As seasonal cycles become increasingly disrupted, our understanding of the ecology and evolution of reproductive seasonality in tropical vertebrates remains limited (Bronson 2009). To predict how changes in seasonality might impact these animals, it is crucial to identify which elements of their varied reproductive patterns are connected to the equally varied patterns of rainfall seasonality (within-year fluctuations) or the significant climatic unpredictability (year-to-year variations) characteristic of the intertropical region. 

Dezeure et al. (2024) provide a comprehensive examination of reproductive seasonality in papionin monkeys across diverse African environments. By investigating the ecological and evolutionary determinants of reproductive timing, the authors offer novel insights into how climatic factors, particularly environmental unpredictability, shape reproductive strategies in these primates. This study stands out not only for its methodological rigour but also for its contribution to our understanding of how primates adapt their reproductive behaviours to varying environmental pressures. The findings have broad implications, particularly in the context of ongoing climate change, which is expected to increase environmental unpredictability globally. The innovative approach of this paper lies in its multifaceted examination of reproductive seasonality, which integrates data from 21 wild populations of 11 papionin species. The study employs a robust statistical framework, incorporating Bayesian phylogenetic generalised linear mixed models to control for phylogenetic relatedness among species. This methodological choice is crucial because it allows the authors to disentangle the effects of environmental variables from evolutionary history, providing a more accurate picture of how current ecological factors influence reproductive strategies.

The study’s focus on environmental unpredictability as a determinant of reproductive seasonality is particularly noteworthy. While previous research has established the importance of environmental seasonality (Janson and Verdolin 2005), this paper breaks new ground by showing that the magnitude of year-to-year variation in rainfall – rather than just the seasonal distribution of rainfall – plays a critical role in determining the intensity of reproductive seasonality. This finding is supported by the significant negative correlation between reproductive seasonality and environmental unpredictability, which the authors demonstrate across multiple populations and species. The results of this study are important for several reasons. First, they challenge the traditional view that reproductive seasonality is primarily driven by within-year environmental fluctuations. By showing that inter-annual variability in rainfall is a stronger predictor of reproductive timing than intra-annual variability, the authors suggest that primates, like papionins, have evolved flexible reproductive strategies to cope with the unpredictable availability of resources. This flexibility is likely an adaptive response to the highly variable environments that many African primates inhabit, where food availability can vary dramatically not just within a year but from year to year. Second, the study highlights the role of reproductive flexibility in the evolutionary success of papionins. The authors provide compelling evidence that species within the Papio genus, for example, exhibit significant variability in reproductive timing both within and between populations. This variability suggests that these species possess a remarkable ability to adjust their reproductive strategies in response to local environmental conditions, which may have contributed to their widespread distribution across diverse habitats in Africa. This finding aligns with the work of Brockman and Schaik (2005), who argued that reproductive flexibility is a key factor in the success of primates in unpredictable environments.

The study also contributes to our understanding of the evolutionary transition from seasonal to non-seasonal breeding in primates. The authors propose that the loss of strict reproductive seasonality in some papionin species may represent an adaptive shift toward greater reproductive flexibility. This shift could be driven by the need to maximise reproductive success in environments where the timing of resource peaks is difficult to predict. The authors’ findings support this hypothesis, as they show that populations living in more unpredictable environments tend to have lower reproductive seasonality. The broader implications of this study (Dezeure et al. 2024) extend beyond the specific case of papionin monkeys. The findings have relevance for the study of reproductive strategies in other long-lived, tropical mammals that face similar environmental challenges. As climate change is expected to increase the frequency and intensity of environmental unpredictability, understanding how species have historically adapted to such conditions can provide valuable insights into their potential resilience or vulnerability to future changes.

Many primate species are already facing significant threats from habitat loss, hunting, and climate change. By identifying the environmental factors that influence reproductive success, Dezeure et al. (2024) study can help inform conservation strategies aimed at protecting the most vulnerable populations. For example, conservation efforts could focus on maintaining or restoring habitat features that promote reproductive flexibility, such as access to a variety of food resources that peak at different times of the year (Chapman et al.).

