ChapterPDF Available

"Specialist" primates can be flexible in response to habitat alteration



Content may be subject to copyright.
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.
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
P. C. Lee
Behavior and Evolution Research Group , Psychology, University of Stirling ,
Stirling FK9 4LA , UK
behavioral plasticity ( Pigliucci 2001 ; Wcislo 1989 ), behavioral geography (van
Schaik 2003 ; van Schaik et al. 2008 ), ecotypic variation (Turesson 1922 ), and
ecological 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
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 ), 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
Primates may be able to “spread the risks” of extinction (Vázquez and Simberloff
2002 ) specifi cally through this behavioral fl exibility.
Behavioral 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
dietary shifts such as black-and-gold howlers ( Alouatta caraya ) preying on birds’
nests in impoverished habitat fragments (Bicca-Marques et al. 2009 ), innovative
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
(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
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
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 ; 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
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
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
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.
Agosta SJ, Klemens JA (2008) Ecological fi tting by phenotypically fl exible genotypes: implica-
tions for species associations, community assembly and evolution. Ecol Lett 11:1123–1134
Bennett PM, Owens IPF, Nussey D, Garnett ST, Crowley G (2005) Mechanisms of extinction in
birds: phylogeny, ecology and threats. In: Purvis A, Gittleman JL, Brooks T (eds) Phylogeny
and conservation. Cambridge University Press, Cambridge, pp 317–336
Bhagwat SA, Willis KJ, Birks HJB, Whittaker RJ (2008) Agroforestry: a refuge for tropical biodi-
versity? Trends Ecol Evol 23:261–267
Bicca-Marques JC, Muhle CB, Prates HM, Oliveira SG, Calegaro-Marques C (2009) Habitat
impoverishment and egg predation by Alouatta caraya . Int J Primatol 30:743–748
Boyle SA, Smith AT (2010) Can landscape and species characteristics predict primate presence in
forest fragments in the Brazilian Amazon? Biol Conserv 143:1134–1143
Boyles JG, Storm JJ (2007) The perils of picky eating: dietary breadth is related to extinction risk
in insectivorous bats. PLoS One 2:e672
Brashares JS (2003) Ecological, behavioural, and life-history correlates of mammal extinctions in
West Africa. Conserv Biol 17:733–743
Brown AD, Zunino GE (1990) Dietary variability in Cebus apella in extreme habitats: evidence for
adaptability. Folia Primatol 54:187–195
Camperio Ciani A, Palentini L, Finotto E (2001) Survival of a small translocated Procolobus kirkii
population on Pemba Island. Anim Biodiver Conserv 24:15–18
Chapman CA, Chapman LJ (1990) Dietary variability in primate populations. Primates
Chapman CA, Chapman LJ (1999) Implications of small scale variation in ecological conditions
for the diet and density of red colobus monkeys. Primates 40:215–232
Chapman CA, Chapman LJ, Cords M, Gathua JM, Gautier-Hion A, Lambert JE, Rode K, Tutin
CEG, White LJT (2002) Variation in the diets of Cercopithecus species: differences within
forests, among forests, and across species. In: Glenn M, Cords M (eds) The Guenons: diversity
and adaptation in African monkeys. Academic/Plenum, New York, pp 325–350
14 “Specialist” Primates Can Be Flexible in Response to Habitat Alteration
Chapman CA, Rothman JM (2009) Within-species differences in primate social structure: evolu-
tion of plasticity and phylogenetic constraints. Primates 50:12–22
Chivers DJ (1994) Functional anatomy of the gastrointestinal tract. In: Davies AG, Oates JF (eds)
Colobine monkeys: their ecology, behavior and evolution. Cambridge University Press,
Cambridge, pp 205–227
Colles A, Liow LH, Prinzing A (2009) Are specialists at risk under environmental change?
Neoecological, paleoecological and phylogenetic approaches. Ecol Lett 12:849–863
Cowlishaw G, Pettifor RA, Isaac NJB (2009) High variability in patterns of population decline: the
importance of local processes in species extinctions. Proc R Soc B 276:63–69
De Vries A (1992) Translocation of mantled howling monkeys ( Alouatta palliata ) in Guanacaste.
Costa Rica 30:1067, MS Abstracts
Diouck D (2002) Dietary changes in red colobus ( Colobus badius temmincki ) in Fathala’s Forest
in the Saloum Delta National Park, Senegal (1972–1996). Folia Primatol 73:149–164
Dittus WPJ (1985) The infl uence of leaf-monkeys on their feeding trees in a cyclone-disturbed
environment. Biotropica 17:100–106
Dukas R (1998) Evolutionary ecology of learning. In: Dukas R (ed) Cognitive ecology: the evolu-
tionary ecology of information processing and decision making. University of Chicago Press,
Chicago, pp 129–174
Dukas R, Ratcliffe JM (eds) (2009) Cognitive ecology II. University of Chicago Press, Chicago
Eppley TM, Donati G (2009) Dietary fl exibility: subsistence of the southern gentle lemur
Hapalemur meriodionalis on a low quality diet in the Mandena littoral forest, SE Madagascar
(abstract). Am J Phys Anthropol 48(Suppl):125
Ehardt C, Struhsaker T, Butynski T (1999) Conservation of the endangered endemic primates of
the Udzungwa Mountains, Tanzania: surveys, habitat assessment, and long-term monitoring.
