (an indirect measure of predatory risk), or by differences in the time to first reproduction (a measure of parental care given). Therefore, group-living among the New World histricognath rodents seems more linked to a strategy aimed to reduce their burrowing cost than to a strategy aimed to reduce their predatory risk, or to extend their parental investment.
Key words: burrows, comparative analysis, parental care, predatory risk, rodent sociality.
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INTRODUCTION |
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Many animal species form groups, which range from temporary associations and aggregations to relatively stable units (Lee, 1994
;
Parrish et al., 1997).
Fidelity to the group and genetic relatedness among individuals within such
groups may vary widely, which influences the nature (e.g., cooperative,
competitive) of social interactions among group members
(Hoogland, 1995;
Parrish et al., 1997).
Because group-living may impose reproductive as well as survival costs to
group members (Armitage, 1999;
Davies et al., 1991; Hoogland,
1979,
1985;
Møller, 1987;
Møller and Birkhead,
1993; Van Vuren,
1996), evolutionary explanations to group-living have relied on
either fitness advantages to individuals that might compensate these costs
(Alexander, 1974,
1991;
Krebs and Davies, 1993;
Madison, 1984;
Slobodchikoff, 1984;
Wrangham and Rubenstein,
1986), or on constraints that might force individuals to form
groups despite of the costs (Brown,
1987; Dunbar,
1996; Rodman,
1988; Van Rhijn,
1990; Waser,
1988).
For rodents, social groups have a variable number of adult individuals that
share a feeding area, a den, and (often) a territory
(Lacey et al., 1997;
Rayor, 1988;
Waterman, 1995). Although
several non-mutually exclusive hypotheses have been suggested to explain the
evolution of rodent group-living (see below), each model is often treated in
isolation and in the context of specific taxonomic groups (e.g.,
Armitage, 1999;
Jones, 1993). Herein, we use
the available data to carry out a comparative analysis and assess the ability
of several factors to explain group size variation across the New World
hystricognath rodents (e.g., guinea pigs, chinchillas, capybaras). We
specifically evaluate three alternative hypotheses posed to explain rodent
group-living (see below). New World hystricognaths are particularly
interesting as group-living in these rodents has not been examined in this
context before (Ebensperger,
1998). Recent evidence based on fossils, number of parasite
species shared, and analysis of molecular sequences supports an African
monophyletic origin for these rodents
(Gardner, 1991;
Nedbal et al., 1994;
Wyss et al., 1993). New World
hystricognaths include species adapted to different modes of life; they are
found in almost every type of habitat, and their social structure ranges from
solitary-living to highly gregarious species
(Eisenberg, 1989;
Eisenberg and Redford, 1999;
Nowak, 1999;
Redford and Eisenberg,
1992).
Hypotheses and predictions
The three hypotheses considered herein have been developed to understand
the evolution of sociality in rodents that carry out most or all of their
activities above ground, even though they may construct under ground burrows
(i.e., being semifossorial; DeBlase and
Martin, 1981).
Group-living has been linked to life in long-lasting, expandable nests
(Alexander et al., 1991). Most
rodents and other mammals need cavities and burrows as refuges to avoid
predators, stressful weather conditions, or as sites for food hoarding and
hibernation (King, 1984;
Kinlaw, 1999;
Reichman and Smith, 1987).
Because constructing and maintaining burrows is energetically costly
(Ebensperger and Bozinovic,
2000b; Lovegrove,
1989), animals may be forced to live in groups to share their use
or minimize such energetic cost (Arnold,
1990; Jarvis and Bennett,
1990; Powell and Fried,
1992; West,
1977). Thus, and under the burrow-sharing hypothesis, active
burrow-digging species are expected to form larger groups than
non-diggers.
Second, individuals may live in groups to reduce their percapita predatory
risk (Alexander, 1974;
Alexander et al., 1991;
Van Schaik, 1983). When
grouped, individual rodents may increase their ability to detect and escape
from predators, gain protection from predators because of simple dilution of
percapita risk, locate themselves such that other group members become more
vulnerable to attacks, or even repeal predators more efficiently
(Bertram, 1978;
Hamilton, 1971;
Romey, 1997). Under the
predatory risk hypothesis, species of more open, riskier habitats should
exhibit larger group sizes than species of more vegetated, safer habitats
(Dunbar, 1989;
Kleiman, 1974;
Lagory, 1986).
