Skip to main content
SpringerLink
Log in

Primate Responses to Changing Environments in the Anthropocene

  • Chapter
  • First Online:
Primate Life Histories, Sex Roles, and Adaptability

Part of the book series: Developments in Primatology: Progress and Prospects ((DIPR))

Abstract

Most primate habitats are undergoing intense and rapid changes due to anthropogenic influences resulting in many primate populations being threatened. Habitat loss and fragmentation are already extensive; thus dispersal to unoccupied habitats is an unlikely adaptive response to these changes. Furthermore, most primates have slow life histories and long generation times, and because environmental change is occurring at an unprecedented rate, gene-based adaptations are also unlikely to evolve fast enough to offer successful responses to these changes. However, long primate life histories are linked to well-developed brains, which may allow primates to respond to environmental change through behavioural flexibility. Here we ask: What are the most common challenges of changing environments for primates and what do we know about their behavioural abilities to respond to such changes? To answer this question, we first review the most common types of habitat/landscape alterations, the extent of human-primate interactions, and the impact of climate change. Next, we evaluate how primates respond to these changes via behavioural flexibility, and using different approaches and datasets, we discuss how to investigate if these responses are beneficial with regard to population persistence. Finally, we discuss how comparisons across species, space, and time can be used to draw generalizations about primate responses to environmental change while considering their behavioural flexibility and the data derived from case studies. We demonstrate how understanding behavioural flexibility as a response to environmental change will be crucial to optimize conservation efforts by constructing informed management plans.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Notes

  1. 1.

    The calculation of age of first birth includes data from 102 primate species, and the calculation of inter-birth intervals included data from 108 primate species. These averages are not corrected for phylogenetic relatedness and might be biased depending on the inclusion of varying number of primates from different taxonomic groups.

  2. 2.

    It seems almost a certainty that with the disappearance of Miss Waldron’s red colobus (Procolobus waldroni), the first primate species has been driven to extinction in modern times (McGraw 2005; Oates et al. 2016).

References

  • Altmann J, Alberts SC, Altmann SA, Roy SB (2002) Dramatic change in local climate patterns in the Amboseli basin, Kenya. Afr J Ecol 40:248–251

    Google Scholar 

  • Andam KS, Ferraro PJ, Pfaff A et al (2008) Measuring the effectiveness of protected area networks in reducing deforestation. Proc Natl Acad Sci 105:16089–16094

    CAS  PubMed  Google Scholar 

  • Arroyo-Rodríguez V, Moral EC, Mandujano S et al (2013) Assessing habitat fragmentation effects on primates: the importance of evaluating questions at the correct scale. In: Marsh LK, Chapman CA (eds) Primates in fragments. Springer, New York, pp 13–28

    Google Scholar 

  • Asquith PJ (1989) Provisioning and the study of free-ranging primates: history, effects, and prospects. Am J Phys Anthropol 32:129–158

    Google Scholar 

  • Barnosky AD, Matzke N, Tomiya S et al (2011) Has the Earth’s sixth mass extinction already arrived? Nature 471:51–57

    CAS  PubMed  Google Scholar 

  • Baya L, Storch I (2010) Status of diurnal primate populations at the former settlement of a displaced village in Cameroon. Am J Primatol 72:645–652

    PubMed  Google Scholar 

  • Beehner JC, Onderdonk DA, Alberts SC, Altmann J (2006) The ecology of conception and pregnancy failure in wild baboons. Behav Ecol Behav Ecol 17:741–750

    Google Scholar 

  • Behie AM, Pavelka MSM (2005) The short-term effects of a hurricane on the diet and activity of black howlers (Alouatta pigra) in Monkey River, Belize. Folia Primatol (Basel) 76:1–9

    Google Scholar 

  • Behie AM, Pavelka MSM (2013) Interacting roles of diet, cortisol levels, and parasites in determining population density of Belizean howler monkeys in a hurricane damaged forest fragment. In: Marsh LK, Chapman CA (eds) Primates in fragments. Springer New York, New York, pp 447–456

    Google Scholar 

  • Behie AM, Pavelka MSM, Hartwell K et al (in press) Alas the storm has come again! The impact of frequent natural disasters on primate conservation. In: Behie AM, Teichroeb JA, Malone N (eds) Primate Research and Conservation in the Anthropocene. Cambridge University Press, Cambridge/New York

    Google Scholar 

  • Bermejo M, Rodríguez-Teijeiro JD, Illera G et al (2006) Ebola outbreak killed 5000 gorillas. Science 314:1564–1564

    CAS  PubMed  Google Scholar 

  • Bicca-Marques JC, Calegaro-Marques C Rylands AB, et al. (2017) Yellow fever threatens Atlantic Forest primates – eLetter in response to “Impending extinction crisis of the world’s primates: why primates matter” (Estrada et al. 2017)

    Google Scholar 

  • Blumstein DT (2012) Social behaviour. In: Candolin U, Wong BBM (eds) Behavioural responses to a changing world: mechanisms and consequences. Oxford University Press, Oxford

    Google Scholar 

  • Blumstein DT, Fernández-Juricic E (2010) A primer of conservation behavior, 1st edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Boesch C (2008) Why do chimpanzees die in the forest? The challenges of understanding and controlling for wild ape health. Am J Primatol 70:722–726

