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26 Mar 2019
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Is behavioral flexibility manipulatable and, if so, does it improve flexibility and problem solving in a new context?

Can context changes improve behavioral flexibility? Towards a better understanding of species adaptability to environmental changes

Recommended by ORCID_LOGO based on reviews by Maxime Dahirel and Andrea Griffin

Behavioral flexibility is a key for species adaptation to new environments. Predicting species responses to new contexts hence requires knowledge on the amount to and conditions in which behavior can be flexible. This is what Logan and collaborators propose to assess in a series of experiments on the great-tailed grackles, in a context of rapid range expansion. This pre-registration is integrated into this large research project and concerns more specifically the manipulability of the cognitive aspects of behavioral flexibility. Logan and collaborators will use reversal learning tests to test whether (i) behavioral flexibility is manipulatable, (ii) manipulating flexibility improves flexibility and problem solving in a new context, (iii) flexibility is repeatable within individuals, (iv) individuals are faster at problem solving as they progress through serial reversals. The pre-registration carefully details the hypotheses, their associated predictions and alternatives, and the plan of statistical analyses, including power tests. The ambitious program presented in this pre-registration has the potential to provide important pieces to better understand the mechanisms of species adaptability to new environments.

Is behavioral flexibility manipulatable and, if so, does it improve flexibility and problem solving in a new context?Corina Logan, Carolyn Rowney, Luisa Bergeron, Benjamin Seitz, Aaron Blaisdell, Zoe Johnson-Ulrich, Kelsey McCuneThis is one of the first studies planned for our long-term research on the role of behavioral flexibility in rapid geographic range expansions. Behavioral flexibility, the ability to adapt behavior to new circumstances, is thought to play an impor...Behaviour & Ethology, Preregistrations, ZoologyAurélie Coulon2018-07-03 13:23:10 View
05 Mar 2019
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Are the more flexible great-tailed grackles also better at inhibition?

Adapting to a changing environment: advancing our understanding of the mechanisms that lead to behavioral flexibility

Recommended by based on reviews by Simon Gingins and 2 anonymous reviewers

Behavioral flexibility is essential for organisms to adapt to an ever-changing environment. However, the mechanisms that lead to behavioral flexibility and understanding what traits makes a species better able to adapt behavior to new environments has been understudied. Logan and colleagues have proposed to use a series of experiments, using great-tailed grackles as a study species, to test four main hypotheses. These hypotheses are centered around exploring the relationship between behavioral flexibility and inhibition in grackles. This current preregistration is a part of a larger integrative research plan examining behavioral flexibility when faced with environmental change. In this part of the project they will examine specifically if individuals that are more flexible are also better at inhibiting: in other words: they will test the assumption that inhibition is required for flexibility.
First, they will test the hypothesis that behavioral flexibility is manipulatable by using a serial reversal learning task. Second, they will test the hypothesis that manipulating behavioral flexibility (improving reversal learning speed through serial reversals using colored tubers) improves flexibility (rule switching) and problem solving in a new context (multi‑access box and serial reversals on a touch screen). Third, they will test the hypothesis that behavioral flexibility within a context is repeatable within individuals, which is important to test if performance is state dependent. Finally, they will test a fourth hypothesis that individuals should converge on an epsilon‑first learning strategy (learn the correct choice after one trial) as they progress through serial reversals. Their innovative approach using three main tasks (delay of gratification, go-no, detour) will allow them to assess different aspects of inhibitory control. They will analyze the results of all three experiments to also assess the utility of these experiments for studying the potential relationship between inhibition and behavioral flexibility.
In their preregistration, Logan and colleagues have proposed to test these hypotheses, each with a set of testable predictions that can be examined with detailed and justified methodologies. They have also provided a comprehensive plan for analyzing the data. All of the reviewers and I agree that this is a very interesting study that has the potential to answer important questions about a critical topic in behavioral ecology: the role of inhibition in the evolution of behavioral flexibility. Given the positive reviews, the comprehensive responses by the PI and her colleagues, and careful revisions, I highly recommend this preregistration.

