Stressed-out primates

The endangered black lion tamarin, (Leontopithecus chrysopygus), lives in mostly degraded and highly fragmented landscape in the state of Sao Paulo, Brazil.  Olivier Kaisin is a PhD student who wants to know whether declining environmental conditions are causing increased stress to the tamarins. Researchers often use glucocorticoid (GC) levels as a measure of physiological stress, as many animals, including primates, produce and release GCs in response to stress.  Many researchers have argued that prolonged elevation of GC levels has a negative impact on individual survival or reproduction, but it is not clear whether this is true for most primates. Given that 60% of primate species are currently threatened with extinction, it would be nice to know whether conservation biologists could use GC levels to identify populations that are at risk.

The black lion tamarin, Leontopithecus chrysopygus.

One of the unadvertised features of graduate programs is that students need to learn about their study system before doing research. In this spirit, before beginning his tamarin study, Kaisin (working with several other researchers) did a meta-analysis of all studies (published until 2020) that compared cortisol levels in primates from disturbed vs. undisturbed habitats to see if the type of disturbance influenced GC levels.  Disturbance types included hunting, tourism, habitat loss, ongoing logging, habitat degradation and other human activities.  Habitat loss was a reduction in forest fragment size to less than 500 hectares.  Habitat degradation resulted from logging in the past 20 years that led to changes in forest structure and diversity, but did not substantially reduce the size of the forest habitat.  Other human activities did not fit into the five disturbance types, and included activities such as mining, urbanization and access to rubbish.

The graph below shows the effects of the different disturbance types.  “Hedges g” is a test statistic used in meta-analyses to look for effects of different variables.  The midpoint of the bar (or the diamond in the case of the overall effect) is the mean value of Hedges g, while the endpoints of each bar (or diamond) indicate the 95% confidence interval.  If the entire interval does not overlap 0, then we can conclude that there is a statistically significant effect of that variable.  Based on this analysis, both hunting and habitat loss were associated with significant increases in glucocorticoid levels in primates, contributing to a significant overall increase in glucocorticoid levels in response to disturbance.

The influence of six types of disturbance on GC levels of 24 different primate species. * indicates statistically significant effects.

As Kaisin and his colleagues point out, six of the studies actually showed a significant decrease in GC levels in association with disturbance.  For example, howler monkeys had reduced GC levels in response to ongoing logging.  The researchers interpret this surprising GC decrease on the elimination of large predators from the logged forest, which substantially reduces howler monkey stress levels. As a second example, in Madagascar, an invasive tree species in the degraded site provided important fruits for red-bellied lemurs, leading to well-fed lemurs with reduced GC levels. Unfortunately, these confounding variables cannot be easily controlled, so researchers need to consider each study on a case-by-case basis. Some families of primates were more influenced by stress than others. In particular, hominids (great apes) and atelids (New World monkeys such as howler, spider and woolly monkeys) both showed significantly greater GC levels in association with stress.  Three families showed smaller increases while three other families of primates were basically unaffected.

The influences of disturbance on eight different primate families (as measured by Hedges g). CI (95%) is the 95 percent confidence interval. Weight is a measure of the contribution of each primate family to the overall effect. Families with more species/studies contribute more weight to the overall effect

The researchers emphasize that many more studies are needed in order to understand when we should expect stress to elevate GC levels in primates.  For example, only one of the studies looked at stress effects on Asian primates. Future studies in endocrinological primatology should relate how prolonged stress influences fitness – including survival, growth and development and reproductive success.  In turn, this would allow the conservation community to understand the relationship between stress and future population viability.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Kaisin, O., Fuzessy, L., Poncin, P., Brotcorne, F. and Culot, L., 2021. A meta‐analysis of anthropogenic impacts on physiological stress in wild primates. Conservation Biology35(1), pp.101-114. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2021 by the Society for Conservation Biology. All rights reserved.

Biodiversity: it’s who you are

It is a massive understatement that ecologists and conservation biologists are profoundly interested in how disturbance affects biological diversity. Humans are disturbing ecosystems by degrading or destroying habitat, by fragmenting habitat into pieces that are too small to sustain populations, by directly overexploiting species for consumption or other purposes, and by introducing non-native species (and there’s more!). Some biologists argue that disturbance has gotten so severe that we need to modify our worldview of ecosystems. They argue, for example, that intact grasslands are so rare that we should stop talking about them as an ecosystem (or biome), but rather should more realistically explore the ecology of different types of croplands, which are, in actuality, primarily disturbed grasslands.