    PubMed  Google Scholar 

  • Bonilla-Sánchez YM, Serio-Silva JC, Pozo-Montuy G, Chapman CA (2012) Howlers are able to survive in eucalyptus plantations where remnant and regenerating vegetation is available. Int J Primatol 33:233–245

    Google Scholar 

  • Borries C, Sandel AA, Koenig A et al (2016) Transparency, usability, and reproducibility: guiding principles for improving comparative databases using primates as examples. Evol Anthropol 25:232–238

    PubMed  Google Scholar 

  • Brook BW, Sodhi NS, Bradshaw CJA (2008) Synergies among extinction drivers under global change. Trends Ecol Evol 23:453–460

    PubMed  Google Scholar 

  • Bruner AG, Gullison RE, Rice RE, da Fonseca GAB (2001) Effectiveness of parks in protecting tropical biodiversity. Science 291:125–128

    CAS  PubMed  Google Scholar 

  • Butchart SHM, Walpole M, Collen B et al (2010) Global biodiversity: indicators of recent declines. Science 328:1164–1168

    CAS  PubMed  Google Scholar 

  • Cai W, Borlace S, Lengaigne M et al (2014) Increasing frequency of extreme El Nino events due to greenhouse warming. Nat Clim Change 4:111–116

    CAS  Google Scholar 

  • Cai W, Santoso A, Wang G et al (2015) ENSO and greenhouse warming. Nat Clim Change 5:849

    Google Scholar 

  • Campos FA (2018) A synthesis of long-term environmental change in Santa Rosa, Costa Rica. In: Kalbitzer U, Jack KM (eds) Primate life histories, sex roles, and adaptability – essays in honour of Linda M. Fedigan. Springer, New York, pp 331–354

    Google Scholar 

  • Campos FA, Jack KM, Fedigan LM (2015) Climate oscillations and conservation measures regulate white-faced capuchin population growth and demography in a regenerating tropical dry forest in Costa Rica. Biol Conserv 186:204–213

    Google Scholar 

  • Campos FA, Morris WF, Alberts SC et al (2017) Does climate variability influence the demography of wild primates? Evidence from long-term life-history data in seven species. Glob Change Biol 23:4907–4921

    Google Scholar 

  • Carey J (2016) Core concept: are we in the “Anthropocene”? Proc Natl Acad Sci 113:3908–3909

    CAS  PubMed  Google Scholar 

  • Carnegie SD, Fedigan LM, Melin AD (2011) Reproductive seasonality in female capuchins (Cebus capucinus) in Santa Rosa (Area de Conservación Guanacaste), Costa Rica. Int J Primatol 32:1076–1090

    Google Scholar 

  • Caro TM, Durant SM (1995) The importance of behavioral ecology for conservation biology: examples from Serengeti carnivores. In: Serengeti II: dynamics, management, and conservation of an ecosystem. Chicago University Press, Chicago, pp 451–472

    Google Scholar 

  • Caro T, Sherman PW (2011) Behavioural ecology cannot profit from unstructured environmental change. Trends Ecol Evol 26:321–322

    Google Scholar 

  • Caro T, Sherman PW (2013) Eighteen reasons animal behaviourists avoid involvement in conservation. Anim Behav 85:305–312

    Google Scholar 

  • Ceballos G, Ehrlich PR, Barnosky AD et al (2015) Accelerated modern human–induced species losses: entering the sixth mass extinction. Sci Adv 1:e1400253

    PubMed  PubMed Central  Google Scholar 

  • Ceballos G, Ehrlich PR, Dirzo R (2017) Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines. Proc Natl Acad Sci 114:E6089–E6096

    CAS  PubMed  Google Scholar 

  • Chapman CA (2018) A road for a promising future for China’s primates: The potential for restoration. Zoological Research 39:244–248

    Google Scholar 

  • Chapman CA, Gogarten JF (2012) Primate conservation: is the cup half empty or half full? Nat Educ Knowl 4:7

    Google Scholar 

  • Chapman CA, Peres CA (2001) Primate conservation in the new millennium: the role of scientists. Evol Anthropol Issues News Rev 10:16–33

    Google Scholar 

  • Chapman CA, Rothman JM (2009) Within-species differences in primate social structure: evolution of plasticity and phylogenetic constraints. Primates 50:12–22

    PubMed  Google Scholar 

  • Chapman CA, Balcomb SR, Gillespie TR et al (2000) Long-term effects of logging on African primate communities: a 28-year comparison from Kibale National Park, Uganda. Conserv Biol 14:207–217

    Google Scholar 

  • Chapman CA, Chapman LJ, Struhsaker TT et al (2005a) A long-term evaluation of fruiting phenology: importance of climate change. J Trop Ecol 21:31–45

    Google Scholar 

  • Chapman CA, Gillespie TR, Goldberg TL (2005b) Primates and the ecology of their infectious diseases: how will anthropogenic change affect host-parasite interactions? Evol Anthropol 14:134–144

    Google Scholar 

  • Chapman CA, Lawes MJ, Eeley HAC (2006) What hope for African primate diversity? Afr J Ecol 44:116–133

