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14 Jun 2024
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Hierarchizing multi-scale environmental effects on agricultural pest population dynamics: a case study on the annual onset of Bactrocera dorsalis population growth in Senegalese orchards

Uncovering the ecology in big-data by hierarchizing multi-scale environmental effects

Recommended by based on reviews by Kévin Tougeron and Jianqiang Sun

Along with the generalization of open-access practices, large, heterogeneous datasets are becoming increasingly available to ecologists (Farley et al. 2018). While such data offer exciting opportunities for unveiling original patterns and trends, they also raise new challenges regarding how to extract relevant information and actually improve our knowledge of complex ecological systems, beyond purely descriptive correlations (Dietze 2017, Farley et al. 2018).

In this work, Caumette et al. (2024) develop an original ecoinformatics approach to relate multi-scale environmental factors to the temporal dynamics of a major pest in mango orchards. Their method relies on the recent tree-boosting method GPBoost (Sigrist 2022) to hierarchize the influence of environmental factors of heterogeneous nature (e.g., orchard composition and management; landscape structure; climate) on the emergence date of the oriental fruit fly, Bactrocera dorsalis. As boosting methods allows the analysis of high-dimensional data, they are particularly adapted to the exploration of such datasets, to uncover unexpected, potentially complex dependencies between ecological dynamics and multiple environmental factors (Farley et al. 2018). In this article, Caumette et al. (2024) make a special effort to guide the reader step by step through their complex analysis pipeline to make it broadly understandable to the average ecologist, which is no small feat. I particularly welcome this commitment, as making new, cutting-edge analytical methods accessible to a large community of science practitioners with varying degrees of statistical or programming expertise is a major challenge for the future of quantitative ecology. 

The main result of Caumette et al. (2024) is that temperature and humidity conditions both at the local and regional scales are the main predictors of B. dorsalis emergence date, while orchard management practices seem to have relatively little influence. This suggests that favourable climatic conditions may allow the persistence of small populations of B. dorsalis over the dry season, which may then act as a propagule source for early re-infestations. However, as the authors explain, the resulting regression model is not designed for predictive purposes and should not at this stage be used for decision-making in pest management. Its main interest rather resides in identifying potential key factors favoring early infestations of B. dorsalis, and help focusing future experimental field studies on the most relevant levers for integrated pest management in mango orchards.

In a wider perspective, this work also provides a convincing proof-of-concept for the use of boosting methods to identify the most influential factors in large, multivariate datasets in a variety of ecological systems. It is also crucial to keep in mind that the current exponential growth in high-throughput environmental data (Lucivero 2020) could quickly come into conflict with the need to reduce the environmental footprint of research (Mariette et al. 2022). In this context, robust and accessible methods for extracting and exploiting all the information available in already existing datasets might prove essential to a sustainable pursuit of science.

References
 
Caumette C, Diatta P, Piry S, Chapuis M-P, Faye E, Sigrist F, Martin O, Papaïx J, Brévault T, Berthier K. 2024. Hierarchizing multi-scale environmental effects on agricultural pest population dynamics: a case study on the annual onset of Bactrocera dorsalis population growth in Senegalese orchards. bioRxiv 2023.11.10.566583, ver. 3 peer-reviewed and recommended by Peer Community in Ecology.  https://doi.org/10.1101/2023.11.10.566583

Dietze MC. 2017. Ecological Forecasting. Princeton University Press
 
Farley SS, Dawson A, Goring SJ, Williams JW. 2018. Situating Ecology as a Big-Data Science: Current Advances, Challenges, and Solutions. BioScience, 68, 563–576, https://doi.org/10.1093/biosci/biy068
 
Lucivero F. 2020. Big Data, Big Waste? A Reflection on the Environmental Sustainability of Big Data Initiatives. Science and Engineering Ethics 26, 1009–1030. https://doi.org/10.1007/s11948-019-00171-7

Mariette J, Blanchard O, Berné O, Aumont O, Carrey J, Ligozat A-L, Lellouch E, Roche P-E, Guennebaud G, Thanwerdas J, Bardou P, Salin G, Maigne E, Servan S, Ben-Ari T 2022. An open-source tool to assess the carbon footprint of research. Environmental Research: Infrastructure and Sustainability, 2022. https://dx.doi.org/10.1088/2634-4505/ac84a4
 
Sigrist F. 2022. Gaussian process boosting. The Journal of Machine Learning Research, 23, 10565-10610. https://jmlr.org/papers/v23/20-322.html
 

Hierarchizing multi-scale environmental effects on agricultural pest population dynamics: a case study on the annual onset of *Bactrocera dorsalis* population growth in Senegalese orchardsCécile Caumette, Paterne Diatta, Sylvain Piry, Marie-Pierre Chapuis, Emile Faye, Fabio Sigrist, Olivier Martin, Julien Papaïx, Thierry Brévault, Karine Berthier<p>Implementing integrated pest management programs to limit agricultural pest damage requires an understanding of the interactions between the environmental variability and population demographic processes. However, identifying key environmental ...Demography, Landscape ecology, Statistical ecologyElodie Vercken2023-12-11 17:02:08 View
05 Jun 2024
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Attracting pollinators vs escaping herbivores: eco-evolutionary dynamics of plants confronted with an ecological trade-off

Plant-herbivore-pollinator ménage-à-trois: tell me how well they match, and I'll tell you if it's made to last

Recommended by ORCID_LOGO based on reviews by Marcos Mendez and Yaroslav Ispolatov

How would a plant trait evolve if it is involved in interacting with both a pollinator and an herbivore species? The answer by Yacine and Loeuille is straightforward: it is not trivial, but it can explain many situations found in natural populations.

Yacine and Loeuille applied the well-known Adaptive Dynamics framework to a system with three interacting protagonists: a herbivore, a pollinator, and a plant. The evolution of a plant trait is followed under the assumption that it regulates the frequency of interaction with the two other species. As one can imagine, that is where problems begin: interacting more with pollinators seems good, but what if at the same time it implies interacting more with herbivores? And that's not a silly idea, as there are many cases where herbivores and pollinators share the same cues to detect plants, such as colors or chemical compounds.