Some types of ecosystems, such as rainforests, have survived human impact more than others, but all have been highly disturbed. So it is fitting that conservation ecologists devote their attentions to understanding how disturbance influences biological diversity. Working in Cameroon in 1998, John Lawton and his colleagues assessed species richness (number of different species) in relation to level of disturbance experienced by eight different animal groups: canopy beetles, flying beetles, butterflies, canopy ants, leaf-litter ants, nematodes, termites, and birds. They discovered that more intense disturbances were associated with a significant reduction in species richness for many of the groups.

Fluss_Dja_Somalomo

Tropical forest in Cameroon. Credit: Earwig via Wikimedia Commons

Nigel Stork worked with Lawton on the original study, and recently reanalyzed the data in the context of changes that have occurred in how conservation biologists view biological diversity. For example, many biologists now argue that conserving biological diversity requires understanding which species are affected by disturbance, rather than the number of species. In addition, not all disturbances have similar impacts on biological diversity. For example, logging with heavy equipment removes trees and compacts soil, while logging with lighter equipment does not compact soil, so the two treatments may have very different impacts. Finally, it may be more informative to group species according to ecosystem function rather than by taxonomic group.

StorkFig1

Locations of sampling plots within the Mbalmayo Forest Reserve, Cameroon.  The three blown-up sites had multiple plots with different levels of disturbance, as indicated by the key.

Stork and his colleagues only had data for six of the original eight taxonomic groups. They categorized intensity of disturbance based on how much tree biomass was removed, level of soil compaction, time since disturbance, and tree cover and diversity at time of sampling. This allowed the researchers to assign a disturbance index to each plot, with 0 indicating least disturbed and 1.0 indicating most disturbed. This analysis showed no significant relationship between disturbance and species richness in five of the six taxonomic groups, with only termites declining in richness in response to disturbance.

StorkFig3

Species richness in relation to intensity of disturbance for six taxonomic groups considered in the study.

Stork and his colleagues used a slightly different approach to assess the response of species composition (the identity of species that are actually present in the community) to disturbance. They compared each pair of surveyed plots in relation to how different they were in disturbance. Plots with very different levels of disturbance had disturbance dissimilarities close to 1.0, while plots with similar levels of disturbance had disturbance dissimilarities near 0. They then looked at community dissimilarity to explore changes in species composition. Plots with a community dissimilarity near 1.0 had very different species, while plots with a community dissimilarity near 0 had very similar species.

Here’s what they found. For five of six groups, disturbance dissimilarity was associated with significant (solid line) or borderline significant (dashed line) increases in community dissimilarity. So even though the number of species was not affected very much by disturbance (excepting termites), species composition was affected in all groups, with the exception of canopy ants. They conclude that a disturbed forest has very different types of species in it, but not necessarily fewer species.

StorkFig2

Community dissimilarity in relation to disturbance dissimilarity. For five taxonomic groups, plots that had the greatest differences in disturbance also had the greatest differences in species composition.

Lastly, this study shows that response to disturbance is related to the functional group – the role that each species plays within the community. For example, beetles showed a strong response to disturbance, but in reality the strong response was only true for the herbivorous beetle functional group. Beetles that ate fungi or were predators or scavengers showed relatively little change in species composition in relation to disturbance.

So what should conservation ecologists do with this information? Given the diversity and intensity of disturbance globally, we need to develop a better understanding of how species and communities respond to global change. Species composition may be a more sensitive indicator of disturbance than is species richness. Functional groups may be more helpful than taxonomic groups in identifying how disturbance influences how ecosystems actually work. Perhaps monitoring particular functional groups can give us insight into how unrelated groups with similar ecology might respond to a world that promises to experience increasing levels of disturbance.

note: I discuss two papers in this blog.  The original is from the journal Nature. The reference is Lawton, J.H., Bignell, D.E., Bolton, B., Bloemers, G.F., Eggleton, P., Hammond, P. M., Hodda, M., Holt, R.D., Larsen, T.B., Mawdsley, N.A., Stork, N.E., Srivastava, D.S., and Watt, A.D. 1998. Biodiversity inventories, indicator taxa and effects of habitat modification in tropical forest. Nature, 391: 72-76. The second paper that reanalyzes the original data is from the journal Conservation Biology. The reference is Stork, N.E., Srivastava, D.S., Eggleton, P., Hodda, M., Lawson, G., Leakey, R.R.B. and Watt, A.D., 2017. Consistency of effects of tropical‐forest disturbance on species composition and richness relative to use of indicator taxa. Conservation Biology 31 (4): 924-933. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2017 by the Society for Conservation Biology. All rights reserved.