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199
L.K. Marsh and C.A. Chapman (eds.), Primates in Fragments: Complexity
and Resilience, Developments in Primatology: Progress and Prospects,
DOI 10.1007/978-1-4614-8839-2_14, © Springer Science+Business Media New York 2013
Abstract An increasing number of fi eld studies on behavioral adaptations and
learning suggest that a capacity for fl exibility in local responses to disturbance
could buffer some so-called specialists against that disturbance. We discuss how
specialization, rather than an intrinsic species trait, appears to be moderated by fl ex-
ible and learned behavior and may not represent a useful trait in comparative analy-
ses of extinction vulnerability. Furthermore, the use of primate species as indicators
of the effects of disturbance on communities needs to be balanced with data on their
capacity to adjust behaviorally. We present recent examples of innovative and fl ex-
ible behavior in primate taxa, some of which have traditionally been viewed as
highly specialized, for example species of red colobus. We also highlight research
gaps in the ecological specialization–behavioral fl exibility domain.
Introduction
We have come a long way since thinking of animal behavior as instinctive or pre-
suming that the behavior of an entire species can be described on the basis of a single
study of one group at one location. Today, it has become fashionable to study “behav-
ioral fl exibility,” but are we seeing more examples of it in nature? There is a rapidly
growing literature on this topic associated with a proliferation of interrelated termi-
nology: cognitive ecology (Dukas 1998 ), behavioral diversity (Whiten et al. 2001 ),
Chapter 14
“Specialist” Primates Can Be Flexible
in Response to Habitat Alteration
Katarzyna Nowak and Phyllis C. Lee
K . N o w a k ( *)
Udzungwa Ecological Monitoring Center , P.O. Box 99 , Mang’ula, Morogoro , Tanzania
e-mail: knowak02@gmail.com
P. C. Lee
Behavior and Evolution Research Group , Psychology, University of Stirling ,
Stirling FK9 4LA , UK
e-mail: phyllis.lee@stir.ac.uk
200
behavioral plasticity ( Pigliucci 2001 ; Wcislo 1989 ), behavioral geography (van
Schaik 2003 ; van Schaik et al. 2008 ), ecotypic variation (Turesson 1922 ), and
ecological fi tting (Agosta and Klemens 2008 ). Following an early defi nition (Poirier
1969 ), here we defi ne behavioral fl exibility generally as adjustments of an organism
in response to ecological conditions and changes.
There are several potential explanations for the current interest in behavioral
fl exibility in primatology: (1) When observing behavior, we measure performance
and cannot detect the capacity for fl exibility until it becomes manifest with changes
in conditions, and given the increasingly mosaic, unpredictable, and dynamic envi-
ronments inhabited by primates, we are now recording apparently novel behaviors
under such changed and changing environments (Marsh 2003 ); (2) fl exibility is
masked by single-population studies that are then generalized to the species, and we
now increasingly draw on multiple-group and multiple-population studies to make
sense of observed variability (Chapman and Rothman 2009 ; Strier 2009 ); (3) we as
observers are becoming more astute at detecting and identifying fl exibility, in part
thanks to emerging fi eld methods and in part because of baseline and long-term
datasets on which basis we can now recognize newly acquired behavior. We can still
ask: Is this apparent increase in reports of fl exibility substantiated—was fl exibility
always there or is it increasingly selected and evident as human disturbance becomes
more widespread and primates inhabit anthropogenic ecotones, forest edges, or
move into radically novel, but less disturbed habitats such as mangrove swamps?
The importance of the existence or emergence of fl exibility is illustrated in that if
behavioral fl exibility is the rule rather than exception, why has it not been consid-
ered in projections of primate extinction risk and why does it continue to be rela-
tively neglected in ecological literature (Sol 2003 ), particularly when ecological
specialization is suggested to be a major correlate of nonhuman primate extinction
risk (Harcourt et al. 2002 )?
These confl icting perspectives are highlighted in that broadly adapted species
are thought to do well in anthropogenic environments and to resist extinction (birds:
Bennett et al. 2005 ; primates: Harcourt 2000 ; Harcourt et al. 2002 ; bats: Boyles and
Storm 2007 ) by comparison to niche specialists. However, other studies have failed
to detect any relationship between specialization and extinction risk (birds: Sol
et al. 2002 ; plant–pollinator communities: Vázquez and Simberloff 2002 ; mammals:
Brashares 2003 ; bats: Safi and Kerth 2004 ). The latter studies analyzed specialization
as an intrinsic trait using measures such as the number of habitat types occupied,
niche breadth, diversity of interaction partners, species to genus ratio, maximum
latitudinal range, and morphology (see Colles et al. 2009 for “ideal” identifi cation
of specialization). Comparative primate studies suggest that less specialized taxa
have wider geographical ranges and that rarity (an “inevitable precursor to extinc-
tion”; Harcourt et al. 2002 , p. 445) has only one correlate in the Primate order:
dietary specialization. While a specifi c dietary guild predicts primates’ use of and
success in fragments (Boyle and Smith 2010 ), fl exible and learned behavioral
responses to dynamic ecosystems may capacitate resilience (Dukas and Ratcliffe
2009 ; Jones 2005 ; Reader and Laland 2003 ), although the links between special-
ization, behavioral fl exibility, and extinction risk in primates remain unclear.
