This Content Downloaded From 189.12.231.59 On Thu, 18 Feb 2021 03:22:44 UTC

Seeing the Forest through the Seeds: Mechanisms of Primate Behavioral Diversity from
Individuals to Populations and Beyond

Author(s): Karen B. Strier
Source: Current Anthropology , Vol. 50, No. 2 (April 2009), pp. 213-228
Published by: The University of Chicago Press on behalf of Wenner-Gren Foundation for
Anthropological Research
Stable URL: https://www.jstor.org/stable/10.1086/592026
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide
range of content in a trusted digital archive. We use information technology and tools to increase productivity and
facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at
https://about.jstor.org/terms
The University of Chicago Press and Wenner-Gren Foundation for Anthropological Research are
collaborating with JSTOR to digitize, preserve and extend access to Current Anthropology
This content downloaded from

189.12.231.59 on Thu, 18 Feb 2021 03:22:44 UTC
All use subject to https://about.jstor.org/terms
Current Anthropology Volume 50, Number 2, 2009 213
Seeing the Forest through the Seeds

Mechanisms of Primate Behavioral Diversity from Individuals to
Populations and Beyond
by Karen B. Strier
Understanding the evolution of primate behavioral diversity requires multilevel approaches that
encompass individuals, populations, and the effects of individuals and populations on each other.
At one level are analyses of individual behavior patterns under different ecological and demographic
conditions. At another level are the effects of individual behavior on the demography and genetics
of local populations, which in turn shape the behavior and biology of their individual members.
Multilevel studies across populations and over time provide insights into the range of behavioral
variation that particular species can express and are necessary for distinguishing the species-specific
behavior patterns on which evolutionary comparisons are based. These studies therefore provide the
insights necessary to incorporate intraspecific variation into comparative models.
The stimulus for this paper was the conference “Evolutionary hand with different types of hominids on the other hand could
Anthropology at the Interface,” held in honor of Cliff Jolly, at least partially control for the phylogenetic differences that
and my title is a tribute to Jolly’s (1970) famous seed-eater set baboons and hominids apart from each other and there-
hypothesis, in which he used comparisons of baboon feeding fore permit a more detailed consideration of the range of the
adaptations as analogies for comparisons among hominids. respective ecological adaptations expressed in each.
It is not his hypothesis per se that interests me here but his Embedded in Jolly’s baboon analysis were also critical ques-
distinctive comparative approach, which not only has per- tions about the range of variation encompassed within a tax-
meated much of his subsequent work but also offers a frame- onomic species and about what this intraspecific variation
work for new ways of thinking about primate behavioral means at both evolutionary and ecological scales. He and his
diversity. colleagues have explored taxonomic questions further in other
In turning to nonhuman primates for comparative per- works (e.g., Jolly 1993), but even in his early seed-eater hy-
spectives on humans, Jolly was following a long interdisci- pothesis, Jolly’s consideration of intraspecific variation relative
plinary and international tradition.1 What distinguished his to interspecific variation anticipated contemporary debates in
approach from those of his predecessors was his more elab- primate taxonomy and conservation.
orate comparative design. Instead of advancing a straightfor- It is common nowadays to employ classifications below the
ward comparison between baboons and hominids, Jolly com- species level, such as subspecies or “biologically significant
pared the feeding adaptations and ecologies of different types units,” that refer to discrete, distinctive populations (Mace
of baboons to those of different types of hominids in a kind 2004). The current practice of counting primate subspecies
of two-by-two design in which he mapped the relationship and of treating discrete populations as legitimate conservation
between the feeding ecologies of baboon types A and B onto units represents a deliberate strategy among conservationists,
an analogous comparison of the relationships between the who regard recognizing (by naming) all diversity as a prereq-
feeding ecologies of hominid types X and Y (Jolly 2001). Jolly’s uisite for preserving diversity (e.g., Rylands, Mittermeier, and
approach involved explicit comparisons among closely related Rodrı́guez Luna 1995). Apart from these practical (and to
taxa in addition to comparisons between more distantly re- some, political; e.g., Isaac, Mallet, and Mace 2004; Marks 2007;
lated taxa. Comparing different types of baboons on the one Tattersall 2007) motives, however, are the valid comparative
perspectives that emerge from this greater sensitivity to ques-
Karen B. Strier is Hilldale Professor of Anthropology in the De- 1. For example, Robert Yerkes, Kinji Imanishi, Junichiro Itani, Louis
partment of Anthropology at the University of Wisconsin–Madison Leakey, Sherwood Washburn, Irven DeVore, and Phyllis Dowlinhow were
(1180 Observatory Drive, Madison, Wisconsin 53706, U.S.A. all explicitly interested in primates for comparisons with humans, re-
[kbstrier@wisc.edu]). This paper was submitted 29 I 08 and accepted flecting a strong anthropocentric perspective in which primates are re-
21 VII 08. garded as closer to humans than to other animals.
䉷 2009 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2009/5002-0004$10.00. DOI: 10.1086/592026

189.12.231.59 on Thu, 18 Feb 2021 03:22:44 UTC
214 Current Anthropology Volume 50, Number 2, April 2009
tions about the extent and underlying causes of genetic, mor- about whether it is justifiable to dismiss so blithely the insights
phological, and behavioral variation within species. into intraspecific variation that long-term studies can provide
The value of within-species comparisons extends beyond (Nunn and Barton 2001, 81; emphasis added):
their use as analogues for hominid evolution, yet the patterns
Analysis of patterns across species is fundamental to the
of intraspecific variation and the mechanisms underlying
study of adaptive evolution, particularly when variation
these patterns of variation have remained largely underex-
needed to test hypotheses is present only at this interspecific
plored. A central point of my paper is the need for greater
level. Examples in primatology include the occurrence of
attention to intraspecific variation in order to advance our
female sexual swellings in species with habitually multimale,
understanding of primate behavioral diversity and better as-
rather than single-male, breeding systems, the relationship
sess the potential of species to adapt under rapid environ-
between polygynandrous mating and relatively large testes
mental change.
size, and the association between brain size and social group
Intraspecific variation in behavior patterns is typically at-
size.
tributed to local ecological conditions such as climate, rainfall,
the availability and distribution of food, predation pressures, I do not dispute that the presence or absence of sexual swell-
and disease, which vary across populations living in diverse ings is a species-specific trait that merits analysis by the com-
habitats as well as seasonally or superannually within popu- parative method. However, relative testis size may vary below
lations in the same habitats over different temporal scales. the species level as well as among different species, as Jolly
However, demographic conditions—such as group size, sex and Phillips-Conroy (2006) have recently shown for baboons,
ratios, and population density—also vary across populations and features of the brain may be sex specific as well as species
and within the same populations over time and are therefore specific, as has long been known for voles (Jacobs et al. 1990).
as important as ecology in shaping behavior. Long-term stud- Indeed, even sex-specific body mass—which represents the
ies can provide unique insights into how primates behave variable against which many biological traits, including testis
under different demographic as well as ecological conditions size or brain size, are typically compared—can vary signifi-
and therefore contribute to our understanding of the mech- cantly in wild primates, depending on season, forest type, and
anisms underlying intraspecific variation. However, despite population (Glander 2006).
the importance of demography in comparative models of Even more questionable than relative testis size or brain
primate behavior and in conservation, attention to demo- size are the categorical distinctions made between behavioral
graphic variables has lagged at least 20 years behind attention traits such as breeding systems, mating systems, and social
to ecological variables. A second point of my paper, therefore, group sizes, because behavioral traits are known to vary within
is to consider some of the ways in which primates adjust their populations and over lifetimes instead of over the generations
behavior in response to demographic fluctuations over the necessary for evolutionary adaptations. We know, for exam-
course of individual lifetimes. ple, that both multimale and single-male breeding systems
occur sympatrically and simultaneously in black howler mon-
Intraspecific Variation: Anecdote or key populations (Van Belle and Estrada 2006) and in moun-
tain gorilla populations, where individual males and females
Missing Chapter? may participate in both multimale and single-male breeding
The importance of intraspecific variation in comparative systems at different times during their lives (Robbins 1995,
models of the evolution of primate behavioral diversity has 2001). Other “polymorphic” breeding systems are known to
been overshadowed by enthusiasm for the power of the com- occur in many other primates (e.g., gibbons, siamangs, golden
parative method, which seeks to identify adaptations by iden- lion tamarins, and saddle-back tamarins), and multimale
tifying changes in character states of species along phyloge- groups can mask what are effectively single-male breeding
netic routes (Harvey and Pagel 1991; Nunn and Barton 2001). systems if dominant males can monopolize all or a dispro-
As advances in genetics have refined our understanding of portionate share of fertilizations (Altmann et al. 1996; Pope
primate phylogeny, confidence in the comparative method, 1990). What, then, are the criteria for identifying the habitual
with its emphasis on species as the units for analyses of be- breeding system of a species when different types of breeding
havioral adaptations, has justifiably increased. It is unfortu- systems occur within and between populations2 and when the
nate that important advances in applications of the compar- same individuals may participate in different types of breeding
ative method seem to have come at the expense of comparable systems at different times during their lives?
methodological advances for analyzing intraspecific variation. Group size is an even more difficult trait to categorize
The unusual, infrequent patterns of behavioral variation because it is a continuous variable. Like breeding systems,
that often emerge only from long-term studies have been group sizes can vary within and across populations and can
dismissed as “anecdotes,” essentially irrelevant for evolution-
ary analyses (Nunn and Barton 2001, 81). However, a quick 2. Jim Moore (1984) posed a similar question about what proportion
glimpse at a portion of the abstract from this otherwise ex- of dispersal events could deviate from the so-called species-specific pat-
cellent review of the comparative method raises questions tern before the idea of a pattern required reconsideration.

