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03 Feb 2023
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The role of climate change and niche shifts in divergent range dynamics of a sister-species pair

Drivers of range expansion in a pair of sister grackle species

Recommended by based on reviews by 2 anonymous reviewers

The spatial distribution of a species is driven by both biotic and abiotic factors that may change over time (Soberón & Nakamura, 2009; Paquette & Hargreaves, 2021).  Therefore, species ranges are dynamic, especially in humanized landscapes where changes occur at high speeds (Sirén & Morelli, 2020). The distribution of many species is being reduced because of human impacts; however, some species are expanding their distributions, even over their niche (Lustenhouwer & Parker, 2022). One of the factors that may lead to a geographic niche expansion is behavioral flexibility (Mikhalevich et al., 2017), but the mechanisms determining range expansion through behavioral changes are not fully understood. 

The PCI Ecology study by Summers et al. (2023) uses a very large database on the current and historic distribution of two species of grackles that have shown different trends in their distribution. The great-tailed grackle has largely expanded its range over the 20th century, while the range of the boat-tailed grackle has remained very similar. They take advantage of this differential response in the distribution of the two species and run several analyses to test whether it was a change in habitat availability, in the realized niche, in habitat connectivity or in in the other traits or conditions that previously limited the species range, what is driving the observed distribution of the species. The study finds a change in the niche of great-tailed grackle, consistent with the high behavioral flexibility of the species.

The two reviewers and I have seen a lot of value in this study because 1) it addresses a very timely question, especially in the current changing world; 2) it is a first step to better understanding if behavioral attributes may affect species’ ability to change their niche; 3) it contrasts the results using several complementary statistical analyses, reinforcing their conclusions; 4) it is based on the preregistration Logan et al (2021), and any deviations from it are carefully explained and justified in the text and 5) the limitations of the study have been carefully discussed. It remains to know if the boat-tailed grackle has more limited behavioral flexibility than the great-tailed grackle, further confirming the results of this study.

Logan CJ, McCune KB, Chen N, Lukas D (2021) Implementing a rapid geographic range expansion - the role of behavior and habitat changes.

Lustenhouwer N, Parker IM (2022) Beyond tracking climate: Niche shifts during native range expansion and their implications for novel invasions. Journal of Biogeography, 49, 1481–1493.

Mikhalevich I, Powell R, Logan C (2017) Is behavioural flexibility evidence of cognitive complexity? How evolution can inform comparative cognition. Interface Focus, 7, 20160121.

Paquette A, Hargreaves AL (2021) Biotic interactions are more often important at species’ warm versus cool range edges. Ecology Letters, 24, 2427–2438.

Sirén APK, Morelli TL (2020) Interactive range-limit theory (iRLT): An extension for predicting range shifts. Journal of Animal Ecology, 89, 940–954.

Soberón J, Nakamura M (2009) Niches and distributional areas: Concepts, methods, and assumptions. Proceedings of the National Academy of Sciences, 106, 19644–19650.

Summers JT, Lukas D, Logan CJ, Chen N (2022) The role of climate change and niche shifts in divergent range dynamics of a sister-species pair. EcoEvoRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Ecology.

The role of climate change and niche shifts in divergent range dynamics of a sister-species pairJeremy Summers, Dieter Lukas, Corina J. Logan, Nancy Chen<p>---This is a POST-STUDY manuscript for the PREREGISTRATION, which received in principle acceptance in 2020 from Dr. Sebastián González (reviewed by Caroline Nieberding, Tim Parker, and Pizza Ka Yee Chow; <a href=" & Ethology, Biogeography, Dispersal & Migration, Human impact, Landscape ecology, Preregistrations, Species distributionsEsther Sebastián González2022-05-26 20:07:33 View
20 Sep 2018
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When higher carrying capacities lead to faster propagation

When the dispersal of the many outruns the dispersal of the few

Recommended by ORCID_LOGO based on reviews by Yuval Zelnik and 1 anonymous reviewer