Are the more flexible great-tailed grackles also better at inhibition?Corina Logan, Kelsey McCune, Zoe Johnson-Ulrich, Luisa Bergeron, Carolyn Rowney, Benjamin Seitz, Aaron Blaisdell, Claudia WascherThis is a PREREGISTRATION. The DOI was issued by OSF and refers to the whole GitHub repository, which contains multiple files. The specific file we are submitting is g_inhibition.Rmd, which is easily accessible at GitHub at https://github.com/cori...Behaviour & Ethology, Preregistrations, ZoologyErin Vogel2018-10-12 18:36:00 View
07 Aug 2019
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Is behavioral flexibility related to foraging and social behavior in a rapidly expanding species?

Understanding geographic range expansions in human-dominated landscapes: does behavioral flexibility modulate flexibility in foraging and social behavior?

Recommended by ORCID_LOGO and ORCID_LOGO based on reviews by Pizza Ka Yee Chow and Esther Sebastián González

Which biological traits modulate species distribution has historically been and still is one of the core questions of the macroecology and biogeography agenda [1, 2]. As most of the Earth surface has been modified by human activities [3] understanding the strategies that allow species to inhabit human-dominated landscapes will be key to explain species geographic distribution in the Anthropocene. In this vein, Logan et al. [4] are working on a long-term and integrative project aimed to investigate how great-tailed grackles rapidly expanded their geographic range into North America [4]. Particularly, they want to determine which is the role of behavioral flexibility, i.e. an individual’s ability to modify its behavior when circumstances change based on learning from previous experience [5], in rapid geographic range expansions. The authors are already working in a set of complementary questions described in pre-registrations that have already been recommended at PCI Ecology: (1) Do individuals with greater behavioral flexibility rely more on causal cognition [6]? (2) Which are the mechanisms that lead to behavioral flexibility [7]? (3) Does the manipulation of behavioral flexibility affect exploration, but not boldness, persistence, or motor diversity [8]? (4) Can context changes improve behavioral flexibility [9]?
In this new pre-registration, they aim to determine whether the more behaviorally flexible individuals have more flexible foraging behaviors (i.e. use a wider variety of foraging techniques in the wild and eat a larger number of different foods), habitat use (i.e. higher microhabitat richness) and social relationships (i.e., are more likely to have a greater number of bonds or stronger bonds with other individuals; [4]). The project is ambitious, combining both the experimental characterization of individuals’ behavioral flexibility and the field characterization of the foraging and social behavior of those individuals and of wild ones.
The current great-tailed grackles project will be highly relevant to understand rapid geographic range expansions in a changing world. In this vein, this pre-registration will particularly help to go one step further in our understanding of behavioral flexibility as a determinant of species geographic distribution. Logan et al. [4] pre-registration is very well designed, main and alternative hypotheses have been thought and written and methods are presented in a very detailed way, which includes the R codes that authors will use in their analyses. Authors have answered in a very detailed way each comment that reviewers have pointed out and modified the pre-registration accordingly, which we consider highly improved the quality of this work. That is why we strongly recommend this pre-registration and look forward to see the results.

References

[1] Gaston K. J. (2003) The structure and dynamics of geographic ranges. Oxford series in Ecology and Evolution. Oxford University Press, New York.
[2] Castro-Insua, A., Gómez‐Rodríguez, C., Svenning, J.C., and Baselga, A. (2018) A new macroecological pattern: The latitudinal gradient in species range shape. Global ecology and biogeography, 27(3), 357-367. doi: 10.1111/geb.12702
[3] Newbold, T., Hudson, L. N., Hill, S. L. L., Contu, S., Lysenko, I., Senior, R. A., et al. (2015). Global effects of land use on local terrestrial biodiversity. Nature, 520(7545), 45–50. doi: 10.1038/nature14324
[4] Logan CJ, McCune K, Bergeron L, Folsom M, Lukas D. (2019). Is behavioral flexibility related to foraging and social behavior in a rapidly expanding species? In principle recommendation by Peer Community In Ecology. http://corinalogan.com/Preregistrations/g_flexforaging.html
[5] Mikhalevich, I., Powell, R., and Logan, C. (2017). Is Behavioural Flexibility Evidence of Cognitive Complexity? How Evolution Can Inform Comparative Cognition. Interface Focus 7: 20160121. doi: 10.1098/rsfs.2016.0121.
[6] Fronhofer, E. (2019) From cognition to range dynamics: advancing our understanding of macroecological patterns. Peer Community in Ecology, 100014. doi: 10.24072/pci.ecology.100014
[7] Vogel, E. (2019) Adapting to a changing environment: advancing our understanding of the mechanisms that lead to behavioral flexibility. Peer Community in Ecology, 100016. doi: 10.24072/pci.ecology.100016
[8] Van Cleve, J. (2019) Probing behaviors correlated with behavioral flexibility. Peer Community in Ecology, 100020. doi: 10.24072/pci.ecology.100020
[9] Coulon, A. (2019) Can context changes improve behavioral flexibility? Towards a better understanding of species adaptability to environmental changes. Peer Community in Ecology, 100019. doi: 10.24072/pci.ecology.100019