    Google Scholar 

  • Chapman CA, Struhsaker TT, Skorupa JP et al (2010) Understanding long-term primate community dynamics: implications of forest change. Ecol Appl 20:179–191

    PubMed  Google Scholar 

  • Chapman CA, Twinomugisha D, Teichroeb JA et al (2016) How do primates survive among humans? Mechanisms employed by vervet monkeys at Lake Nabugabo, Uganda. In: Waller MT (ed) Ethnoprimatology – primate conservation in the 21st century. Springer, New York, pp 77–94

    Google Scholar 

  • Chapman CA, Bortolamiol S, Matsuda I, Omeja PA, Paim FP, Reyna-Hurtado R, Sengupta R, Valenta K (2018) Primate population dynamics: variation in abundance over space and time. Biodivers Conserv 27:1221–1238

    Google Scholar 

  • Chapman CA, Valenta K, Bonnell TR, Brown KA, Chapman LJ (2018). Solar radiation and ENSO predict fruiting phenology patterns in a 15-year record from Kibale National Park. Uganda. Biotropica 50:384–395

    Google Scholar 

  • Chapman CA, Valenta K, Bortolamiol S (2018) How variable is a primate’s world: spatial and temporal variation in potential ecological drivers of behaviour? In: Kalbitzer U, Jack KM (eds) Primate life histories, sex roles, and adaptability – essays in honour of Linda M. Fedigan. Springer, New York, pp 359–371

    Google Scholar 

  • Clarke MR, Glander KE (2010) Secondary transfer of adult mantled howlers (Alouatta palliata) on Hacienda La Pacifica, Costa Rica: 1975–2009. Primates 51:241–249

    PubMed  Google Scholar 

  • Conly JM, Johnston BL (2008) The infectious diseases consequences of monkey business. Can J Infect Dis Med Microbiol 19:12–14

    PubMed  PubMed Central  Google Scholar 

  • Corlett RT (2012) Climate change in the tropics: the end of the world as we know it? Biol Conserv 151:22–25

    Google Scholar 

  • Crutzen PJ, Stoermer EF (2000) The “anthropocene”, global change. IGBP Newsl 41:17–18

    Google Scholar 

  • de Almeida-Rocha JM, Peres CA, Oliveira LC (2017) Primate responses to anthropogenic habitat disturbance: a pantropical meta-analysis. Biol Conserv 215:30–38

    Google Scholar 

  • Diffenbaugh NS, Singh D, Mankin JS et al (2017, 114) Quantifying the influence of global warming on unprecedented extreme climate events. Proc Natl Acad Sci:4881–4886

    Google Scholar 

  • Dillis C, Beaudrot L, Feilen KL et al (2015) Modeling the ecological and phenological predictors of fruit consumption by gibbons (hylobates albibarbis). Biotropica 47:85–93

    Google Scholar 

  • Dittus WPJ (1988) Group fission among wild toque macaques as a consequence of female resource competition and environmental stress. Anim Behav 36:1626–1645

    Google Scholar 

  • Dunham AE, Erhart EM, Wright PC (2011) Global climate cycles and cyclones: consequences for rainfall patterns and lemur reproduction in southeastern Madagascar. Glob Change Biol 17:219–227

    Google Scholar 

  • Emrich A, Pokorny B, Sepp C (2000) The significance of secondary forest management for development policy. Deutsche Gesellschaft für Technische Zusammenarbeit (GTZ), Eschborn, Germany

    Google Scholar 

  • Erhart EM, Overdorff DJ (2008) Population demography and social structure changes in Eulemur fulvus rufus from 1988 to 2003. Am J Phys Anthropol 136:183–193

    PubMed  Google Scholar 

  • Espinosa S, Branch LC, Cueva R (2014) Road development and the geography of hunting by an Amazonian indigenous group: consequences for wildlife conservation. PLOS ONE 9:e114916

    PubMed  PubMed Central  Google Scholar 

  • Estrada A, Raboy BE, Oliveira LC (2012) Agroecosystems and primate conservation in the tropics: a review. Am J Primatol 74:696–711

    PubMed  Google Scholar 

  • Estrada A, Garber PA, Rylands AB et al (2017) Impending extinction crisis of the world’s primates: why primates matter. Sci Adv 3:e1600946

    PubMed  PubMed Central  Google Scholar 

  • Fa JE, Brown D (2009) Impacts of hunting on mammals in African tropical moist forests: a review and synthesis. Mammal Rev 39:231–264

    Google Scholar 

  • FAO (2016) Global Forest Resources Assessment 2015: how are the world’s forest changing? 2nd edn. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • FAO (2017) Food and Agriculture Organization of the United Nations – FAOSTAT Database. http://www.fao.org/faostat/en/#data. Accessed 27 Nov 2017

  • Fedigan LM, Jack K (2001) Neotropical primates in a regenerating Costa Rican dry forest: a comparison of howler and capuchin population patterns. Int J Primatol 22:689–713

    Google Scholar 

  • Fedigan LM, Jack KM (2012) Tracking neotropical monkeys in Santa Rosa: lessons from a regenerating Costa Rican dry forest. In: Kappeler PM, Watts DP (eds) Long-term field studies of primates. Springer, Berlin/Heidelberg, pp 165–184