Are biological invasions driven by a few pioneers, running ahead of their conspecifics? Or are these pioneers constantly being caught up by, and folded into, the larger flux of propagules from the established populations behind them?
In ecology and beyond, these two scenarios are known as "pulled" and "pushed" fronts, and they come with different expectations. In a pushed front, invasion speed is not just a matter of how good individuals are at dispersing and settling new locations. It becomes a collective, density-dependent property of population fluxes. And in particular, it can depend on the equilibrium abundance of the established populations inside the range, i.e. the species’ carrying capacity K, factoring in its abiotic environment and biotic interactions.
This realization is especially important because it can flip around our expectations about which species expand fast, and how to manage them. We tend to think of initial colonization and long-term abundance as two independent axes of variation among species or indeed as two ends of a spectrum, in the classic competition-colonization tradeoff [1]. When both play into invasion speed, good dispersers might not outrun good competitors. This is useful knowledge, whether we want to contain an invasion or secure a reintroduction.
In their study "When higher carrying capacities lead to faster propagation", Haond et al [2] combine mathematical analysis, Individual-Based simulations and experiments to show that various mechanisms can cause pushed fronts, whose speed increases with the carrying capacity K of the species. Rather than focus on one particular angle, the authors endeavor to demonstrate that this qualitative effect appears again and again in a variety of settings.
It is perhaps surprising that this notable and general connection between K and invasion speed has managed to garner so little fame in ecology. A large fraction of the literature employs the venerable Fisher-KPP reaction-diffusion model, which combines local logistic growth with linear diffusion in space. This model has prompted both considerable mathematical developments [3] and many applications to modelling real invasions [4]. But it only allows pulled fronts, driven by the small populations at the edge of a species range, with a speed that depends only on their initial growth rate r.
This classic setup is, however, singular in many ways. Haond et al [2] use it as a null model, and introduce three mechanisms or factors that each ensure a role of K in invasion speed, while giving less importance to the pioneers at the border.
Two factors, the Allee effect and demographic stochasticity, make small edge populations slower to grow or less likely to survive. These two factors are studied theoretically, and to make their claims stronger, the authors stack the deck against K. When generalizing equations or simulations beyond the null case, it is easy to obtain functional forms where the parameter K does not only play the role of equilibrium carrying capacity, but also affects dynamical properties such as the maximum or mean growth rate. In that case, it can trivially change the propagation speed, without it meaning anything about the role of established populations behind the front. Haond et al [2] avoid this pitfall by disentangling these effects, at the cost of slightly more peculiar expressions, and show that varying essentially nothing but the carrying capacity can still impact the speed of the invasion front.
The third factor, density-dependent dispersal, makes small populations less prone to disperse. It is well established empirically and theoretically that various biological mechanisms, from collective organization to behavioral switches, can prompt organisms in denser populations to disperse more, e.g. in such a way as to escape competition [5]. The authors demonstrate how this effect induces a link between carrying capacity and invasion speed, both theoretically and in a dispersal experiment on the parasitoid wasp, Trichogramma chilonis.
Overall, this study carries a simple and clear message, supported by valuable contributions from different angles. Although some sections are clearly written for the theoretical ecology crowd, this article has something for everyone, from the stray physicist to the open-minded manager. The collaboration between theoreticians and experimentalists, while not central, is worthy of note. Because the narrative of this study is the variety of mechanisms that can lead to the same qualitative effect, the inclusion of various approaches is not a gimmick, but helps drive home its main message. The work is fairly self-contained, although one could always wish for further developments, especially in the direction of more quantitative testing of these mechanisms.
In conclusion, Haond et al [2] effectively convey the widely relevant message that, for some species, invading is not just about the destination, it is about the many offspring one makes along the way.


[1] Levins, R., & Culver, D. (1971). Regional Coexistence of Species and Competition between Rare Species. Proceedings of the National Academy of Sciences, 68(6), 1246–1248. doi: 10.1073/pnas.68.6.1246
[2] Haond, M., Morel-Journel, T., Lombaert, E., Vercken, E., Mailleret, L., & Roques, L. (2018). When higher carrying capacities lead to faster propagation. BioRxiv, 307322. doi: 10.1101/307322
[3] Crooks, E. C. M., Dancer, E. N., Hilhorst, D., Mimura, M., & Ninomiya, H. (2004). Spatial segregation limit of a competition-diffusion system with Dirichlet boundary conditions. Nonlinear Analysis: Real World Applications, 5(4), 645–665. doi: 10.1016/j.nonrwa.2004.01.004
[4] Shigesada, N., & Kawasaki, K. (1997). Biological Invasions: Theory and Practice. Oxford University Press, UK.
[5] Matthysen, E. (2005). Density-dependent dispersal in birds and mammals. Ecography, 28(3), 403–416. doi: 10.1111/j.0906-7590.2005.04073.x

