In our Master of Research in Primate Biology, Behaviour and Conversation, students acquire a good knowledge of the major areas of primate biology, behaviour and conservation, and of current debates and approaches in the discipline. This week we are featuring a literature review by Anna Cryer.
Anna’s bio: I’m a master’s student on the MRes Primate Biology, Behaviour and Conservation course. I’m interested in all things primate and primate conservation and behaviour in particular.
Introduction
Globally, 75% of all nonhuman primate (hereafter primate) species are declining and without effective action, there will be a major extinction (Feistner and Price, 2002; Estrada et al., 2017). Deforestation, hunting, wood extraction and illegal trade are the main drivers of primate decline, with unsustainable human activity threatening 60% of primate species with extinction (Estrada et al., 2017). The expansion of agriculture in primate regions is estimated to have resulted in 2 million km2 of forest loss between 1990-2010 (Estrada et al., 2017; Graham et al., 2016). There is little research yet into individual specialisation in primates but research from other species and on how primate populations respond to environmental change can be drawn on.
The ability to adapt to environmental changes varies both between species and amongst populations (Sih, 2013). Genetic adaptions allow some animals species to cope better with human disturbance, however species with slow life histories cannot adapt over a short period of time (Gruber et al., 2019), as is true for many primate species. Species must develop their own behaviour strategies to counter rapid environmental changes, with innovations often arising out of necessity (Gruber et al., 2019). On an individual level, personality or behaviour may inhibit or aid their response to environmental changes, with bold individuals better equipped to adopt new valuable resources (Sih, 2013).
Behavioural flexibility allows animals to adapt their behaviour in response to ecological change (Nowak and Lee, 2013) and this influences how well species can adapt to environmental changes (Sih, 2013; Snell-Rood, 2013). Habitat loss, fragmentation and degradation affects species differently and is dependent on species-specific traits (Estrada et al., 2017). A number of primate species have adapted to living in human-altered environments or using alternative food sources, for example long-tailed and rhesus macaques (Marty et al., 2020), Red-colobus (Milich et al., 2014), Barbary macaques (Ménard et al., 2014), Hamadryas baboons (Schreier and Swedell, 2008), and black-and-gold howlers (Bicca-Marques et al., 2009). Long-tailed macaque populations in Malaysia inhabit popular tourist sites, relying on visitors for food handouts (Marty et al., 2020). In India, Hanuman langurs living in urban areas were buffered against catastrophic droughts due to novel food sources while populations living in protected areas suffered severe declines (Waite et al., 2007). While some species benefit from their interactions with humans, others are being pushed to the remaining, rapidly decreasing habitat. In Madagascar, 87% of primates are threatened (Estrada et al., 2017) and severe environmental change means that it is likely lemurs now inhabit very different environments than they evolved to live in (Cuozzo and Sauther, 2015).
Individual Specialisation
Emerging from the belief that individual variation was rare or not enough to make a difference to the population level diet studies, traditional foraging theory considered population niches to be the same for all individuals across a population (Bolnick et al., 2002). Populations historically were classified as either specialist or generalist (Dermond et al., 2018), however studies across a range of species have found that there are levels of specialisation within a population, with individuals having different dietary niches, for example oystercatchers (Goss-Custard and Durell, 1988), sea otters (Tinker et al., 2008), European badgers (Robertson et al., 2015), bottlenose dolphins (Rossman et al., 2015), brown trout (Dermond et al., 2018), North American moose (Jesmer et al., 2020) and banded mongoose (Sheppard et al., 2018). An individual specialist is an individual who occupies a dietary niche that is substantially narrower than its populations niche and this narrowing is not a result of age, sex or morphological group (Bolnick et al., 2003; Araújo et al., 2011). Individual specialisation, the overall presence of individual specialists in a population (Bolnick et al., 2003), can arise under different circumstances and effects differ between populations. In populations without individual specialisation, all individuals can survive until the food supply is exhausted and then the population may crash, whereas in populations with specialists, resource declines may affect individuals differently (Durell, 2000), increasing survival chances.
The total niche width (TNW) framework, initially proposed by Roughgarden (1972) to assess between and within phenotype dietary differences, has been adapted to assess individual specialisation in a population, measuring between and within individual differences (Bolnick et al., 2003). TNW is divided into two components, the within-individual component (WIC) and the between-individual component (BIC). WIC is the average variance of resources found within an individual’s diet while BIC measures the dietary variation between individuals (Figure 1) (Bolnick et al., 2003; Araújo et al., 2011). Research into individual specialisation in vertebrates is biased towards fish (Araújo et al., 2011) with currently little research published into individual specialisation in primates.