Finally, group-living among the North American sciurids (ground squirrels
and marmots) is hypothesized to be the consequence of additional reproductive
investment required beyond weaning age (Armitage,
1981,
1988,
1999). Sciurid social groups
are often the result of offspring delaying dispersal
(Armitage, 1999;
Blumstein and Armitage, 1998;
Michener, 1983). Dispersal is
retarded in relatively large body-sized species, which require extended times
to reach adult size and maturity, relative to time of active (growing) season
of the habitat. A relatively long time to reach maturity in turn demands
additional investment from the parents (Armitage,
1981,
1988,
1999; Barash,
1974,
1989). The extended parental
investment hypothesis predicts that body size and age to first reproduction of
social species should be larger than the corresponding figures of
solitary-living or less social species.
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METHODS |
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The data
We used the available literature to collect basic information about behavior, life history, and ecology of New World hystricognath rodents (Appendix). We considered every cursorial species with available data on group size. We also collected information on body mass, time to first reproduction, and the amount of plant cover in the habitat as an indicator of predatory risk. We determined plant cover after ranking the habitat of each species, from totally open (i.e., consisting of mostly bare ground) to dense forest patches. Finally, we categorized species as being either active burrow diggers or not (Appendix).
In contrast to the burrow-sharing and the predatory risk hypotheses, the
significance of group size to the extended parental investment hypothesis
seems more limited as this hypothesis has been posed to explain social
structure or complexity rather than group size
(Armitage, 1981;
Blumstein and Armitage, 1998).
Social complexity involves the nature, number, and stability of individual
interactions within groups (Blumstein and
Armitage, 1998; Lee,
1994). Although such information is available for some rodent
groups (Blumstein and Armitage,
1998), this is not so for most of New World hystricognaths.
Despite this caveat, group size still may be used to examine the overall
influence (or its absence) of life-history, as well as other (e.g.,
Faulkes et al., 1997;
Hoogland, 1981) factors, on
rodent group living. In fact, as the number of group members increases, there
is an opportunity for more social interactions
(Blumstein and Armitage,
1998).
There is no published hystricognath phylogeny that includes all cursorial
species of interest. Therefore we combined partial phylogenies giving priority
to studies based on molecular evidence. Nonetheless, we needed to use
phylogenetic relations based on other sources of information (e.g.,
morphology), along with taxonomy to include additional species and resolve
some soft polytomies. The use of different sources of information to infer
phylogenies is not uncommon when performing comparative studies
(Blumstein and Armitage, 1998;
Dubois et al., 1998). Familial
relationships (Figure 1) are
largely based on molecular data (Nedbal
et al., 1994). Relationships within Octodontidae and the placement
of Abrocomidae were determined following the karyotypic analysis of Gallardo
(1997). We used information on
blood protein and taxonomy to determine the placement of Agoutidae and
Dinomyidae (Woods, 1982).
Relationships within Chinchillidae (Spotorno AE, unpublished data), and those
between Cavia and Microcavia (Caviidae;
Marín,
1999) were derived from molecular evidence, whereas the placement
of Kerodon and Dolichotis were based on morphological data
(Quintana, 1996). Relations
within Echimyidae and Dasyproctidae were derived solely from taxonomy
(Woods, 1993). When analyzing
the influence of time to first reproduction on group size, we needed to trim
our phylogeny from 26 to 16 species as data on this life-history variable was
not available for the remaining 10 species. We followed Woods
(1993) for species names and
overall taxonomy. Since branch lengths of our phylogenies were generally
unknown, we considered three arbitrary algorithms, which differ in the model
of evolution assumed (Harvey and Pagel,
1991). Under the first of these approaches, all branch lengths
were left constant and equal to unity, which assumes that evolutionary change
is punctuational, occurring only at speciation events
(Blumstein and Armitage,
1998). In addition, we considered the Grafen's arbitrary method,
which assumes a gradual Brownian motion model of evolution
(Harvey and Pagel, 1991).