They found that depending on the trade-off between the two types of interactions and their density-dependent effects on plant fitness, the possible joint ecological and evolutionary outcomes are numerous. When herbivory prevails, evolution can make the ménage-à-trois ecologically unstable, as one or even two species can go extinct, leaving the plant alone. Evolution can also make the coexistence of the three species more stable when pollination services prevail, or lead to the appearance of a second plant species through branching diversification of the plant trait when herbivory and pollination are balanced.

Yacine and Loeuille did not only limit themselves to saying "it is possible," but they also did much work evaluating when each evolutionary outcome would occur. They numerically explored in great detail the adaptive landscape of the plant trait for a large range of parameter values. They showed that the global picture is overall robust to parameter variations, strengthening the plausibility that the evolution of a trait involved in antagonistic interactions can explain many of the correlations between plant and animal traits or phylogenies found in nature.

Are we really there yet? Of course not, as some assumptions of the model certainly limit its scope. Are there really cases where plants' traits evolve much faster than herbivores' and pollinators' traits? Certainly not, but the model is so general that it can apply to any analogous system where one species is caught between a mutualistic and a predator species, including potential species that evolve much faster than the two others. And even though this limitation might cast doubt on the generality of the model's predictions, studying a system where a species' trait and a preference trait coevolve is possible, as other models have already been studied (see Fritsch et al. 2021 for a review in the case of evolution in food webs). We can bet this is the next step taken by Yacine and Loeuille in a similar framework with the same fundamental model, promising fascinating results, especially regarding the evolution of complex communities when species can accumulate after evolutionary branchings.

Relaxing another assumption seems more challenging as it would certainly need to change the model itself: interacting species generally do not play fixed roles, as being mutualistic or antagonistic might generally be density-dependent (Holland and DeAngelis 2010). How would the exchange of resources between three interacting species evolve? It is an open question.

References

Fritsch, C., Billiard, S., & Champagnat, N. (2021). Identifying conversion efficiency as a key mechanism underlying food webs adaptive evolution: a step forward, or backward? Oikos, 130(6), 904-930.
https://doi.org/10.1111/oik.07421
 
Holland, J. N., & DeAngelis, D. L. (2010). A consumer-resource approach to the density‐dependent population dynamics of mutualism. Ecology, 91(5), 1286-1295.
https://doi.org/10.1890/09-1163.1

Yacine, Y., & Loeuille, N. (2024) Attracting pollinators vs escaping herbivores: eco-evolutionary dynamics of plants confronted with an ecological trade-off. bioRxiv 2021.12.02.470900; doi: https://doi.org/10.1101/2021.12.02.470900

Attracting pollinators vs escaping herbivores: eco-evolutionary dynamics of plants confronted with an ecological trade-offYoussef Yacine, Nicolas Loeuille<p style="text-align: justify;">Many plant traits are subject to an ecological trade-off between attracting pollinators and escaping herbivores. The interplay of both plant-animal interaction types determines their evolution. As most studies focus...Eco-evolutionary dynamics, Herbivory, Pollination, Theoretical ecologySylvain Billiard2023-03-21 14:23:12 View
30 May 2024
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Disentangling the effects of eutrophication and natural variability on macrobenthic communities across French coastal lagoons

Untangling Eutrophication Effects on Coastal Lagoon Ecosystems

Recommended by ORCID_LOGO based on reviews by Kaylee P. Smit, Matthew J. Pruden and Kendyl Wright

Disentangling the effects on ecosystem structure and functioning of natural and human-induced impacts in transitional waters is a great challenge in coast ecology. This is due to the observation that the ecosystems of transitional waters are naturally dynamic systems with characteristics of stressed systems. For example, the benthic communities present low species richness and high abundance of species with a high tolerance to variations, e.g., salinity. This general observation is known as the paradigm of the “Transitional Waters Quality Paradox” (Zaldívar et al., 2008) derived from the previously described “Estuarine Quality Paradox” (Elliott and Quintino, 2007). 

In Jones et al. (2024) “Disentangling the effects of eutrophication and natural variability on macrobenthic communities across French coastal lagoons”, a great diversity of lagoons is analyzed to disentangle the effects of eutrophication from those of natural environmental variability on benthic macroinvertebrates and understanding the links between environmental variables affecting benthic macroinvertebrates. These authors use a very elegant set of numerical approaches, including correlograms, linear models and variance partitioning. They apply this suite to a dataset of macrobenthic invertebrate abundances and environmental variables from 29 Mediterranean coastal lagoons in France.

Through this suite of analyses, they demonstrate the strong complexity of the mechanisms interplaying in a situation of eutrophication on lagoon macrobenthos. The mechanisms involved are direct, like toxicity, or indirect, for example, through modifications of the sediment's biogeochemistry. Such a result on the different interactions involved is very important in the context of the search for indicators to define ecosystem status. Improving the definition of metrics is essential in environmental management decisions.

References

Elliott, M. and Quintino, V. (2007) The estuarine quality paradox, environmental homeostasis and the difficulty of detecting anthropogenic stress in naturally stressed areas. Marine Pollution Bulletin 54, 640–645. https://doi.org/10.1016/j.marpolbul.2007.02.003

Jones et al. (2024) Disentangling the effects of eutrophication and natural variability on macrobenthic communities across French coastal lagoons bioRxiv, 2022.08.18.504439, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.08.18.504439

Zaldívar, J. (2008). Eutrophication in transitional waters: an overview. https://doi.org/10.1285/I18252273V2N1P1

Disentangling the effects of eutrophication and natural variability on macrobenthic communities across French coastal lagoonsAuriane G. Jones, Gauthier Schaal, Aurélien Boyé, Marie Creemers, Valérie Derolez, Nicolas Desroy, Annie Fiandrino, Théophile L. Mouton, Monique Simier, Niamh Smith, Vincent Ouisse<p style="text-align: justify;">Coastal lagoons are transitional ecosystems that host a unique diversity of species and support many ecosystem services. Owing to their position at the interface between land and sea, they are also subject to increa...Biodiversity, Community ecology, Ecosystem functioning, Marine ecologyNathalie Niquil Matthew J. Pruden2023-09-08 11:26:01 View
24 May 2024
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Effects of water nutrient concentrations on stream macroinvertebrate community stoichiometry: a large-scale study