Figure 1: Schematic illustrating how individual diets can differ in a population. Dotted line is the TNW and solid lines are the resources used by individuals in a population. The TNW = BIC + WIC. A is a population of generalists where the WIC is large relative to TNW. B is a population of individual specialists with a small WIC relative to TNW (adapted from Bolnick et al. 2003).
Benefits of specialisation
Specialists are generally assumed to be more efficient foragers than generalists (Robertson et al., 2015) as specialisation allows individuals to become experts in a specific food item and increase their processing time (Bernstein, 1979). Sea otters who had specialised to a specific prey type are able to process 25% more prey items per unit of time compared to those who have not specialised (Tinker et al., 2008). For primate species dealing with changing environments, being able to process food faster could have many benefits. If resource competition is increasing due to restricting habitat sizes (Durell, 2000), the ability to process food faster than conspecifics may allow individuals to outcompete others and access more food. Specialising in a food processing technique can reduce susceptibility to interference from peers. Oystercatchers of the same rank, specialising in stabbing technique to open mussels were less vulnerable to interference than those who specialised in a hammering technique (Goss-Custard and Durell, 1988).
For group living primates, individual specialisation may be a strategy to cope with group living (Sheppard et al., 2018), reducing within group conflict for food (Rossman et al., 2015; Sheppard et al., 2018). Intraspecies competition can lead to an increase in individual specialisation (Araújoe et al., 2011; Jones et al., 2020), widening the TNW of a population (Paz Cardozo et al., 2020). Habitat change or loss creates increased competition for the remaining resources (Durell, 2000) and individuals who are already specialised may benefit from using alternative food sources. Individual specialisation in fur seals allows mothers to adapt to intense intraspecies resource competition, aiding their own and their offspring’s survival (Jones et al., 2020).
In socially grouped primates, there is an overall agreement in research that social bonds influence foraging through rank, kinship and social bond strength (Marshall et al., 2012, 2015). Individual specialisation requires time spent learning new resource capturing techniques which could be spent foraging on an already known resource (Woo et al., 2008). High-ranked individuals have overall better fitness (Marty et al., 2020), enabling them to afford this risk and learn new techniques. High-ranked rhesus macaques in India had better access to human food, dominating this food source and maintaining their rank by increased fitness from high calorie food sources (Marty et al., 2020). Individual specialisation as a result of rank is not considered true specialisation from an evolutionary perspective as foraging behaviour is restricted to a subset of the populations but not as a result of choice (Bolnick et al., 2003). In studies of individual specialisation where subordinates were excluded from preferred feeding sites, they moved into these areas when mature or dominant individuals were removed, suggesting that these feeding sites were preferred and more profitable (Durell, 2000). Despite this, when high-ranking individuals are present, individual specialisation will persist and those who are able to specialise may continue to profit from human environments.
Dietary flexibility and environmental changes
Some populations of primates are able to thrive in human altered environments, such as Olive baboons (Warren et al., 2008) and rhesus and long-tailed macaques (Marty et al., 2020); however, others – like Sumatran orangutans (Carne et al., 2012) and pied tamarins (Farias et al., 2015) – will suffer. Dietary flexibility allows primates to adapt to environments which differ from their natural habitat. Barbary macaques have been recorded feeding on a different herbaceous layer to domestic herbivores with whom they are in direct competition, accessing new food sources from arboreal or underground layers (Ménard et al., 2014). Red colobus monkeys in Uganda have adapted to living in a logged habitat with population densities similar to an old-growth forest environment (Milich et al., 2014). By expanding their diets, red colobus females were able to live successfully in an altered environment and this dietary expansion appears to be a common response in primates to ecological stressors (Milich et al., 2014). Black-and-gold howlers have been recorded consuming chicken eggs in Brazil, where one sub-adult male in particular learned to raid chicken roosts, accessing a novel protein source (Bicca-Marques et al., 2009). Dietary flexibility in these primate populations has allowed species to expand their TNW to adapt to habitat loss or agricultural expansion.
Chacma baboons in Cape Town are a prime example of primates adapting to environmental change. Displaced from large areas of their natural home range due to expanding agriculture or urbanisation, baboons have adapted to the transformed landscapes where people now dominate and who provide abundant resources for the baboons to feed on (van Doorn and O’Riain, 2020). Specialisation has allowed individuals (usually adult males) to access high energy resources; food in urban environment has a 10x greater energy intake per bite compared with food sources in their natural environment (Fehlmann et al., 2017). However, there are increased risks associated with this through human-wildlife conflict and encounters with domestic animals (Fehlmann et al., 2017). Individual specialisation mean that the risks faced by a population are not equally distributed across the population (Durell, 2000) as it can alter an individual’s predation risk, reproductive success or pathogen exposure (Rossman et al., 2015).