189.12.231.59 on Thu, 18 Feb 2021 03:22:44 UTC
Strier Primate Behavioral Diversity 215
change dramatically within the same population over the life size can vary across populations or within the same popu-
spans of its individual members through the agency of indi- lation over time. This question is different from the one that
vidual dispersal decisions as well as through stochastic events. the comparative method aims to address, but I believe that
Most long-term field studies of unprovisioned primates have it is fundamental for interpreting behavioral adaptations from
documented changes in group sizes associated with either a comparative evolutionary perspective (Strier 1997a).
population declines or population growth, both of which can Thomas Struhsaker made a similar point more explicitly in
be attributed to a combination of natural demographic pro- a review of variation in the adult sex ratios of red colobus
cesses—such as predation (or the local extirpation of pred- monkey social groups: “Unless the variation within popula-
ators), disease, or intraspecific aggression—and intensified tions, species and superspecies is taken into account, inter-
human activities—such as harvesting and habitat disturbance specific comparisons based on mean values are of limited
(or increased conservation efforts). utility, if not counterproductive, in understanding evolution
Our long-term study of northern muriqui monkeys pro- and behavioral plasticity” (Struhsaker 2000, 108).
vides an example of how much primate group sizes can change To compress intraspecific behavioral variation into discrete,
over a 25-year period. During this time, our main study group static, species-specific character traits is also to ignore one of
has nearly quadrupled in size, growing from 23 to 89 mem- the most distinctive characteristics of primates as an order,
bers, and this has been accompanied by a comparable increase that is, their behavioral plasticity, or the ability of primates
in the size of the entire population, which grew from some to make behavioral adjustments in response to fluctuating
60 individuals distributed in two groups to 256 individuals ecological and demographic conditions (Jay 1968; Moore
living in four groups (as of December 2007; updated from 1999). We must at least understand the species-specific pat-
Strier et al. 2006). For many years, our main study group was terns that these behavioral adjustments take before we can
the only source of information on this species, and its group fully describe patterns in the evolution of behavioral adap-
size has been used to represent this species in various com- tations.
parative analyses by authors who have calculated means or Characterizing the range of intraspecific variation in be-
medians from whatever published values were available at the havior and the mechanisms underlying this variation can ex-
time of their analyses. But what, in this case, is a biologically tend our perspectives on primate behavioral diversity in two
meaningful representation of the size of this group, and how directions. First, understanding the extent of intraspecific var-
accurately can this growing group represent a typical group iation is necessary for distinguishing behavior patterns that
size for this species? Calculating an average or median group are phylogenetically conservative from those that are facul-
size is arbitrary when the value obtained varies so much de- tatively responsive to local conditions. These distinctions
pending on the time period included. Clearly, our impressions show us the range of adaptive variation that is possible within
of muriqui group sizes would have been different if the study the constraints of an organism’s reaction norm, or “phenotype
had ended after the first few years or had been initiated just set,” which includes development and life history as well as
last year. behavior tendencies and morphology (Maynard Smith 1978).
The rate of growth in this muriqui group is obviously ex- Distinguishing conservative from facultative behavior traits is
traordinary and unlikely to persist once the habitat is satu- necessary for making informed inferences about past evolu-
rated. But even the inclusion of new data that are now avail- tionary selection pressures that have shaped the behavior pat-
able on group sizes from other northern muriqui populations terns, or more precisely the ranges of behavior patterns, that
is misleading because we also know that these other popu- we observe within and between species of primates today.
lations occur in habitats that have been altered to various Second, understanding the mechanisms underlying intra-
degrees and in which the muriquis have been subjected to specific variation in behavior patterns is necessary for ex-
different kinds of anthropogenic pressures (Mendes et al. trapolations about the capacity of primates to respond to
2005). If, after 25 years, we still do not know what a typical rapid changes in environmental conditions, whether ecolog-
group size for this species might be, one has to at least wonder ical or demographic in kind. Many organisms have evolved
about the so-called average group sizes of other species of to respond to environmental cues that were once accurate
primates based on data from shorter studies and how they predictors of optimal conditions but are no longer so because
might also vary over a 25-year period under changing envi- local habitat alterations, global climate change, or recent hunt-
ronmental conditions and in response to stochastic demo- ing pressures have disassociated the original cues from the
graphic events. conditions that they historically represented and to which the
My objective here is not to critique the comparative responses were selected. Behavioral responses that were once
method, which is a powerful approach when appropriately highly adaptive but are now maladaptive are known as “eco-
applied. Instead, I want to call attention to the limitations logical traps,” and they can lead to “evolutionary traps” when
inherent in any method that requires compressing intraspe- they cause populations to decline and extinction risks to in-
cific variation into modal, species-specific values without first crease (Schlaepfer, Runge, and Sherman 2002). With nearly
understanding the extent to which and the conditions under one-half of all primates now threatened with extinction, un-
which a species’ breeding system, mating system, or group derstanding both the ways in which primates adjust their

189.12.231.59 on Thu, 18 Feb 2021 03:22:44 UTC
behavior and the extent to which they are capable of adjusting and has persisted to the present. The first inclusion of de-
would seem to be of vital importance for identifying conser- mography as a keyword occurred in the 1960s, fully two decades
vation priorities among the many taxa and populations at behind the first inclusion of ecology.3 In the 1970s, some field
risk. primatologists (e.g., Altmann and Altmann 1979; Dunbar 1979)
had begun explicitly writing about the role of demography in
Levels of Analyses and Determinants shaping primate social environments, and by the mid-1980s,
demography appeared as a keyword for major textbooks on
of Behavior primate ecology (Richard 1985) and primate social behavior
Ethologist Niko Tinbergen (1951) defined the four major cat- (Jolly 1985). In the 1980s, demography, with 256 references,
egories of questions that are still asked in behavioral analyses: had nearly caught up to where ecology had been in the 1960s,
causation, ontogenetic, functional, and phylogenetic. Causa- with 269 references, and in the current (still incomplete) decade,
tion questions refer to the biological mechanisms, such as demography, with 1,315 references, is only slightly ahead of
genetics, endocrinology, and neurophysiology, that regulate where ecology was in the 1970s, with 1,275 references. Not
the behavior. Ontogenetic questions refer to developmental surprisingly, during the past five decades, demography
processes, which would also include life-history components publications have been nearly 10 times as likely to also refer
of behavior. Functional questions refer to the adaptive value to ecology (mean Ⳳ SD p 59.6% Ⳳ 5.2%) as ecology publi-
of the behavior. Phylogenetic questions refer to the evolu- cations have been to refer to demography (6.7% Ⳳ 5.8%). The
tionary history of the behavior. Causation and ontogenetic percentage of ecology publications referring to demography has
questions involve proximate levels of analyses; functional and increased from 1.5% and 1.1% in the 1960s and 1970s, re-
phylogenetic questions involve ultimate levels of analyses. spectively, to 12% and 13.5% in the past two decades, consistent
Many contemporary primatologists studying the behavior with the rise in the number of publications on demography
of wild primates work at multiple levels of analyses simul- since the 1980s. These statistics indicate that primatologists have
taneously. We collect data on ecological, biological, and be- not deliberately ignored demographic explanations but rather
havioral variables to address both proximate and ultimate that demographic explanations have been slower than ecolog-
questions about causation, ontogeny, and function, which we ical explanations to emerge from field studies.
then interpret by comparisons with similar data on other The faster pace of advancement of ecological explanations
primates to gain a phylogenetic perspective. Thus, measures of behavior relative to demographic explanations may be at-
of food availability provide insights into the variation we ob- tributed, as least in part, to the much faster rate at which
serve in dietary preferences; hormonal analyses provide in- ecological data can be collected. For example, a 1-year field
sights into the reproductive status of our study subjects and study (the length of most doctoral dissertation field studies,
how this varies with their ecology and behavior; and genetic as well as the duration of most faculty sabbaticals) is usually
studies provide insights into the fitness consequences of be- sufficient to evaluate seasonality in food resources and the
havioral variation. effects of seasonality on primate feeding, ranging, grouping,
When we compare our own findings with those for other and even social patterns. Demographic data, by contrast, min-
species, it is common to assume that phylogeny accounts for imally require either simultaneous studies on multiple groups
differences among distantly related taxa and similarities that differ sufficiently in size or composition to affect behavior
among closely related taxa and that one or more ecological or else longitudinal studies that encompass fluctuations in
variables account for similarities among distantly related taxa group size or composition or a sufficient number of demo-
and differences between closely related taxa. Our interpre- graphic events (e.g., births, deaths, and migrations into and
tations, however, are limited both by the degree of consistency out of groups) to influence behavior in measurable ways.
in our behavioral, physiological, and genetic data over time Moreover, demographic changes, such as fluctuations in sex
and by the ecological and demographic conditions that prevail ratios, may take months or even years before they influence
when our data are collected. behaviors related to dispersal, reproduction, competition, or
Our understanding of the relevant ecological variables that cooperation.
shape primate behavior and the ways in which primates re- The increased interest in demography in the 1980s may be
spond to changes in these variables is much more advanced related to the time lag between the onset of the first wave of
than our understanding of the corresponding effects of de- what have become longitudinal studies, which were initiated
mographic variables. A quick perusal of the prevalence and
temporal distribution of these two terms as keywords in 3. It may be of some historical interest to note that the first PrimateLit
PrimateLit (http://primatelit.library.wisc.edu) demonstrates references in which demography is listed as a keyword were both pub-
the historic extent of the bias in favor of ecology over de- lished in Sherwood Washburn’s (1961) edited volume, Social Life of Early
Man, based on his Wenner-Gren symposium of June 22–30, 1959. One
mography in primatology. From 1940 to 2007, “ecology” ap-
of these papers, by A. H. Schultz (1961), was entitled “Some factors
pears as a keyword in a total of 15,684 publications, whereas influencing the social life of primates in general and of early man in
“demography” appears in only 2,717 publications. particular”; the other, by M. R. A. Chance (1961), was entitled, “The
The surge of interest in demography began in the 1980s nature and special features of the instinctive social bond of primates.”