Is behavioral flexibility related to foraging and social behavior in a rapidly expanding species?Corina Logan, Luisa Bergeron, Carolyn Rowney, Kelsey McCune, Dieter LukasThis is one of the first studies planned for our long-term research on the role of behavioral flexibility in rapid geographic range expansions. Project background: Behavioral flexibility, the ability to change behavior when circumstances change ba...Behaviour & Ethology, Preregistrations, ZoologyJulia Astegiano2018-10-23 00:47:03 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
12 May 2020
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On the efficacy of restoration in stream networks: comments, critiques, and prospective recommendations

A stronger statistical test of stream restoration experiments

Recommended by based on reviews by Eric Harvey and Mariana Perez Rocha

The metacommunity framework acknowledges that local sites are connected to other sites through dispersal, and that these connectivity patterns can influence local dynamics [1]. This framework is slowly moving from a framework that guides fundamental research to being actively applied in for instance a conservation context (e.g. [2]). Swan and Brown [3,4] analyzed the results of a suite of experimental manipulations in headwater and mainstem streams on invertebrate community structure in the context of the metacommunity concept. This was an important contribution to conservation ecology.
However, David Murray-Stoker [5] was not satisfied with their statistical analyses, and recreated, and more importantly, improved their original analyses in the peer-reviewed article. The new analyses are based on a combination of a more consistent site selection, checking the model assumptions, using different estimation procedures, and focusing more on effect size calculations versus statistical significance. This peer-reviewed article is thus the perfect example of the advantages of open research: the original authors making available both the data and their R script files, initially first updating the analyses and results themselves, followed by more in-depth analyses of the original data and question.
This peer reviewed went through a very in-depth process itself, with several rounds of questions and feedback that addressed both the statistical analyses, the interpretation of the results, and the conclusions. It also, however, addressed something that is often harder to provide feedback on, for instance the tone of the argument. I hope that scientists interested in these issues will not only read the final manuscript, but also the different steps of the peer review processes. These are very informative, I think, and provide a more complete picture of mainly the raison for certain decisions.
Not only does this provide the reader interested in stream conservation with the opportunity to make up their own mind on the appropriateness of these decisions, but it could potentially lead to more analyses of this important data set. For instance, maybe a formal meta-analysis that starts with the effect sizes of all the original studies might bring some new insights into this question?

References

[1] Leibold, M. A., Holyoak, M., Mouquet, N. et al. (2004). The metacommunity concept: a framework for multi‐scale community ecology. Ecology letters, 7(7), 601-613. doi: 10.1111/j.1461-0248.2004.00608.x
[2] Heino, J. (2013). The importance of metacommunity ecology for environmental assessment research in the freshwater realm. Biological Reviews, 88(1), 166-178. doi: 10.1111/j.1469-185X.2012.00244.x
[3] Swan, C. M., and Brown, B. L. (2017). Metacommunity theory meets restoration: isolation may mediate how ecological communities respond to stream restoration. Ecological Applications, 27(7), 2209-2219. doi: 10.1002/eap.1602
[4] Swan, C. M., and Brown, B. L. (2018). Erratum for: Metacommunity theory meets restoration: isolation may mediate how ecological communities respond to stream restoration. Ecological Applications 28:1370–1371. doi: 10.1002/eap.1738
[5] Murray-Stoker, D. (2020). On the efficacy of restoration in stream networks: comments, critiques, and prospective recommendations. bioRxiv, 611939, ver. 7 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/611939

On the efficacy of restoration in stream networks: comments, critiques, and prospective recommendationsDavid Murray-Stoker<p>Swan and Brown (2017) recently addressed the effects of restoration on stream communities under the meta-community framework. Using a combination of headwater and mainstem streams, Swan and Brown (2017) evaluated how position within a stream ne...Community ecology, Freshwater ecology, Spatial ecology, Metacommunities & MetapopulationsKarl Cottenie2019-09-21 22:12:57 View
20 Jun 2024
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Spider mites collectively avoid plants with cadmium irrespective of their frequency or the presence of competitors