K. Nowak and P.C. Lee
201
Primates may be able to “spread the risks” of extinction (Vázquez and Simberloff
2002 ) specifi cally through this behavioral fl exibility.
Behavioral fl exibility among primates in human altered environments includes
dietary and habitat switching, use of invasive and nonnative plant species, opportun-
ism, novel or more frequent interspecifi c and polyspecifi c interactions, and increased
terrestriality. Dietary shifts appear to make up the majority of documented innova-
tions (Reader and Laland 2003), with costs likely to differ across dietary guilds
(e.g., fruits are less likely to contain toxins). Bigger-brained primates are more inno-
vative (Reader and Laland 2002 ); but what remains to be examined is whether “spe-
cialists” are relatively less innovative and smaller-brained.
Large brains relative to body size are generally accepted as advantageous in
facilitating behavioral fl exibility for individuals facing novel or altered environ-
ments (the “cognitive buffer hypothesis”). For example, Sol et al. ( 2002 , 2007 )
found that big-brained birds have higher invasion success and that big-brained
mammals survive better following introductions (Sol et al. 2008 ). Yet again, the
evidence is contradictory in that big-brained birds are not less extinction-prone
(Nicolakakis et al. 2003 ). Even primates, such as lemurs with relatively small brain
to body ratios, switch diets and habitats when faced with environmental disturbance
or variation in abundance (e.g., Lemur catta , Soma 2006 ) which begets the further
question: is there any causal relationship between relative brain size, dietary spe-
cialization, and the capacity for behavioral fl exibility?
Leaving aside the question of cognitive capacity and ability to cope with environ-
mental disturbance, at least 48 % of primate species and subspecies are already
threatened with extinction (IUCN Red List 2010 ). Whatever categories of risk are
used, no single measure will capture traits of both vulnerability and persistence. We
suggest that the extent of behavioral diversity across populations and subpopula-
tions of the same species indicate the ability to adjust responses and act adaptively
in heterogeneous habitats. We refer to fl exibility here as encapsulating behavioral
modifi cation of diet, exploitation of alternative food sources, and changing activity
and typically used vertical strata in response to new foods or substrate opportunities.
The ability to expand niche breadth via resource-switching is key to withstanding
risks due to habitat modifi cation (Lee 2003 ).
Recent Examples of Behavioral Flexibility
For many primates, local fl exibility and reactive responses to habitat changes are
broadly part of their selective history. Island or coastal populations have always
been subject to catastrophic large-scale habitat modifi cation due to tropical storms
or hurricanes (Dittus 1985 ; Rebecchini et al. 2008 ). In many areas of low rainfall in
Africa, nonequilibrium ecosystems are the norm (Niamir-Fuller 2002 ), again mean-
ing that primates which live in such habitats probably have evolved to cope with the
unpredictable and noncyclical dynamics of their habitats (de Vries
1992 ; Lee and
Hauser 1998 ). Thus, we should not be wholly surprised by examples of major
14 “Specialist” Primates Can Be Flexible in Response to Habitat Alteration
202
dietary shifts such as black-and-gold howlers ( Alouatta caraya ) preying on birds’
nests in impoverished habitat fragments (Bicca-Marques et al. 2009 ), innovative
fi shing by long-tailed macaques ( Macaca fascicularis ) (Stewart et al. 2008 ), or
prey-capture and meat-eating by Sichuan snub-nosed monkeys ( Rhinopithecus
bieti ) in Yunnan, China ( Ren et al. 2009 ).
The capacity to exploit nonnative species when natural species are limited is also
common; for example hamadryas baboons ( Papio hamadryas ) use palm trees rather
than cliffs as sleeping sites in Ethiopia (Schreier and Swedell 2008 ) and howlers
( Alouatta palliata ) forage in cacao plantations (Munoz et al. 2006 ) and inhabit shade
coffee plantations (McCann et al. 2003 ). Black-and-white colobus ( Colobus guer-
eza ) live in the Entebbe Botanical Gardens, Uganda eating novel foods without
changing their species-typical home range size (Grimes and Paterson
2000 ), while
the endangered lion-tailed macaques ( Macaca silenus ) can subsist off exotic food
items such as tea, eucalyptus, and coffee in the Anaimalai Hills, India (Singh et al.