References

Brockman D, Schaik C (2005) Seasonality in Primates: Studies of Living and Extinct Human and Non-Human Primates. Cambridge University Press. https://doi.org/10.1017/CBO9780511542343

Bronson FH (2009) Climate change and seasonal reproduction in mammals. Philos Trans R Soc B Biol Sci 364:3331–3340. https://doi.org/10.1098/rstb.2009.0140

Chapman CA, Gogarten JF, Golooba M, et al Fifty+ years of primate research illustrates complex drivers of abundance and increasing primate numbers. Am J Primatol n/a:e23577. https://doi.org/10.1002/ajp.23577

Jules Dezeure, Julie Dagorrette, Lugdiwine Burtschell, Shahrina Chowdhury, Dieter Lukas, Larissa Swedell, Elise Huchard (2024) Flexible reproductive seasonality in Africa-dwelling papionins is associated with low environmental productivity and high climatic unpredictability. bioRxiv, ver.2 peer-reviewed and recommended by PCI Ecology https://doi.org/10.1101/2024.05.01.591991

Janson C, Verdolin J (2005) Seasonality of primate births in relation to climate. In: Schaik CP van, Brockman DK (eds) Seasonality in Primates: Studies of Living and Extinct Human and Non-Human Primates. Cambridge University Press, Cambridge, pp 307–350 https://doi.org/10.1017/CBO9780511542343.012

Urbanisation modifies species’ habitats affecting their density, distribution, fitness, and behaviour with knock-on effects for their parasites’ abundance and transmission (Bradley & Altizer 2007). A meta-analysis found that changes in resource provisioning due to anthropogenic change can have both positive and negative effects on parasite infection in wildlife populations, but that feeding on urban waste had an effect of reducing infection, especially for helminths and protozoa (Becker, Streicker & Altizer 2015). Another study found that urbanisation reduced ectoparasite load in birds, but had no effect on endoparasites or avian flu (Reid et al. 2024). These changes may be due to novel diets reducing transmission via predation upon trophic hosts (Becker, Streicker & Altizer 2015) or behavioural, leading to more time available to preen (Reid et al. 2024). Less is known about how urbanisation affects invertebrates (but see Lewthwaite et al., 2024) and their parasites. This is important considering that invertebrates are often intermediate hosts of, and/or vector other parasites.

Recent work has found that snails and slugs can trap nematodes in their shells to prevent infection (Rae 2017). This newly discovered resistance mechanism reveals that the shell serves an immune defence function. It also provides a record of nematode exposure and documents incidences of resistance to infection as the trapped nematode becomes fixed onto the shell surface (Rae 2017). Dahirel and co-authors exploit this to investigate whether snail-nematode interactions change in response to increasing levels of urbanisation (Dahirel et al. 2024).

They explore whether the proportion of Cepaea nemoralis snails with trapped nematodes in their shell changes across an urbanisation gradient. They also explore whether different phenotypic snail traits, notably shell size, colour, band number and fusion explain the likelihood of having trapped nematodes in their shells. An increase in urbanisation was associated with a decrease in the proportion of snails with trapped nematodes in their shells. At the same time larger shells were more likely to have trapped nematodes, but this effect did not change across the urbanisation gradient. 

The authors discuss that reduced nematode encapsulation in urban environments may be due to lower encounter rate due to either fewer nematodes in urban environments, changes in snail behaviour reducing exposure, or alternatively that urban snails were less resistant to nematode infection. 

It will be interesting to investigate how this resistance mechanism is related to other forms of snail immunity and whether high rates of nematode encapsulation are an indicator of high resistance or high exposure. This will enable nematode trapping to be used as a marker to indicate environments and/or snail populations harbouring high levels of parasitism and further exploitation of museum collections to understand host-parasite interactions in the past (Rae 2017).

References

Becker, D.J., Streicker, D.G. & Altizer, S. (2015) Linking anthropogenic resources to wildlife-pathogen dynamics: a review and meta-analysis. Ecol Lett, 18, 483-495. https://doi.org/10.1111/ele.12428

Bradley, C.A. & Altizer, S. (2007) Urbanization and the ecology of wildlife diseases. Trends Ecol Evol, 22, 95-102. https://doi.org/10.1016/j.tree.2006.11.001

Maxime Dahirel, Hannah Reyné, Katrien De Wolf, Dries Bonte (2024) Urban Cepaea nemoralis snails are less likely to have nematodes trapped within their shells. bioRxiv, ver.4 peer-reviewed and recommended by PCI Ecology https://doi.org/10.1101/2024.03.07.583959

Lewthwaite, J.M.M., Baiotto, T.M., Brown, B.V., Cheung, Y.Y., Baker, A.J., Lehnen, C., McGlynn, T.P., Shirey, V., Gonzalez, L., Hartop, E., Kerr, P.H., Wood, E. & Guzman, L.M. (2024) Drivers of arthropod biodiversity in an urban ecosystem. Sci Rep, 14, 390. https://doi.org/10.1038/s41598-023-50675-3

Rae, R. (2017) The gastropod shell has been co-opted to kill parasitic nematodes. Sci Rep, 7, 4745. https://doi.org/10.1038/s41598-017-04695-5