189.12.231.59 on Thu, 18 Feb 2021 03:22:44 UTC
in the 1960s, and the demographic perspectives that these some additional advantages over shorter-term comparative
studies had begun to provide. By the late 1980s, we had well- studies of different populations of a species. Observations of
developed evolutionary theories from which to evaluate pre- behavioral changes over time can serve as a surrogate for
dictions about how social patterns, such as rates of aggressive extrapolating information about the range of intraspecific be-
or affiliative interactions, vary with the size and sex ratios of havioral variation while also controlling for genetic continuity,
study groups. Concurrently, advances in methods of genetic which is likely to be greater among members of the same
analyses were providing necessary data for testing predictions populations than between individuals of different popula-
about how social behavior varies with the genetic composition tions. In addition, longitudinal studies can document not only
of groups and therefore for testing the evolutionary function the ontogeny, or life histories, of individuals but also that of
of behavior (e.g., Altmann et al. 1996). their groups, which change over time with their membership.
It is also no coincidence that the 1980s were marked by Longitudinal studies also provide perspectives on how de-
the development of conservation biology as a separate aca- mographic conditions fluctuate in response to changing eco-
demic discipline and growing concerns about the threatened logical conditions4 and on the interacting effects of individual
status of wild primate populations and their habitats. Con- behavior on the one hand and group- and population-level
servation biology’s interest in populations echoed the call demography on the other hand. Thus, long-term studies pro-
from ecologists for behavioral ecologists, which include most vide insights into how primates adjust their behavior in re-
field primatologists, to “work up toward the population con- sponse to environmental (physical and social) variables. These
sequences of behavior” (May and Seger 1986, 267) by moving responses reflect the adaptive potential of species over evo-
beyond comparisons of how individuals behave in their re- lutionary time.
spective social groups to considerations of individuals and For demographic purposes, long-term studies can be de-
groups within the context of their local (and often, isolated) fined as those that span multiple overlapping generations and
populations. Recognition of the importance of populations therefore capture behavioral responses to demographic as well
as units of analyses for conservation purposes has also directly as ecological fluctuations that occur during the course of an
and indirectly stimulated interest in the effects of demo- individual life span (Strier and Mendes 2009). Characterizing
graphic processes on behavior. behavioral adjustments to demographic conditions requires a
longer-term perspective than characterizing behavioral ad-
Units of Analyses: Populations justments to predictable ecological fluctuations. For example,
and Beyond the different ways in which primates respond to seasonal fluc-
tuations in the availability of their preferred food resources
Most of our current understanding of primate behavioral var- can usually be characterized over an annual cycle (although,
iation has been based on patterns that we observe among clearly, more information about these responses can be
individual members of one or more social groups, which we gleaned from multiyear studies that capture interannual as
then compare with similar data on individual members of well as seasonal variation). Looking at the range of responses
social groups of the same or different species. We sometimes
that primates exhibit to food seasonality provides a framework
have sufficient data to compare the behavior patterns of in-
for thinking about adaptive potentials in response to de-
dividuals in single groups across different populations or
mographic fluctuations. Thus, when preferred foods are sea-
across multiple groups within the same populations, but usu-
sonally scarce, primates make various adjustments in (1) their
ally these comparisons are based on synchronic or static prop-
diets, by consuming more abundant but less preferred foods;
erties of the groups during the relatively brief periods of time
(2) their ranging patterns, by shifting their core areas or by
they are studied. There are surprisingly few cases for which
ranging farther to increase their encounter rates with scarce
we have sufficient comparative data to characterize the range
patches of preferred foods; and (3) their grouping patterns,
of intraspecific or interpopulation variation in the behavioral
via fission-fusion dynamics, which reduce competition at lim-
responses of more than single study groups of the same species
ited patches of preferred food resources. All primates respond
over extended periods of time. The lack of comparative di-
to seasonal food shortages to varying degrees in at least one
achronic studies on different populations of the same species
of these ways, and some primates adjust their behavior in all
represents a fundamental limitation in our ability to under-
three ways. The degree to which different taxa can make di-
stand behavioral diversity at a phylogenetic level. Indeed, Tin-
bergen (1951) identified populations (and species) as the units etary (versus social) adjustments tends to correspond to their
of analyses for addressing ultimate-level questions, and con- biogeographic distribution and reflects something about the
temporary ecologists have extended the relevance of popu- levels of seasonality and the diverse ecological conditions to
lations to include proximate-level questions (e.g., Ricklefs and which they have adapted over evolutionary time. Conversely,
Wikelski 2002). Primatology is now at a stage where patterns
4. For example, climate change that affects food availability and sea-
of intraspecific variation can begin to be recognized and in- sonality may result in shifts in reproductive and mortality rates. Similarly,
corporated into comparative evolutionary models. habitat alterations, or shifts in competitor or predator communities, can
Longitudinal studies of the same populations may have affect demographic conditions.

189.12.231.59 on Thu, 18 Feb 2021 03:22:44 UTC
the degree to which primates adjust their grouping patterns cercopithecines and is absent among apes (Di Fiore and Ren-
provides some insights into the nature of their social bonds dall 1994; Strier 1994).
and the relative importance of the non-food-related functions Just as the morphological and physiological adaptations
of their groups (e.g., predation pressures or access to mates help define the phenotype sets that constrain or facilitate sea-
or caretakers of infants). sonal dietary versus social adjustments to shifts in food avail-
We tend to characterize primate ecological adaptations ac- ability, dispersal patterns may represent the phenotype sets
cording to the proportion of different food types in their that determine the range of most likely behavioral responses
annual diets, but perhaps a more relevant way of character- to population growth. In both cases, behavioral adjustments
izing their adaptive potential would be based on which aspects are the product of individual decisions that are made in eco-
of their behavior are most labile. Indeed, overall diets tell us logical time in response to local ecological or demographic
little about the “critical functions” of morphological traits conditions, respectively (Jones 2005). However, in contrast to
associated with food processing when preferred foods are morphological and physiological feeding adaptations, indi-
scarce (Rosenberger and Kinzey 1976). It may be more in- vidual dispersal decisions also affect the demographic con-
formative to consider the ability to process alternative foods, ditions to which they and other individuals respond. Thus,
which may constitute a relatively low proportion of the overall one male’s decision to disperse from his natal group or to
diet but are nonetheless critical to survival during stressful secondarily disperse from a group with an unfavorable sex
times, when selection pressures are expected to be strongest. ratio has the result of improving that group’s sex ratio for
By this logic, it may be that identifying the diverse configu- the other males that remain or that may subsequently join it.
rations of adjustments in feeding, ranging, and grouping be- Secondary dispersal is more common among males in
havior in response to food shortages can tell us more about male-biased dispersal systems than it is among females in
evolutionary adaptations to ecological fluctuations than de- female-biased dispersal systems, which undoubtedly reflects
pictions of overall diets per se. Adjustments in feeding, rang- sex differences in the costs and benefits of dispersing relative
ing, or grouping patterns are behavioral responses to ecolog- to male reproductive opportunities and female reproductive
ical problems, but the propensity to respond in one way versus energetics. Curiously, however, this sex difference in second-
ary dispersal is less evident in primates in which both sexes
another reflects the evolutionary processes that define the
disperse from their natal groups (Strier 2004). Even more
species’ phenotype set. An interesting empirical experiment
intriguing, shifts from male philopatry to bisexual dispersal
might be to apply the comparative method to investigate pat-
appear to be more feasible than shifts from female philopatry
terns in how different taxa respond to seasonal food shortages
to bisexual dispersal. For example, two “philopatric” male
instead of characterizing them by what types of foods con-
bonobos (Hohmann 2001) and two cohorts of philopatric
stitute the bulk of their diets.
male northern muriquis (Strier et al. 2006) have been reported
Like ecological fluctuations, changing demographic con-
to leave or fission from their natal groups to associate with
ditions can also elicit a range of behavioral responses, al-
neighboring groups where more favorable sex ratios prevailed.
though the time lags involved in demographic fluctuations
Although these examples of male cohorts transferring in two
may exceed seasonal cycles. We can consider two types of
species that are ordinarily male philopatric are clearly anec-
demographic fluctuations, population growth and sex ratios,
dotes, I am not aware of any comparable anecdotes in which
to which primates are known to exhibit a range of behavioral
cohorts of philopatric female primates, such as rhesus ma-
responses. As with behavioral responses to seasonal food avail-
caques or yellow baboons, have transferred between extant
ability, there appear to be a finite number of behavioral ad- groups, even in populations that have been studied system-
justments primates make when their populations grow. Pri- atically for many more decades than bonobos or muriquis.
mates can (1) permit the size of cohesive groups to increase This example of variation in patterns of dispersal is helpful
until the groups ultimately (and permanently) fission, (2) in highlighting three points. First, it illustrates that some types
increase the density (but not the size) of cohesive groups, or of dispersal patterns appear to be more labile than others.
(3) shift from cohesive to increasingly fluid associations with- Consequently, even if we categorize primate dispersal systems
out permanent group fissioning. The distribution of these as male biased, female biased, or bisexual, the demographic
alternative ways of responding to population growth maps thresholds for individual dispersal decisions, including deci-
neatly onto the distribution of dispersal patterns (Strier 2000). sions that result in deviating from philopatry to disperse,
Thus, female philopatry tends to promote the growth of co- appear to vary in predictable and therefore potentially bio-
hesive groups until they fission, often but not always along logically meaningful ways.
matrilines, whereas bisexual dispersal liberates both sexes to Second, the routes by which different taxa arrive at their
establish new groups instead of joining extant groups, and respective dispersal systems can vary. Populations that ex-
male philopatry permits females to adjust their association perience extreme fluctuations in adult sex ratios may shift
patterns without sacrificing their membership in a group. from sex-biased to bisexual dispersal or from female-biased
Dispersal patterns across primates correspond somewhat with to male-biased dispersal via a transitional phase of bisexual
phylogeny, such that female philopatry is concentrated among dispersal. Recent data from our northern muriqui population

