Primates and climate change: A review of current knowledge

Source: Korstjens, A. H., & Hillyer, A. P. (2016). Primates and climate change: A review of current knowledge. An introduction to primate conservation, 175-192.

Part Two: Vulnerability

One of the major issues for conservation is trying to determine which species needs conserving more urgently. Vulnerability, in special regard to climate change, is complex and all the issues and how they interact must be considered.

With that, I’d like to introduce the below framework created by Foden et al. (2013), which identifies the species most vulnerable to extinction from a range of climate change-induced stressors. Three dimensions of vulnerability were identified:

  • Sensitivity (the lack of potential for a species to persist in situ)
  • Exposure (the extent to which each species’ physical environment will change)
  • Low adaptive capacity (a species’ inability to avoid the negative impacts of climate change through dispersal and/or micro-evolutionary change)

There are also five species-typical biological traits associated with vulnerability: (1) diet and dietary specialization, (2) life-history traits and phenology, (3) biogeographical range, rarity, and dispersal system, (4) social system and behaviour, and (5) physical traits.

A climate change vulnerability framework showing four levels of vulnerability. Foden et al. (2013) used biological traits from
amphibian, bird, and coral species to illustrate how climate change exposure, species’ sensitivity (affected by specialization, rarity, physiological
tolerance, and dependence on environmental triggers or inter-specific interactions), and low adaptive capacity (determined by gene flow, genetic
diversity, and reproductive rates) influence the vulnerability of a species. Examples for primates for each category could be (see text to understand
why species are included in particular categories): 1. Many of the Malagasy lemurs, especially specialist folivores, and Pongo spp.; 2. Colobus spp.;
Macaca sylvanus; and 4. few primate habitats are unaffected (low exposure), although Neotropical endemics in the Amazon and Pan paniscus
may currently fall into this category. Reproduced with permission from Foden and PLoS One.

Diet and dietary specialisation

The more specialised a species’ diet, the more vulnerable they are to environmental change because they won’t be able to adapt to changes through dietary shifts. The most obvious example would be the giant panda which survives almost entirely on bamboo. The good news is that primates tend to be reasonably flexible in their diets, compared to other mammals and will often eat a mixture of vegetative plant matter, reproductive plant parts (fruit, seeds and flowers), gum and sap, and insects/fauna.

Species that are specialist folivores are particularly vulnerable because of the effect rising temperatures and lower rainfall will have on plant matter. Leaves would become less digestible, have lower quality and higher concentrations of toxins. This has already been documented in a study by King et al. (2005), where decreased rainfall led to more fibrous leaves. This in turn, wore down the animals’ teeth and older females were unable to produce sufficient milk during drier periods, leading to infant mortality.

Higher temperatures have also been linked with smaller livers (Moore et al. 2015) which means specialist folivores may be unable to deal with more toxic diets. Ultimately this means that folivores could be especially vulnerable to global warming.

There are potential benefits for some species, as fruit production should theoretically increase with rising CO2 levels. However, as described in my last post, the impact of climate change could cause phenological shifts in food sources so the life cycles between primates and their food becomes desynchronised. There is also the potential for any positive effects to be offset by other climatic stressors such as intensive rain or drought.

Drought could be a particular issue in Africa, as detailed by Tutin et al. (1997). They found that food scarcity can last for up to eight months during the dry season in the Lopé Reserve (Gabon), and while two out of eight primate species will change to nonfruit diets, chimpanzees and three guenon species do not.

Life-history traits and phenology

The particularly vulnerable primates are those with slow life cycles, small litters and low reproductive rates. Whilst most primates share these characteristics, it is the Haplorrhines that are especially vulnerable. Known as the “dry-nosed” primates, they include new world monkeys and old world monkeys, including the apes. These primates mostly have single births and larger new-borns who have a longer dependency on their mother. Climate change will affect many species of primates, but it is the ones that have slow life-cycles that will face the greatest pressure.

I wrote about phenology last time, but primates living in low and high latitudes are more likely to have synchronised their breeding events with their seasonal habitats. Disruption of this synchrony can lead to infant and mother mortality, lower reproductive rates, higher vulnerability to disease and later age at maturity. It’s those who cannot response to changes through diet switching and range change that will be most vulnerable.

Biogeographical range, rarity and dispersal system

It’s important to consider that risks to a population come in all shapes and sizes. Across time, populations and ranges are shaped by random factors (such as disease outbreaks or natural disasters), historical patterns, dispersal ability and habitat fragmentation. These risks aren’t necessarily that problematic, however climate change will make them far worse. Species with restricted ranges, low density populations or those with limited dispersal ability won’t be able to recruit individuals into the population and with have a limited ability to spread to new areas.

This dispersal limitation has been shown to be a stronger determinant of community composition than ecological niche availability for primates. Ultimately, this means that dispersal limitations could determine the ability of a species to adapt to climate change via range shifting (Beaudrot & Marshall 2011).

You can apply it to the human world – If you have a mortgage, elderly parents or sick children, you may not be able to just up sticks and leave. You’re limited to your area. This applies to primates too. Those that are reliant on close-kin and/or long-term alliance partners have the greatest level of dispersal limitation. Leaving an area can be costly because it exposes the individual to predation and without local knowledge of food sources.

