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

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

The manuscript by Beck et al. (2024) investigates the effects of water phosphorus and nitrogen loads on stream macroinvertebrate community stoichiometry across France. Utilizing data from over 1300 standardized sampling events, this research finds that community stoichiometry is significantly influenced by water phosphorus concentration, with the strongest effects at low nitrogen levels.

The results demonstrate that the assumptions of Ecological Stoichiometry Theory apply at the community level for at least two dominant taxa and across a broad spatial scale, with probable implications for nutrient cycling and ecosystem functionality.

This manuscript contributes to ecological theory, particularly by extending Ecological Stoichiometry Theory to include community-level interactions, clarifying the impact of nutrient concentrations on community structure and function, and informing nutrient management and conservation strategies.

In summary, this study not only addresses a gap in community-level stoichiometric research but also delivers crucial empirical support for advancing ecological science and promoting environmental stewardship.

References

Beck M, Billoir E, Usseglio-Polatera P, Meyer A, Gautreau E and Danger M (2024) Effects of water nutrient concentrations on stream macroinvertebrate community stoichiometry: a large-scale study. bioRxiv, 2024.02.01.574823, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2024.02.01.574823

As biodiversity has become a major global concern for a variety of stakeholders, and society in general, assessments of biodiversity trends at all spatial scales have flourished in the past decades. To assess trends, one needs data, and the more precise the data, the more precise the trend. Or, if precision is not perfect, uncertainty in the data must be acknowledged and accounted for. Such considerations have already been raised in ecology, most notably regarding the value of species distribution data to model the current and future distribution of species (Rocchini et al., 2011, Duputié et al., 2014, Tessarolo et al., 2021), leading to serious doubts regarding the value of public databases (Maldonado et al., 2015). And more recently similar issues have been raised regarding databases of species traits (Augustine et al., 2024), emphasizing the importance of good data practice and traceability.

Science is by nature a self-correcting human process, with many steps of the scientific activity prone to errors and misinterpretations. Collation of ecological data, sadly, is proof of this. Spurred by the astonishing results of Hallmann et al. (2017) regarding the decline of insect biomass, and to more precisely answer the question of biodiversity trends in insects and settle an ongoing debate (Cardinale et al., 2018), van Klink et al. (2020, 2021) established the InsectChange database. Several perceptive comments have already been made regarding the possible issues in the methods and interpretations of this study (Desquilbet et al., 2020, Jähnig et al., 2021, Duchenne et al., 2022). However, the biggest issue might have been finally unearthed by Gaume & Desquilbet (2024): with poorly curated data, the InsectChange database is unlikely to support most of the initial claims regarding insect biodiversity trends.

The compilation of errors and inconsistencies present in InsectChange and evinced by Gaume & Desquilbet (2024) is stunning to say the least, with a mix of field and experimental data combined without regard for experimental manipulation of environmental factors, non-standardised transformations of abundances, the use of non-insect taxa to compute insect trends, and inadequate geographical localizations of samplings. I strongly advise all colleagues interested in the study of biodiversity from global databases to consider the points raised by the authors, as it is quite likely that other databases might suffer from the same ailments as well. Reading this paper is also educating and humbling in its own way, since the publication of the original papers based on InsectChange seems to have proceeded without red flags from reviewers or editors. The need for publishing fast results that will make the next buzz, thus obeying the natural selection of bad science (Smaldino and McElreath, 2016), might be the systemic culprit. However, this might also be the opportunity ecology needs to consider the reviewing and curation of data as a crucial step of science quality assessment. To make final assessments, let us proceed with less haste.