    Google Scholar 

  • Fernandes NCC d A, Cunha MS, Guerra JM et al (2017) Outbreak of yellow fever among nonhuman primates, Espirito Santo, Brazil, 2017. Emerg Infect Dis 23:2038–2041

    PubMed  PubMed Central  Google Scholar 

  • Foster RB (1982) The seasonal rhythm of fruitfall on Barro Colorado Island. In: Leigh EG Jr, Rand AS, Windsor DM (eds) The ecology of a tropical forest: seasonal rhythms and long-term changes. Smithsonian Institution Press, Washington, DC, pp 151–172

    Google Scholar 

  • Fuentes A, Gamerl S (2005) Disproportionate participation by age/sex classes in aggressive interactions between long-tailed macaques (Macaca fascicularis) and human tourists at Padangtegal Monkey Forest, Bali, Indonesia. Am J Primatol 66:197–204

    PubMed  Google Scholar 

  • Gaveau DLA, Wich SA, Marshall AJ (2016) Are protected areas conserving primate habitat in Indonesia? In: Wich SA, Marshall AJ (eds) An introduction to primate conservation. Oxford University Press, Oxford, pp 193–204

    Google Scholar 

  • Gogarten JF, Jacob AL, Ghai RR et al (2015) Group size dynamics over 15+ years in an African forest primate community. Biotropica 47:101–112

    Google Scholar 

  • Goldberg TL, Gillespie TR, Rwego IB et al (2008) Forest fragmentation as cause of bacterial transmission among nonhuman primates, humans, and livestock, Uganda. Emerg Infect Dis 14:1375–1382

    PubMed  PubMed Central  Google Scholar 

  • González-Suárez M, Revilla E (2013) Variability in life-history and ecological traits is a buffer against extinction in mammals. Ecol Lett 16:242–251

    PubMed  Google Scholar 

  • González-Suárez M, Gómez A, Revilla E (2013) Which intrinsic traits predict vulnerability to extinction depends on the actual threatening processes. Ecosphere 4:1–16

    Google Scholar 

  • Gonzalez-Voyer A, González-Suárez M, Vilà C, Revilla E (2016) Larger brain size indirectly increases vulnerability to extinction in mammals. Evolution 70:1364–1375

    PubMed  Google Scholar 

  • Gouveia SF, Villalobos F, Dobrovolski R et al (2014) Forest structure drives global diversity of primates. J Anim Ecol 83:1523–1530

    PubMed  Google Scholar 

  • Graham TL, Matthews HD, Turner SE (2016) A global-scale evaluation of primate exposure and vulnerability to climate change. Int J Primatol 37:158–174

    Google Scholar 

  • Hahn BH, Shaw GM, De KM et al (2000) AIDS as a zoonosis: scientific and public health implications. Science 287:607–614

    CAS  PubMed  Google Scholar 

  • Hanya G, Chapman CA (2012) Linking feeding ecology and population abundance: a review of food resource limitation on primates. Ecol Res 28:183–190

    Google Scholar 

  • Harper GJ, Steininger MK, Tucker CJ et al (2007) Fifty years of deforestation and forest fragmentation in Madagascar. Environ Conserv 34:325–333

    Google Scholar 

  • Hartter J, Ryan SJ, Southworth J, Chapman CA (2011) Landscapes as continuous entities: forest disturbance and recovery in the Albertine Rift landscape. Landsc Ecol 26:877

    Google Scholar 

  • Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford

    Google Scholar 

  • Hill CM (2000) Conflict of interest between people and baboons: crop raiding in Uganda. Int J Primatol 21:299–315

    Google Scholar 

  • Hill R (2005) Day length seasonality and the thermal environment. In: Brockman DK, van Schaik CP (eds) Seasonality in primates – studies of living and extinct human and non-human primates. Cambridge University Press, Cambridge/New York, pp 197–213

    Google Scholar 

  • Hoffman TS, O’Riain MJ (2011) The spatial ecology of chacma baboons (Papio ursinus) in a human-modified environment. Int J Primatol 32:308–328

    Google Scholar 

  • Hoffman TS, O’Riain MJ (2012) Landscape requirements of a primate population in a human-dominated environment. Front Zool 9:1

    PubMed  PubMed Central  Google Scholar 

  • Hogan JD, Melin AD (2018) Intra- and interannual variation in the fruit diet of wild capuchins: impact of plant phenology. In: Kalbitzer U, Jack KM (eds) Primate life histories, sex roles, and adaptability – essays in honour of Linda M. Fedigan. Springer, New York, pp 193–210

    Google Scholar 

  • IPCC (2013) Summary for policymaker. In: Stocker TF, Qin D, Plattner GK et al (eds) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge/New York, pp 1–30

    Google Scholar 

  • IPCC (2014) Climate change 2014: synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland

    Google Scholar 

  • Isbell LA (1991) Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behav Ecol 2:143–155

    Google Scholar 

  • IUCN (2016) IUCN Red List of Threatened Species. Version 2016–1

    Google Scholar 

  • Jack KM, Fedigan LM (2018) Alpha male capuchins (Cebus capucinus imitator) as keystone individuals. In: Kalbitzer U, Jack KM (eds) Primate life histories, sex roles, and adaptability – essays in honour of Linda M. Fedigan. Springer, New York, pp 91–109