The influence of water phosphorus and nitrogen loads on stream macroinvertebrate community stoichiometry

Recommended by ORCID_LOGO based on reviews by Thomas Guillemaud, Jun Zuo and 1 anonymous reviewer

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

Effects of water nutrient concentrations on stream macroinvertebrate community stoichiometry: a large-scale studyMiriam Beck, Elise Billoir, Philippe Usseglio-Polatera, Albin Meyer, Edwige Gautreau, Michael Danger<p>Basal resources generally mirror environmental nutrient concentrations in the elemental composition of their tissue, meaning that nutrient alterations can directly reach consumer level. An increased nutrient content (e.g. phosphorus) in primary...Community ecology, Ecological stoichiometryHuihuang Chen Thomas Guillemaud, Jun Zuo, Anonymous2024-02-02 10:14:01 View
13 May 2024
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Getting More by Asking for Less: Linking Species Interactions to Species Co-Distributions in Metacommunities

Beyond pairwise species interactions: coarser inference of their joined effects is more relevant

Recommended by ORCID_LOGO based on reviews by Frederik De Laender, Hao Ran Lai and Malyon Bimler

Barbier et al. (2024) investigated the dynamics of species abundances depending on their ecological niche (abiotic component) and on (numerous) competitive interactions. In line with previous evidence and expectations (Barbier et al. 2018), the authors show that it is possible to robustly infer the mean and variance of interaction coefficients from species co-distributions, while it is not possible to infer the individual coefficient values.

The authors devised a simulation framework representing multispecies dynamics in an heterogeneous environmental context (2D grid landscape). They used a Lotka-Volterra framework involving pairwise interaction coefficients and species-specific carrying capacities. These capacities depend on how well the species niche matches the local environmental conditions, through a Gaussian function of the distance of the species niche centers to the local environmental values.

They considered two contrasted scenarios denoted as « Environmental tracking » and « Dispersal limited ». In the latter case, species are initially seeded over the environmental grid and cannot disperse to other cells, while in the former case they can disperse and possibly be more performant in other cells.

The direct effects of species on one another are encoded in an interaction matrix A, and the authors further considered net interactions depending on the inverse of the matrix of direct interactions (Zelnik et al., 2024). The net effects are context-dependent, i.e., it involves the environment-dependent biotic capacities, even through the interaction terms can be defined between species as independent from local environment.

The results presented here underline that the outcome of many individual competitive interactions can only be understood in terms of macroscopic properties. In essence, the results here echoe the mean field theories that investigate the dynamics of average ecological properties instead of the microscopic components (e.g., McKane et al. 2000). In a philosophical perspective, community ecology has long struggled with analyzing and inferring local determinants of species coexistence from species co-occurrence patterns, so that it was claimed that no universal laws can be derived in the discipline (Lawton 1999). Using different and complementary methods and perspectives, recent research has also shown that species assembly parameter values cannot be unambiguously inferred from species co-occurrences only, even in simple designs where an equilibrium can be reached (Poggiato et al. 2021). Although the roles of high-order competitive interactions and intransivity can lead to species coexistence, the simple view of a single loop of competitive interactions is easily challenged when further interactions and complexity is added (Gallien et al. 2024). But should we put so much emphasis on inferring individual interaction coefficients? In a quest to understand the emerging properties of elementary processes, ecological theory could go forward with a more macroscopic analysis and understanding of species coexistence in many communities.

The authors referred several times to an interesting paper from Schaffer (1981), entitled « Ecological abstraction: the consequences of reduced dimensionality in ecological models ». It proposes that estimating individual species competition coefficients is not possible, but that competition can be assessed at the coarser level of organisation, i.e., between ecological guilds. This idea implies that the dimensionality of the competition equations should be greatly reduced to become tractable in practice. Taking together this claim with the results of the present Barbier et al. (2024) paper, it becomes clearer that the nature of competitive interactions can be addressed through « abstracted » quantities, as those of guilds or the moments of the individual competition coefficients (here the average and the standard deviation).

Therefore the scope of Barbier et al. (2024) framework goes beyond statistical issues in parameter inference, but question the way we must think and represent the numerous competitive interactions in a simplified and robust way.

References

Barbier, Matthieu, Jean-François Arnoldi, Guy Bunin, et Michel Loreau. 2018. « Generic assembly patterns in complex ecological communities ». Proceedings of the National Academy of Sciences 115 (9): 2156‑61. https://doi.org/10.1073/pnas.1710352115
 
Barbier, Matthieu, Guy Bunin, et Mathew A Leibold. 2024. « Getting More by Asking for Less: Linking Species Interactions to Species Co-Distributions in Metacommunities ». bioRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2023.06.04.543606
 
Gallien, Laure, Maude  Charlie Cavaliere, Marie  Charlotte Grange, François Munoz, et Tamara Münkemüller. 2024. « Intransitive stability collapses under the influence of dominant competitors ». The American Naturalist. https://doi.org/10.1086/730297
 
Lawton, J. H. 1999. « Are There General Laws in Ecology? » Oikos 84 (février):177‑92. https://doi.org/10.2307/3546712
 
McKane, Alan, David Alonso, et Ricard V Solé. 2000. « Mean-field stochastic theory for species-rich assembled communities ». Physical Review E 62 (6): 8466. https://doi.org/10.1103/PhysRevE.62.8466
 
Poggiato, Giovanni, Tamara Münkemüller, Daria Bystrova, Julyan Arbel, James S. Clark, et Wilfried Thuiller. 2021. « On the Interpretations of Joint Modeling in Community Ecology ». Trends in Ecology & Evolution. https://doi.org/10.1016/j.tree.2021.01.002
 
Schaffer, William M. 1981. « Ecological abstraction: the consequences of reduced dimensionality in ecological models ». Ecological monographs 51 (4): 383‑401. https://doi.org/10.2307/2937321
 
Zelnik, Yuval R., Nuria Galiana, Matthieu Barbier, Michel Loreau, Eric Galbraith, et Jean-François Arnoldi. 2024. « How collectively integrated are ecological communities? » Ecology Letters 27 (1): e14358. https://doi.org/10.1111/ele.14358