189.12.231.59 on Thu, 18 Feb 2021 03:22:44 UTC
suggest that the latter case could occur, especially given the of intraspecific variation that can provide insights into be-
three (of some 40) atypical females that have remained and havioral evolution.
reproduced in their natal group instead of dispersing (Strier
et al. 2006). Models of the various possible routes by which Demography and Mechanisms
similar social systems may evolve (e.g., Lee 1994) provide
intriguing insights into the importance of understanding the
of Behavior
patterns of behavioral responses to demographic conditions Most discussions of behavioral responses to changing de-
at both intra- and interspecific levels and therefore merit more mographic conditions carry an implicit assumption that there
attention than they have so far received. is a unidirectional, cause-effect relationship between demog-
A third important point about behavioral adjustments to raphy and behavior. This is misleading, however, because be-
demographic conditions pertains to the units at which these havior and demography are clearly dynamic processes that
dynamics occur. Individuals make dispersal decisions based can feed back on one another and therefore shape one another
on demographic conditions in their current groups relative in a sequential way.
to demographic conditions in other groups. In extreme cases, Dispersal decisions in response to relative group size or sex
such as when dispersal opportunities or access to unfamiliar, ratios have an obvious corresponding effect on the size and
unrelated mates is limited, subordinate female callitrichines composition of groups left, joined, or formed, which then
may remain in their natal groups as nonreproductive helpers. provide the cues by which other individuals make dispersal
However, these females abandon their inclusive fitness con- decisions. In this respect, behavioral responses to demo-
cerns at the first opportunity to either mate with an unfamiliar graphic conditions represent some of the mechanisms that
neighboring male or disperse to establish their own breeding regulate demography in the same way that neuroendocri-
groups. In saturated habitats, buffy-headed marmoset groups nology, physiology, and genetics are mechanisms that regulate
and red howler monkey groups can grow into extended female behavior in ethology (e.g., Gould 1982). Some of these mech-
matrilines through the retention of successive cohorts of natal anisms, such as the hormonal regulation of ovarian cycling,
females (Ferrari, Correa, and Coutinho 1996; Pope 1998, occur without individual control, just as some aspects of pop-
2000). Female matrilines either fail to form at lower popu- ulation demography, such as birth rates or infant sex deter-
lation densities or else disintegrate as natal females disperse mination, are not ordinarily ones that individuals (at least
in response to vacancies created by the deaths of breeding nonhuman primates) can control. But other mechanisms,
females in neighboring groups or to increases in population- such as cortisol levels, both reflect and are affected by eco-
wide sex ratios that create opportunities to establish their own logical and social stress, just as group size and composition
breeding groups. both reflect and are affected by individual dispersal decisions.
The demographic conditions that affect female dispersal Thus, cortisol elevation occurs in response to stressful stimuli
decisions can vary over the course of an individual’s lifetime (or to cues associated with stressful stimuli) and also permits
as well as across populations of the same and closely related the physiological mobilization of energy reserves for behav-
species. Examining how different taxa respond to demo- ioral responses to the stressors. And, just as there are indi-
graphic variables provides a deeper level of understanding vidual and species differences in cortisol response thresholds,
about their behavioral adaptations than categorizations of dis- there are also individual and species differences in the de-
persal regimes or group compositions at a particular moment mographic thresholds to which primates respond. Distin-
in time. guishing the range of individual versus species differences in
Just as we would never claim to know the full range of responses to demographic thresholds is similar to distinguish-
food items in the diet of a species that had been observed ing the hormonal responses of high- versus low-ranking males
only during a 3-month study at one field site, we should be (or females) of different species to similar social and seasonal
similarly wary about drawing conclusions about dispersal pat- stimuli.
terns (or other social patterns) under a particular, limited set Thinking about behavioral responses to demographic con-
of demographic conditions. We now know enough about eco- ditions as regulating mechanisms helps to situate intraspecific
logical seasonality to qualify a 3-month feeding study as rep- behavioral variation within an adaptive framework while also
resenting only a partial glimpse into a primate’s diet in that identifying both the sources of variation and the temporal
particular season and habitat, but our ability to describe the scale at which behavioral adjustments can occur. Behavioral
relevant variables associated with demographic fluctuations polymorphisms, such as unimale versus multimale groups of
or to predict the full range of behavioral responses to these mountain gorillas or black howler monkeys, can be main-
fluctuations is still limited by at least three factors: (1) the tained in populations by the fluctuations in population den-
relatively short duration of most field studies, (2) the tradition sities and sex ratios that occur within life spans. Perhaps the
of focusing on study groups instead of populations in be- more interesting evolutionary question is not why mountain
havioral analyses, and (3) the tendency to treat demographic gorillas or black howler monkeys exhibit so much intraspecific
variables such as group size and composition as fixed, species- variation in their group compositions and corresponding
specific character states instead of as facultative components mating and social systems but rather why some species of

189.12.231.59 on Thu, 18 Feb 2021 03:22:44 UTC
primates appear to be so much more “fixated” on their re- the ground to cross the pastures that surround the forests in
spective particular social patterns, especially when the sto- which they were born in order to disperse into neighboring
chastic components of demography (as opposed to those as- fragments. Females that make it to the safety of an adjacent
pects of demography that are affected by individual behaviors) patch of forest may then spend the rest of their lives alone
are considered. unless they encounter other muriquis to join or humans in-
Female philopatry, for example, may become fixated more tervene to translocate them to populated areas. Female mu-
easily than male philopatry once it is established because the riquis are not expelled from their natal groups, so it is likely
benefits of residing with familiar, matrilineal kin may be that their dispersal decisions are triggered by demographic
greater for females than the corresponding benefits (e.g., ac- cues in their natal groups. These cues clearly function to
cess to patrilineal kin) for males, which may gain more than stimulate female dispersal in larger forests that support mul-
females by dispersing in response to group sex ratios. How- tiple groups in which unrelated mates can be found, but
ever, it is possible to envision a demographic scenario in which dispersing into an unfamiliar forest that is uninhabited by
an extended shortage of female baboons (due, for example, other muriquis is not an adaptive response under contem-
to a stochastic skew of infant sex ratios over successive co- porary conditions of forest fragmentation. Indeed, there is
horts) might disrupt their extended matrilines, making it fea- already one known case of a small population that has effec-
sible for individual males to monopolize individual females. tively become extinct due, in part, to unsuccessful dispersal
These males might add unrelated females to their units as attempts by some of its females (de Melo et al. 2005).
population sex ratios shift, and as female numbers increase, Muriquis provide additional examples for thinking about
their relationships with one another might begin to resemble ecological traps involving primates because their forests and
their relationships with unit males. The result might be similar populations have been so severely altered. Similar kinds of
to the intraspecific variation that Swedell (2006) has described anthropogenic pressures are now devastating the habitats and
in the social relations of female hamadryas baboons in larger populations of other primates worldwide, and understanding
versus smaller groups as well as to the variation between how muriquis have coped with rapid ecological and demo-
hamadryas and other baboon taxa with more explicit mat- graphic changes can be useful for understanding the potential
rilocal societies and correspondingly stronger female bonds. responses of other primates that are only now beginning to
There are other examples of variation in dispersal patterns experience similar pressures. For example, by the behavioral
that corresponds to local demographic conditions, such as responses that have accompanied the fourfold increase in
the local communities in which some populations of male group and population size, we can distinguish features of
hylobatids (Fuentes 2000) and western gorillas (Bradley et al. behavior that have remained constant from those that have
2004) live. However, without understanding the ways in which changed over time. Thus, although our main study group’s
gibbons or western gorillas adjust their dispersal patterns un- home range has more than doubled in size, their day ranges
der varying demographic conditions, it is difficult to identify have remained constant, which is likely to reflect their shift
whether these extended male communities reflect a phylo- from cohesive to fluid grouping patterns as a way of adjusting
genetic propensity for male bonding among hominoids or a feeding requirements without increasing either distances trav-
proximate, behavioral solution to skewed sex ratios. eled or levels of overt feeding competition (Dias and Strier
2003).
Female-biased dispersal continues to predominate, but
Ecological Traps
some females have remained in their natal group and repro-
Behavioral plasticity is adaptive under changing environmen- duced earlier than the majority of females that successfully
tal (ecological and demographic) conditions, provided that disperse into one of the other three groups in this population
the match between cues and behavioral responses remains (Martins and Strier 2004). Females that remain and reproduce
accurate. But just as humans with rapid physiological and in their natal group may be at greater risk of inbreeding than
endocrinological stress responses may have an immediate ad- females that disperse unless they have been sired by extra-
vantage in fight-or-flight situations, chronically high stress group males or can recognize close relatives and avoid mating
levels can also lead to serious, even fatal, medical conditions with them. We know that copulations between mothers and
as a consequence of what would be an adaptive response to their mature sons are extremely rare, so there is reason to
acute stressful stimuli (Sapolsky 2002). Behavioral responses suspect they possess mechanisms of inbreeding avoidance
can become similarly disconnected from demographic cues (Strier 1997b). In addition, on two occasions, different co-
and with similarly serious consequences for the individuals horts of males from one group have maintained transient
and local populations involved. Consider, for example, the associations with other groups when their natal group fis-
consequences of habitat fragmentation, which severs gene sioned, copulating with females in different groups. Some
flow between small, isolated populations. In heavily frag- males were transient for more than a decade until they ul-
mented landscapes, such as what remains of southeastern Bra- timately followed their cohort by joining the new group that
zil’s Atlantic forest, adolescent female muriquis risk attacks arose from their natal group’s fissioning. This flexibility in
from feral dogs (and other predators) when they descend to dispersal patterns may reflect adaptive responses to increases