References

Augustine, S. P., Bailey-Marren, I., Charton, K. T., Kiel, N. G. & Peyton, M. S. (2024) Improper data practices erode the quality of global ecological databases and impede the progress of ecological research. Global Change Biology, 30, e17116. https://doi.org/10.1111/gcb.17116

Cardinale, B. J., Gonzalez, A., Allington, G. R. H. & Loreau, M. (2018) Is local biodiversity declining or not? A summary of the debate over analysis of species richness time trends. Biological Conservation, 219, 175-183. https://doi.org/10.1016/j.biocon.2017.12.021

Desquilbet, M., Gaume, L., Grippa, M., Céréghino, R., Humbert, J.-F., Bonmatin, J.-M., Cornillon, P.-A., Maes, D., Van Dyck, H. & Goulson, D. (2020) Comment on “Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances”. Science, 370, eabd8947. https://doi.org/10.1126/science.abd8947

Duchenne, F., Porcher, E., Mihoub, J.-B., Loïs, G. & Fontaine, C. (2022) Controversy over the decline of arthropods: a matter of temporal baseline? Peer Community Journal, 2. https://doi.org/10.24072/pcjournal.131

Duputié, A., Zimmermann, N. E. & Chuine, I. (2014) Where are the wild things? Why we need better data on species distribution. Global Ecology and Biogeography, 23, 457-467. https://doi.org/10.1111/geb.12118

Gaume, L. & Desquilbet, M. (2024) InsectChange: Comment. biorXiv, ver.4 peer-reviewed and recommended by PCI Ecology https://doi.org/10.1101/2023.06.17.545310

Hallmann, C. A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., Schwan, H., Stenmans, W., Müller, A., Sumser, H., Hörren, T., Goulson, D. & de Kroon, H. (2017) More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLOS ONE, 12, e0185809. https://doi.org/10.1371/journal.pone.0185809

Jähnig, S. C., Baranov, V., Altermatt, F., Cranston, P., Friedrichs-Manthey, M., Geist, J., He, F., Heino, J., Hering, D., Hölker, F., Jourdan, J., Kalinkat, G., Kiesel, J., Leese, F., Maasri, A., Monaghan, M. T., Schäfer, R. B., Tockner, K., Tonkin, J. D. & Domisch, S. (2021) Revisiting global trends in freshwater insect biodiversity. WIREs Water, 8, e1506. https://doi.org/10.1002/wat2.1506

Maldonado, C., Molina, C. I., Zizka, A., Persson, C., Taylor, C. M., Albán, J., Chilquillo, E., Rønsted, N. & Antonelli, A. (2015) Estimating species diversity and distribution in the era of Big Data: to what extent can we trust public databases? Global Ecology and Biogeography, 24, 973-984. https://doi.org/10.1111/geb.12326

Rocchini, D., Hortal, J., Lengyel, S., Lobo, J. M., Jiménez-Valverde, A., Ricotta, C., Bacaro, G. & Chiarucci, A. (2011) Accounting for uncertainty when mapping species distributions: The need for maps of ignorance. Progress in Physical Geography, 35, 211-226. https://doi.org/10.1177/0309133311399491

Smaldino, P. E. & McElreath, R. (2016) The natural selection of bad science. Royal Society Open Science, 3. https://doi.org/10.1098/rsos.160384

Tessarolo, G., Ladle, R. J., Lobo, J. M., Rangel, T. F. & Hortal, J. (2021) Using maps of biogeographical ignorance to reveal the uncertainty in distributional data hidden in species distribution models. Ecography, 44, 1743-1755. https://doi.org/10.1111/ecog.05793

van Klink, R., Bowler, D. E., Comay, O., Driessen, M. M., Ernest, S. K. M., Gentile, A., Gilbert, F., Gongalsky, K. B., Owen, J., Pe'er, G., Pe'er, I., Resh, V. H., Rochlin, I., Schuch, S., Swengel, A. B., Swengel, S. R., Valone, T. J., Vermeulen, R., Wepprich, T., Wiedmann, J. L. & Chase, J. M. (2021) InsectChange: a global database of temporal changes in insect and arachnid assemblages. Ecology, 102, e03354. https://doi.org/10.1002/ecy.3354

van Klink, R., Bowler, D. E., Gongalsky, K. B., Swengel, A. B., Gentile, A. & Chase, J. M. (2020) Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances. Science, 368, 417-420. https://doi.org/10.1126/science.aax9931