We are better together: Spider mites running away from Cadmium contaminated plants make better decisions collectively than individually

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

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

 

Spider mites collectively avoid plants with cadmium irrespective of their frequency or the presence of competitorsDiogo Prino Godinho*, Ines Fragata*, Maud Charlery de la Masseliere, Sara Magalhaes<p>1. Plants can accumulate heavy metals from polluted soils on their shoots and use this to defend themselves against herbivory. One possible strategy for herbivores to cope with the reduction in performance imposed by heavy metal accumulation in...Behaviour & Ethology, Competition, Habitat selection, HerbivoryRuben Heleno2023-11-09 11:52:58 View
11 Aug 2023
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Implementing Code Review in the Scientific Workflow: Insights from Ecology and Evolutionary Biology

A handy “How to” review code for ecologists and evolutionary biologists

Recommended by ORCID_LOGO based on reviews by Serena Caplins and 1 anonymous reviewer

Ivimey Cook et al. (2023) provide a concise and useful “How to” review code for researchers in the fields of ecology and evolutionary biology, where the systematic review of code is not yet standard practice during the peer review of articles. Consequently, this article is full of tips for authors on how to make their code easier to review. This handy article applies not only to ecology and evolutionary biology, but to many fields that are learning how to make code more reproducible and shareable. Taking this step toward transparency is key to improving research rigor (Brito et al. 2020) and is a necessary step in helping make research trustable by the public (Rosman et al. 2022).

References

Brito, J. J., Li, J., Moore, J. H., Greene, C. S., Nogoy, N. A., Garmire, L. X., & Mangul, S. (2020). Recommendations to enhance rigor and reproducibility in biomedical research. GigaScience, 9(6), giaa056. https://doi.org/10.1093/gigascience/giaa056

Ivimey-Cook, E. R., Pick, J. L., Bairos-Novak, K., Culina, A., Gould, E., Grainger, M., Marshall, B., Moreau, D., Paquet, M., Royauté, R., Sanchez-Tojar, A., Silva, I., Windecker, S. (2023). Implementing Code Review in the Scientific Workflow: Insights from Ecology and Evolutionary Biology. EcoEvoRxiv, ver 5 peer-reviewed and recommended by Peer Community In Ecology. https://doi.org/10.32942/X2CG64

Rosman, T., Bosnjak, M., Silber, H., Koßmann, J., & Heycke, T. (2022). Open science and public trust in science: Results from two studies. Public Understanding of Science, 31(8), 1046-1062. https://doi.org/10.1177/09636625221100686

Implementing Code Review in the Scientific Workflow: Insights from Ecology and Evolutionary BiologyEdward Ivimey-Cook, Joel Pick, Kevin Bairos-Novak, Antica Culina, Elliot Gould, Matthew Grainger, Benjamin Marshall, David Moreau, Matthieu Paquet, Raphaël Royauté, Alfredo Sanchez-Tojar, Inês Silva, Saras Windecker<p>Code review increases reliability and improves reproducibility of research. As such, code review is an inevitable step in software development and is common in fields such as computer science. However, despite its importance, code review is not...Meta-analyses, Statistical ecologyCorina Logan2023-05-19 15:54:01 View
11 Mar 2021
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Size-dependent eco-evolutionary feedbacks in fisheries

“Hidden” natural selection and the evolution of body size in harvested stocks

Recommended by based on reviews by Jean-François Arnoldi and 1 anonymous reviewer

Humans are exploiting biological resources since thousands of years. Exploitation of biological resources has become particularly intense since the beginning of the 20th century and the steep increase in the worldwide human population size. Marine and freshwater fishes are not exception to that rule, and they have been (and continue to be) strongly harvested as a source of proteins for humans. For some species, fishery has been so intense that natural stocks have virtually collapsed in only a few decades. The worst example begin that of the Northwest Atlantic cod that has declined by more than 95% of its historical biomasses in only 20-30 years of intensive exploitation (Frank et al. 2005). These rapid and steep changes in biomasses have huge impacts on the entire ecosystems since species targeted by fisheries are often at the top of trophic chains (Frank et al. 2005). 