Getting More by Asking for Less: Linking Species Interactions to Species Co-Distributions in MetacommunitiesMatthieu Barbier, Guy Bunin, Mathew A. Leibold<p>AbstractOne of the more difficult challenges in community ecology is inferring species interactions on the basis of patterns in the spatial distribution of organisms. At its core, the problem is that distributional patterns reflect the ‘realize...Biogeography, Community ecology, Competition, Spatial ecology, Metacommunities & Metapopulations, Species distributions, Statistical ecology, Theoretical ecologyFrançois Munoz2023-10-21 14:14:16 View
18 Apr 2024
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The large and central Caligo martia eyespot may reduce fatal attacks by birds: a case study supports the deflection hypothesis in nature

Intimidation or deflection: field experiments in a tropical forest to simultaneously test two competing hypotheses about how butterfly eyespots confer protection against predators

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

Eyespots—round or oval spots, usually accompanied by one or more concentric rings, that together imitate vertebrate eyes—are found in insects of at least three orders and in some tropical fishes (Stevens 2005). They are particularly frequent in Lepidoptera, where they occur on wings of adults in many species (Monteiro et al. 2006), and in caterpillars of many others (Janzen et al. 2010). The resemblance of eyespots to vertebrate eyes often extends to details, such as fake « pupils » (round or slit-like) and « eye sparkle » (Blut et al. 2012). Larvae of one hawkmoth species even have fake eyes that appear to blink (Hossie et al. 2013). Eyespots have interested evolutionary biologists for well over a century. While they appear to play a role in mate choice in some adult Lepidoptera, their adaptive significance in adult Lepidoptera, as in caterpillars, is mainly as an anti-predator defense (Monteiro 2015). However, there are two competing hypotheses about the mechanism by which eyespots confer defense against predators. The « intimidation » hypothesis postulates that eyespots intimidate potential predators, startling them and reducing the probability of attack. The « deflection » hypothesis holds that eyespots deflect attacks to parts of the body where attack has relatively little effect on the animal’s functioning and survival. In caterpillars, there is little scope for the deflection hypothesis, because attack on any part of a caterpillar’s body is likely to be lethal. Much observational and some experimental evidence supports the intimidation hypothesis in caterpillars (Hossie & Sherratt 2012). In adult Lepidoptera, however, both mechanisms are plausible, and both have found support (Stevens 2005). The most spectacular examples of intimidation are in butterflies in which eyespots located centrally in hindwings and hidden in the natural resting position are suddenly exposed, startling the potential predator (e.g., Vallin et al. 2005). The most spectacular examples of deflection are seen in butterflies in which eyespots near the hindwing margin combined with other traits give the appearance of a false head (e.g., Chotard et al. 2022; Kodandaramaiah 2011). 

Most studies have attempted to test for only one or the other of these mechanisms—usually the one that seems a priori more likely for the butterfly species being studied. But for many species, particularly those that have neither spectacular startle displays nor spectacular false heads, evidence for or against the two hypotheses is contradictory.  

Iserhard et al. (2024) attempted to simultaneously test both hypotheses, using the neotropical nymphalid butterfly Caligo martia. This species has a large ventral hindwing eyespot, exposed in the insect’s natural resting position, while the rest of the ventral hindwing surface is cryptically coloured. In a previous study of this species, De Bona et al. (2015) presented models with intact and disfigured eyespots on a computer monitor to a European bird species, the great tit (Parus major). The results favoured the intimidation hypothesis. Iserhard et al. (2024) devised experiments presenting more natural conditions, using fairly realistic dummy butterflies, with eyespots manipulated or unmanipulated, exposed to a diverse assemblage of insectivorous birds in nature, in a tropical forest. Using color-printed paper facsimiles of wings, with eyespots present, UV-enhanced, or absent, they compared the frequency of beakmarks on modeling clay applied to wing margins (frequent attacks would support the deflection hypothesis) and (in one of two experiments) on dummies with a modeling-clay body (eyespots should lead to reduced frequency of attack, to wings and body, if birds are intimidated). Their experiments also included dummies without eyespots whose wings were either cryptically coloured (as in unmanipulated butterflies) or not. Their results, although complex, indicate support for the deflection hypothesis: dummies with eyespots were mostly attacked on these less vital parts. Dummies lacking eyespots were less frequently attacked, especially when they were camouflaged. Camouflaged dummies without eyespots were in fact the least frequently attacked of all the models. However, when dummies lacking eyespots were attacked, attacks were usually directed to vital body parts. These results show some of the complexity of estimating costs and benefits of protective conspicuous signals vs. camouflage (Stevens et al. 2008).

Two complementary experiments were conducted. The first used facsimiles with « wings » in a natural resting position (folded, ventral surfaces exposed), but without a modeling-clay « body ». In the second experiment, facsimiles had a modeling-clay « body », placed between the two unfolded wings to make it as accessible to birds as the wings. However, these dummies displayed the ventral surfaces of unfolded wings, an unnatural resting position. The study was thus not able to compare bird attacks to the body vs. wings in a natural resting position. One can understand the reason for this methodological choice, but it is a limitation of the study.

The naturalness of the conditions under which these field experiments were conducted is a strong argument for the biological significance of their results. However, the uncontrolled conditions naturally result in many questions being left open. The butterfly dummies were exposed to at least nine insectivorous bird species. Do bird species differ in their behavioral response to eyespots? Do responses depend on the distance at which a bird first detects the butterfly? Do eyespots and camouflage markings present on the same animal both function, but at different distances (Tullberg et al. 2005)? Do bird responses vary depending on the particular light environment in the places and at the times when they encounter the butterfly (Kodandaramaiah 2011)? Answering these questions under natural, uncontrolled conditions will be challenging, requiring onerous methods, (e.g., video recording in multiple locations over time). The study indicates the interest of pursuing these questions.