Reid, R., Capilla-Lasheras, P., Haddou, Y., Boonekamp, J. & Dominoni, D.M. (2024) The impact of urbanization on health depends on the health metric, life stage and level of urbanization: a global meta-analysis on avian species. Proc Biol Sci, 291, 20240617. https://doi.org/10.1098/rspb.2024.0617

 Understanding the effects of environmental perturbations on coexistence is a key challenge in ecology, and models have played an important role in structuring our ideas and generating predictions, leading to quantitative hypotheses. In such models, environmental perturbations are often captured by changes in parameter values, such as the intrinsic growth rates of species (1–3). The question then becomes how much one can change these parameters without breaking coexistence and thus losing species (4). 
 
An intuitively appealing approach to address this question is to calculate a model’s feasibility domain (5–7). Loosely defined, it is the fraction of parameter settings leading to the coexistence of all species. Mathematically speaking, it is a high-dimensional triangle, of which one can calculate the size, just as for plain two-dimensional triangles. Parameter settings outside of this triangle break coexistence. Thus, it seems logical that greater feasibility domains would make for more robust ecosystems. However, careful interpretation is key: a greater feasibility domain merely implies that across many attempts at running a model with different random parameter settings, coexistence will be more frequent. It does not necessarily inform us how much one can perturb the parameters of a community with a predefined parameter setting. To get this information, we also need to know the shape of the triangle (7): perturbations more easily knock the parameter setting out of a flat triangle than out of an equilateral triangle. 
 
Desaillais et al. (8) develop a new theory that sheds light on what drives the shape of the feasibility domain. Specifically, they present the probability distribution that tells how close to the edge of the feasibility domain the parameter settings in that domain tend to be. For example, all points in a very flat triangle are close to its edge, while in an equilateral triangle, most points are safely stowed inside. The results show how, in a Lotka-Volterra model, the matrix of species interactions fully defines this distribution, which makes the technique empirically applicable in so far as one can estimate these interactions. The analysis then continues to explore the role of specific species in putative loss of coexistence. Desaillais et al. identify two species-level quantities: the first measures the total influence of the surrounding community on a focal species, while the second is a proxy for how close that focal species is to being lost, should a perturbation occur. While these two quantities are not mathematically independent, their correlation is not perfect, allowing one to categorize species into distinct ecological roles. A dataset of plant communities with different compositions illustrates how to apply this idea and gain some additional insight into the robustness of coexistence. These results pave the way for a number of potentially rewarding applications. How does the robustness of coexistence differ across network types? For which network types do we find back a more diverse set of ecological roles for species, i.e. for which networks are the two quantities least correlated? 

References

1. Baert, J.M., Janssen, C.R., Sabbe, K., and De Laender, F. (2016). Per capita interactions and stress tolerance drive stress-induced changes in biodiversity effects on ecosystem functions. Nat. Commun. 7, 12486. https://doi.org/10.1038/ncomms12486

2. Pásztor, L., Botta-Dukat, Z., Magyar, G., Czaran, T., and Meszéna, G. (2016). Theory-based ecology: A Darwinian approach 1st ed. (Oxford University Press).

3. Cenci, S., Montero-Castaño, A., and Saavedra, S. (2018). Estimating the effect of the reorganization of interactions on the adaptability of species to changing environments. J. Theor. Biol. 437, 115–125. https://doi.org/10.1016/j.jtbi.2017.10.016

4. Spaak, J.W., Baert, J.M., Baird, D.J., Eisenhauer, N., Maltby, L., Pomati, F., Radchuk, V., Rohr, J.R., Van den Brink, P.J., and De Laender, F. (2017). Shifts of community composition and population density substantially affect ecosystem function despite invariant richness. Ecol. Lett. 20, 1315–1324. https://doi.org/10.1111/ele.12828

5. Meszéna, G., Gyllenberg, M., Pásztor, L., and Metz, J.A.J. (2006). Competitive exclusion and limiting similarity: A unified theory. Theor. Popul. Biol. 69, 68–87. https://doi.org/10.1016/j.tpb.2005.07.001

6. Saavedra, S., Rohr, R.P., Bascompte, J., Godoy, O., Kraft, N.J.B., and Levine, J.M. (2017). A structural approach for understanding multispecies coexistence. Ecol. Monogr. 87, 470–486. https://doi.org/10.1002/ecm.1263

7. Grilli, J., Adorisio, M., Suweis, S., Barabás, G., Banavar, J.R., Allesina, S., and Maritan, A. (2017). Feasibility and coexistence of large ecological communities. Nat. Commun. 8. https://doi.org/10.1038/ncomms14389