189.12.231.59 on Thu, 18 Feb 2021 03:22:44 UTC
in population density and increasingly male-biased sex ratios as they have been when adult sex ratios were more favorably
that lead to obvious predictions about other behavioral female biased, or will their egalitarian society begin to break
changes that may occur if the number of adult males relative down? Will the baseline levels of testosterone that males were
to females continues to rise (Strier et al. 2006). More relevant, found to exhibit year-round (Strier, Ziegler, and Wittwer
perhaps, is what observed deviations in dispersal patterns im- 1999) persist, or will their testosterone levels rise as compe-
ply about the routes by which dispersal patterns can shift in tition for access to females increases with the changes in adult
response to local demographic conditions and about the con- sex ratios?
sequences of these shifts for individual life histories and social Questions such as these are about behavioral (and endo-
dynamics within and between groups. crinological) responses to a changing demographic environ-
ment, and the outcome of these responses will affect the ge-
netics of this population as well as its viability. The answers
Diversions and Directions
to these questions require comparative data, whether from
I have focused on demography and how it changes over time different populations living under different but identifiable
and how behavioral responses to demographic, as well as demographic and ecological conditions or from the same pop-
ecological, changes provide insights into intraspecific varia- ulation whose ecology and demography has changed over
tion in behavior patterns. Demography is also a key com- time. Understanding the range of intraspecific variation in
ponent in assessing the viabilities of endangered populations, behavior and the thresholds at which different primates adjust
and my interest in demography can be traced directly to my their behavior provides insights into mechanisms and there-
long-term involvement with the current status and future of fore into the evolutionary adaptations and adaptive potentials
a critically endangered species. Because my field project trains of primate behavior. It is time to incorporate these attributes
new teams of Brazilian students on an annual basis, I have of intraspecific variation into the comparative methods
also been challenged to see the muriquis through a new set around which evolutionary models are based.
of eyes each year, and this has served as a constant reminder
of how different the muriquis are today from when I first Acknowledgments
met them in 1982, even though some of the original members
of that group are still alive. I am grateful to Jane Phillips-Conroy, Jeff Rogers, and Terry
During the first month of the training period in 1996, the Harrison for inviting me to participate in their conference
only adult males that the new students encountered were six “Evolutionary Anthropology at the Interface” (October 5–6,
transients that were following our females while our own 2007) and to New York University’s Center for the Study of
group’s males were off on their own in a remote part of their Human Origins and the Wenner-Gren Foundation for their
home range. The students did not understand why we referred support. I also thank Susan Alberts, Jonathon Marks, and
to the six males associating with our females as transients Sarie Van Belle for their comments on an earlier version of
until their second month on the project, when our group this manuscript.
males rejoined and remained with the females and the tran-
sient males disappeared. The current team of students is also
encountering a very different muriqui group, because in con-
trast to 1996, there are no transient males associating with Comments
our females right now. Observers in 2008 saw the 89 indi-
viduals in our main study group as members of a fluid society S. Peter Henzi and Louise Barrett
that routinely splits up and reunites and spends a considerable Department of Psychology, University of Lethbridge, Leth-
amount of its time resting and socializing on the ground bridge, Alberta T1K 3M4, Canada (peter.henzi@uleth.ca). 19
(Mourthé et al. 2007). This is very different from the cohesive IX 08
group of 23 individuals I habituated more than a quarter of
a century ago. We are encouraged by Karen Strier’s call for the recognition
As in the past, there are still more adult females than males, of the complex interplay of individual and population pro-
but a steady shift in infant sex ratios over the past 7 years cesses in the structuring of manifest behavior across space
has resulted in there now being twice as many males as females and time. Primatologists have generally lagged far behind
in the younger age classes in both our main group and the ecologists (Lomnicki 1988; Sutherland 1996) in their appre-
other groups in this population. The first male-biased age ciation of these dialectic forces (but see Dunbar 1984; Henzi,
cohort is beginning to reach sexual maturity, and the addition Lycett, and Piper 1997), a consequence, perhaps, of inherent
of these and subsequent cohorts to the adult breeding pop- difficulties in the gathering of detailed observational data in
ulation is likely to alter individual mating and reproductive the field and the subsequent sacrifice of breadth for varying
opportunities as well as the social dynamics within and be- degrees of depth.
tween this group and the other groups in the population. Will At the same time, however, a strong essentialist streak runs
this new generation of males be as tolerant of one another through primatology, stemming in part from its roots in an-

189.12.231.59 on Thu, 18 Feb 2021 03:22:44 UTC
thropology and reinforced by the empirical vigor of the so- ecology of wild primates, it also highlights the need for a
cioecological approach (Henzi and Barrett 2005). We still de- properly collaborative enterprise. Part of the reason why com-
fine monkey species in terms of their “despotism” or parative analysis serves species so poorly is tied to that other
“egalitarianism,” for example, despite strong theoretical rea- primatological touchstone, the field site, and the assumption
sons to suspect that individual strategies should be primed by the people who work there that their data are in some way
to vary in response to the strategies of others (Sutherland canonical rather than part of a broader reality. Publications,
1996) and empirical evidence that this is so (Henzi and Barrett consequently, very often talk past one another rather than
2007). The comparative approach to socioecological evolution strive for synthesis. If properly historical studies are to serve
that Strier rightly berates for its reductionist treatment of their subjects well, it would be best for us all to understand
species’ norms is essentialist not only for its snap judgments that what we know is only interesting in relation to what
about trait values but also for its reification of the species as others know. We would all be comparative analysts then.
the unit of analysis.
Strier’s arguments for the need to consider diachronic pro-
cesses in order to gauge a species’ range of response reflect a Robert D. Martin
reading of Cliff Jolly’s views (e.g., Jolly 2001). For the sake Department of Anthropology, The Field Museum, 1400
of conversation, because we broadly agree, we here use an- South Lake Shore Drive, Chicago, Illinois 60605-2496,
other of Jolly’s (1993) insights—that there are crucial evo- U.S.A. (rdmartin@fieldmuseum.org). 31 VII 08
lutionary processes happening below the level of the species—
to suggest that the goal of comparative investigation might Strier justifiably emphasizes the importance of a multilevel
better be the various constituents of the species itself (the intraspecific perspective on primate behavioral ecology, rais-
allotaxa that constitute it) rather than the derivation of a ing the core issue of intraspecific variability and its possible
species-level descriptor—no matter how comprehensive or correlates. This, in turn, underlines the crucial importance of
nuanced—to be submitted for interspecific comparison. long-term studies for achieving a proper understanding of
While this might misrepresent the scope of her argument, natural processes shaping primate behavior. Primates are
much of Strier’s paper seems to us to indicate that the point long-lived species with overlapping generations, so sound in-
of intraspecific ecological and demographic data collection is terpretation requires studies covering 25 years or more. Long-
to derive an understanding, through triangulation, of some term studies of individual primate species are rare, but their
measure, such as a norm of reaction, that typifies the species number is steadily growing, exemplified by Strier’s own long-
(Henzi and Barrett 2005). To the extent to which this is a fair term study of Brachyteles. We can only hope that major fund-
reflection, it continues to commit us to the idea of the species ing sources will recognize the unique value of long-term
as the unit of comparison on the grounds, we presume, that studies.
this is the field of gene recombination. As Strier notes, most primate field studies continue to be
Putting to one side the problems associated with the ap- relatively brief, and with gregarious species forming recog-
propriate designation of species, Jolly and his group’s un- nizable groups there is a long-standing tendency to focus on
folding of the complex history of Papio baboons, together a single main study group. Ironically, a population-level per-
with the demonstration that subspecific differences cannot be spective is more often developed in studies of “solitary” pri-
explained by current ecology (Bergman and Beehner 2004; mate species that do not live in social groups. Such species
Henzi and Barrett 2003), suggests that history, as a shaper of typically have well-developed social networks that can be ad-
response norms, goes all the way down and can at no point dressed only by examining populations.
be ignored. That is, it is not likely to be the case, very often Demographic variables are enormously important for a
(see Linklater 2000 for an apparent exception), that there will proper understanding of primate behavioral ecology. As Strier
be a uniform reaction norm characterizing the species. Or, shows, field primatologists initially tended to focus on ecology,
to put it another way, it will take more than an adjustment and awareness of demographic factors was slow to emerge.
of local ecology or demography to bring all allotaxa into line. However, this is largely due to the need for long-term studies
This is likely to be true for most taxa (see Ossi and Kamilar to obtain reliable demographic data, although cross-sectional
2006 for the Eulemur group). Consequently, the determina- surveys of several primate groups can yield some indication
tion of phenotypic distinctiveness within a taxon is more of demographic variables. Some short-term field studies have
pertinent than trying to square some kind of socioecological included such surveys, but one important take-home message
circle. To do so requires, in Jolly’s terms, a reconstruction of from Strier’s review is that more should be done. Short-term
the interplay between phenostructure and zygostructure. field studies will doubtless continue, notably as PhD projects,
What this means, of course, is both more work for everyone so cross-sectional demographic surveys should be built into
and a seriously integrative approach that brings together ge- study designs.
netics, ecology (current and paleo-), and behavior in the at- Newton’s (1988) analysis of data for social groups of the
tempt to parse a species’ history. Given the constraints of time Hanuman langur (Semnopithecus entellus) provides an in-
and money that face most of us who work on the behavioral structive example of cross-sectional intraspecific data. He used