Beyond demographic impacts, fisheries also have evolutionary impacts on populations, which can also indirectly alter ecosystems (Uusi-Heikkilä et al. 2015; Palkovacs et al. 2018). Fishermen generally focus on the largest specimens, and hence exert a strong selective pressure against these largest fish (which is called “harvest selection”). There is now ample evidence that harvest selection can lead to rapid evolutionary changes in natural populations toward small individuals (Kuparinen & Festa-Bianchet 2017). These evolutionary changes are of course undesirable from a human perspective, and have attracted many scientific questions. Nonetheless, the consequence of harvest selection is not always observable in natural populations, and there are cases in which no phenotypic change (or on the contrary an increase in mean body size) has been observed after intense harvest pressures. In a conceptual Essay, Edeline and Loeuille (Edeline & Loeuille 2020) propose novel ideas to explain why the evolutionary consequences of harvest selection can be so diverse, and how a cross talk between ecological and evolutionary dynamics can explain patterns observed in natural stocks.

 The general and novel concept proposed by Edeline and Loeuille is actually as old as Darwin’s book; The Origin of Species (Darwin 1859). It is based on the simple idea that natural selection acting on harvested populations can actually be strong, and counter-balance (or on the contrary reinforce) the evolutionary consequence of harvest selection. Although simple, the idea that natural and harvest selection are jointly shaping contemporary evolution of exploited populations lead to various and sometimes complex scenarios that can (i) explain unresolved empirical patterns and (ii) refine predictions regarding the long-term viability of exploited populations. 

The Edeline and Loeuille’s crafty inspiration is that natural selection acting on exploited populations is itself an indirect consequence of harvest (Edeline & Loeuille 2020). They suggest that, by modifying the size structure of populations (a key parameter for ecological interactions), harvest indirectly alters interactions between populations and their biotic environment through competition and predation, which changes the ecological theatre and hence the selective pressures acting back to populations. They named this process “size-dependent eco-evolutionary feedback loops” and develop several scenarios in which these feedback loops ultimately deviate the evolutionary outcome of harvest selection from expectation. The scenarios they explore are based on strong theoretical knowledge, and range from simple ones in which a single species (the harvest species) is evolving to more complex (and realistic) ones in which multiple (e.g. the harvest species and its prey) species are co-evolving.

I will not come into the details of each scenario here, and I will let the readers (re-)discovering the complex beauty of biological life and natural selection. Nonetheless, I will emphasize the importance of considering these eco-evolutionary processes altogether to fully grasp the response of exploited populations. Edeline and Loeuille convincingly demonstrate that reduced body size due to harvest selection is obviously not the only response of exploited fish populations when natural selection is jointly considered (Edeline & Loeuille 2020). On the contrary, they show that –under some realistic ecological circumstances relaxing exploitative competition due to reduced population densities- natural selection can act antagonistically, and hence favour stable body size in exploited populations. Although this seems further desirable from a human perspective than a downsizing of exploited populations, it is actually mere window dressing as Edeline and Loeuille further showed that this response is accompanied by an erosion of the evolvability –and hence a lowest probability of long-term persistence- of these exploited populations.

Humans, by exploiting biological resources, are breaking the relative equilibrium of complex entities, and the response of populations to this disturbance is itself often complex and heterogeneous. In this Essay, Edeline and Loeuille provide –under simple terms- the theoretical and conceptual bases required to improve predictions regarding the evolutionary responses of natural populations to exploitation by humans (Edeline & Loeuille 2020). An important next step will be to generate data and methods allowing confronting the empirical reality to these novel concepts (e.g. (Monk et al. 2021), so as to identify the most likely evolutionary scenarios sustaining biological responses of exploited populations, and hence to set the best management plans for the long-term sustainability of these populations.

References

Darwin, C. (1859). On the Origin of Species by Means of Natural Selection. John Murray, London.