When higher carrying capacities lead to faster propagationMarjorie Haond, Thibaut Morel-Journel, Eric Lombaert, Elodie Vercken, Ludovic Mailleret & Lionel Roques<p>This preprint has been reviewed and recommended by Peer Community In Ecology ( Finding general patterns in the expansion of natural populations is a major challenge in ecology and invasion biology...Biological invasions, Colonization, Dispersal & Migration, Experimental ecology, Population ecology, Spatial ecology, Metacommunities & Metapopulations, Theoretical ecologyMatthieu Barbier Yuval Zelnik2018-04-25 10:18:48 View
23 Mar 2020
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Intraspecific difference among herbivore lineages and their host-plant specialization drive the strength of trophic cascades

Tell me what you’ve eaten, I’ll tell you how much you’ll eat (and be eaten)

Recommended by and based on reviews by Bastien Castagneyrol and 1 anonymous reviewer

Tritrophic interactions have a central role in ecological theory and applications [1-3]. Particularly, systems comprised of plants, herbivores and predators have historically received wide attention given their ubiquity and economic importance [4]. Although ecologists have long aimed to understand the forces that govern alternating ecological effects at successive trophic levels [5], several key open questions remain (at least partially) unanswered [6]. In particular, the analysis of complex food webs has questioned whether ecosystems can be viewed as a series of trophic chains [7,8]. Moreover, whether systems are mostly controlled by top-down (trophic cascades) or bottom-up processes remains an open question [6].
Traditionally, studies have addressed how species diversity at different food chain compartments affect the strength and direction of trophic cascades [9]. For example, many studies have tested whether biological control was more efficient with more than one species of natural enemies [10-12]. Much less attention has been given to the role of within-species variation in shaping trophic cascades [13]. In particular, whereas the impact of trait variation within species of plants or predators on successive trophic levels has been recently addressed [14,15], the impact of intraspecific herbivore variation is in its infancy (but see [16]). This is at odds with the resurgent acknowledgment of the importance of individual variation for several ecological processes operating at higher levels of biological organization [17].
Sources of variation within species can come in many flavours. In herbivores, striking ecological variation can be found among populations occurring on different host plants, which become genetically differentiated, thus forming host races [18,19]. Curiously, the impact of variation across host races on the strength of trophic cascades has, to date, not been explored. This is the gap that the manuscript by Sentis and colleagues [20] fills. They experimentally studied a curious tri-trophic system where the primary consumer, pea aphids, specializes in different plant hosts, creating intraspecific variation across biotypes. Interestingly, there is also ecological variation across lineages from the same biotype. The authors set up experimental food chains, where pea aphids from different lineages and biotypes were placed in their universal legume host (broad bean plants) and then exposed to a voracious but charming predator, ladybugs. The full factorial design of this experiment allowed the authors to measure vertical effects of intraspecific variation in herbivores on both plant productivity (top-down) and predator individual growth (bottom-up).
The results nicely uncover the mechanisms by which intraspecific differences in herbivores precipitates vertical modulation in food chains. Herbivore lineage and host-plant specialization shaped the strength of trophic cascades, but curiously these effects were not modulated by density-dependence. Further, ladybugs consuming pea aphids from different lineages and biotypes grew at distinct rates, revealing bottom-up effects of intraspecific variation in herbivores.
These findings are novel and exciting for several reasons. First, they show how intraspecific variation in intermediate food chain compartments can simultaneously reverberate both top-down and bottom-up effects. Second, they bring an evolutionary facet to the understanding of trophic cascades, providing valuable insights on how genetically differentiated populations play particular ecological roles in food webs. Finally, Sentis and colleagues’ findings [20] have critical implications well beyond their study systems. From an applied perspective, they provide an evident instance on how consumers’ evolutionary specialization matters for their role in ecosystems processes (e.g. plant biomass production, predator conversion rate), which has key consequences for biological control initiatives and invasive species management. From a conceptual standpoint, their results ignite the still neglected value of intraspecific variation (driven by evolution) in modulating the functioning of food webs, which is a promising avenue for future theoretical and empirical studies.