    Google Scholar 

  • Jack KM, Kalbitzer U (2017) How to cultivate a tree: celebrating the career of Linda Marie Fedigan. Evol Anthropol Issues News Rev 26:139–142

    Google Scholar 

  • Jacob AL, Vaccaro I, Sengupta R et al (2008) Integrating landscapes that have experienced rural depopulation and ecological homogenization into tropical conservation planning. Trop Conserv Sci 1:307–320

    Google Scholar 

  • Janson C, Verdolin J (2005) Seasonality of primate births in relation to climate. In: Brockman DK, van Schaik CP (eds) Seasonality in primates – studies of living and extinct human and non-human primates. Cambridge University Press, Cambridge/New York, pp 307–350

    Google Scholar 

  • Johnson SE, Brown KA (2018) The specialist capuchin? Using ecological niche models to compare niche breadth in Mesoamerican primates. In: Kalbitzer U, Jack KM (eds) Primate life histories, sex roles, and adaptability – essays in honour of Linda M. Fedigan. Springer, New York, pp 311–326

    Google Scholar 

  • Johnson SE, Ingraldi C, Ralainasolo FB et al (2011) Gray-headed lemur (Eulemur cinereiceps) abundance and forest structure dynamics at Manombo, Madagascar. Biotropica 43:371–379

    Google Scholar 

  • Jones KE, Bielby J, Cardillo M et al (2009) PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals: ecological archives E090-184. Ecology 90:2648–2648

    Google Scholar 

  • Jones-Engel L, Engel GA, Schillaci MA et al (2005) Primate-to-human retroviral transmission in Asia. Emerg Infect Dis 11:1028

    PubMed  PubMed Central  Google Scholar 

  • Jones-Engel L, Engel GA, Heidrich J et al (2006a) Temple monkeys and health implications of commensalism, Kathmandu, Nepal. Emerg Infect Dis 12:900–906

    PubMed  PubMed Central  Google Scholar 

  • Jones-Engel L, Engel GA, Schillaci MA et al (2006b) Considering human–primate transmission of measles virus through the prism of risk analysis. Am J Primatol 68:868–879

    PubMed  Google Scholar 

  • Jones-Engel L, May CC, Engel GA et al (2008) Diverse contexts of zoonotic transmission of simian foamy viruses in Asia. Emerg Infect Dis 14:1200–1208

    CAS  PubMed  PubMed Central  Google Scholar 

  • Joppa LN, Pfaff A (2009) High and far: biases in the location of protected areas. PLOS ONE 4:e8273

    PubMed  PubMed Central  Google Scholar 

  • Joppa L, Pfaff A (2010) Reassessing the forest impacts of protection. Ann N Y Acad Sci 1185:135–149

    PubMed  Google Scholar 

  • Joppa LN, Loarie SR, Pimm SL (2008) On the protection of “protected areas”. Proc Natl Acad Sci 105:6673–6678

    CAS  PubMed  Google Scholar 

  • Kalbitzer U, Heistermann M, Cheney D et al (2015) Social behavior and patterns of testosterone and glucocorticoid levels differ between male chacma and Guinea baboons. Horm Behav 75:100–110

    CAS  PubMed  Google Scholar 

  • Kamilar JM, Baden AL (2014) What drives flexibility in primate social organization? Behav Ecol Sociobiol 68:1677–1692

    Google Scholar 

  • Kavanagh M (1980) Invasion of the forest by an African savannah monkey: behavioural adaptations. Behaviour 73:238–260

    Google Scholar 

  • Koenig A, Scarry CJ, Wheeler BC, Borries C (2013) Variation in grouping patterns, mating systems and social structure: what socio-ecological models attempt to explain. Philos Trans R Soc B Biol Sci 368:20120348–20120348

    Google Scholar 

  • Köndgen S, Kühl H, N’Goran PK et al (2008) Pandemic human viruses cause decline of endangered great apes. Curr Biol 18:260–264

    PubMed  Google Scholar 

  • Köndgen S, Calvignac-Spencer S, Grützmacher K et al (2017) Evidence for human Streptococcus pneumoniae in wild and captive chimpanzees: a potential threat to wild populations. Sci Rep 7:14581

    PubMed  PubMed Central  Google Scholar 

  • Laurance WF, Goosem M, Laurance SGW (2009) Impacts of roads and linear clearings on tropical forests. Trends Ecol Evol 24:659–669

    PubMed  Google Scholar 

  • Laurance WF, Sayer J, Cassman KG (2014) Agricultural expansion and its impacts on tropical nature. Trends Ecol Evol 29:107–116

    PubMed  Google Scholar 

  • Leroy EM, Rouquet P, Formenty P et al (2004) Multiple Ebola virus transmission events and rapid decline of central African wildlife. Science 303:387–390

    CAS  PubMed  Google Scholar 

  • Linder JM (2008) The impact of hunting on primates in Korup National Park, Cameroon: implications for primate conservation. City University of New York, New York

    Google Scholar 

  • Linder JM (2013) African primate diversity threatened by “new wave” of industrial oil palm expansion. Afr Primates 8:25–38

    Google Scholar 

  • Linder JM, Oates JF (2011) Differential impact of bushmeat hunting on monkey species and implications for primate conservation in Korup National Park, Cameroon. Biol Conserv 144:738–745