Edeline, E. & Loeuille, N. (2021) Size-dependent eco-evolutionary feedbacks in fisheries. bioRxiv, 2020.04.03.022905, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: https://doi.org/10.1101/2020.04.03.022905

Frank, K.T., Petrie, B., Choi, J. S. & Leggett, W.C. (2005). Trophic Cascades in a Formerly Cod-Dominated Ecosystem. Science, 308, 1621–1623. doi: https://doi.org/10.1126/science.1113075

Kuparinen, A. & Festa-Bianchet, M. (2017). Harvest-induced evolution: insights from aquatic and terrestrial systems. Philos. Trans. R. Soc. B Biol. Sci., 372, 20160036. doi: https://doi.org/10.1098/rstb.2016.0036

Monk, C.T., Bekkevold, D., Klefoth, T., Pagel, T., Palmer, M. & Arlinghaus, R. (2021). The battle between harvest and natural selection creates small and shy fish. Proc. Natl. Acad. Sci., 118, e2009451118. doi: https://doi.org/10.1073/pnas.2009451118 

Palkovacs, E.P., Moritsch, M.M., Contolini, G.M. & Pelletier, F. (2018). Ecology of harvest-driven trait changes and implications for ecosystem management. Front. Ecol. Environ., 16, 20–28. doi: https://doi.org/10.1002/fee.1743

Uusi-Heikkilä, S., Whiteley, A.R., Kuparinen, A., Matsumura, S., Venturelli, P.A., Wolter, C., et al. (2015). The evolutionary legacy of size-selective harvesting extends from genes to populations. Evol. Appl., 8, 597–620. doi: https://doi.org/10.1111/eva.12268

Size-dependent eco-evolutionary feedbacks in fisheriesEric Edeline and Nicolas Loeuille<p>Harvesting may drive body downsizing along with population declines and decreased harvesting yields. These changes are commonly construed as direct consequences of harvest selection, where small-bodied, early-reproducing individuals are immedia...Biodiversity, Community ecology, Competition, Eco-evolutionary dynamics, Evolutionary ecology, Food webs, Interaction networks, Life history, Population ecology, Theoretical ecologySimon Blanchet2020-04-03 16:14:05 View
01 Mar 2023
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Effects of adaptive harvesting on fishing down processes and resilience changes in predator-prey and tritrophic systems

Adaptive harvesting, “fishing down the food web”, and regime shifts

Recommended by based on reviews by Pierre-Yves HERNVANN and 1 anonymous reviewer

The mean trophic level of catches in world fisheries has generally declined over the 20th century, a phenomenon called "fishing down the food web" (Pauly et al. 1998). Several mechanisms have been proposed to explain this decline including the collapse of, or decline in, higher trophic level stocks leading to the inclusion of lower trophic level stocks in the fishery. Fishing down the food web may lead to a reduction in the resilience, i.e., the capacity to rebound from change, of the fished community, which is concerning given the necessity of resilience in the face of climate change. 

The practice of adaptive harvesting, which involves fishing stocks based on their availability, can also result in a reduction in the average trophic level of a fishery (Branch et al. 2010). Adaptive harvesting, similar to adaptive foraging, can affect the resilience of fisheries. Generally, adaptive foraging acts as a stabilizing force in communities (Valdovinos et al. 2010), however it is not clear how including harvesters as the adaptive foragers will affect the resilience of the system.

Tromeur and Loeuille (2023) analyze the effects of adaptively harvesting a trophic community. Using a system of ordinary differential equations representing a predator-prey model where both species are harvested, the researchers mathematically analyze the impact of increasing fishing effort and adaptive harvesting on the mean trophic level and resilience of the fished community. This is achieved by computing the equilibrium densities and equilibrium allocation of harvest effort.  In addition, the researchers numerically evaluate adaptive harvesting in a tri-trophic system (predator, prey, and resource). The study focuses on the effect of adaptively distributing harvest across trophic levels on the mean trophic level of catches, the propensity for regime shifts to occur, the ability to return to equilibrium after a disturbance, and the speed of this return. 

The results indicate that adaptive harvesting leads to a decline in the mean trophic level of catches, resulting in “fishing down the food web”. Furthermore, the study shows that adaptive harvesting may harm the overall resilience of the system. Similar results were observed numerically in a tri-trophic community.

While adaptive foraging is generally a stabilizing force on communities, the researchers found that adaptive harvesting can destabilize the harvested community. One of the key differences between adaptive foraging models and the model presented here, is that the harvesters do not exhibit population dynamics. This lack of a numerical response by the harvesters to decreasing population sizes of their stocks leads to regime shifts. The realism of a fishery that does not respond numerically to declining stock is debatable, however it is very likely that there will a least be significant delays due to social and economic barriers to leaving the fishery, that will lead to similar results.