189.12.231.59 on Thu, 18 Feb 2021 03:22:44 UTC
data from 24 populations to test hypotheses concerning in- significance with a second-order polynomial (r p 0.53 ; P p
fanticide, which is linked to single-male troops. Some have 0.060). In sum, Newton’s data set clearly shows that single-
interpreted infant killing by male langurs as adaptive, while male groups are relatively infrequent (reflected in high sex
others have seen it as a pathological consequence of high ratios) at both very low and high densities, whereas they are
population density. Newton concluded that troop structure common (reflected by low ratios) at intermediate densities.
is unrelated to population density. Unfortunately, this con- Laudably, while robustly advocating increased attention to
clusion illustrates Strier’s point that increased attention to intraspecific variation, Strier does not question the value of
statistical methods is needed in intraspecific analyses. Newton
interspecific comparisons. There is often a gulf between those
inherently assumed that any relationship between troop size
conducting penetrating studies of individual species and those
and population density must be linear. A simple correlation
carrying out (necessarily more superficial) studies of variation
is nonsignificant (r p 0.045; P p 0.852). As noted by Moore
across species by using average (hopefully representative) val-
(1999), the apparent lack of correlation between population
ues for individual species. In fact, full understanding of be-
density and infanticide has been cited as a fatal flaw in the
pathology hypothesis. Moore’s paper presents an economic- havioral ecology demands both approaches, which are united
defendability model explicitly rejecting a linear relationship by a common platform of correlation-based interpretation.
between social behavior and population density. In fact, a In principle, single-species studies have the advantage that
second-order polynomial fitted to Newton’s data reveals a experiments might clarify causal relationships. In practice,
significant curvilinear relationship (r p 0.56 ; P p 0.041; fig. experimentation with natural primate populations is largely
1). Male : female sex ratio shows an inverse curvilinear rela- prohibited. Most species are threatened in the wild, and field
tionship with population density. Again, a simple correlation primatologists (notably including Strier) now usually combine
based on assumed linearity indicates no trend whatsoever conservation with fundamental research. In this context, ex-
(r p 0.003; P p 0.991), but a curvilinear trend almost reaches perimentation to satisfy scientific curiosity is virtually un-
Figure 1. Relationships between frequency of single-male troops (top) or

sex ratio (bottom) and population density. Left, Simple correlations in-
dicate no significant associations, and least squares regressions indicate
no linear trends. Right, Second-order polynomials indicate curvilinear
trends in both cases, significant for frequency of single-male troops and
close to significance for sex ratio. (Data from Newton 1988.)

189.12.231.59 on Thu, 18 Feb 2021 03:22:44 UTC
thinkable. Hence, intraspecific and interspecific studies are in showing an annual pattern. As Strier notes, it is particularly
the same boat, and the best way forward is to combine forces. interesting to examine the relationship to seasonal food short-
Strier specifically stresses the need for improved methods age. A common response is reduction in activity, leading at
in intraspecific studies. This is all well and good, but the the extreme to complete cessation of activity in hibernating
“important advances” she notes in interspecific studies have dwarf lemurs (Cheirogaleus). However, some primate species
been a mixed blessing. One development arises from the ob- actually show the opposing strategy of increasing foraging
servation that data points for individual species in interspecific distance during seasonal food shortage. Exactly what drives
comparisons may not be statistically independent because of this contrast in strategies remains to be determined. However,
differential relatedness accompanied by “phylogenetic inertia” the key point is that interesting, complementary insights can
(Felsenstein 1985). Concern about this potential problem has be derived from interspecific and intraspecific studies of a
generated an extensive literature promoting methods designed particular variable in primate field studies.
to eliminate it, notably using “independent contrasts” (e.g.,
Garland, Midford, and Ives 1999; Harvey and Pagel 1991;
Martins 1996). However, there are several problems with both
the underlying rationale and its implementation (Martin,
Genoud, and Hemelrijk 2005; Ricklefs and Starck 1996). A Reply
major argument supporting the supposed prevalence of phy-
logenetic inertia was the apparent concentration of variability It is heartening to receive such thoughtful comments that
at high taxonomic levels. However, this is largely due to re- agree overall with the need for greater consideration of in-
stricted variation in body mass within taxa. Residual variation traspecific variation in behavioral analyses and that also offer
(reflecting divergent adaptation in scaling to body mass) is useful suggestions for advancing the field. Recognition of the
actually quite high at lower taxonomic levels. It is therefore importance of behavioral plasticity and its implications for
questionable whether biological variables are generally prone understanding intraspecific variation has continued to grow
to marked phylogenetic inertia lasting millions of years. Fur- (e.g., Struhsaker 2008; Thierry 2008), but the challenge of
thermore, calculation of independent contrasts has a major how to incorporate this kind of variation into comparative
drawback: it greatly exaggerates the influence of error terms models remains. Both the integration of studies that combine
and may therefore eradicate meaningful signals in data sets, genetics and paleoecology with contemporary socioecology,
particularly if assembled with insufficient attention to data as Henzi and Barrett advocate, and the development of ap-
quality. propriate analytical methods, as Martin proposes, represent
Curiously, the thinking that led to widely enforced appli- alternative and mutually compatible approaches for charac-
cation of independent contrasts in interspecific comparisons terizing and interpreting behavioral variation below the spe-
has seemingly not penetrated significantly to the intraspecific cies level and ultimately for increasing our understanding of
level. Yet inertia due to genetic relatedness must surely be far behavioral diversity among species and at higher taxonomic
more pronounced within species. In comparing the behavior levels.
of two primate social groups or populations, how can we Henzi and Barrett invoke allotaxa, morphologically distinct
partition observed differences between the influence of genetic forms that can interbreed (Jolly 2001), and deep history to
relatedness and effects of ecological or demographic factors? contextualize contemporary behavioral variation, as exem-
I make this comment not to promote heavy-handed statistical plified in their comparative analyses of baboons (Henzi and
intervention but (to paraphrase Felsenstein [1978, 27] from Barrett 2003, 2005). The persistence of allotaxa has been at-
another context) “to frighten field primatologists.” tributed to population fluctuations (Jolly 2001), which is con-
The complementary benefits of comparative analyses at sistent with my emphasis on the influence of demographic
both interspecific and intraspecific levels can be aptly illus- variation in populations but is extended to include a longer
trated by daily travel distance. It was initially reported that temporal perspective than even the longest-running field
there is an overall trend for average day-travel distance to study can provide. Nonetheless, to calibrate these deeper his-
increase with increasing body mass across primate species torical influences on behavior with the variation we observe
(Clutton-Brock and Harvey 1977a, 1977b). However, a still requires a comprehensive understanding of the range of
marked distinction in travel distance separates terrestrial from behavioral responses that primates, which are distributed into
arboreal species. Separate analysis reveals that travel distance populations, exhibit under the varied conditions they expe-
does not increase with body mass among arboreal primates rience during their life spans.
(Martin 1981). Regardless of body size, a typical arboreal The ranges of primate responses can be documented
primate travels about 1 kilometer per day. Exuberant species through careful comparisons of the particular conditions
travel more, while sluggish species travel less. This interspecific found in different populations, as Martin and others (e.g.,
perspective is useful for interpreting the average travel dis- Moore 1999) have shown, or through long-term studies of
tance of any arboreal primate species. However, daily travel particular populations, which have the advantage of also pro-
distance varies widely within individual species, commonly viding insights into the causal relationships between local eco-