Unpublished report for the Margot Marsh Biodiversity Fund and World Wide Fund for
Fimbel C (1994) Ecological correlates of species success in modifi ed habitats may be disturbance-
and site-specifi c: the primates of Tiwai Island. Conserv Biol 8:106–113
Fox LR, Morrow PA (1981) Specialization: species property or local phenomenon? Science
Ganzhorn JU, Klaus S, Ortmann S, Schmid J (2003) Adaptations to seasonality: some primate and
nonprimate examples. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecol-
ogy. The University of Chicago Press, Chicago, pp 132–144
Galat-Luong A, Galat G (2005) Conservation and survival adaptations of Temminck’s red colobus
( Procolobus badius temmincki ) in Senegal. Int J Primatol 26:585–603
Grimes K, Paterson JD (2000) Colobus guereza and exotic plant species in the Entebbe Botanical
Gardens. Am J Primatol 51(Suppl):59–60
Guo S, Ji W, Li B, Li M (2008) Response of a group of Sichuan snub-nosed monkeys to commer-
cial logging in the Qinling Mountains, China. Conserv Biol 22:1055–1064
Harcourt AH (2000) Ecological indicators of risk for primates, as judged by species' susceptibility
to logging. In: Caro TM (ed) Behavioural ecology and conservation. Oxford University Press,
Oxford, pp 56–79
Harcourt AH, Coppeto SA, Parks SA (2002) Rarity, specialization and extinction in primates. J
Biogeogr 29:445–456
Hauser MD (1988) Invention and social transmission: new data from wild vervet monkeys. In:
Byrne R, Whiten A (eds) Machiavellian intelligence: social expertise and the evolution of intel-
lect in monkeys, apes, and humans. Clarendon Press, Oxford, pp 327–343
Irschick D, Dyer L, Sherry TW (2005) Phylogenetic methodologies for studying specialization.
Oikos 110:404–408
Isabirye-Basuta GM, Lwanga JS (2008) Primate populations and their interactions with changing
habitats. Int J Primatol 29:35–48
IUCN (2010) IUCN red list of threatened species.
Johns AD (1986) Effects of selective logging on the behavioural ecology of West Malaysian
primates. Ecology 67:684–694
K. Nowak and P.C. Lee
Johns AD, Skorupa JP (1987) Responses of rain-forest primates to habitat disturbance: a review.
Int J Primatol 8:157–192
Jones CB (2005) Behavioral exibility in primates: causes and consequences. Springer, New York
Laurance W (1991) Ecological correlates of extinction proneness in Australian tropical rainforest
mammals. Conserv Biol 5:79
Lee PC (2003) Innovation as a behavioural response to environmental challenges: a cost and
benefi t approach. In: Reader SM (ed) Animal innovation. Oxford University Press, Oxford, pp
Lee PC, Hauser MD (1998) Long-term consequences of changes in territory quality on feeding and
reproductive strategies of vervet monkeys. J Anim Ecol 67:347–358
Lee PC, Kappeler PM (2003) Socioecological correlates of phenotypic plasticity of primate life
histories. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. The
University of Chicago Press, Chicago, pp 41–65
Lee PC, Priston N (2005) Human attitudes to primates: perceptions of pests, confl ict and conse-
quences for conservation. In: Paterson JD, Wallis J (eds) Commensalism and confl ict: the
human-primate interface. American Society of Primatologists, Norman, OK, pp 1–23
Marsh LK (2003) Primates in Fragments. In: Marsh LK (ed) Primates in fragments. Kluwer
Academic, New York, pp 6–7
Marshall AR, Rovero F, Struhsaker TT (in press) Procolobus gordonorum. In: Rowe N (ed) All the
world’s primates.
Marshall AR, Topp-Jorgensen JE, Brink H, Fanning E (2005) Monkey abundance and social
structure in two high-elevation forest reserves in the Udzungwa Mountains of Tanzania. Int
J Primatol 26:127–145
Martins MM (2009) Lianas as a food resource for brown howlers ( Alouatta guariba ) and southern
muriquis ( Brachyteles arachnoides ) in a forest fragment. Anim Biodivers Conserv 32:51–58
McCann C, Williams-Guillen K, Koontz F, Roque Espinoza AA, Martinez Sanchez JC, Koontz C
(2003) Shade coffee plantations as wildlife refuge for mantled howler monkeys ( Alouatta pal-
liata ) in Nicaragua. In: Marsh LK (ed) Primates in fragments. Kluwer Academic, New York,
pp 321–341
Mourthe IM, Guedes D, Fidelis J, Boubli JP, Mendes SL, Strier KB (2007) Ground use by northern
muriquis ( Brachyteles hypoxanthus ). Am J Primatol 69:706–712
Munoz D, Estrada A, Naranjo E, Ochoa S (2006) Foraging ecology of howler monkeys in a cacao
( Theobroma cacao ) plantation in Comalcalco, Mexico. Am J Primatol 68:127–142
Myers N, Knoll AH (2001) The biotic crisis and the future of evolution. Proc Natl Acad Sci U S A
Niamir-Fuller M (2002) Non-equilibrium theory of African arid ecosystems: designing for moni-
toring and evaluation. In: Abaza H, Baranzini A (eds) Implementing sustainable development.
Edward Elgar for UNEP, Cheltenham, pp 235–253
Nicolakakis N, Sol D, Lefebvre L (2003) Behavioural fl exibility predicts species richness in birds,
but not extinction risk. Anim Behav 65:445–452
Nowak K (2007) Behavioral exibility and demography of Procolobus kirkii across fl oristic and
disturbance gradients. Dissertation, University of Cambridge, Cambridge
Nowak K (2008) Frequent water drinking by Zanzibar red colobus ( Procolobus kirkii ) in a man-
grove forest refuge. Am J Primatol 70:1081–1092
Nowak K, Lee PC (2011a) Demographic structure of Zanzibar red colobus populations in unpro-
tected coral rag and mangrove forests. Int J Primatol 32:24–45
Nowak K, Lee PC (2011b) Consumption of cycads by Zanzibar red colobus. J East Afr Nat Hist
Nowak K (2012) Mangrove and peat swamp forests: refuge habitats for primates and felids. Folia
Primatol 83:361–376
Pigliucci M (2001) Behavior and phenotypic plasticity. In: Pigliucci M (ed) Phenotypic plasticity:
beyond nature and nurture. John Hopkins University Press, Baltimore, MD, pp 182–196
Poirier FE (1969) Behavioral exibility and intergroup variation among Nilgiri langurs ( Presbytis
johnii ) of South India. Folia Primatol 11:119–133
14 “Specialist” Primates Can Be Flexible in Response to Habitat Alteration
Pozo-Montuy G, Serio-Silva JC (2006) Movement and resource use by a group of Alouatta pigra
in a forest fragment in Balancán, México. Primates 48:102–107
Pozo-Montuy G, Serio-Silva JC, Bonilla-Sánchez YM (2011) Infl uence of the landscape matrix on
the abundance of arboreal primates in fragmented landscapes. Primates 52:139–147
Quinten M, Waltert M, Syamsuri F, Hodges K (2009) Peat swamp forest supports high primate
densities on Siberut Island, Sumatra, Indonesia. Oryx 44:147–151
Ralainasolo FB, Ratsimbazafy JH, Stevens NJ (2008) Behavior and diet of the critically endan-
gered Eulemur cinereiceps in Manombo forest, southeast Madagascar. Madagascar Conservat
Dev 3:38–43
Reader SM, Laland KN (2002) Social intelligence, innovation, and enhanced brain size in primates.