References

Blut, C., Wilbrandt, J., Fels, D., Girgel, E.I., & Lunau, K. (2012). The ‘sparkle’ in fake eyes–the protective effect of mimic eyespots in Lepidoptera. Entomologia Experimentalis et Applicata, 143, 231-244. https://doi.org/10.1111/j.1570-7458.2012.01260.x

Chotard, A., Ledamoisel, J., Decamps, T., Herrel, A., Chaine, A.S., Llaurens, V., & Debat, V. (2022). Evidence of attack deflection suggests adaptive evolution of wing tails in butterflies. Proceedings of the Royal Society B, 289, 20220562. https://doi.org/10.1098/rspb.2022.0562

De Bona, S., Valkonen, J.K., López-Sepulcre, A., & Mappes, J. (2015). Predator mimicry, not conspicuousness, explains the efficacy of butterfly eyespots. Proceedings of the Royal Society B, 282, 1806. https://doi.org/10.1098/RSPB.2015.0202

Hossie, T.J., & Sherratt, T.N. (2012). Eyespots interact with body colour to protect caterpillar-like prey from avian predators. Animal Behaviour, 84, 167-173. https://doi.org/10.1016/j.anbehav.2012.04.027

Hossie, T.J., Sherratt, T.N., Janzen, D.H., & Hallwachs, W. (2013). An eyespot that “blinks”: an open and shut case of eye mimicry in Eumorpha caterpillars (Lepidoptera: Sphingidae). Journal of Natural History, 47, 2915-2926. https://doi.org/10.1080/00222933.2013.791935

Iserhard, C.A., Malta, S.T., Penz, C.M., Brenda Barbon Fraga; Camila Abel da Costa; Taiane Schwantz; & Kauane Maiara Bordin (2024). The large and central Caligo martia eyespot may reduce fatal attacks by birds : a case study supports the deflection hypothesis in nature. Zenodo, ver. 1 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.5281/zenodo.10980357

Janzen, D.H., Hallwachs, W., & Burns, J.M. (2010). A tropical horde of counterfeit predator eyes. Proceedings of the National Academy of Sciences, USA, 107, 11659-11665. https://doi.org/10.1073/pnas.0912122107

Kodandaramaiah, U. (2011). The evolutionary significance of butterfly eyespots. Behavioral Ecology, 22, 1264-1271. https://doi.org/10.1093/beheco/arr123

Monteiro, A. (2015). Origin, development, and evolution of butterfly eyespots. Annual Review of Entomology, 60, 253-271. https://doi.org/10.1146/annurev-ento-010814-020942

Monteiro, A., Glaser, G., Stockslager, S., Glansdorp, N., & Ramos, D. (2006). Comparative insights into questions of lepidopteran wing pattern homology. BMC Developmental Biology, 6, 1-13. https://doi.org/10.1186/1471-213X-6-52

Stevens, M. (2005). The role of eyespots as anti-predator mechanisms, principally demonstrated in the Lepidoptera. Biological Reviews, 80, 573–588. https://doi.org/10.1017/S1464793105006810

Stevens, M., Stubbins, C.L., & Hardman C.J. (2008). The anti-predator function of ‘eyespots’ on camouflaged and conspicuous prey. Behavioral Ecology and Sociobiology, 62, 1787-1793. https://doi.org/10.1007/s00265-008-0607-3

Tullberg, B.S., Merilaita, S., & Wiklund, C. (2005). Aposematism and crypsis combined as a result of distance dependence: functional versatility of the colour pattern in the swallowtail butterfly larva. Proceedings of the Royal Society B, 272, 1315-1321. https://doi.org/10.1098/rspb.2005.3079

Vallin, A., Jakobsson, S., Lind, J., & Wiklund, C. (2005). Prey survival by predator intimidation: an experimental study of peacock butterfly defence against blue tits. Proceedings of the Royal Society B, 272, 1203-1207. https://doi.org/10.1098/rspb.2004.3034

The large and central *Caligo martia* eyespot may reduce fatal attacks by birds: a case study supports the deflection hypothesis in natureCristiano Agra Iserhard, Shimene Torve Malta, Carla Maria Penz, Brenda Barbon Fraga, Camila Abel da Costa, Taiane Schwantz, Kauane Maiara Bordin<p>Many animals have colorations that resemble eyes, but the functions of such eyespots are debated. Caligo martia (Godart, 1824) butterflies have large ventral hind wing eyespots, and we aimed to test whether these eyespots act to deflect or to t...Biodiversity, Community ecology, Conservation biology, Life history, Tropical ecologyDoyle Mc Key2023-11-21 15:00:20 View
18 Apr 2024
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Insights on the effect of mega-carcass abundance on the population dynamics of a facultative scavenger predator and its prey

Unveiling the influence of carrion pulses on predator-prey dynamics

Recommended by ORCID_LOGO based on reviews by Eli Strauss and 1 anonymous reviewer

Most, if not all, predators consume carrion in some circumstances (Sebastián-Gonzalez et al. 2023). Consequently, significant fluctuations in carrion availability can impact predator-prey dynamics by altering the ratio of carrion to live prey in the predators' diet (Roth 2003). Changes in carrion availability may lead to reduced predation when carrion is more abundant (hypo-predation) and intensified predation if predator populations surge in response to carrion influxes but subsequently face scarcity (hyper-predation), (Moleón et al. 2014, Mellard et al. 2021). However, this relationship between predation and scavenging is often challenging because of the lack of empirical data.
 
In the study conducted by Sidous et al. (2024), they used a large database on the abundance of spotted hyenas and their prey in Zimbabwe and Multivariate Autoregressive State-Space Models to calculate hyena and prey population densities and trends over a 60-year span. The researchers took advantage of abrupt fluctuations in elephant carcass availability that produced alternating periods of high and low carrion availability related to changing management strategies (i.e., elephant culling and water supply).
 
Interestingly, their analyses reveal a coupling of predator and prey densities over time, but they do not detect an effect of carcass availability on predator and prey dynamics. However, the density of prey and hyena was partially driven by the different temporal periods, suggesting some subtle effects of carrion availability on population trends. While it is acknowledged that other variables likely impact the population dynamics of hyenas and their prey, this is the first attempt to understand the influence of carrion pulses on predator-prey interactions across an extensive temporal scale. I hope this helps to establish a new research line on the effect of large carrion pulses, as this is currently largely understudied, even though the occurrence of carrion pulses, such as mass mortality events, is expected to increase over time (Fey et al. 2015).
 