Under Grafen's approach, the height of each node is assumed to be directly
proportional to the number of species derived from it. The length of the
branch linking any two nodes is thus the difference between their heights
(Grafen, 1992). Last, we used
the arbitrary method of Pagel
(1992), which also assumes a
gradual model of evolution. All three branch length algorithms were
implemented with the use of the PDTREE module of the Phenotypic Diversity
Analysis Program (Garland et al.,
1993).
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Phylogenetically based statistical analyses
To control for possible phylogenetic non-independence of group size and of
the independent variables analyzed, we used the independent contrasts method
for continuous variables (Felsenstein,
1985; Martins and Hansen,
1996), and the autocorrelation method for categorical variables
(Cheverud et al., 1985;
Martins and Hansen, 1996).
When using the first method, we regressed the standardized contrasts of group
size against those of body mass, time to first reproduction, and plant cover
of habitat. All regressions were forced through the origin
(Garland et al., 1992). When
examining the influence of time to first reproduction, a life history
variable, we regressed the contrasts of this variable against the contrasts of
body mass and used the residuals for subsequent analyses
(Blumstein and Armitage, 1998;
Martins and Garland,
1991).
Under the autocorrelation method, the phenotype of each species is
represented as a sum of phylogenetic and non-phylogenetic components
(Cheverud et al., 1985;
Martins and Hansen, 1996).
Thus, and when using the autocorrelation method, we took the non-phylogenetic
component of group size and used two sample Student-t tests to
examine the influence of burrow digging on group size.
Independent contrasts were obtained using the Compare 4.2 program
(Martins, 1999). Polytomies
in our phylogenetic hypothesis were accounted for by bounding degrees of
freedom (Purvis and Garland,
1993). Accordingly, degrees of freedom in tests were calculated as
the total number of nodes in the phylogeny minus one
(Garland and
Díaz-Uriarte, 1999;
Purvis and Garland, 1993).
This correction was unnecessary in the case of tests using our trimmed
phylogeny as it did not contain polytomies.
We also used the Compare 4.2 program to implement the autocorrelation
method. As recommended by Martins
(1996), we conducted our
analysis both with and without the alpha parameter. The alpha parameter was
introduced by Gittleman and Kot
(1990) to improve the
efficiency of the spatial auto-corregressive model in removing phylogenetic
correlation from the database. However, and according to recent computer
simulation studies, the use of this correction factor may or may not improve
the efficiency of the method (Martins,
1996). When used, the alpha parameter was estimated by the program
using maximum likelihood. When not used, the alpha parameter was left fixed
and equal to unity.
Regular statistical methods were implemented with the use of Statistica 5.1
for Windows (StatSoft Inc., Tulsa, Oklahoma, USA). We report results for
one-tailed tests because of a-priori directional hypotheses
(Zar, 1996). Data are
presented as mean ± SD.
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RESULTS |
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Data on group size were available for a total of 26 species of cursorial hystricognaths (Appendix). Overall, the three arbitrary algorithms used to estimate the length of branches of our topology rendered consistent results in terms of the sign of each regression after using the independent contrasts method. Our regression analysis revealed that body mass weakly but significantly influenced group size, where large body sized species exhibited larger group sizes than small sized species (Figure 2). In contrast, the tendency of group size to increase with time to first reproduction (Figure 3), and with the amount of plant cover in the habitat (Figure 4) were not statistically significant.
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The raw across-species data showed that species that actively dig and maintain subterranean burrows tend to form larger groups than species that do not dig such burrows (Figure 5). Such a trend between burrow digging and group size was generally confirmed in a phylogenetic context. Thus and after using the autocorrelation method, the non-phylogenetic component of group size of species that dig burrows tended to be greater than that of cursorial species that do not dig burrows (Table 1). This tendency was significant particularly when the program computed the alpha parameter using maximum likelihood (Table 1).