Proc Natl Acad Sci U S A 99:4436–4441
Reader SM, Laland KN (2003) Animal innovation: an introduction. In: Reader SM, Laland KN
(eds) Animal innovation. Oxford University Press, Oxford, pp 3–35
Rebecchini L, Schaffner CM, Aureli F, Vick L, Ramos-Fernandez G (2008) The impact of
Hurricane Emily on the activity budget, diet and subgroup composition of wild spider monkeys
( Ateles geoffroyi yucatanensis ) (abstract). Primate Eye 96:Abst#147
Ren BP, Li DY, Liu ZJ, Li BG, Wei FW, Li M (2009) First evidence of prey capture and meat eating by
wild Yunnan snub-nosed monkeys Rhinopithecus bieti in Yunnan, China. Curr Zool 56:227–231.
Riley EP (2007) Flexibility in diet and activity patterns of Macaca tonkeana in response to anthro-
pogenic habitat alteration. Int J Primatol 28:107–133
Riley EP, Priston NE (2010) Macaques in farms and folklore: exploring the human-nonhuman
primate interface in Sulawesi, Indonesia. Am J Primatol 10:848–854
Ross C (1992) Environmental correlates of the intrinsic rate of natural increase in primates.
Oecologia 90:383–390
S a K, Kerth G (2004) A comparative analysis of specialization and extinction risk in temperate-
zone bats. Conserv Biol 18:1293–1303
Schreier A, Swedell L (2008) Use of palm trees as a sleeping site for hamadryas baboons ( Papio
hamadryas hamadryas ) in Ethiopia. Am J Primatol 70:107–113
Silver SC, Marsh LK (2003) Dietary fl exibility, behavioral plasticity, and survival in fragments:
Lessons from translocated howlers. In: Marsh LK (ed) Primates in fragments. Kluwer
Academic, New York, pp 251–265
Singh M, Kumara HN, Kumar MA, Sharma AK (2001) Behavioural responses of lion-tailed
macaques ( Macaca silenus ) to a changing habitat in a tropical rain forest fragment in the
Western Ghats, India. Folia Primatol 72:278–291
Sol D, Timmermans S, Lefebvre L (2002) Behavioural fl exibility and invasion success in birds.
Anim Behav 63:495–502
Sol D (2003) Behavioural exibility: a neglected issue in the ecological and evolutionary literature?
In: Reader SM, Laland KN (eds) Animal innovation. Oxford University Press, Oxford, pp 63–82
Sol D, Szekely T, Liker A, Lefebvre L (2007) Big-brained birds survive better in nature. Proc R
Soc B 274:763–769
Sol D, Bacher S, Reader SM, Lefebvre L (2008) Brain size predicts the success of mammal species
introduced into novel environments. Am Nat 172:S63–S71
Soma T (2006) Tradition and novelty: Lemur catta feeding strategy on introduced tree species at
Berenty Reserve. In: Jolly A, Sussman RW, Koyama N, Rasamimanana HR (eds) Ringtailed
lemur biology. Springer, New York, pp 141–159
Stewart AE, Gordon CH, Wich SA, Schroor P, Meijaard E (2008) Fishing in Macaca fascicularis :
a rarely observed innovative behavior. Int J Primatol 29:543–548
Strier K (2009) Seeing the forest through the seeds: mechanisms of primate behavioral diversity
from individuals to populations and beyond. Curr Anthropol 50:213–228
Struhsaker TT, Cooney DO, Siex KS (1997) Charcoal consumption by Zanzibar red colobus mon-
keys: its function and its ecological and demographic consequences. Int J Primatol 18:61–72
Talebi MG, Lee PC (2008) Nutritional ecology of southern muriquis ( Brachyteles arachnoids )
inhabiting continuous Brazilian Atlantic Forest (abstract). Primate Eye 96:Abst#907
K. Nowak and P.C. Lee
Turesson G (1922) The species and variety as ecological units. Hereditas 3:100–113
van Schaik CP (2003) Social learning and social tolerance in orangutans and chimpanzees. In:
Fragaszy DM, Perry S (eds) The biology of traditions. Cambridge University Press, Cambridge,
pp 297–328
van Schaik CP, Marshall AJ, Wich SA (2008) Geographic variation in orangutan behavior and
biology: its functional interpretation and its mechanistic basis. In: Wich SA, Utami Atmoko
SS, Setia TM, van Schaik CO (eds) Orangutans: geographic variation in behavioral ecology
and conservation. Oxford University Press, Oxford, pp 351–361
Vázquez DP, Simberloff D (2002) Ecological specialization and susceptibility to disturbance: con-
jectures and refutations. Am Nat 159:606–623
Vermeij GJ (1986) Survival during biotic crises: the properties and evolutionary signifi cance of
refuges. In: Elliott DK (ed) Dynamics of extinction. Wiley, New York, pp 231–246
Wcislo WT (1989) Behavioural environments and evolutionary change. Ann Rev Ecol Syst
Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V, Sugiyama Y, Tutin CEG, Wrangham
RW, Boesch C (2001) Charting cultural variation in chimpanzees. Behaviour 138:1481–1516
14 “Specialist” Primates Can Be Flexible in Response to Habitat Alteration
... The howlers and colobus monkeys (genus Colobus) are informally perceived as regenerating forest specialists, but the literature for these genera usually describe them using a complex, heterogeneous landscape that includes mature forests, farmlands, and other modified landscapes in addition to regenerating forests; roughly 50% of species from each genus are known to live in regenerating forests (Fig. 3.1; Galán-Acedo et al. 2019b). Both groups are adapted for folivory but can use a range of food resources according to seasonal availability (Lambert, 2007;Nowak & Lee, 2013). Despite the broad trend of success in these genera, survival in anthropogenic landscapes is not guaranteed, nor is it exclusive to these highly folivorous primates. ...