References
 
Courchamp, F. et al. 2000. Rabbits killing birds: modelling the hyperpredation process. J. Anim. Ecol. 69: 154-164.
https://doi.org/10.1046/j.1365-2656.2000.00383.x

Fey, S. B. et al. 2015. Recent shifts in the occurrence, cause, and magnitude of animal mass mortality events. PNAS 112: 1083-1088.
https://doi.org/10.1073/pnas.1414894112
 
Mellard, J. P. et al. 2021. Effect of scavenging on predation in a food web. Ecol. Evol. 11: 6742- 6765.
https://doi.org/10.1002/ece3.7525

Moleón, M. et al. 2014. Inter-specific interactions linking predation and scavenging in terrestrial vertebrate assemblages. Biol. Rev. Camb. Philos. Soc. 89: 1042-1054.
https://doi.org/10.1111/brv.12097
 
Roth, J. 2003. Variability in marine resources affects arctic fox population dynamics. J. Anim. Ecol. 72: 668-676.
https://doi.org/10.1046/j.1365-2656.2003.00739.x
 
Sebastián-González, E. et al. 2023. The underestimated role of carrion in diet studies. Global Ecol. Biogeogr. 32: 1302-1310.
https://doi.org/10.1111/geb.13707
 
Sidous, M. et al. 2024. Insights on the effect of mega-carcass abundance on 1 the population dynamics of a facultative scavenger predator and its prey. bioRxiv, ver. 2 peer-reviewed and recommended by PCI Ecology.
https://doi.org/10.1101/2023.11.08.566247

Insights on the effect of mega-carcass abundance on the population dynamics of a facultative scavenger predator and its preyMellina Sidous; Sarah Cubaynes; Olivier Gimenez; Nolwenn Drouet-Hoguet; Stephane Dray; Loic Bollache; Daphine Madhlamoto; Nobesuthu Adelaide Ngwenya; Herve Fritz; Marion Valeix<p>The interplay between facultative scavenging and predation has gained interest in the last decade. The prevalence of scavenging induced by the availability of large carcasses may modify predator density or behaviour, potentially affecting prey....Community ecologyEsther Sebastián González Eli Strauss2023-11-14 15:27:16 View
28 Mar 2024
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Changes in length-at-first return of a sea trout (Salmo trutta) population in northern France

Why are trout getting smaller?

Recommended by based on reviews by Jan Kozlowski and 1 anonymous reviewer

Decline in body size over time have been widely observed in fish (but see Solokas et al. 2023), and the ecological consequences of this pattern can be severe (e.g., Audzijonyte et al. 2013, Oke et al. 2020). Therefore, studying the interrelationships between life history traits to understand the causal mechanisms of this pattern is timely and valuable. 

This phenomenon was the subject of a study by Josset et al. (2024), in which the authors analysed data from 39 years of trout trapping in the Bresle River in France. The authors focused mainly on the length of trout on their first return from the sea.   

The most important results of the study were the decrease in fish length-at-first return and the change in the age structure of first-returning trout towards younger (and earlier) returning fish. It seems then that the smaller size of trout is caused by a shorter time spent in the sea rather than a change in a growth pattern, as length-at-age remained relatively constant, at least for those returning earlier. Fish returning after two years spent in the sea had a relatively smaller length-at-age. The authors suggest this may be due to local changes in conditions during fish's stay in the sea, although there is limited environmental data to confirm the causal effect. Another question is why there are fewer of these older fish. The authors point to possible increased mortality from disease and/or overfishing.

These results may suggest that the situation may be getting worse, as another study finding was that “the more growth seasons an individual spent at sea, the greater was its length-at-first return.” The consequences may be the loss of the oldest and largest individuals, whose disproportionately high reproductive contribution to the population is only now understood (Barneche et al. 2018, Marshall and White 2019). 

References

Audzijonyte, A. et al. 2013. Ecological consequences of body size decline in harvested fish species: positive feedback loops in trophic interactions amplify human impact. Biol Lett 9, 20121103. https://doi.org/10.1098/rsbl.2012.1103

Barneche, D. R. et al. 2018. Fish reproductive-energy output increases disproportionately with body size. Science Vol 360, 642-645. https://doi.org/10.1126/science.aao6868

Josset, Q. et al. 2024. Changes in length-at-first return of a sea trout (Salmo trutta) population in northern France. biorXiv, 2023.11.21.568009, ver 4, Peer-reviewed and recommended by PCI Ecology. https://doi.org/10.1101/2023.11.21.568009

Marshall, D. J. and White, C. R. 2019. Have we outgrown the existing models of growth? Trends in Ecology & Evolution, 34, 102-111. https://doi.org/10.1016/j.tree.2018.10.005

Oke, K. B. et al. 2020. Recent declines in salmon body size impact ecosystems and fisheries. Nature Communications, 11, 4155. https://doi.org/10.1038/s41467-020-17726-z

Solokas, M. A. et al. 2023. Shrinking body size and climate warming: many freshwater salmonids do not follow the rule. Global Change Biology, 29, 2478-2492. https://doi.org/10.1111/gcb.16626

Changes in length-at-first return of a sea trout (*Salmo trutta*) population in northern FranceQuentin Josset, Laurent Beaulaton, Atso Romakkaniemi, Marie Nevoux<p style="text-align: justify;">The resilience of sea trout populations is increasingly concerning, with evidence of major demographic changes in some populations. Based on trapping data and related scale collection, we analysed long-term changes ...Biodiversity, Evolutionary ecology, Freshwater ecology, Life history, Marine ecologyAleksandra Walczyńska2023-11-23 14:36:39 View
19 Mar 2024
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How does dispersal shape the genetic patterns of animal populations in European cities? A simulation approach

Gene flow in the city. Unravelling the mechanisms behind the variability in urbanization effects on genetic patterns.