8. Desallais M, Loreau M, Arnoldi J.F. (2024) The distribution of distances to the edge of species coexistence. bioRxiv, ver.4 peer-reviewed and recommended by PCI Ecology https://doi.org/10.1101/2024.01.21.575550

Estimating populations size of widespread, common species in a relatively large and heterogeneous country like France is difficult for several reasons, from having a sample covering well the diverse ecological gradients to accounting for detectability, the fact that absence of a species may represent a false negative, the species being present but not detected. Bird communities have been the focus of a very large number of studies, with some countries like the UK having long traditions of monitoring both common and rare species. Nabias et al. use a large, structured citizen science project to provide new estimates of common bird species, accounting for detectability and using different habitat and climate covariates to extrapolate abundance to non-sampled areas. About 2/3 of the species had estimates higher than what would have been expected using a previous attempt at estimating population size based in part on expert knowledge and projected using estimates of trends to the period covered by the citizen science sampling. Some species showed large differences between the two estimates, which could be in part explained by accounting for detectability.

This paper uses what is called model-based inference (as opposed to design-based inference, that uses the design to make inferences about the whole population; Buckland et al. 2000), both in terms of detectability and habitat suitability. The estimates obtained depend on how well the model components approximate the underlying processes, which in a complex dataset like this one is not easy to assess. But it clearly shows that detectability may have substantial implications for the population size estimates. This is of course not new but has rarely been done at this scale and using a large sample obtained on many species. Interesting further work could focus on testing the robustness of the model-based approach by for example sampling new plots and compare the expected values to the observed values. Such a sampling could be stratified to maximize the discrimination between expected low and high abundances, at least for species where the estimates might be considered as uncertain, or for which estimating population sizes is deemed important.

References

Buckland, S. T., Goudie, I. B. J., & Borchers, D. L. (2000). Wildlife Population Assessment: Past Developments and Future Directions. Biometrics, 56(1), 1-12. https://doi.org/10.1111/j.0006-341X.2000.00001.x

 Nabias, J., Barbaro, L., Fontaine, B., Dupuy, J., Couzi, L., et al. (2024) Reassessment of French breeding bird population sizes using citizen science and accounting for species detectability. HAL, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://hal.science/hal-04478371

Hyperaccumulator plants can concentrate heavy metals present on the soil in their tissues, avoiding their toxic effects and potentially discouraging herbivores (Martens & Boyd, 1994). But not all herbivores are necessarily discouraged, and access to locally abundant resources with low interspecific competition from other herbivores, can affect feeding choices. Godinho et al. performed a series of controlled laboratorial trials to evaluate if herbivores (spider mites) avoid tomato plants with high concentrations of Cadmium under alternative scenarios, namely: the presence/absence of conspecifics, the presence/absence of a competitor species (a congeneric mite), and the relative abundance of contaminated plants.

They found that when looking for plants to lay their eggs, individual spider-mites (females) do not seem to discriminate between plants with or without cadmium, despite a significantly lower performance on the former. However, they consistently chose plants without Cadmium in set-ups where 200 mites are faced with this decision together. This preference was consistent and independent from the relative abundance of cadmium-free plants, but only when mites do this decision collectively. In addition, this preference was stronger than that for plants where interspecific competition was lower, with mites preferring to face high competition from congeneric herbivores than laying their eggs on Cadmium contaminated plants. 

Taken together these experiments suggest that aggregation is a key mechanism by which spider mites can avoid metal contaminated plants. As good research often does, these experiments open several important questions that will need to be addressed in the future. In particular, it will be important to clarify what are the sensorial and behavioural mechanisms that allow this decision/outcome when spider mites make this choice collectively but lead to a different outcome (no choice) when they face this decision alone. Additionally, it will be interesting to explore the potentially adaptive (or non-adaptive) consequences of this behaviour in terms of individual and inclusive fitness. One thing seems certain: both the abiotic and the biotic context can affect spider mite choices, and both need to be considered to advance our understanding about the trade-offs between plant defence mechanisms and associated herbivore decisions and fitness. 

References

Martens, S. N., & Boyd, R. S. (1994). The ecological significance of nickel hyperaccumulation: a plant chemical defense. Oecologia, 98(3–4), 379–384. https://doi.org/10.1007/BF00324227

Godinho, D. P., I. Fragata, M. C. de la Masseliere, S. Magalhaes 2024 Spider mites collectively avoid plants with cadmium irrespective of their frequency or the presence of competitors. bioRxiv, ver. 4, peer-reviewed and recommended by PCI Ecology 2023.08.17.553707. https://doi.org/10.1101/2023.08.17.553707