... Whether a primate species can survive in regenerating forests is often attributed to the species' perceived ecological flexibility. It is widely assumed that generalist species will survive better than specialist species in changing habitats, but in fact there is no clear link between specialization and extinction risk (Nowak & Lee, 2013). Labels such as "folivore" or "frugivore" may mask a primate's true dietary flexibility, and specialist primates are probably less constrained by dietary preferences than we think -most primates switch their primary foods as resource availability fluctuates throughout the year (Lambert, 2007;Nowak & Lee, 2013). ...
... It is widely assumed that generalist species will survive better than specialist species in changing habitats, but in fact there is no clear link between specialization and extinction risk (Nowak & Lee, 2013). Labels such as "folivore" or "frugivore" may mask a primate's true dietary flexibility, and specialist primates are probably less constrained by dietary preferences than we think -most primates switch their primary foods as resource availability fluctuates throughout the year (Lambert, 2007;Nowak & Lee, 2013). Likewise, behavioral flexibility may be overlooked in less-studied species; animals considered to be strict habitat specialists, for example, often prove to be more flexible than previously believed upon further study (Hansen et al., 2020;Nowak & Lee, 2013). ...
Habitat loss is the greatest threat to primate survival. However, land altered for logging or agricultural developments is often abandoned and can regenerate after use. These regenerating forests are critical for the future of primate conservation as they provide habitats and connectivity between mature forest fragments. They can also contribute to climate change mitigation. In this chapter, we introduce what constitutes a regenerating forest, how widespread they are, and how secondary succession varies depending on disturbance history and ecological characteristics. We also examine the role primate seed-dispersal plays in forest regeneration: from the transportation of seeds to changes that occur within a primate’s gut that facilitate germination and impacts on plant communities. We consider how primates might cope with living in a regenerating forest, in terms of behavioral plasticity, from changes in diet to ranging patterns or group cohesion. We argue that the study of primates in regenerating forests is currently lacking and will be pivotal for future primate conservation planning.
... In many cases specialist and generalist consumers entirely switch to abundant resources such that trophic niche breadth remains the same though trophic position might change; while proportion of resources taken are the same the types of resources differ. Diet switching may also occur under natural seasonal or temporal conditions due to fruiting phenology or other trophic flexibility (Nowak and Lee 2013;Clare et al. 2014). Typically, animals-particularly frugivores as a result of fruiting and flowering phenology-will switch from previously abundant resources to resources which may have been present before but were passed over in contiguous forests (Dunn et al. 2010;Boyle et al. 2012;Chaves et al. 2012). ...
... Given that C. perspicillata prefer early successional "pioneer" fruit species like Piper spp., this trend likely reflects the availability of this type of fruit, as sparse fragments are more likely to have more of this preferred resource (Mello et al. 2004;Thies and Kalko 2004). Similar to studies of primates in a fragmented landscape (Boyle et al. 2012;Nowak and Lee 2013), when preferred resources are abundant, narrowranging fruit bats exploit them, and when they are rare exhibit a more flexible diet. ...
Species distribution and persistence have long been known to vary with landscape structure; however, continued human activities in altered landscapes raise many questions as to how habitat fragmentation impacts the biology of persistent animal populations. Using carbon and nitrogen stable isotope analysis, we examined interspecific variation in the diet of frugivorous bats among remnant habitat patches of Brazil’s Atlantic Forest. We hypothesized that the diet of individuals captured in habitat patches would be different than those captured in contiguous habitats. We predicted that bats would alter their realized dietary niche breadth, taking food items (i.e., fruits or insects) according to landscape structure. However, more mobile species should be less impacted by small-scale landscape changes. We predicted that (1) a wide-ranging species (Artibeus lituratus), which move through open areas, will be less affected by small-scale landscape attributes, patch size, composition, and isolation; while (2) two narrow-ranging species (Carollia perspicillata and Sturnira lilium) will have more variation between populations in niche breadth and isotopic ratio ranges dependant on the local environment. Using Akaike’s Information Criterion (AIC) to rank a priori selected candidate models to explain variation, we found that fragment composition, largely involving vegetation density rather than spatial aspects of landscape structure (i.e., patch area, isolation) best explained diet variation in frugivorous bats. Additionally, there was evidence that wide-ranging A. lituratus were less impacted by differences in the landscape than narrow-ranging species. This supports the prediction that bats resident to fragments have altered feeding behaviour, in response to environmental perturbation.
... Increased threats to biodiversity, including primates, over the past two decades include natural habitat loss related to deforestation and forest fragmentation promoted by human activities (Boyle, 2014;Estrada et al., 2017). Wildlife researchers recently highlighted the need for more information on natural history to better understand species' ecological flexibility, i.e., their ability to cope with changes in environmental conditions (Casse & Milhøj, 2013;Isaac & Cowlishaw, 2004;Hoffman and O'Riain, 2012;McLennan et al., 2017;Nowak & Lee, 2013;Strum, 2019). This knowledge is necessary to develop effective conservation plans to preserve viable populations of threatened species (Boyle, 2014). ...