This study is not unique in demonstrating the ability of adaptive harvesting to result in “fishing down the food web”. As pointed out by the researchers, the same results have been shown with several different model formulations (e.g., age and size structured models). Similarly, this study is not unique to showing that increasing adaptation speeds decreases the resilience of non-linear predator-prey systems by inducing oscillatory behaviours. Much of this can be explained by the destabilising effect of increasing interaction strengths on food webs (McCann et al. 1998). 

By employing a straightforward model, the researchers were able to demonstrate that adaptive harvesting, a common strategy employed by fishermen, can result in a decline in the average trophic level of catches, regime shifts, and reduced resilience in the fished community. While previous studies have observed some of these effects, the fact that the current study was able to capture them all with a simple model is notable. This modeling approach can offer insight into the role of human behavior on the complex dynamics observed in fisheries worldwide.

References

Branch, T. A., R. Watson, E. A. Fulton, S. Jennings, C. R. McGilliard, G. T. Pablico, D. Ricard, et al. 2010. The trophic fingerprint of marine fisheries. Nature 468:431–435. https://doi.org/10.1038/nature09528

Tromeur, E., and N. Loeuille. 2023. Effects of adaptive harvesting on fishing down processes and resilience changes in predator-prey and tritrophic systems. bioRxiv 290460, ver 5 peer-reviewed and recommended by PCI Ecology. https://doi.org/10.1101/290460

McCann, K., A. Hastings, and G.R. Huxel. 1998. Weak trophic interactions and the balance of nature. Nature 395: 794-798. https://doi.org/10.1038/27427

Pauly, D., V. Christensen, J. Dalsgaard, R. Froese, and F. Torres Jr. 1998. Fishing down marine food webs. Science 279:860–86. https://doi.org/10.1126/science.279.5352.860

Valdovinos, F.S., R. Ramos-Jiliberto, L. Garay-Naravez, P. Urbani, and J.A. Dunne. 2010. Consequences of adaptive behaviour for the structure and dynamics of food webs. Ecology Letters 13: 1546-1559. https://doi.org/10.1111/j.1461-0248.2010.01535.x

Effects of adaptive harvesting on fishing down processes and resilience changes in predator-prey and tritrophic systemsEric Tromeur, Nicolas Loeuille<p>Many world fisheries display a declining mean trophic level of catches. This "fishing down the food web" is often attributed to reduced densities of high-trophic-level species. We show here that the fishing down pattern can actually emerge from...Biodiversity, Community ecology, Food webs, Foraging, Population ecology, Theoretical ecologyAmanda Lynn Caskenette2022-05-03 21:09:35 View
11 Mar 2022
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Comment on “Information arms race explains plant-herbivore chemical communication in ecological communities”

Does information theory inform chemical arms race communication?

Recommended by based on reviews by Claudio Ramirez and 2 anonymous reviewers

One of the long-standing questions in evolutionary ecology is on the mechanisms involved in arms race coevolution. One way to address this question is to understand the conditions under which one species evolves traits in response to the presence of a second species and so on. However, specialized pairwise interactions are by far less common in nature than interactions involving a higher number of interacting species (Bascompte, Jordano 2013). While interactions between large sets of species are the norm rather than the exception in mutualistic (pollination, seed dispersal), and antagonist (herbivory, parasitism) relationships, few is known on the way species identify, process, and respond to information provided by other interacting species under field conditions (Schaefer, Ruxton 2011). 

Zu et al. (2020) addressed this general question by developing an interesting information theory-based approach that hypothesized conditional entropy in chemical communication plays a role as proxy of fitness in plant-herbivore communities. More specifically, plant fitness was assumed to be related to the efficiency to code signals by plant species, and herbivore fitness to the capacity to decode plant signals. In this way, from the plant perspective, the elaboration of plant signals that elude decoding by herbivores is expected to be favored, as herbivores are expected to attack plants with simple chemical signals. The empirical observation upon which the model was tested was the redundancy in volatile organic compounds (VOC) found across plant species in a plant-herbivore community. Interestingly, Zu et al.’s model predicted successfully that VOC redundancy in the plant community associates with increased conditional entropy, which conveys herbivore confusion and plant protection against herbivory. In this way, plant species that evolve VOCs already present in the community might be benefitted, ultimately leading to the patterns of VOC redundancy commonly observed in nature.