    Google Scholar 

  • Lovett JC, Marshall AR (2006) Why should we conserve primates? Afr J Ecol 44:113–115

    Google Scholar 

  • Marchal V, Hill C (2009) Primate crop-raiding: a study of local perceptions in four villages in north Sumatra, Indonesia. Primate Conserv 24:107–116

    Google Scholar 

  • Mbora DNM, Wieczkowski J, Munene E (2009) Links between habitat degradation, and social group size, ranging, fecundity, and parasite prevalence in the Tana River mangabey (Cercocebus galeritus). Am J Phys Anthropol 140:562–571

    PubMed  Google Scholar 

  • McDougall P, Forshaw N, Barrett L, Henzi SP (2010) Leaving home: responses to water depletion by vervet monkeys. J Arid Environ 74:924–927

    Google Scholar 

  • McGraw WS (2005) Update on the search for Miss Waldron’s red colobus monkey. Int J Primatol 26:605–619

    Google Scholar 

  • McKinney T (2015) A classification system for describing anthropogenic influence on nonhuman primate populations. Am J Primatol 77:715–726

    PubMed  Google Scholar 

  • McLennan MR, Spagnoletti N, Hockings KJ (2017) The implications of primate behavioral flexibility for sustainable human–primate coexistence in anthropogenic habitats. Int J Primatol 38:105–121

    Google Scholar 

  • Meijaard E, Albar G, Nardiyono et al (2010) Unexpected ecological resilience in Bornean orangutans and implications for pulp and paper plantation management. PLOS ONE e12813:5

    Google Scholar 

  • Mekonnen A, Fashing PJ, Bekele A et al (2017) Impacts of habitat loss and fragmentation on the activity budget, ranging ecology and habitat use of Bale monkeys (Chlorocebus djamdjamensis) in the southern Ethiopian Highlands. Am J Primatol 79:e22644

    Google Scholar 

  • Milton K (1982) Dietary quality and demographic regulation in a howler monkey population. In: Leigh EG Jr, Rand AS, Windsor DM (eds) The ecology of a tropical forest: seasonal rhythms and long-term changes. Smithsonian Institution Press, Washington, DC, pp 273–289

    Google Scholar 

  • Milton K, Giacalone J (2014) Differential effects of unusual climatic stress on capuchin (Cebus capucinus) and howler monkey (Alouatta palliata) populations on Barro Colorado Island, Panama. Am J Primatol 76:249–261

    PubMed  Google Scholar 

  • Moore RS, Nekaris KAI, Eschmann C (2010) Habitat use by western purple-faced langurs Trachypithecus vetulus nestor (Colobinae) in a fragmented suburban landscape. Endanger Species Res 12:227–234

    Google Scholar 

  • Morellato LPC, Alberton B, Alvarado ST et al (2016) Linking plant phenology to conservation biology. Biol Conserv 195:60–72

    Google Scholar 

  • Nunn CL, Barton RA (2001) Comparative methods for studying primate adaptation and allometry. Evol Anthropol Issues News Rev 10:81–98

    Google Scholar 

  • Oates JF (1996) Habitat alteration, hunting and the conservation of folivorous primates in African forests. Aust J Ecol 21:1–9

    Google Scholar 

  • Oates JF, Struhsaker T, McGraw S (2016) Piliocolobus waldronae. The IUCN red list of threatened species 2016: e.T18248A92649220. International Union for Conservation of Nature and Natural Resources (IUCN)

    Google Scholar 

  • Omeja PA, Obua J, Rwetsiba A, Chapman CA (2012) Biomass accumulation in tropical lands with different disturbance histories: contrasts within one landscape and across regions. For Ecol Manag 269:293–300

    Google Scholar 

  • Omeja PA, Jacob AL, Lawes MJ et al (2014) Changes in elephant abundance affect forest composition or regeneration. Biotropica 46:704–711

    Google Scholar 

  • Omeja PA, Lawes MJ, Corriveau A et al (2016) Recovery of tree and mammal communities during large-scale forest regeneration in Kibale National Park, Uganda. Biotropica 48:770–779

    Google Scholar 

  • Pacifici M, Visconti P, Butchart SHM et al (2017) Species’ traits influenced their response to recent climate change. Nat Clim Change 7:205

    Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Google Scholar 

  • Pebsworth PA, MacIntosh AJJ, Morgan HR, Huffman MA (2012) Factors influencing the ranging behavior of chacma baboons (Papio hamadryas ursinus) living in a human-modified habitat. Int J Primatol 33:872–887

    Google Scholar 

  • Peres CA, Dolman PM (2000) Density compensation in neotropical primate communities: evidence from 56 hunted and nonhunted amazonian forests of varying productivity. Oecologia 122:175–189

    CAS  PubMed  Google Scholar 

  • Phalan B, Bertzky M, Butchart SHM et al (2013) Crop expansion and conservation priorities in tropical countries. PLOS ONE 8:e51759

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pozo-Montuy G, Serio-Silva JC, Chapman CA, Bonilla-Sánchez YM (2013) Resource use in a landscape matrix by an arboreal primate: evidence of supplementation in black howlers (Alouatta pigra). Int J Primatol 34:714–731