189.12.231.59 on Thu, 18 Feb 2021 03:22:44 UTC
logical and demographic conditions and the behavioral re- Altmann, S. A., and J. Altmann. 1979. Demographic con-
sponses that changes in these conditions elicit. Long-term straints on behavior and social organization. In Primate
studies have the potential to identify these causal relationships ecology and human origins: ecological influences on social
through close observations of natural phenomena (Grant and organization. I. S. Bernstein and E. O. Smith, eds. Pp.
Grant 2002), even without the kinds of controlled experiments 47–63. New York: Garland STPM.
to which Martin alludes. Bergman, T. J., and J. C. Beehner. 2004. Social system of a
There is no doubt that field experiments could accelerate hybrid baboon group (Papio anubis # P. hamadryas). In-
our learning curve, but in addition to sharing Martin’s views ternational Journal of Primatology 25:1313–1330. [SPH/
about the ethical reasons against them, I will go a step further LB]
and suggest that many such experiments are actively under Bradley, B. J., D. M. Doran-Sheehy, D. Lukas, C. Boesch, and
way. However we might wish it otherwise, most wild primate L. Vigilant. 2004. Dispersed male networks in western go-
populations are already serving as experimental subjects in rillas. Current Biology 14:510–513.
the rapidly changing environments caused by anthropogenic Chance, M. R. A. 1961. The nature and special features of
activities, which range from local and regional disturbances the instinctive social bond of primates. In Social life of
to global climate change. The pace and scale of these changes early man. S. L. Washburn, ed. Pp. 17–33. Chicago: Aldine.
create new kinds of selection pressures that may or may not Clutton-Brock, T. H., and P. H. Harvey. 1977a. Primate ecol-
be continuous with the selection pressures to which primates ogy and social organization. Journal of Zoology (London)
have adapted in the past. We can learn a great deal about the 183:1–39. [RDM]
causal factors underlying both intra- and interspecific behav- ———. 1977b. Species differences in feeding and ranging
ioral variation if we can be in the field long enough to doc- behaviour in primates. In Primate ecology. T. H. Clutton-
ument how primates respond to the new challenges that we Brock, ed. Pp. 557–579. London: Academic Press. [RDM]
humans inadvertently pose. Cortés-Ortiz, L., T. F. Duda Jr., D. Canales-Espinosa, F.
The speed with which humans are altering the environment Garcı́a-Orduña, E. Rodrı́guez-Luna, and E. Bermingham.
has stimulated “contemporary evolution” in other organisms 2007. Hybridization in large-bodied New World primates.
(Stockwell, Hendry, and Kinnison 2003) and has implications Genetics 176:2421–2425.
for our assumptions about the adaptiveness of the behaviors de Melo, F. R., B. A. P. Cosenza, D. F. Ferraz, S. L. F. Souza,
we observe in primates today. Whether previously adaptive M. S. Nery, and M. J. R. Rocha. 2005. The near extinction
responses will continue to be adaptive or will lead to evo- of a population of northern muriquis (Brachyteles hypo-
lutionary traps under current conditions is not always clear xanthus) in Minas Gerais, Brazil. Neotropical Primates 13:
(Schlaepfer, Runge, and Sherman 2002). Analyses of the ef- 10–14.
fects of human impact on hybridization among cercopithecine Detwiler, K. M., A. S. Burrell, and C. J. Jolly. 2005. Conser-
monkeys by Jolly and his colleagues (Detwiler, Burell, and vation implications of hybridization in African cercopithe-
Jolly 2005) and among New World monkeys (e.g., Cortés- cine monkeys. International Journal of Primatology 26:
Ortiz et al. 2007) provide intriguing glimpses into the future 661–684.
evolutionary pathways that at least some primates may take. Dias, L. G., and K. B. Strier. 2003. Effects of group size on
I concur with Martin’s views on the complementarity of ranging patterns in Brachyteles arachnoides hypoxanthus.
intra- and interspecific studies. Both the units we compare— International Journal of Primatology 24:209–221.
whether populations, allotaxa, or unambiguous species—and Di Fiore, A., and D. Rendall. 1994. Evolution of social or-
the temporal scales we examine can lead to different kinds ganization: a reappraisal for primates by using phylogenetic
of insights into different kinds of behavioral variation with methods. Proceedings of the National Academy of Sciences,
different underlying causes. But it will be the behavioral re- U.S.A. 91:9941–9945.
sponses of contemporary populations to contemporary con- Dunbar, R. I. M. 1979. Population demography, social or-
ditions that determine which primates survive and which be- ganization, and mating strategies. In Primate ecology and
come extinct. Understanding these responses may be our best human origins: ecological influences on social organization.
chance of insuring that there will be primates in the future I. S. Bernstein and E. O. Smith, eds. Pp. 65–88. New York:
to compare. Garland STPM.
—Karen B. Strier ———. 1984. Reproductive decisions: an economic analysis
of gelada baboon social strategies. Princeton, NJ: Princeton
University Press. [SPH/LB]
References Cited Felsenstein, J. 1978. The number of evolutionary trees. Sys-
tematic Zoology 27:27–33. [RDM]
Altmann, J., S. C. Alberts, S. A. Haines, J. Dubach, P. Muruthi, ———. 1985. Phylogenies and the comparative method.
T. Coote, E. Geffen, et al. 1996. Behavior predicts genetic American Naturalist 125:1–15. [RDM]
structure in a wild primate group. Proceedings of the Na- Ferrari, S. F., H. K. M. Correa, and P. E. G. Coutinho. 1996.
tional Academy of Sciences, U.S.A. 93:5797–5801. The ecology of the “southern” marmosets (Callithrix aurita

fff:ffff:ffff:ffff:ffff:ffff:ffff on Thu, 01 Jan 1976 12:34:56 UTC
and Callithrix flaviceps). In Adaptive radiations of Neo- ———. 2001. A proper study for mankind: analogies from
tropical primates. M. A. Norconk, A. L. Rosenberger, and the papionin monkeys and their implications for human
P. A. Garber, eds. Pp. 157–171. New York: Plenum. evolution. Yearbook of Physical Anthropology 44:177–204.
Fuentes, A. 2000. Hylobatid communities: changing views on Jolly, C. J., and J. E. Phillips-Conroy. 2006. Testicular size,
pair bonding and social organization in hominoids. Year- developmental trajectories, and male life history strategies
book of Physical Anthropology 43:33–60. in four baboon taxa. In Reproduction and fitness in ba-
Garland, T., Jr., P. E. Midford, and A. R. Ives. 1999. An in- boons: behavioral, ecological, and life history perspectives.
troduction to phylogenetically based statistical methods, L. Swedell and S. R. Leigh, eds. Pp. 257–275. New York:
with a new method for confidence intervals on ancestral Springer.
values. American Zoologist 39:374–388. [RDM] Jones, C. B. 2005. Behavioral flexibility in primates: causes
Glander, K. E. 2006. Average body weight for mantled howling and consequences. New York: Springer.
monkeys (Alouatta palliata): an assessment of average val- Lee, P. C. 1994. Social structure and evolution. In Behaviour
ues and variability. In New perspectives in the study of and evolution. P. J. B. Slater and T. R. Halliday, eds. Pp.
Mesoamerican primates: distribution, ecology, behavior, 266–337. Cambridge: Cambridge University Press.
and conservation. A. Estrada, P. A. Garber, M. Pavelka, and Linklater, W. L. 2000. Adaptive explanation in socio-ecology:
L. Luecke, eds. Pp. 247–263. New York: Springer. lessons from the Equidae. Biological Reviews 75:1–20.
Gould, J. L. 1982. Ethology: the mechanisms and evolution [SPH/LB]
of behavior. New York: Norton. Lomnicki, A. 1988. Population ecology of individuals. Prince-
Grant, P. R., and B. R. Grant. 2002. Unpredictable evolution ton, NJ: Princeton University Press. [SPH/LB]
in a 30-year study of Darwin’s finches. Science 296: Mace, G. M. 2004. The role of taxonomy in species conser-
707–711. vation. Philosophical Transactions of the Royal Society
Harvey, P. H., and M. D. Pagel. 1991. The comparative London B: Biological Sciences 359:711–719.
method in evolutionary biology. Oxford: Oxford University Marks, J. 2007. Anthropological taxonomy as both subject
Press. and object: the consequences of descent from Darwin and
Henzi, S. P., and L. Barrett. 2003. Evolutionary ecology, sexual Durkheim. Anthropology Today 23:7–12.
conflict, and behavioral differentiation among baboon pop- Martin, R. D. 1981. Field studies of primate behaviour. Sym-
ulations. Evolutionary Anthropology 12:217–230. posia of the Zoological Society of London 46:287–336.
———. 2005. The historical socioecology of savannah ba- [RDM]
boons (Papio hamadryas). Journal of Zoology (London) Martin, R. D., M. Genoud, and C. K. Hemelrijk. 2005. Prob-
265:215–226. lems of allometric scaling analysis: examples from mam-
———. 2007. Coexistence in female-bonded primate groups. malian reproductive biology. Journal of Experimental Bi-
Advances in the Study of Behaviour 37:43–81. [SPH/LB] ology 208:1731–1747. [RDM]
Henzi, S. P., J. E. Lycett, and S. E. Piper. 1997. Fission and Martins, E. P., ed. 1996. Phylogenies and the comparative
troop size in a mountain baboon population. Animal Be- method in animal behavior. New York: Oxford University
haviour 53:525–535. [SPH/LB] Press. [RDM]
Hohmann, G. 2001. Association and social interactions be- Martins, W. P., and K. B. Strier. 2004. Age at first reproduction
tween strangers and residents in bonobos (Pan paniscus). in philopatric female muriquis (Brachyteles arachnoids hy-
Primates 42:91–99. poxanthus). Primates 45:63–67.
Isaac, N. J., J. Mallet, and G. M. Mace. 2004. Taxonomic May, R. M., and J. Seger. 1986. Ideas in ecology. American
inflation: its influence on macroecology and conservation. Scientist 74:256–267.
Trends in Ecology and Evolution 19:464–469. Maynard Smith, J. 1978. Optimization theory in evolution.
Jacobs, L. F., S. J. Gaulin, D. F. Sherry, and G. E. Hoffman. Annual Review of Ecology and Systematics 9:31–56.
1990. Evolution of spatial cognition: sex-specific patterns Mendes, S. L., F. R. de Melo, J. P. Boubli, L. G. Dias, K. B.
of spatial behavior predict hippocampal size. Proceedings Strier, L. P. S. Pinto, V. Fagundes, B. Consenza, and P. De
of the National Academy of Sciences, U.S.A. 87:6349–6352. Marco Jr. 2005. Directives for the conservation of the
Jay, P. C., ed. 1968. Primates: studies in adaptation and var- northern muriqui, Brachyteles hypoxanthus (Primates, Atel-
iability. New York: Holt, Rinehart & Winston. idae). Neotropical Primates 13(suppl.):7–18.
Jolly, A. 1985. The evolution of primate behavior. New York: Moore, J. 1984. Female transfer in primates. International
Macmillan. Journal of Primatology 5:537–589.
Jolly, C. J. 1970. The seed-eaters: a new model of hominid ———. 1999. Population density, social pathology, and be-
differentiation based on a baboon analogy. Man 5:5–26. havioral ecology. Primates 40:1–22.
———. 1993. Species, subspecies, and baboon systematics. Mourthé, I., D. Guides, J. Fidelis, J. P. Boubli, S. L. Mendes,
In Species, species concepts, and primate evolution. W. H. and K. B. Strier. 2007. Ground use by northern muriquis
Kimbel and L. B. Martin, eds. Pp. 67–107. New York: (Brachyteles hypoxanthus). American Journal of Primatol-
Plenum. ogy 69:706–712.