2001 ). A single population of Udzungwa red colobus ( Procolobus gordonorum ) in
Tanzania, having lost the small isolated Kalunga forest to agriculture in the early
2000s, now inhabit an adjacent rubber ( Hevea brasiliensis ) plantation eating leaves,
buds, and fruit; how long they can persist is open to question, as the decline of the
subpopulation from an estimated 400 to 50 individuals since 2007 suggests that the
plantation habitat is not ideal (Ehardt et al. 1999 ; Marshall et al. in press ; pers.
comm. with Ruth Steel and Andrew Marshall 2010). Like other red colobus which
exploit habitats with low plant species diversity (Zanzibar red colobus P. kirkii in
mangroves: Nowak 2008 ), these colobus crop-raid in the surrounding agricultural
matrix to supplement their monotonous diet (Fig. 14.1 ). As a result, they are perse-
cuted by people (Marshall et al. in press ). Agro-forests are likely to be better refuges
for wildlife, from birds to elephants and including primates, than are plantations
Fig. 14.1 A Zanzibar red colobus ( P. kirkii ) eating a young coconut. Photo by Katarzyna Nowak
K. Nowak and P.C. Lee
203
(Bhagwat et al. 2008 ), where even the most behaviorally fl exible of species may
not persist for long, at least not without access to other/additional habitat and
vegetation types.
Although high dietary diversity is proposed to buffer primates against extinction
(Harcourt et al. 2002 ), primates can and do exchange a high dietary diversity for
reliability in availability. For example the Sulawesi Tonkean macaque ( Macaca
tonkeana ) has a diet of >50 % palm fruits in fragmented forest (Riley 2007 ), while
a Zanzibar red colobus population in a fragmented coastal forest have a diet that is
>47 % mangrove (Nowak 2008 ). The white-collared lemur ( Eulemur cinereiceps )
eats fungi and nonnative plants such as the spicy fruits of Cameroon cardamon
( Aframomum angustifolium ) in highly degraded environments possibly avoiding
competition with sympatric lemur species. “Such dietary fl exibility and opportunis-
tic behavior may prove to be the key to survival of this critically endangered lemur
in an ever-changing and often challenging landscape” (Ralainasolo et al. 2008 ,
p. 43). Again, no simple correlation between survival probabilities and dietary
diversity exists. Dietary diversity may be better treated as facultative, rather than
obligate, for many primates (Johns and Skorupa 1987 ).
The interplay between diversity and selectivity can result in greater risk when
habitats change; species which are highly selective indeed suffer from the loss of
key resources (e.g., vervet monkeys Chlorocebus aethiops : Lee and Hauser 1998 ,
despite being generally considered to be opportunistic feeders with diverse diets).
Low selectivity and high opportunism enhance resilience (Sichuan snub-nosed
monkeys in commercially logged areas: Guo et al. 2008 ; Sulawesi Tonkean
macaques in farms: Riley and Priston 2010 ).
Entirely new mechanisms for exploiting altered habitats are also widespread.
Shifting from arboreal to terrestrial travel is a frequent response to fragmentation,
especially if the risks of predation are relatively low (e.g., northern muriqui
Brachyteles hypoxanthus : Mourthe et al. 2007 ). Ground travel by black howler
monkeys ( Alouatta pigra ) has been observed in forest fragments in Mexico, as
well as water foraging (Pozo-Montuy and Serio-Silva 2006 ). Water scarcity,
which may present increasing challenges for primates with climate change, also
prompts innovative behavior, for example Acacia tortilis pod-dipping by vervets
(Hauser 1988 ). Extreme habitats lead to innovative reliance on water-collecting
species like bromeliads for capuchins ( Sapajus apella : Brown and Zunino 1990 )
or cycads for Zanzibar red colobus exploiting disturbed coral rag forest (Nowak
and Lee 2011a , b ). When alternatives to disturbed or degraded habitats are avail-
able (for example, mangrove swamps), even so-called specialists, such as red
colobus, can successfully exploit these (Galat-Luong and Galat 2005 ; Nowak
2008 ). Facultative use of swamps and wetlands may become obligate if primates’
upland, preferred habitats are heavily disturbed (Nowak in press ; Quinten et al.