    Google Scholar 

  • Purvis A, Gittleman JL, Cowlishaw G, Mace GM (2000) Predicting extinction risk in declining species. Proc R Soc Lond B Biol Sci 267:1947–1952

    CAS  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Raftery AE, Zimmer A, Frierson DMW et al (2017) Less than 2 °C warming by 2100 unlikely. Nat Clim Change 7:637–641

    CAS  Google Scholar 

  • Rands MRW, Adams WM, Bennun L et al (2010) Biodiversity conservation: challenges beyond 2010. Science 329:1298–1303

    CAS  PubMed  Google Scholar 

  • Reader SM, Laland KN (2002) Social intelligence, innovation, and enhanced brain size in primates. Proc Natl Acad Sci 99:4436–4441

    CAS  PubMed  Google Scholar 

  • Reed KE, Fleagle JG (1995) Geographic and climatic control of primate diversity. Proc Natl Acad Sci 92:7874–7876

    CAS  PubMed  Google Scholar 

  • Remis MJ, Jost Robinson CA (2012) Reductions in primate abundance and diversity in a multiuse protected area: synergistic impacts of hunting and logging in a congo basin forest. Am J Primatol 74:602–612

    PubMed  Google Scholar 

  • Rigby HT White CJ (2017) Amazon deforestation, once tamed, comes roaring back. N. Y. Times

    Google Scholar 

  • Robbins MM, Gray M, Fawcett KA et al (2011) Extreme conservation leads to recovery of the Virunga mountain gorillas. PLOS ONE 6:e19788

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rothman JM, Chapman CA, Struhsaker TT et al (2015) Long-term declines in nutritional quality of tropical leaves. Ecology 96:873–878

    PubMed  Google Scholar 

  • Rudran R, Fernandez-Duque E (2003) Demographic changes over thirty years in a red howler population in Venezuela. Int J Primatol 24:925–947

    Google Scholar 

  • Sapolsky RM, Share LJ (2004) A pacific culture among wild baboons: its emergence and transmission. PLoS Biol 2:534–541

    CAS  Google Scholar 

  • Schaffner CM, Rebecchini L, Ramos-Fernandez G et al (2012) Spider monkeys (Ateles geoffroyi yucatenensis) cope with the negative consequences of hurricanes through changes in diet, activity budget, and fission–fusion dynamics. Int J Primatol 33:922–936

    Google Scholar 

  • Schroeder J, Nakagawa S, Hinsch M (2011) Behavioural ecology is not an endangered discipline. Trends Ecol Evol 26:320–321. https://doi.org/10.1016/j.tree.2011.03.013

    Article  PubMed  Google Scholar 

  • Schwitzer C, Glatt L, Nekaris K, Ganzhorn J (2011) Responses of animals to habitat alteration: an overview focussing on primates. Endanger Species Res 14:31–38

    Google Scholar 

  • Scully EJ, Basnet S, Wrangham RW et al (2018) Lethal respiratory disease associated with human rhinovirus C in wild chimpanzees, Uganda, 2013. Emerg Infect Dis J 24:2

    Google Scholar 

  • Snaith TV, Chapman CA (2007) Primate group size and interpreting socioecological models: do folivores really play by different rules? Evol Anthropol Issues News Rev 16:94–106

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Sterck EHM (1999) Variation in langur social organization in relation to the socioecological model, human habitat alteration, and phylogenetic constraints. Primates 40:199–213

    CAS  PubMed  Google Scholar 

  • Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309

    Google Scholar 

  • Strier KB (2009) Seeing the forest through the seeds: mechanisms of primate behavioral diversity from individuals to populations and beyond. Curr Anthropol 50:213–228

    PubMed  Google Scholar 

  • Strier KB (2017) What does variation in primate behavior mean? Am J Phys Anthropol 162:4–14

    PubMed  Google Scholar 

  • Strier KB (2018) The temporal scale of behavioral and demographic flexibility: implications for comparative analyses and conservation. In: Kalbitzer U, Jack KM (eds) Primate life histories, sex roles, and adaptability – essays in honour of Linda M. Fedigan. Springer, New York, pp 19–33

    Google Scholar 

  • Strier KB, Ives AR (2012) Unexpected demography in the recovery of an endangered primate population. PLOS ONE 7:e44407

    CAS  PubMed  PubMed Central  Google Scholar 

  • Strier KB, Mendes SL (2012) The northern muriqui (brachyteles hypoxanthus): lessons on behavioral plasticity and population dynamics from a critically endangered species. In: Kappeler PM, Watts DP (eds) Long-term field studies of primates. Springer, Berlin/Heidelberg, pp 125–140

    Google Scholar 

  • Strier KB, Altmann J, Brockman DK et al (2010) The primate life history database: a unique shared ecological data resource. Methods Ecol Evol 1:199–211

    PubMed  PubMed Central  Google Scholar 

  • Strier KB, Lee PC, Ives AR (2014) Behavioral flexibility and the evolution of primate social states. PLoS ONE 9:e114099

    PubMed  PubMed Central  Google Scholar 

  • Struhsaker TT 1999 Ecology of an African rain forest: logging in Kibale and the conflict between conservation and exploitation. University Press of Florida, Gainesville, Fla