... Variation in the availability of food resources determines the ecological flexibility of primate species, which can be reflected in their diet, behavior, and ranging patterns (Boyle & Smith, 2010;Eppley et al., 2017;Nowak & Lee, 2013). Seasonal variation in food resources represents the most recurrent challenge that primates must cope with (Hemingway & Bynum, 2005;van Schaik et al., 1993). ...
Full-text available
In the face of reduced food availability, primates must choose between expending energy to look for adequate foraging options, or saving energy by reducing activity and intake requirements. In a 1-year study of two groups of Olalla’s titi monkey (Plecturocebus olallae) in the fragmented forests of the Llanos de Moxos, Bolivia, we assessed seasonal variations in behavior, ranging, and diet to examine their ecological flexibility. We observed groups in the wet and dry seasons, recording behavior with instantaneous group scan sampling (743.5 observation hours in the dry season and 733.0 hours in the wet season) and ranging and feeding data with all occurrence sampling. At the same time, we collected data on food availability via monthly phenology monitoring. The titi monkeys fed mainly on fruits and significantly reduced the time they spent consuming fruit during the dry season compared with the wet season while showing some (nonsignificant) increase in their consumption of leaves, and other foods (seeds, lichens, and fungi). Home ranges remained relatively constant, but titi monkeys spent less time moving in the dry season than in the wet season, although this difference was not significant. The observed shift in diet toward consuming alternative foods during the fruit lean period and reducing movement instead of expanding ranging behavior to look for higher-quality foods suggests that P. olallae follows an energy–area minimizing strategy that may enable these primates to inhabit fragmented forests. Nevertheless, deforestation and further fragmentation in the range of these endemic and Critically Endangered primates must be addressed, as they represent significant threats to the severely range-restricted P. olallae populations. Our study illustrates the relevance of understanding primate ecological flexibility in response to food reductions to the development of conservation actions, especially in the light of increasing forest degradation and loss in the study region.
... As deforestation and habitat fragmentation continue at alarming rates throughout the world, the survival of many forest species largely depends on their ability to cope with such changes (Robinson and Ramirez, 1982;Marsh et al., 1987;Noss and Csuti, 1994). Different primate species respond differently to habitat loss and fragmentation (Bicca-Marques, 2003;Chapman et al., 2006Chapman et al., , 2007Anderson et al., 2007aAnderson et al., , 2007bArroyo Rodriguez et al., 2007;Bicca-Marques et al., 2009;Boyle and Smith, 2010) and their persistence depends on the ability of species' social and ecological flexibility (Marsh, 2003;Boyle and Smith, 2010;Nowak and Lee, 2013). ...
Hylobatids (gibbons and siamangs) are the smallest of the apes distinguished by their coordinated duets, territorial songs, arm-swinging locomotion, and small family group sizes. Although they are the most speciose of the apes boasting twenty species living in eleven countries, ninety-five percent are critically endangered or endangered according to the IUCN's Red List of Threatened Species. Despite this, gibbons are often referred to as being 'forgotten' in the shadow of their great ape cousins because comparably they receive less research, funding and conservation attention. This is only the third book since the 1980s devoted to gibbons, and presents cutting-edge research covering a wide variety of topics including hylobatid ecology, conservation, phylogenetics and taxonomy. Written by gibbon researchers and practitioners from across the world, the book discusses conservation challenges in the Anthropocene and presents practice-based approaches and strategies to save these singing, swinging apes from extinction.
... Our study at WWNSF suggests that guerezas generally do well in UDNF, DNF, and MPF, but far less well in EJMF, and are unable to survive in EBL. The MPF, in particular, covers only a small portion of WWNSF and the population density reached there could be an outcome of population compression (Dunbar 1987;Nowak and Lee 2013a) or may simply be a sign of the ecological flexibility of guerezas in plantation habitat and their ability to rely intensively on non-native food items (Fashing et al. 2012;Nowak and Lee 2013b;Eppley et al. 2015Eppley et al. , 2017Galán-Acedo et al. 2019b;Tesfaye et al. 2021). ...
Full-text available
Given the current rate of habitat degradation and loss in the tropics, data on primate population densities and habitat use are indispensable for assessing conservation status and designing feasible management plans for primates. The Omo River guereza (Colobus guereza guereza) is a subspecies of the eastern black-and-white colobus monkey endemic to the western Rift Valley forests of Ethiopia. Their restricted distribution along with habitat loss and hunting within their range render them vulnerable to local extirpation and extinction. Furthermore, there are no published data available on the population status and habitat use patterns of the Omo River guereza. We therefore aimed to assess the population size of Omo River guerezas in diferent habitats (Erica-Juniperus mixed forest, mixed plantation forest, undisturbed natural forest, disturbed natural forest) using transect surveys at Wof-Washa Natural State Forest (WWNSF) in central Ethiopia. Our surveys covered a cumulative distance of 88.5 km in four diferent habitats, during which we recorded a total of 140 Omo River guereza groups. The average group density was 14.3 groups/km 2 , average individual density was 94.4 individuals/km , and we estimated the total population size within WWNSF to be 2549 individuals. The sex ratio of the population was split evenly between males and females, though the age classes skewed strongly towards adults. Of the habitats surveyed, the highest group encounter rate (1.83 groups/km) occurred in the disturbed natural forest. However, the highest individual density (110.1 individuals/ km 2 ) was recorded in undisturbed natural forest. Still, sizable densities (group and individual) were recorded in three of the disturbed habitats (disturbed natural forest, mixed plantation forest, and to a lesser extent Erica-Juniperus mixed forest). Our study ofers the irst baseline information with which to compare future population density estimates and habitat use in the range of Omo River guerezas.