2009 ), suggesting that habitat preferences may be poor indicators of primary pref-
erences, degree of disturbance, or fl exibility (Pozo-Montuy et al. 2011 ). Enforced
habitat shifts can benefi t a population if the new habitat offers a safer, possibly
less seasonal environment; the already swamp- obligate Allen’s swamp monkey
( Allenopithecus nigroviridis ) may evade human disturbance for these reasons
(of Least Concern; IUCN Red List 2010 ).
14 “Specialist” Primates Can Be Flexible in Response to Habitat Alteration
204
Species which colonize unfamiliar forest patches or are translocated into areas
outside their natal range may have to shift diets and foraging strategies to include
novel foods (e.g., Alouatta pigra : Silver and Marsh 2003 ). The Zanzibar red colobus
has been successfully translocated to a plantation forest and introduced to a novel,
but protected, area on Pemba Island outside its natural range (Camperio Ciani et al.
2001 ). This species shows higher colonizing ability than would be expected given
traditional models of colobus socioecology and the fact that red colobus cannot
survive in captivity (Fig. 14.2 ).
How Constrained Are Primates by Their Physiology
and Metabolism?
It has long been argued that gut physiology limits the capacity for primates to be
both frugivorous and folivorous in equal proportions (Chivers 1994 ). However, evi-
dence of alternative switching between digestive types (structural vs. simple carbo-
hydrate) is more common than used to be thought. Southern muriquis ( Brachyteles
arachnoides ) facultatively alter their digestive regimes from fruit to leaf as a func-
tion of food availability (Talebi and Lee 2008 ) and the digestively specialized fru-
givorous white-handed gibbon ( Hylobates lar ) subsists off leaf material in selectively
logged areas (Johns 1986 ). Senegal red colobus ( Procolobus badius temmincki ) in
Fathala’s forest in the Saloum Delta National Park shift from folivory to frugivory
where their habitat has become degraded and during times of food shortage; fruits
represented up to 50 % observations of feeding, while the number of species in their
Fig. 14.2 Subadult P. kirkii grooming a calf. Photo by Katarzyna Nowak
K. Nowak and P.C. Lee
205
diet decreased by 50 % (Diouck 2002 ). Translocated howler monkeys ( Alouatta
pigra ) feed longer on fruit (Silver and Marsh 2003 ), and lianas are an important
food source for brown howlers ( Alouatta guariba ) and southern muriquis in dis-
turbed forests (Martins 2009 ). Innovations such as charcoal-eating by Zanzibar red
colobus can potentially overcome the ingestion of toxins from nonnative plants,
such as Indian almonds and mangoes (Struhsaker et al. 1997 ), and possibly from
mangroves as well. Bamboo lemurs are exceptionally specialized and among the
smallest herbivores in existence. However, the vulnerable rusty-gray lesser bamboo
lemur ( Hapalemur meridionalis ) can supplement its bamboo diet by grazing on
grass species (Poaceae), thus allowing it to forage outside forest habitats (Eppley
and Donati 2009 ). Its digestive processing is faster than would be predicted for such
a small and specialized herbivore.
Questions About Flexibility
The questions we raise are: Do specialist primates persist because:
1. They are not specialists? If so, we suggest that the defi nition of a specialist needs
reconsideration, taking into account those examples where physiology, foraging
behavior, dietary breadth, and exploitation of exotic, naturally disturbed or
anthropogenic habitats varies over time with species persistence.
2. They are specialists and are at risk? Their fl exible responses are short-term and
transitory with a time lag between apparently fl exible responses and their ulti-
mate population collapse (Struhsaker pers. comm. 2008).
3. Do specialist primates persist because specialization is mediated by behavior
(and especially learning in primates)? As noted above, opportunistic behavior,
innovation, and social fl exibility (e.g., uni-male howler monkey, Alouatta palli-
ata, groups in shade coffee plantations, McCann et al. 2003 ; fi ssion-fusion in the
genera of red colobus inhabiting human-disturbed forests ( P. gordonorum,
Marshall et al. 2005 ; P. kirkii, Nowak 2007 and Nowak and Lee 2011a , b ) can all
allow for population persistence (Lee 2003 ).
4. Specialization is not a single “trait”? Rather it represents three separate but inter-
acting components: ecological, behavioral, and functional or morphological
(Irschick et al. 2005 ); each component represents phylogenetic and evolved
responses to past environments but as these traits are not necessarily linked they
thus can co-vary in response to environmental dynamics.
5. Does a relationship between specialization and population responses to disturbance
at a species level exist (Vázquez and Simberloff 2002 )? Rather, species may
exhibit asymmetries, as well as variance, in their capacities to respond to disturbance.
Generalists should therefore receive as much conservation attention as specialists
(Colles et al. 2009 ).