Currently, sex-biased dispersal is the typical form of dispersal in primates because it mostly functions to prevent inbreeding. Individuals will move out of their natal group and find another group to breed into. However, sex-biased dispersal limits the species because only one sex with seek out new areas and multi-sex groups need a long time to establish themselves.

Realistically, this would mean that nearly all primates would be unable to disperse fast enough to keep pace with the habitat shifting associated with climate change. It is estimated that the average range reduction in primates could be close to 75% (Schloss et al. 2012).

Social system

Very similar to the point above, those species that are reliant on close bonds are vulnerable because of their reduced ability to adapt to change. Most primates need bonded social groups for access to food, thermoregulation, information transfer and reduced predation risk. Climate change will cause a cascade of issues and behaviour changes that’ll put primates at greater risk.

Climate change leads to ecological stress, which leads to increased competition, which leads to smaller, dispersed groups, which leads to increased vulnerability to predation or thermal stress. This is particularly true for those who live in temperate regions or high altitudes, where they may need large groups for survival.

Ecological stress could lead to food shortages and higher competition among individuals. This in turn, could lead to reduced group sizes.

Primate physiological and anatomical functions

The physical characteristics of a species can determine how flexibly they can respond to fast-changing environmental conditions. For example, highly arboreal primates may struggle to cross open areas in between trees or forest patches to reach emerging habitats or resources. The more fragmented the environment becomes, the harder it will be to move between areas.

Body size is another predictor of vulnerability. For example, small body size in mammals is correlated with a fast metabolic rate that increases with rising temperatures (the Arrhenius effect). This means that small primates will have greater energy expenditure in warmer climates.

Predicting species’ responses to climate change

We shouldn’t forget that primates are reasonably adaptable and there are papers detailing how they have successfully adapted to environmental changes:

  • Long-tailed macaques successfully adapted to habitat damage caused by severe drought and fire through: diet-shifting, increasing the size of their home range; and increasing terrestrial travel (Berenstain 1986).
  • Geoffroy’s spider monkey adapted to habitat change caused by a hurricane through time budget changes, increased fission-fusion dynamics and dietary shifting.

However, some species may well struggle. For example, the barbary macaques of the Atlas Mountains in Morocco are unable to keep up with demands on feeding time during extreme winters, leading to high mortality. Gorillas would need to adopt a greater level of fission-fusion dynamics and increased reliance on fruit to be able to adapt to changes and orang-utans would need to adopt extremely dispersed social systems.

Conclusion

Vulnerability to climate change is not as simple as producing a list of different areas as I have just done. They all interconnected and will hit primates at the same time. Apply it to the small lemurs that I was writing about earlier on:

A small lemur species would face:

  • Higher disease rates, with the most harmful parasites expanding the greatest
  • Leaves with higher toxic chemical concentrations, but smaller livers
  • More fibrous leaves leading to insufficient milk production in older females
  • Disruption of synchrony leading to higher infant mortality rates, lower reproductive rates, higher vulnerability to disease and later age at maturity (<– which also links to above point)
  • Increasingly unreliable food sources, but higher energy expenditure
  • Greater climatic stress caused by drought or intensive rain
  • We also add to the list: increasing damage by humans through hunting, the pet trade, deforestation and habitat fragmentation

And we’re talking about one individual species only, let alone all the other primate species.


References:

Beaudrot, L. H. and Marshall, A. J. (2011). Primate communities are structured more by dispersal limitation than by niches. Journal of Animal Ecology 80: 332–341.

Berenstain, L. (1986). Responses of long-tailed macaques to drought and fire in Eastern Borneo: a preliminary report. Biotropica 18: 257–262.

Foden, W. B., Butchart, S. H. M., Stuart, S. N., Vié, J.-C., Akçakaya, H. R., et al. (2013). Identifying the world’s most climate change vulnerable species: a systematic trait-based assessment of all birds, amphibians and corals. PLoS One 8: e65427.

King, S. J., Godfrey, L. R., Arrigo-Nelson, S. J., Pochron, S. T., Wright, P. C., et al. (2005). Dental senescence in.a long-lived primate links infant survival to rainfall. Proceedings of the National Academy of Sciences of the United States of America 102: 16579–16583.

Moore, B. D., Wiggins, N. L., Marsh, K. J., Dearing, M. D., and Foley, W. J. (2015). Translating physiological signals to changes in feeding behaviour in mammals and the future effects of global climate change. Animal Production Science 55: 272–283.

Schloss, C. A., Nuñez, T. A., and Lawler, J. J. (2012). Dispersal will limit ability of mammals to track climate change in the Western Hemisphere. Proceedings of the National Academy of Sciences 109: 8606–8611.

Tutin, C. E. G., Ham, R. M., White, L. J. T., and Harrison, M. J. S. (1997). The primate community of the Lopé reserve, Gabon: diets, responses to fruit scarcity, and effects on biomass. American Journal of Primatology 42: 1–24.

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