... Studies, for instance, focus on evolutionary consequences (Kinnison and Hairston 2007;Hendry et al. 2017) or the potential of the species to adapt, with special reference to behavioral responses to rapidly changing environments (Hendry et al. 2011;Tuomainen and Candolin 2011;Candolin and Wong 2012). Studies focusing on the behavioral adaptations or flexibility of primates in response to human-induced environmental changes contribute to our understanding of primate adaptive potentials and can be useful to optimize conservation efforts (Nowak and Lee 2013;Hockings et al. 2015;Strier 2017). ...
Full-text available
Based on the recent international studbook, we here investigate the history and development of the global captive population of the Endangered lion-tailed macaque. Of particular interest is whether the development and management of the population has contributed to its persistence as a reserve population for the conservation of the species. Of the 2,734 individuals, 80% were born over 119 years. About 16% were wild-born and 4% were of unknown origin. The population was kept in two large differently managed subpopulations in North American and European zoos. It revealed a slow but steady increase from the 1960s onward with a period of 60 years of persistence till 2018 without imports of wild-caught individuals. The population grew under conditions of low productivity: only a small proportion of the females bred, and infant mortality was high. Overall, the number of births was slightly higher than the number of deaths. Reductions in population size and birth control measures due to space problems in both subpopulations led to a reduction of phenotypic diversity and a currently stagnating global population, mainly housed in European zoos. It still has the potential for developing toward a diversified and persistent population. The discussion suggests the need to: 1. Investigate the breeding problems; 2. Use adaptive management based on the “declining population” paradigm; 3. Consider the reproductive and social system as known from field studies; and 4. Emphasize international management structures especially with Indian zoos and conservation biologists.
... With the aim of promoting primate conservation a growing number of studies have surveyed the impact of monkeys on human interests [Else, 1991;Naughton-Treves, 2001;Fuentes and Wolfe, 2002;Fuentes et al., 2008;Hambali et al., 2012;Barua, 2013;Habiba et al., 2013;Garriga, 2014;Chakravartty, 2015;Saraswat, 2015], human attitudes towards monkeys in places where natural primate habitats have been converted for human use [Bishop et al., 1981;Harcourt, 1986;King and Lee, 1987;Siex and Struhsaker, 1999;Lee and Priston, 2005;Srivastava and Begum, 2005;Watanabe and Muroyama, 2005;Sha et al., 2009;Campbell-Smith et al., 2010;Chauhan and Pirta, 2010;Habiba et al., 2013;Regmi et al., 2013] as well as suggestions on how best to reduce HMC [e.g., Silero-Zubiri and Switzer, 2001;Hill, 2002;Chakravarthy and Thyagaraj, 2005;Osborne and Hill, 2005;Riley, 2007;Shek and Cheng, 2010;Jones-Engel et al., 2011a, b;Sharma et al., 2011;Nowak and Lee, 2013;Chaturvedi and Mishra, 2014;Singh, 2019;Rudran et al., 2020]. ...
Many investigators of human-monkey competition (HMC) in Sri Lanka have revealed some common threads. Except at temple and protected sites, all monkeys were considered as household or agricultural pests wherever they shared space with humans. This included the widely distributed toque macaque (Macaca sinica), the grey langur (Semnopithecus priam thersites) of the Dry Zone, and the purple-faced langur (S. vetulus) of the southwestern and central rain forests where human densities and habitat fragmentation were greatest. People sharing space with monkeys resorted to various non-lethal methods to chase monkeys away from their properties and most preferred to have monkeys removed to protected areas; such translocations have been politically popular, though contrary to ecological principles. The main cause of HMC near primate habitats has been environmental conversion to agriculture, whereas in many towns the refuse generated in the wake of widespread growing tourism lured omnivorous macaques towards human habitation and stimulated macaque population growth. While most Sri Lankans share space with monkeys reluctantly, only a minority, flouting cultural restraints, want monkeys destroyed. Nonetheless, a major threat to primate conservation has been habitat loss and the killing of monkeys, especially in the densely populated southwestern area of the island where recent surveys showed that most macaques have been wiped out. Two subspecies, S. v. nestor of the rain forest lowlands and M. s. opisthomelas of the montane forests, are Critically Endangered. Sharing space with monkeys rests on public tolerance, understanding, and empathy with monkeys. Religious concepts venerating monkeys provide fertile ground for this. Our science-based educational documentaries (n > 35), among other efforts, also have contributed to these human sentiments in Sri Lanka and globally. The trends in HMC suggest that protected nature reserves for all wildlife are more secure for primate survival than ethnoprimatology by itself would be. Rudran [Folia Primatologica 2021, DOI: 10.1159/000517176] criticized our recent publication on HMC in Sri Lanka [Dittus et al., Folia Primatologica 2019, 90: 89-108]. We consider his comments as misconstruing efforts in primate conservation through denying the importance of traditional protected areas, overlooking our achievements in educating the public and reducing HMC, as well as misunderstanding the limits of marketing monkeys to tourists as a source of income to support conservation.
... While the external shape of carpal bones is critical to the functional integrity of the wrist, primates display behavioral and postural flexibility such that external morphology will not accurately reflect all aspects of a species' or individual's behavior (Kivell, 2016b;Nowak & Lee, 2013;Schmitt et al., 2016). Furthermore, with fossil specimens it can be challenging to discern functionally significant features from non-functional aspects of morphology representative of phylogenetic lag, particularly as behavioral adaptations precede morphological ones (Kivell, 2016b;Lieberman, 1997;Tocheri, 2007;Ward, 2002). ...