Clearly, the relationships between behavioral fl exibility, the specialist–generalist
continuum, and extinction probability or risk require further exploration in both
14 “Specialist” Primates Can Be Flexible in Response to Habitat Alteration
206
comparative analyses and at the population level. We need better measures of spe-
cialization, of resource dynamics and the ability to model the consequences for
sociality (Chapman and Rothman 2009 ; Strier 2009 ) and for reproductive rates
(Cowlishaw et al. 2009 ; Lee and Hauser 1998 ). In addition, we have almost no asso-
ciations between habitat or diet type and reproductive rate or reproductive output for
comparative analyses of resilience (Lee and Kappeler 2003 ; but see Ross 1992 ).
We know that many specialists can compensate for morphological specializa-
tions and that behavioral alternatives can evolve alongside established specializa-
tions (Wcislo 1989 ), rendering specialization alone inadequate in extinction
forecasts; while specialization can be useful for predicting potential risks, the con-
struct does not necessarily predict what happens while a population is at risk.
Specialization, we suggest, is a local population phenomenon, rather than a species
intrinsic trait (Fox and Morrow 1981 ) and specialists and generalists appear not to
be types, but temporary states as a response, and fi ne-tuned, to local conditions
(e.g., primate diets at local scales: Chapman and Chapman 1990 , 1999 ; Chapman
et al. 2002 ). Behavioral fl exibility may be a mechanism for response generalization
in specialists with relatively nonplastic traits (e.g., constraints due to body size,
dental or skeletal morphology, locomotory mode).
Fimbel ( 1994 ) notes the hazard of generalizing about ecological correlates of
species failure or success in disturbed habitats, emphasizing that such correlates are
often site- or disturbance-specifi c. Furthermore, the ability to use human-modifi ed
habitats—although an alleged determinant of extinction proneness—has not been
found to be associated with any single suite of traits (Laurance 1991 ). We might
therefore learn more about extinction by studying populations that survive and per-
sist following episodes of biological impoverishment than by searching for causes
of extinction (Vermeij 1986 ). Investigating the signifi cance of behavioral fl exibility
for survival in a systematic way could inform conservation action plans, and be
valuable for the study of extinction biology (Strier 2009 ); however, as long as gen-
eral patterns continue to be sought, we will carry on fi nding high variability and
heterogeneity in primates’ responses to disturbance at the species level (Cowlishaw
et al. 2009 ). It has long been recognized that intraspecifi c comparative work is
imperative before, if at all, any particular behavioral pattern is viewed as species-
typical (Poirier 1969 ). How then can we compile reports of fl exibility in ways that
are useful and informative (Isabirye-Basuta and Lwanga 2008 )?
If species are unable to change behavior suffi ciently or rapidly enough in
response to continuing habitat degradation, then we ask: “Does the future include a
proliferation of opportunistic species or emergent novelties?” (Myers and Knoll
2001 , p. 5390) and “will the environmental constraints humans place on surviving
populations channel innovations toward properties we associate with pests?” If we
see crop-raiding as innovative behavior, then the extent to which crop-raiding is
widespread suggests the “creation” of pests in areas of high human density or where
buffer zones between forests and farms are lacking. Yet again, we ask: do “general-
ists” crop-raid more than “specialists”? It would appear that, given opportunities,
almost all species of primate will crop raid (Lee and Priston
2005 ).
K. Nowak and P.C. Lee
207
More optimistically, “It is likely that there are adaptational ‘treasures’ that we
have as yet failed to discover in primates, due partly to our own (hominid) biases in
expectation” (Ganzhorn et al. 2003 , p. 133). Behavioral fl exibility, innovation, and
reproductive plasticity are by and large the norm, rather than exception in primates,
and we must collect data on primate responses to disturbance in more systematic
ways that facilitate comparisons across not just taxa, but populations (Isabirye-
Basuta and Lwanga 2008 ; Strier 2009 ). In an age where molecular biology is out-
pacing behavioral ecology and conservation biology (for example, we now recognize
24 species of Lepilemur yet know the conservation status of only three of them, the
rest being “Data-Defi cient”; IUCN Red List 2010 ), we also need to stimulate (and
revive interest and investment in) ongoing fi eld studies of behavior to seek to under-
stand ramifi cations of continuing anthropogenic change to habitats and the capacity
and expression of primate behavioral responses to this change. Primates, whether
fl exible or specialized, mostly frugivorous or folivorous, will be increasingly prone
to extinction (see Conservation International’s “Top 25 Most Endangered Primate
List”) unless there are both habitats and protection that safeguard their capacity for
and existing expression of innovation and behavioral variability and fl exibility.
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