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DISCUSSION |
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Group-living and burrows
The observation that group size of burrow digging species tended to be larger than that of non-digging species supports the burrow-sharing hypothesis. This finding suggests that the habit of burrow digging has been a major influence favoring the evolution of group-living of New World histricognath rodents. Overall, the relationship between burrows and rodent social systems has received little attention, and current evidence supporting this hypothesis is largely circumstantial (King, 1984
). For New World
hystricognaths, the influence of burrow digging on group-living is supported
by the observation that all group members of social plains vizcachas
(Lagostomus maximus) participate equally in digging
(Branch, 1993b), and that
common degus (Octodon degus) in groups coordinate their digging and
remove more soil per capita than solitary diggers
(Ebensperger and Bozinovic,
2000a).
Group-living and predatory risk
Our analysis also revealed that species of more open, riskier habitats do
not form significantly larger group sizes than species of more vegetated,
safer habitats, which contradicts expectations by the predatory risk
hypothesis (Dunbar, 1989;
Kleiman, 1974;
Lagory, 1986). It can be
argued that plant cover may not adequately measure overall predatory risk in
the habitat. Plant cover not only may provide prey with hiding places, but
obstruct and make predator detection more difficult to the prey
(Schooley et al., 1996;
Sharpe and Van Horne, 1998).
Despite this, rodent behavior generally support an inverse relationship
between the amount of plant cover and predatory risk. Guinea pigs (Cavia
aperea), spiny rats (Proechimys sp.), and California ground
squirrels (Spermophilus beecheyi) seek shrub cover upon the approach
of potential (terrestrial or aerial) predators
(Emmons, 1982;
Hanson and Coss, 1977;
Rood, 1972;
Sherman, 1985). Individual
wild guinea pigs and California ground squirrels spend more time alert when
foraging far from shrub or tree cover
(Cassini, 1991;
Leger et al., 1983). Eastern
chipmunks (Tamias striatus) and grey squirrels (Sciurus
carolinensis) also spend more time pausing (a behavior that seems to
improve anti-predator vigilance) when away from forest cover than when
traveling back towards forest cover
(McAdam and Kramer, 1998).
Experimental evidence also support the predicted relationship between
predatory risk and plant cover. Thus, red-backed voles (Clethrionomys
gapperi) and northern pygmy gerbils (Gerbillus
pyramidum) are less vulnerable to mammalian predators when in patches
of greater density of cover than in patches of less cover (Kotler et al.,
1991,
1992;
Longland and Price, 1991;
Wywialowski, 1987). Indeed,
northern pygmy gerbils (G. allenbyi and G. pyramidum) limit their
activity to safer shrub microhabitat when direct risk from aerial predators is
increased, but they switch to using open, less protected patches when such
predation risk decreases (Abramsky et al.,
1996).
Our finding that predatory risk does not explain any variation in group
size across cursorial hystricognath species does not negate that this factor
may have influenced group-living of some particular species, as it occurs in
other rodents (Hoogland, 1981;
Kildaw, 1995). Thus,
group-living capybaras (Hydrochaeris hydrochaeris) seem to rely on
selfish herd effects (Hamilton,
1971), and group defense to decrease their predatory risk. In
these rodents, individuals located at the periphery of a group devote more
time to scan their surroundings than individuals at more central positions
(Yáber
and Herrera, 1994), and groups coordinate themselves to protect
juveniles from the attack of feral dogs
(Macdonald, 1981). Besides,
overall group alertness has been shown to increase with group size in
capybaras and degus
(Vásquez,
1997;
Yáber and
Herrera, 1994), which may result in increased probabilities of
detecting an approaching predator (e.g.,
Hoogland, 1981).
Group-living and parental care
The observation that group size of large sized hystricognaths tended to be
larger than that of small sized species gave initial support to the extended
parental investment hypothesis. However, our finding of no significant
association between group size and time to first reproduction contradicted the
hypothesis. One can criticize this conclusion as the extended parental
investment hypothesis has been posed in a context of social complexity rather
than group size (Armitage,
1981,
1999;
Blumstein and Armitage, 1998).