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

Worldwide, city expansion is happening at a fast rate and at the same time, urbanists are more and more required to make place for biodiversity. Choices have to be made regarding the area and spatial arrangement of suitable spaces for non-human living organisms, that will favor the long-term survival of their populations. To guide those choices, it is necessary to understand the mechanisms driving the effects of land management on biodiversity.

Research results on the effects of urbanization on genetic diversity have been very diverse, with studies showing higher genetic diversity in rural than in urban populations (e.g. Delaney et al. 2010), the contrary (e.g. Miles et al. 2018) or no difference (e.g. Schoville et al. 2013). The same is true for studies investigating genetic differentiation. The reasons for these differences probably lie in the relative intensities of gene flow and genetic drift in each case study, which are hard to disentangle and quantify in empirical datasets.

In their paper, Savary et al. (2024) used an elegant and powerful simulation approach to better understand the diversity of observed patterns and investigate the effects of dispersal limitation on genetic patterns (diversity and differentiation). Their simulations involved the landscapes of 325 real European cities, each under three different scenarios mimicking 3 virtual urban tolerant species with different abilities to move within cities while genetic drift intensity was held constant across scenarios. The cities were chosen so that the proportion of artificial areas was held constant (20%) but their location and shape varied. This design allowed the authors to investigate the effect of connectivity and spatial configuration of habitat on the genetic responses to spatial variations in dispersal in cities. 

The main results of this simulation study demonstrate that variations in dispersal spatial patterns, for a given level of genetic drift, trigger variations in genetic patterns. Genetic diversity was lower and genetic differentiation was larger when species had more difficulties to move through the more hostile components of the urban environment. The increase of the relative importance of drift over gene flow when dispersal was spatially more constrained was visible through the associated disappearance of the pattern of isolation by resistance. Forest patches (usually located at the periphery of the cities) usually exhibited larger genetic diversity and were less differentiated than urban green spaces. But interestingly, the presence of habitat patches at the interface between forest and urban green spaces lowered those differences through the promotion of gene flow. 

One other noticeable result, from a landscape genetic method point of view, is the fact that there might be a limit to the detection of barriers to genetic clusters through clustering analyses because of the increased relative effect of genetic drift. This result needs to be confirmed, though, as genetic structure has only been investigated with a recent approach based on spatial graphs. It would be interesting to also analyze those results with the usual Bayesian genetic clustering approaches. 

Overall, this study addresses an important scientific question about the mechanisms explaining the diversity of observed genetic patterns in cities. But it also provides timely cues for connectivity conservation and restoration applied to cities.  
 
References

Delaney, K. S., Riley, S. P., and Fisher, R. N. (2010). A rapid, strong, and convergent genetic response to urban habitat fragmentation in four divergent and widespread vertebrates. PLoS ONE, 5(9):e12767.
https://doi.org/10.1371/journal.pone.0012767
 
Miles, L. S., Dyer, R. J., and Verrelli, B. C. (2018). Urban hubs of connectivity: Contrasting patterns of gene flow within and among cities in the western black widow spider. Proceedings of the Royal Society B, 285(1884):20181224. https://doi.org/10.1098/rspb.2018.1224
 
Savary P., Tannier C., Foltête J.-C., Bourgeois M., Vuidel G., Khimoun A., Moal H., and Garnier S. (2024). How does dispersal shape the genetic patterns of animal populations in European cities? A simulation approach. EcoEvoRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.32942/X2JS41.
 
Schoville, S. D., Widmer, I., Deschamps-Cottin, M., and Manel, S. (2013). Morphological clines and weak drift along an urbanization gradient in the butterfly, Pieris rapae. PLoS ONE, 8(12):e83095.
https://doi.org/10.1371/journal.pone.0083095

How does dispersal shape the genetic patterns of animal populations in European cities? A simulation approachPaul Savary, Cécile Tannier, Jean-Christophe Foltête, Marc Bourgeois, Gilles Vuidel, Aurélie Khimoun, Hervé Moal, Stéphane Garnier<p><em>Context and objectives</em></p> <p>Although urbanization is a major driver of biodiversity erosion, it does not affect all species equally. The neutral genetic structure of populations in a given species is affected by both genetic drift a...Biodiversity, Conservation biology, Dispersal & Migration, Eco-evolutionary dynamics, Human impact, Landscape ecology, Molecular ecology, Population ecology, Spatial ecology, Metacommunities & Metapopulations, Terrestrial ecologyAurélie Coulon2023-07-25 19:09:16 View
11 Mar 2024
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Sex differences in the relationship between maternal and neonate cortisol in a free-ranging large mammal

Stress and stress hormones’ transmission from mothers to offspring

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

Individuals can respond to environmental changes that they undergo directly (within-generation plasticity) but also through transgenerational plasticity, providing lasting effects that are transmitted to the next generations (Donelson et al. 2012; Munday et al. 2013; Kuijper & Hoyle 2015; Auge et al. 2017, Tariel et al. 2020). These parental effects can affect offspring via various mechanisms, notably via maternal transmission of hormones to the eggs or growing embryos (Mousseau & Fox 1998). While the effects of environmental quality may simply carry-over to the next generation (e.g., females in stressful environments give birth to offspring in poorer condition), parental effects may also be a mechanism that adjusts offspring phenotype in response to environmental variation and predictability, and thereby match offspring's phenotype to future environmental conditions (Gluckman et al. 2005; Marshall & Uller 2007; Dey et al. 2016; Yin et al. 2019), for example by preparing their offspring to an expected stressful environment.

When females experience stress during gestation or egg formation, elevations in glucocorticoids (GC) are expected to affect offspring phenotype in many ways, from the offspring's own GC levels, to their growth and survival (Sheriff et al. 2017). This is a well established idea, but how strong is the evidence for this? A meta-analysis on birds found no clear effect of corticosterone manipulation on offspring traits (38 studies on 9 bird species for corticosterone manipulation; Podmokła et al. 2018). Another meta-analysis including 14 vertebrate species found no clear effect of prenatal stress on offspring GC (Thayer et al. 2018). Finally, a meta-analysis on wild vertebrates (23 species) found no clear effect of GC-mediated maternal effects on offspring traits (MacLeod et al. 2021). As often when facing such inconclusive results, context dependence has been suggested as one potential reason for such inconsistencies, for exemple sex specific effects (Groothuis et al. 2019, 2020). However, sex specific measures on offspring are scarce (Podmokła et al. 2018). Moreover, the literature available is still limited to a few, mostly “model” species.