In unstable environments, specialisation can be more difficult (Dermond et al., 2018) which may force individuals to become more generalist. North American moose expanded their TNW when food sources became limited with increased WIC making individuals more generalist foragers (Jesmer et al., 2020). When food sources were not limited, TNW was smaller and individuals were more specialised (Jesmer et al., 2020). As climate change and human disturbance continues, many environments will become more unstable and less predictable, which may force individuals to generalise in order to maintain their energetic requirements or face extinction.
Conclusion
Dietary flexibility and individual specialisation will affect how primate species are impacted by environmental changes. Individual specialisation can increase food processing time and help reduce intraspecies competition which could aid population survival in shrinking habitats. The social structure of a primate group will affect how individuals respond to environmental change, with high-ranked individuals likely to do better. Species that are relatively dietarily flexible will be more resilient and cope better with changes. However, the increasing unpredictability of environmental change will make it harder for populations to maintain a low WIC and may push individuals to become more generalist if they cannot acquire novel food sources. To effectively implement conservation measures, understanding primate foraging patterns in the ecosystems they inhabit is critical.
References
Araújo, M. S., Bolnick, D. I. and Layman, C. A. (2011) ‘The ecological causes of individual specialisation’, Ecology Letters, 14(9), pp. 948–958. doi: 10.1111/j.1461-0248.2011.01662.x.
Bernstein, R. A. (1979) ‘Evolution of Niche Breadth in Populations of Ants’, The American Naturalist, 114(4), pp. 533–544. doi: 10.1086/283500.
Bicca-Marques, J. C. et al. (2009) ‘Habitat impoverishment and egg predation by Alouatta caraya’, International Journal of Primatology, 30(5), pp. 743–748. doi: 10.1007/s10764-009-9373-y.
Bolnick, D. I. et al. (2002) ‘Measuring individual-level resource specialization’, Ecology, 83(10), pp. 2936–2941. doi: 10.1890/0012-9658(2002)083[2936:MILRS]2.0.CO;2.
Bolnick, D. I. et al. (2003) ‘The ecology of individuals: Incidence and implications of individual specialization’, American Naturalist, 161(1), pp. 1–28. doi: 10.1086/343878.
Cuozzo, F. P. and Sauther, M. L. (2015) ‘Patterns of dental macrowear in subfossil lemur catta from ankilitelo cave, madagascar: Indications of ecology and habitat use over time’, Folia Primatologica, 86(1–2), pp. 140–149. doi: 10.1159/000369900.
Dermond, P., Thomas, S. M. and Brodersen, J. (2018) ‘Environmental stability increases relative individual specialisation across populations of an aquatic top predator’, Oikos, 127(2), pp. 297–305. doi: 10.1111/oik.04578.
van Doorn, A. C. and O’Riain, M. J. (2020) ‘Nonlethal management of baboons on the urban edge of a large metropole’, American Journal of Primatology, 82(8), pp. 1–8. doi: 10.1002/ajp.23164.
Durell, S. E. A. L. V. D. (2000) ‘Individual feeding specialisation in shorebirds: Population consequences and conservation implications’, Biological Reviews, 75(4), pp. 503–518. doi: 10.1111/j.1469-185X.2000.tb00053.x.
Estrada, A. et al. (2017) ‘Impending extinction crisis of the world’s primates: Why primates matter’, Science Advances, 3(1). doi: 10.1126/sciadv.1600946.
Farias, I. P. et al. (2015) ‘Effects of Forest Fragmentation on Genetic Diversity of the Critically Endangered Primate, the Pied Tamarin (Saguinus bicolor): Implications for Conservation’, Journal of Heredity, 106(S1), pp. 512–521. doi: 10.1093/jhered/esv048.
Fehlmann, G. et al. (2017) ‘Extreme behavioural shifts by baboons exploiting risky, resource-rich, human-modified environments’, Scientific Reports, 7(1), pp. 1–8. doi: 10.1038/s41598-017-14871-2.
Feistner, A. T. C. and Price, E. C. (2002) ‘Zoos and Universities: Collaborating for Primate Conservation’, Evolutionary Anthropology, 11(SUPPL. 1), pp. 7–11. doi: 10.1002/evan.10042.
Goss-Custard, J. D. and Durell, S. E. A. L. V. D. (1988) ‘The Effect of Dominance and Feeding Method on the Intake Rates of Oystercatchers, Haematopus ostralegus, Feeding on Mussels’, The Journal of Animal Ecology, 57(3), p. 827. doi: 10.2307/5095.