189.12.231.59 on Thu, 18 Feb 2021 03:22:44 UTC
Newton, P. 1988. The variable social organization of Hanu- Social life of early man. S. L. Washburn, ed. Pp. 58–90.
man langurs (Presbytis entellus), infanticide, and the mo- Chicago: Aldine.
nopolization of females. International Journal of Prima- Stockwell, C. A., A. P. Hendry, and M. T. Kinnison. 2003.
tology 9:59–77. [RDM] Contemporary evolution meets conservation biology.
Nunn, C. L., and R. A. Barton. 2001. Comparative methods Trends in Ecology and Evolution 18:94–101.
for studying primate adaptation and allometry. Evolution- Strier, K. B. 1994. Myth of the typical primate. Yearbook of
ary Anthropology 10:81–98. Physical Anthropology 37:233–271.
Ossi, K., and J. M. Kamilar. 2006. Environmental and phy- ———. 1997a. Behavioral ecology and conservation biology
logenetic correlates of Eulemur behavior and ecology (Pri- of primates and other animals. Advances in the Study of
mates: Lemuridae). Behavioral Ecology and Sociobiology Behavior 26:101–158.
61:53–64. [SPH/LB] ———. 1997b. Mate preferences of wild muriqui monkeys
Pope, T. R. 1990. The reproductive consequences of male (Brachyteles arachnoides): reproductive and social corre-
cooperation in the red howler monkey: paternity exclusion lates. Folia Primatologica 68:120–133.
in multi-male and single-male troops using genetic mark- ———. 2000. From binding brotherhoods to short-term sov-
ers. Behavioral Ecology and Sociobiology 27:439–446. ereignty: the dilemma of male Cebidae. In Primate males:
———. 1998. Effects of demographic change on group kin causes and consequences of variation in group composi-
structure and gene dynamics of populations of red howling tion. P. M. Kappeler, ed. Pp. 72–83. Cambridge: Cambridge
monkeys. Journal of Mammology 79:692–712. University Press.
———. 2000. Reproductive success increases with degree of ———. 2004. Patrilineal kinship and primate behavior. In
kinship in cooperative coalitions of female red howler mon- Kinship and behavior in primates. B. Chapais and C. M.
keys (Alouatta seniculus). Behavioral Ecology and Socio- Berman, eds. Pp. 177–199. Oxford: Oxford University
biology 48:253–267. Press.
Richard, A. F. 1985. Primates in nature. New York: W. H. Strier, K. B., J. P. Boubli, C. B. Possamai, and S. L. Mendes.
Freeman. 2006. Population demography of northern muriquis
Ricklefs, R. E., and J. M. Starck. 1996. Applications of phy- (Brachyteles hypoxanthus) at the Estação Biológica de Cara-
logenetically independent contrasts: a mixed progress re- tinga/Reserva Particular do Patrimônio Natural-Feliciano
port. Oikos 77:167–172. [RDM] Miguel Abdala, Minas Gerais, Brazil. American Journal of
Ricklefs, R. E., and M. Wikelski. 2002. The physiology/life Physical Anthropology 130:227–237.
history nexus. Trends in Ecology and Evolution 17: Strier, K. B., and S. L. Mendes. 2009. Long-term field studies
462–468. of South American primates. In South American primates:
Robbins, M. M. 1995. A demographic analysis of male life comparative perspectives in the study of behavior, ecology,
history and social structure of mountain gorillas. Behaviour and conservation. P. A. Garber, A. Estrada, J. C. Bicca-
132:21–47. Marques, E. W. Heymann, and K. B. Strier, eds. Pp.
———. 2001. Variation in the social system of mountain 139–155. New York: Springer.
gorillas: the male perspective. In Mountain gorillas. M. M. Strier, K. B., T. E. Ziegler, and D. Wittwer. 1999. Seasonal and
Robbins, P. Sicotte, and K. J. Stewart, eds. Pp. 29–58. Cam- social correlates of fecal testosterone and cortisol in wild
bridge: Cambridge University Press. male muriquis (Brachyteles arachnoides). Hormones and
Rosenberger, A. L., and W. G. Kinzey. 1976. Functional pat- Behavior 35:125–134.
terns of molar occlusion in platyrrhine primates. American Struhsaker, T. T. 2000. Variation in adult sex ratios of red
Journal of Physical Anthropology 45:281–298. colobus monkey social groups: implications for interspe-
Rylands, A. B., R. A. Mittermeier, and E. Rodrı́guez Luna. cific comparisons. In Primate males: causes and conse-
1995. A species list for the New World primates (Platyr- quences of variation in group composition. P. M. Kappeler,
rhini): distribution by country, endemism, and conserva- ed. Pp. 108–119. Cambridge: Cambridge University Press.
tion status according to the Mace-Land system. Neotropical ———. 2008. Demographic variability in monkeys: impli-
Primates 3(suppl.):113–160. cations for theory and conservation. International Journal
Sapolsky, R. M. 2002. Endocrinology of stress response. In of Primatology 29:19–34.
Behavioral endocrinology. 2nd edition. J. B. Becker, S. M. Sutherland, W. J. 1996. From individual behaviour to pop-
Breedlove, D. Crews, and M. McCarthy, eds. Pp. 409–450. ulation ecology. Oxford: Oxford University Press. [SPH/
Cambridge: MIT Press. LB]
Schlaepfer, M. A., M. C. Runge, and P. W. Sherman. 2002. Swedell, L. 2006. Strategies of sex and survival in hamadryas
Ecological and evolutionary traps. Trends in Ecology and baboons: through a female lens. Upper Saddle River, NJ:
Evolution 17:474–480. Pearson Prentice Hall.
Schultz, A. H. 1961. Some factors influencing the social life Tattersall, I. 2007. Madagascar’s lemurs: cryptic diversity or
of primates in general and of early man in particular. In taxonomic inflation? Evolutionary Anthropology 16:12–23.

189.12.231.59 on Thu, 18 Feb 2021 03:22:44 UTC
Thierry, B. 2008. Primate socioecology, the lost dream of eco- ests. In New perspectives in the study of Mesoamerican
logical determinism. Evolutionary Anthropology 17:93–96. primates: distribution, ecology, behavior, and conservation.
Tinbergen, N. 1951. The study of instinct. New York: Oxford A. Estrada, P. A. Garber, M. Pavelka, and L. Luecke, eds.
University Press. Pp. 121–142. New York: Springer.
Van Belle, S., and A. Estrada. 2006. Demographic features of Washburn, S. L., ed. 1961. Social life of early man. Chicago:
Alouatta pigra populations in extensive and fragmented for- Aldine.

189.12.231.59 on Thu, 18 Feb 2021 03:22:44 UTC

This Content Downloaded From 189.12.231.59 On Thu, 18 Feb 2021 03:22:44 UTC

Uploaded by

Copyright:

Available Formats

This Content Downloaded From 189.12.231.59 On Thu, 18 Feb 2021 03:22:44 UTC

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

This Content Downloaded From 189.12.231.59 On Thu, 18 Feb 2021 03:22:44 UTC

Uploaded by

Copyright:

Available Formats

Seeing the Forest through the Seeds: Mechanisms of Primate Behavioral Diversity from

Individuals to Populations and Beyond

This content downloaded from

Seeing the Forest through the Seeds

This content downloaded from

This content downloaded from

This content downloaded from

This content downloaded from

This content downloaded from

This content downloaded from

This content downloaded from

This content downloaded from

This content downloaded from

This content downloaded from

Figure 1. Relationships between frequency of single-male troops (top) or

This content downloaded from

This content downloaded from

This content downloaded from

This content downloaded from

This content downloaded from

This content downloaded from

You might also like

Pfad - The Proxy pFad of © 2024 Garber Painting. All rights reserved.