The morphology of the proximal carpals (scaphoid, lunate, triquetrum) are linked to the range of motion (ROM) at the radiocarpal and midcarpal joints. While the relationship between ROM and habitual locomotor mode is well established, it has yet to be investigated whether relative patterns of internal bone architecture reflect the kinematics and kinetics at the proximal row. As internal bone is known to model its structure to habitually incurred forces, internal architecture has the potential to provide insight into how joints have been loaded during the lifetime of an individual. Using a broad sample of extant great apes and humans (n = 177 total bones), this study investigates whether relative differences in the bone volume to total volume (BV/TV) and degree of anisotropy (DA) across the scaphoid, lunate and triquetrum correlate with the presumed force transfer and biomechanics of the hominoid wrist. Results reveal that broad patterns in BV/TV and DA differentiate hominoids by their predominant locomotor mode. The human pattern suggests the lunate may be the most highly strained bone within the proximal row. Both knuckle-walking taxa (Gorilla, Pan) exhibited similar architectural patterns suggesting they are adapted to resist similar forces in this region of the wrist. The relatively high DA across all Pongo carpals suggests it may have more stereotypical wrist loading than commonly assumed. Finally, the distinctly low DA in the triquetrum across all taxa suggests force transfer via the synapomorphic triangular fibrocartilage complex may leave a distinctive signature in the internal bone architecture that requires further investigation. Objectives Functional adaptation in the trabecular and cortical bone of individual wrist bones has been investigated across hominoid species but functional conclusions remain limited. This study examines whether relative patterns in internal bone architecture across multiple carpal bones can be correlated to the known or assumed kinetics and kinematics of the wrist joint in extant hominoids. Materials and Methods This study applied a whole-bone methodology to quantify the internal architecture (cortical and trabecular bone) of the scaphoid, lunate, and triquetrum of suspensory (Pongo sp.), knuckle-walking (Pan paniscus, Pan troglodytes, Gorilla sp.) and bipedal (Homo sapiens) hominoids (n = 177 total bones). Results H. sapiens showed unique patterns in both measured parameters: a decrease in degree of anisotropy (DA) from the scaphoid to the triquetrum with higher bone volume to total volume (BV/TV) in the lunate relative to the other bones. Knuckle-walking taxa had similar patterns in both parameters: highest mean DA in the lunate and lowest in the triquetrum while significantly higher BV/TV was recorded the triquetrum. Pongo exhibited the same DA pattern as knuckle-walking taxa but a distinct pattern of continual decrease in BV/TV from scaphoid to triquetrum. Discussion Relative differences in the internal bone structure across multiple carpals differentiated locomotor modes in extant hominoids. The triquetrum and lunate are particularly understudied but their importance to differentiating locomotor mode indicates further research is warranted. Establishing patterns across more carpal joints in primates should be a research priority as they will provide critical context to interpreting fossil species represented by single or few carpal elements.
... contributes to the general understanding of the ability of primates to adapt to modified landscapes (Cameron and Gould 2013;Nowak and Lee 2013). Therefore, the secondary and regenerated forests in RNP could provide M. rufus with long-term habitats since these habitats are part of the continuous forest block. ...
Full-text available
Microhabitat preference among primates, which provides them with the niche they need to survive, often conditions primate diversity, abundance, and coexistence. Vegetation alteration and recovery have built heterogeneous forest landscapes that may influence primates’ microhabitat preference. We compared the diversity and size of trees/shrubs and the presence of lianas in 132 sites where we captured the rufous mouse lemur (Microcebus rufus), with that of 240 sites where we did not capture this species, to investigate the aspects of microhabitat structure they prefer. We then examined how this structural preference varies across a heterogeneous landscape of forests with different disturbance levels. Overall, microhabitats used by M. rufus differed significantly from unused ones in densities of small size, understory, and midstory plants. Microcebus rufus frequented microhabitats with significantly denser small- and medium-size (DBH 2.5-10 cm) trees/shrubs without lianas in the primary forest and small-size plants (DBH 2.5-4.9 cm) with one liana in other forest types. Compared to the microhabitats they used in the primary forest, the microhabitats in other forest types had lower densities of trees/shrubs with lianas. Additionally, the secondary forests and forest fragments also had significantly lower DBH. Although this variation in microhabitat use may represent an opportunity for M. rufus to live in disturbed habitats, it may expose them to additional threats, affecting their long-term survival. These findings emphasize the need to examine potential changes in microhabitat use among primates living in anthropogenic landscapes, which could help optimize long-term conservation and management of threatened primate species in heterogeneous landscapes.
Full-text available
Primates in the tropics are highly vulnerable to habitat loss and fragmentation as they depend on the forest for survival. Thus, reliable population and distribution data are crucial to identifying priority sites for conservation and designing effective management plans in the deforested region. To date, the population size and distribution of black-and-white colobus monkeys ( Colobus guereza guereza ) are unknown along the Ethiopian Highlands. Therefore, this study aimed to determine the relative abundance of black-and-white colobus monkeys and their current distribution pattern in the Awi Zone of the northwestern Ethiopia. We conducted population survey of black-and-white colobus monkeys using line transects between Oct 2020 and Sep 2021 in 27 forest patches of the region. We surveyed 27 forest patches and found black-and-white colobus monkeys in all patches. Overall, we recorded 328 group sightings of black-and-white colobus monkeys in these forest patches ranging between 1859 and 2557 m asl. We counted a total mean of 2897 individuals ranging from 5–16 individuals per group (mean = 8.8, SD = 2.5) within the sampling transects. Overall, the sighting encounter frequency of this monkey was 5.5 groups/km, while the relative mean population abundance was 48.2 individuals/km. Our study offers the first baseline information for future absolute abundance and population density estimates of black-and-white colobus monkeys and the forest patches they inhabit. Thus, this region should be considered as key habitat for future black-and-white colobus monkeys and other conservation initiatives. Establishment protected areas (national parks), improved law enforcement, population trend monitoring, and engagement with adjacent local communities are imperative to secure the long-term survival and conservation of black-and-white colobus monkeys and their habitats in the region. In addition, conservation measures like educational awareness programs, modern beekeeping, and alternative biofuel use should be initiated to stop further deforestation.