Graham, T. L., Matthews, H. D. and Turner, S. E. (2016) ‘A Global-Scale Evaluation of Primate Exposure and Vulnerability to Climate Change’, International Journal of Primatology, 37(2), pp. 158–174. doi: 10.1007/s10764-016-9890-4.
Gruber, T. et al. (2019) ‘Cultural change in animals: a flexible behavioural adaptation to human disturbance’, Palgrave Communications, 5(1), pp. 1–9. doi: 10.1057/s41599-019-0271-4.
Jesmer, B. R. et al. (2020) ‘A test of the Niche Variation Hypothesis in a ruminant herbivore’, Journal of Animal Ecology, (September), pp. 2825–2839. doi: 10.1111/1365-2656.13351.
Jones, K. A. et al. (2020) ‘Stable Isotope Values in South American Fur Seal Pup Whiskers as Proxies of Year-round Maternal Foraging Ecology’, Marine Biology, 167(10), pp. 1–11. doi: 10.1007/s00227-020-03760-4.
Marshall, H. H. et al. (2012) ‘Exploring foraging decisions in a social primate using discrete-choice models’, American Naturalist, 180(4), pp. 481–495. doi: 10.1086/667587.
Marshall, H. H. et al. (2015) ‘Social effects on foraging behavior and success depend on local environmental conditions’, Ecology and Evolution, 5(2), pp. 475–492. doi: 10.1002/ece3.1377.
Marty, P. R. et al. (2020) ‘Individuals in urban dwelling primate species face unequal benefits associated with living in an anthropogenic environment’, Primates, 61(2), pp. 249–255. doi: 10.1007/s10329-019-00775-4.
Ménard, N. et al. (2014) ‘Effect of habitat quality on diet flexibility in Barbary macaques’, American Journal of Primatology, 76(7), pp. 679–693. doi: 10.1002/ajp.22262.
Milich, K. M. et al. (2014) ‘Female red colobus monkeys maintain their densities through flexible feeding strategies in logged forests in Kibale National Park, Uganda’, American Journal of Physical Anthropology, 154(1), pp. 52–60. doi: 10.1002/ajpa.22471.
Nowak, K. and Lee, P. C. (2013) ‘Specialist primates can be flexible in response to habitat Alteration’, Primates in Fragments: Complexity and Resilience, (July 2014), pp. 199–211. doi: 10.1007/978-1-4614-8839-2_14.
Paz Cardozo, A. L. et al. (2020) ‘Habitat complexity and individual variation in diet and morphology of a fish species associated with macrophytes’, Ecology of Freshwater Fish, (August), pp. 1–13. doi: 10.1111/eff.12574.
Robertson, A. et al. (2015) ‘Resource availability affects individual niche variation and its consequences in group-living European badgers Meles meles’, Oecologia, 178(1), pp. 31–43. doi: 10.1007/s00442-014-3202-5.
Rossman, S. et al. (2015) ‘Individual specialization in the foraging habits of female bottlenose dolphins living in a trophically diverse and habitat rich estuary’, Oecologia, 178(2), pp. 415–425. doi: 10.1007/s00442-015-3241-6.
Sheppard, C. E. et al. (2018) ‘Intragroup competition predicts individual foraging specialisation in a group-living mammal’, Ecology Letters, 21(5), pp. 665–673. doi: 10.1111/ele.12933.
Sih, A. (2013) ‘Understanding variation in behavioural responses to human-induced rapid environmental change: A conceptual overview’, Animal Behaviour, 85(5), pp. 1077–1088. doi: 10.1016/j.anbehav.2013.02.017.
Snell-Rood, E. C. (2013) ‘An overview of the evolutionary causes and consequences of behavioural plasticity’, Animal Behaviour, 85(5), pp. 1004–1011. doi: 10.1016/j.anbehav.2012.12.031.
Tinker, M. T., Bentall, G. and Estes, J. A. (2008) ‘Food limitation leads to behavioral diversification and dietary specialization in sea otters’, Proceedings of the National Academy of Sciences of the United States of America, 105(2), pp. 560–565. doi: 10.1073/pnas.0709263105.
Waite, T. A. et al. (2007) ‘Sanctuary in the city: Urban monkeys buffered against catastrophic die-off during ENSO-related drought’, EcoHealth, 4(3), pp. 278–286. doi: 10.1007/s10393-007-0112-6.
Woo, K. J. et al. (2008) ‘Individual specialization in diet by a generalist marine predator reflects specialization in foraging behaviour’, Journal of Animal Ecology, 77(6), pp. 1082–1091. doi: 10.1111/j.1365-2656.2008.01429.x.