    Google Scholar 

  • Sussman RW, Richard AF, Ratsirarson J et al (2012) Beza Mahafaly Special Reserve: long-term research on lemurs in southwestern Madagascar. In: Long-Term Field Studies of Primates. Springer, Berlin, Heidelberg, pp 45–66

    Google Scholar 

  • Tacutu R, Craig T, Budovsky A et al (2013) Human ageing genomic resources: integrated databases and tools for the biology and genetics of ageing. Nucleic Acids Res 41:D1027–D1033

    CAS  PubMed  Google Scholar 

  • Vidal-García F, Serio-Silva JC (2011) Potential distribution of Mexican primates: modeling the ecological niche with the maximum entropy algorithm. Primates 52:261

    PubMed  Google Scholar 

  • Vilela B, Villalobos F (2015) letsR: a new R package for data handling and analysis in macroecology. Methods Ecol Evol 6:1229–1234

    Google Scholar 

  • Weng L, Boedhihartono AK, Dirks PHGM et al (2013) Mineral industries, growth corridors and agricultural development in Africa. Glob Food Secur 2:195–202

    Google Scholar 

  • Wheeler CE, Omeja PA, Chapman CA et al (2016) Carbon sequestration and biodiversity following 18 years of active tropical forest restoration. For Ecol Manag 373:44–55

    Google Scholar 

  • Wilkie DS, Wieland M, Boulet H et al (2016) Eating and conserving bushmeat in Africa. Afr J Ecol 54:402–414

    Google Scholar 

  • Wong BBM, Candolin U (2015) Behavioral responses to changing environments. Behav Ecol 26:665–673

    Google Scholar 

  • Wong SNP, Sicotte P (2007) Activity budget and ranging patterns of Colobus vellerosus in forest fragments in central Ghana. Folia Primatol (Basel) 78:245–254

    Google Scholar 

  • Wong SNP, Saj TL, Sicotte P (2006) Comparison of habitat quality and diet of Colobus vellerosus in forest fragments in Ghana. Primates 47:365–373

    PubMed  Google Scholar 

  • Woodford MH, Butynski TM, Karesh WB (2002) Habituating the great apes: the disease risks. Oryx 36(2)

    Google Scholar 

  • Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300

    Google Scholar 

  • Wright SJ, Calderón O (2006) Seasonal, El Niño and longer term changes in flower and seed production in a moist tropical forest. Ecol Lett 9:35–44

    CAS  PubMed  Google Scholar 

  • Wright SJ, Muller-Landau HC (2006) The future of tropical forest species. Biotropica 38:287–301

    Google Scholar 

  • Wright SJ, Carrasco C, Calderón O, Paton S (1999) The El Niño Southern Oscillation, variable fruit production, and famine in a tropical forest. Ecology 80:1632–1647

    Google Scholar 

  • Yamagiwa J (2010) Research history of Japanese macaques in Japan. In: The Japanese macaques. Springer, Tokyo, pp 3–25

    Google Scholar 

Download references

Acknowledgements

Most importantly, we want to thank Linda Fedigan for her inspiring research and the great collaboration during the last 3+ years (UK) and for the last 40+ years (CAC) and for giving us a good reason to having a great symposium in honour of her academic career (Jack and Kalbitzer 2017). Our motivation for this chapter came from our work in different primate habitats across the globe and the observation that some species are very successful in dealing with human pressures, while others disappear. Furthermore, UK is grateful that he had the opportunity to work with the PACE database at the University of Calgary for the last few years, which was very inspiring regarding the discovery of the potential lying in such datasets. We also thank Katharine Jack, Peter Henzi, and one anonymous reviewer for providing us with constructive feedback on earlier drafts of this manuscript. UK was funded by an Eyes High Postdoctoral Fellowship from the University of Calgary while writing this manuscript.

Author information

Authors and Affiliations

  1. Department of Anthropology and Archaeology, University of Calgary, Calgary, AB, Canada

    Urs Kalbitzer

  2. Department of Anthropology and McGill School of Environment, McGill University, Montreal, QC, Canada

    Urs Kalbitzer & Colin A. Chapman

  3. Makerere University Biological Field Station, Fort Portal, Uganda

    Colin A. Chapman

  4. Wildlife Conservation Society, Bronx, NY, USA

    Colin A. Chapman

  5. Section of Social Systems Evolution, Primate Research Institute, Kyoto University, Kyoto, Japan

    Colin A. Chapman

Authors
  1. Urs Kalbitzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Colin A. Chapman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Urs Kalbitzer .

Editor information

Editors and Affiliations

  1. Department of Anthropology and McGill School of Environment, McGill University, Montreal, QC, Canada, Department of Anthropology and Archaeology, University of Calgary, Calgary, AB, Canada

    Urs Kalbitzer

  2. Department of Anthropology, Tulane University, New Orleans, LA, USA

    Katharine M. Jack

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Kalbitzer, U., Chapman, C.A. (2018). Primate Responses to Changing Environments in the Anthropocene. In: Kalbitzer, U., Jack, K. (eds) Primate Life Histories, Sex Roles, and Adaptability. Developments in Primatology: Progress and Prospects. Springer, Cham. https://doi.org/10.1007/978-3-319-98285-4_14

Download citation

Publish with us

Policies and ethics

Search

Navigation