However, additional considerations also point toward the unimportance of
breeding constraints during the evolution of hystricognath group-living. The
extended parental investment hypothesis is posed to explain the evolution of
group-living among ground squirrels and marmots (Sciuridae), where social
complexity has been shown to increase with body size and with time to first
reproduction (Armitage, 1981,
1999;
Blumstein and Armitage, 1998).
Time to first reproduction in these rodents ranges from 1 year in the least
social sciurids to 2-3 years in the most social species
(Blumstein and Armitage,
1998). By contrast, most hystricognaths considered in this study
are sexually mature before their first year of life (Appendix). Only the males
of plains vizcachas and the large sized male and female capybaras attain
sexual maturity within one to 1frac12; years old
(Jackson, 1989;
Mones and Ojasti, 1986;
Weir, 1971). Such differences
cannot be attributed to body size differences as mass of sciurids ranges from
100 g up to slightly more than 7 kg
(Armitage and Blumstein,
2000), whereas size of hystricognaths used in this study goes from
near 200 g to near 60 kg (Appendix). Finally, hystricognath rodents generally
produce off-spring that is more precocial than other similarly sized rodents,
including sciurids (Eisenberg,
1981;
Künkele and
Trillmich, 1997). All of these considerations suggest that
breeding constraints hypothesized to favor group-living in the sciurid rodents
seems much less likely to apply in the case of New World hystricognaths.
Group-living and body size
The observed relationship between body mass and group size could be a
secondary effect of an association between body size and the size of brain's
neocortex. The size of brain, including the neocortex, of mammals increases
with body size (Gittleman,
1986; Harvey et al.,
1980; Mace et al.,
1981), and the neocortex in turn tends to be correlated with group
size (Dunbar, 1995). The size
of neocortex is suggested to limit the number of social relationships an
individual can keep track of within its social group (Dunbar,
1992,
1995,
1996;
Gittleman, 1986).
Interestingly, a preliminary comparison using a few species of New World
hystricognaths shows that the neocortex of the most social species is larger
than that of the least social species (Bee
de Speroni, 1995).
Future prospects
Our study provides a starting point to begin unraveling the evolutionary
causes of group-living in the New World hystricognaths. Nonetheless, future
analyses should address some pending issues. First, our analysis is about
group size but the ultimate goal should be about social complexity. Second,
phylogenetic information about New World hystricognaths is still incomplete.
Both the autocorrelation and the independent contrasts methods may loose power
in detecting significant trends when phylogenies are not well resolved (e.g.,
when the number of species is < 40, or when soft polytomies are present;
Díaz-Uriarte
and Garland, 1998; Garland and
Díaz-Uriarte, 1999;
Martins, 1996;
Martins and Hansen, 1996;
Purvis et al., 1994). Indeed,
absence of well resolved phylogenies may explain partially why we almost lack
modern comparative analyses of rodent group-living and social systems (see
Blumstein and Armitage, 1998
for an exception), which contrasts with the situation of mammals other than
rodents (Brashares et al.,
2000; Di Fiore and Rendall,
1994; Geffen et al.,
1996). We hope our study will stimulate others to fill these
gaps.
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APPENDIX |
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ACKNOWLEDGEMENTS |
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We thank Emilia Martins and Ted Garland for giving us advise on the use of comparative methods, as well as for providing some of their publications and software on this matter. Advice also was given by Antonieta Labra. We are greatly indebted to Angel Spotorno for making his unpublished phylogeny on Chinchillidae available to us. Suggestions and comments made by Dan Blumstein and by an anonymous reviewer greatly improved earlier versions of this manuscript. Thanks to Fabian Jaksic and Pablo Marquet for allowing us to dive into their personal libraries, which increased our data set greatly. Similarly, Cody Arenz, D. Blumstein, Hynek Burda, Louise Emmons, Milton Gallardo, Guila Ganem, Jennifer Jarvis, Norbert Sachser, Andreas Scharff, and Nancy Solomon provided us with some of their articles. Our gratitude to Francisco Bozinovic for providing the facilities to carry out our research. This study was partially funded by a post-doctorate FONDECYT grant 3970028 to the senior author. During this study, H.C. was supported by a Doctoral Fellowship from CONICYT (Comisión Nacional de Investigación Científica y Tecnológica).
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