Bass & Kessler performed a series of interesting observations on Zu et al. (2020), that can be organized along three lines of reasoning. First, from an evolutionary perspective, Bass & Kessler note the important point that accepting that conditional information entropy, estimated from the contribution of every plant species to volatile redundancy implies that average plant fitness seems to depend on community-level properties (i.e., what the other species in the community are doing) rather than on population-level characteristics (I.e., what the individuals belonging a population are doing). While the level at which selection acts upon is a longstanding debate (e.g., Goodnight, 1990; Williams, 1992), the model seems to contradict one of the basic tenets of Darwinian evolution. The extent to which this important observation invalidates the contribution of Zu et al. (2020) is open to scrutiny. However, one can indulge the evolutionary criticism by arguing that every theoretical model performs a number of assumptions to preserve the simplicity of analyses. Furthermore, even accepting the criticism, the overall information-based framework is valuable as it provides a fresh perspective to the way coding and decoding chemical information in plant-herbivore interactions may result in arm race coevolution. The question to be assessed by members of the scientific community is how strong the evolutionary assumptions are to be acceptable. A second line of reasoning involves consideration of additional routes of chemical information transfer. If chemical volatiles are involved in another ecological function unrelated to arm race (as they are) such as toxicity, crypsis, aposematism, etc., the conditional information indices considered as proxy to plant and herbivore fitness may be only secondarily related to arms race. This is an interesting observation, which suggests that VOC production may have more than one ecological function, as it often happens in “pleiotropic” traits (Strauss, Irwin 2004). This is an exciting avenue for future research. Finally, a third category of comments involves the relationship between conditional information entropy and plant and herbivore fitness. Bass & Kessler developed a Bayesian treatment of the community-level information developed by Zu et al. (2020) that permitted to estimate fitness on a species rather than community level. Their results revealed that community conditional entropies fail to align with species-level indices, suggesting that conclusions of Strauss & Irwin (2004) are not commensurate with fitness at the species level, where the analysis seems to be pertinent. In general, I strongly recommend Bass & Kessler’s contribution as it provides a series of observations and new perspectives to Zu et al. (2020). Rather than restricting their manuscript to blind criticisms, Bass & Kessler provides new interesting perspectives, which is always welcome as it improves the value and scope of the original work.

References

Bascompte J, Jordano P (2013) Mutualistic Networks. Princeton University Press. https://doi.org/10.23943/princeton/9780691131269.001.0001

Bass E, Kessler A (2022) Comment on “Information arms race explains plant-herbivore chemical communication in ecological communities.” EcoEvoRxiv, ver. 8 peer-reviewed and recommended by Peer Community in Ecology.  https://doi.org/10.32942/osf.io/xsbtm

Goodnight CJ (1990) Experimental Studies of Community Evolution I: The Response to Selection at the Community Level. Evolution, 44, 1614–1624. https://doi.org/10.1111/j.1558-5646.1990.tb03850.x

Schaefer HM, Ruxton GD (2011) Plant-Animal Communication. Oxford University Press, Oxford. https://doi.org/10.1093/acprof:osobl/9780199563609.001.0001

Strauss SY, Irwin RE (2004) Ecological and Evolutionary Consequences of Multispecies Plant-Animal Interactions. Annual Review of Ecology, Evolution, and Systematics, 35, 435–466. https://doi.org/10.1146/annurev.ecolsys.35.112202.130215

Williams GC (1992) Natural Selection: Domains, Levels, and Challenges. Oxford University Press, Oxford, New York.

Zu P, Boege K, del-Val E, Schuman MC, Stevenson PC, Zaldivar-Riverón A, Saavedra S (2020) Information arms race explains plant-herbivore chemical communication in ecological communities. Science, 368, 1377–1381. https://doi.org/10.1126/science.aba2965

Comment on “Information arms race explains plant-herbivore chemical communication in ecological communities”Ethan Bass, André Kessler<p style="text-align: justify;">Zu et al (Science, 19 Jun 2020, p. 1377) propose that an ‘information arms-race’ between plants and herbivores explains plant-herbivore communication at the community level. However, the analysis presented here show...Chemical ecology, Community ecology, Eco-evolutionary dynamics, Evolutionary ecology, Herbivory, Interaction networks, Theoretical ecologyRodrigo Medel2021-10-02 06:06:07 View