Full-text available
Cultural variation among chimpanzee communities or unit-groups at nine long-term study sites was charted through a systematic, collaborative procedure in which the directors of the sites first agreed a candidate list of 65 behaviour patterns (here fully defined), then classifed each pattern in relation to its local frequency of occurrence. Thirty-nine of the candidate behaviour patterns were discriminated as cultural variants, sufficiently frequent at one or more sites to be consistent with social transmission, yet absent at one or more others where environmental explanations were rejected. Each community exhibited a unique and substantial profile of such variants, far exceeding cultural variation reported before for any other non-human species. Evaluation of these pan-African distributions against three models for the diffusion of traditions identified multiple cases consistent with cultural evolution involving differentiation in form, function and targets of behaviour patterns.
Full-text available
Cycads and colobus monkeys occur together in many parts of tropical Africa; we present the first records of colobus feeding on these plants. On 22 occasions, the Endangered Zanzibar red colobus Procolobus kirkii fed on the leaves of Encephalartos hildebrandtii, a Near Threatened species, in the Kiwengwa-Pongwe Forest Reserve, north-eastern Unguja. A total of 92 minutes of cycad feeding were observed during a 14-month, 678-hour study of three focal groups, suggesting rare but consistent use of cycads. We analyzed HCN content in a small sample of browsed and unbrowsed cycad leaves for a preliminary analysis of toxicity, but toxicity was similar (and high) across leaves. Colobus appear to be one of the few mammal species able to exploit this abundant food source (277 cycads/ha) in the 33 km2 coral rag forest. Both colobus and cycads of this region need urgent protection; in August 2011, much tree cutting was observed resulting in a discontinuous canopy which will threaten both colobus and cycads.
Examining the behavioral response of howler monkeys (Alouatta pigra) to translocation may lend some insight into their ability to repopulate and persist in tropical forest fragments. In fragmented landscapes, forest patches may be large enough to sustain small numbers of individuals and social groups, but not at levels high enough for populations to persist solely in these patches. In fragmented forest landscapes, the ability to colonize unfamiliar forest patches is necessary to maintain demographic and genetic variability. In effect, translocated individuals successfully migrate to another fragment and have to depend upon their ability to include novel food items and strata. Survival depends on the level of dietary flexibility and behavioral plasticity.
This chapter states that innovative behaviours are of considerable importance for understanding the ecology and, in turn, the evolution of animals. From an ecological perspective, innovatory propensity may influence biodiversity patterns through its influence on some of the processes that determine the gain and loss of species within the community. From an evolutionary standpoint, it may affect the rate of evolutionary divergence by altering the selective pressures to which individuals are exposed. The growing needs to understand the consequences of innovative behaviours and novel improvements in methods to measure innovation have stimulated a number of recent studies. Here, the chapter uses these new advances to illustrate the importance of behavioural innovation in some of the ecological and evolutionary processes that govern biodiversity. It examines the adaptive value of behaving in a flexible way and discusses new developments in the methods of quantifying innovatory capacity. The chapter further presents a series of comparative studies that seek to understand the role of this capacity in three different biological processes: the invasion of new environments, the risk of extinction, and the rate of evolutionary diversification.
This chapter presents a general review of how non-human primates adjust to environmental variability via behavioural innovation, and place innovation into context as an adaptive strategy for coping with unpredictability. It explains that primates as a group are renowned for their behavioural flexibility, their technical capacities, and for creating new contexts for social opportunities. Both phylogeny and life history underlie differences between species in their capacity to innovate, while within species, local ecological opportunities and constraints affect when, where, how often and among which age-sex classes innovations may arise and become fixed within behavioural repertoires. The chapter outlines here in a theoretical context how modelling costs and benefits could increase our understanding of innovation and dissemination of novel behaviour.
A cyclone in November 1978 caused extensive damage to a site of natural dry evergreen forest in Sri Lanka. The cyclone destroyed more than 50 percent of the woody vegetation that had produced most of the food for two species of leaf-eating monkeys or langurs. Apparently, this caused an imbalance between these langur populations and their natural food supply and resulted in overbrowsing on those feeding trees which were not destroyed by the cyclone. Preferentially browsed tree species that were relatively rare and/or small in size died at significantly greater rates due to overbrowsing than those which were buffered against overbrowsing by virtue of being large in tree size and/or relatively abundant in the forest. The virtual disappearance of three overbrowsed tree species from the forest suggests that langurs may contribute to the change in floristic diversity in cyclone-disturbed areas. However, such an effect of langur folivory is thought to be short-lived and specific to this kind of rare disastrous environmental situation.
Identifying the biological traits of species that predispose them to extinction is a focus of research in evolutionary ecology and conservation biology. This research has traditionally been divided between studies of extinction or decline in undisturbed habitat islands and studies of the persistence of species affected adversely by human influence. I combined these approaches to test for correlations between nine ecological, behavioral, and life-history traits and vulnerability to local extinction for 41 species of carnivores, primates, and ungulates in fragmented and exploited habitats in Ghana, West Africa, while accounting statistically for phylogeny. Species distributed in isolated populations were most prone to local extinction, and monogamous species and those wherein males defended small harems were also prone to extinction. Body size, fecundity, abundance, habitat specialization, trophic group, and the degree to which hunters and consumers preferred a species generally were unrelated to species persistence. Although population isolation and mating system were the only traits that explained a significant amount of the observed variation in persistence of all species, analyses of carnivores, primates, and ungulates as groups yielded varied results. Mammals most prone to local extinction in my study reserves were also those listed by the World Conservation Union as being at greatest risk of global extinction. Thus, my results suggest that the relative isolation of populations and the mating system displayed by mammals may be good general predictors of their persistence.
MASSIMO PICLIUCCI Phenotypic Plasticity BEYOND NATURE AND NURTURE tor more than nvo decades rlic concept of phenotypic plasticity has allowed re- searchers to go beyond the nature-nurture dichotomy to gain deeper insights into how organisms arc shaped by the