With their study, Amin et al. (2024) show the way to improve our understanding on GC transmission from mother to offspring and its effects in several aspects. First they used innovative non-invasive methods (which could broaden the range of species available to study) by quantifying cortisol metabolites from faecal samples collected from pregnant females, as proxy for maternal GC level, and relating it to GC levels from hairs of their neonate offspring. Second they used a free ranging large mammal (taxa from which literature is missing): the fallow deer (Dama dama). Third, they provide sex specific measures of GC levels. And finally but importantly, they are exemplary in their transparency regarding 1) the exploratory nature of their study, 2) their statistical thinking and procedure, and 3) the study limitations (e.g., low sample size and high within individual variation of measurements). I hope this study will motivate more research (on the fallow deer, and on other species) to broaden and strengthen our understanding of sex specific effects of maternal stress and CG levels on offspring phenotype and fitness.

References

Amin, B., Fishman, R., Quinn, M., Matas, D., Palme, R., Koren, L., & Ciuti, S. (2024). Sex differences in the relationship between maternal and foetal glucocorticoids in a free-ranging large mammal. bioRxiv, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2023.05.04.538920 

Auge, G.A., Leverett, L.D., Edwards, B.R. & Donohue, K. (2017). Adjusting phenotypes via within-and across-generational plasticity. New Phytologist, 216, 343–349. https://doi.org/10.1111/nph.14495

Dey, S., Proulx, S.R. & Teotonio, H. (2016). Adaptation to temporally fluctuating environments by the evolution of maternal effects. PLoS biology, 14, e1002388. https://doi.org/10.1371/journal.pbio.1002388

Donelson, J.M., Munday, P.L., McCormick, M.I. & Pitcher, C.R. (2012). Rapid transgenerational acclimation of a tropical reef fish to climate change. Nature Climate Change, 2, 30. https://doi.org/10.1038/nclimate1323

Gluckman, P.D., Hanson, M.A. & Spencer, H.G. (2005). Predictive adaptive responses and human evolution. Trends in ecology & evolution, 20, 527–533. https://doi.org/10.1016/j.tree.2005.08.001

Groothuis, Ton GG, Bin-Yan Hsu, Neeraj Kumar, and Barbara Tschirren. "Revisiting mechanisms and functions of prenatal hormone-mediated maternal effects using avian species as a model." Philosophical Transactions of the Royal Society B 374, no. 1770 (2019): 20180115. https://doi.org/10.1098/rstb.2018.0115

Groothuis, Ton GG, Neeraj Kumar, and Bin-Yan Hsu. "Explaining discrepancies in the study of maternal effects: the role of context and embryo." Current Opinion in Behavioral Sciences 36 (2020): 185-192. https://doi.org/10.1016/j.cobeha.2020.10.006 

Kuijper, B. & Hoyle, R.B. (2015). When to rely on maternal effects and when on phenotypic plasticity? Evolution, 69, 950–968. https://doi.org/10.1111/evo.12635   

MacLeod, Kirsty J., Geoffrey M. While, and Tobias Uller. "Viviparous mothers impose stronger glucocorticoid‐mediated maternal stress effects on their offspring than oviparous mothers." Ecology and Evolution 11, no. 23 (2021): 17238-17259.

Marshall, D.J. & Uller, T. (2007). When is a maternal effect adaptive? Oikos, 116, 1957–1963. https://doi.org/10.1111/j.2007.0030-1299.16203.x       

Mousseau, T.A. & Fox, C.W. (1998). Maternal effects as adaptations. Oxford University Press.

Munday, P.L., Warner, R.R., Monro, K., Pandolfi, J.M. & Marshall, D.J. (2013). Predicting evolutionary responses to climate change in the sea. Ecology Letters, 16, 1488–1500. https://doi.org/10.1111/ele.12185

Podmokła, Edyta, Szymon M. Drobniak, and Joanna Rutkowska. "Chicken or egg? Outcomes of experimental manipulations of maternally transmitted hormones depend on administration method–a meta‐analysis." Biological Reviews 93, no. 3 (2018): 1499-1517. https://doi.org/10.1111/brv.12406 

Sheriff, M. J., Bell, A., Boonstra, R., Dantzer, B., Lavergne, S. G., McGhee, K. E., MacLeod, K. J., Winandy, L., Zimmer, C., & Love, O. P. (2017). Integrating ecological and evolutionary context in the study of maternal stress. Integrative and Comparative Biology, 57(3), 437–449. https://doi.org/10.1093/icb/icx105

Tariel, Juliette, Sandrine Plénet, and Émilien Luquet. "Transgenerational plasticity in the context of predator-prey interactions." Frontiers in Ecology and Evolution 8 (2020): 548660. https://doi.org/10.3389/fevo.2020.548660 

Thayer, Zaneta M., Meredith A. Wilson, Andrew W. Kim, and Adrian V. Jaeggi. "Impact of prenatal stress on offspring glucocorticoid levels: A phylogenetic meta-analysis across 14 vertebrate species." Scientific Reports 8, no. 1 (2018): 4942. https://doi.org/10.1038/s41598-018-23169-w 

Yin, J., Zhou, M., Lin, Z., Li, Q.Q. & Zhang, Y.-Y. (2019). Transgenerational effects benefit offspring across diverse environments: a meta-analysis in plants and animals. Ecology letters, 22, 1976–1986. https://doi.org/10.1111/ele.13373

Sex differences in the relationship between maternal and neonate cortisol in a free-ranging large mammalAmin, B., Fishman, R., Quinn, M., Matas, D., Palme, R., Koren, L., Ciuti, S.<p style="text-align: justify;">Maternal phenotypes can have long-term effects on offspring phenotypes. These maternal effects may begin during gestation, when maternal glucocorticoid (GC) levels may affect foetal GC levels, thereby having an orga...Evolutionary ecology, Maternal effects, Ontogeny, Physiology, ZoologyMatthieu Paquet2023-06-05 09:06:56 View