[1] Price, P. W., Bouton, C. E., Gross, P., McPheron, B. A., Thompson, J. N., & Weis, A. E. (1980). Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual review of Ecology and Systematics, 11(1), 41-65. doi: 10.1146/
[2] Olff, H., Brown, V.K. & Drent, R.H. (1999). Herbivores: between plants and predators. Blackwell Science, Oxford.
[3] Tscharntke, T. & Hawkins, B.A. (2002). Multitrophic level interactions. Cambridge University Press. doi: 10.1017/CBO9780511542190
[4] Agrawal, A. A. (2000). Mechanisms, ecological consequences and agricultural implications of tri-trophic interactions. Current opinion in plant biology, 3(4), 329-335. doi: 10.1016/S1369-5266(00)00089-3
[5] Pace, M. L., Cole, J. J., Carpenter, S. R., & Kitchell, J. F. (1999). Trophic cascades revealed in diverse ecosystems. Trends in ecology & evolution, 14(12), 483-488. doi: 10.1016/S0169-5347(99)01723-1
[6] Abdala‐Roberts, L., Puentes, A., Finke, D. L., Marquis, R. J., Montserrat, M., Poelman, E. H., ... & Mooney, K. (2019). Tri‐trophic interactions: bridging species, communities and ecosystems. Ecology letters, 22(12), 2151-2167. doi: 10.1111/ele.13392
[7] Polis, G.A. & Winemiller, K.O. (1996). Food webs. Integration of patterns and dynamics. Chapmann & Hall, New York. doi: 10.1007/978-1-4615-7007-3
[8] Torres‐Campos, I., Magalhães, S., Moya‐Laraño, J., & Montserrat, M. (2020). The return of the trophic chain: Fundamental vs. realized interactions in a simple arthropod food web. Functional Ecology, 34(2), 521-533. doi: 10.1111/1365-2435.13470
[9] Polis, G. A., Sears, A. L., Huxel, G. R., Strong, D. R., & Maron, J. (2000). When is a trophic cascade a trophic cascade?. Trends in Ecology & Evolution, 15(11), 473-475. doi: 10.1016/S0169-5347(00)01971-6
[10] Sih, A., Englund, G., & Wooster, D. (1998). Emergent impacts of multiple predators on prey. Trends in ecology & evolution, 13(9), 350-355. doi: 10.1016/S0169-5347(98)01437-2
[11] Diehl, E., Sereda, E., Wolters, V., & Birkhofer, K. (2013). Effects of predator specialization, host plant and climate on biological control of aphids by natural enemies: a meta‐analysis. Journal of Applied Ecology, 50(1), 262-270. doi: 10.1111/1365-2664.12032
[12] Snyder, W. E. (2019). Give predators a complement: conserving natural enemy biodiversity to improve biocontrol. Biological control, 135, 73-82. doi: 10.1016/j.biocontrol.2019.04.017
[13] Des Roches, S., Post, D. M., Turley, N. E., Bailey, J. K., Hendry, A. P., Kinnison, M. T., ... & Palkovacs, E. P. (2018). The ecological importance of intraspecific variation. Nature Ecology & Evolution, 2(1), 57-64. doi: 10.1038/s41559-017-0402-5
[14] Bustos‐Segura, C., Poelman, E. H., Reichelt, M., Gershenzon, J., & Gols, R. (2017). Intraspecific chemical diversity among neighbouring plants correlates positively with plant size and herbivore load but negatively with herbivore damage. Ecology Letters, 20(1), 87-97. doi: 10.1111/ele.12713
[15] Start, D., & Gilbert, B. (2017). Predator personality structures prey communities and trophic cascades. Ecology letters, 20(3), 366-374. doi: 10.1111/ele.12735
[16] Turcotte, M. M., Reznick, D. N., & Daniel Hare, J. (2013). Experimental test of an eco-evolutionary dynamic feedback loop between evolution and population density in the green peach aphid. The American Naturalist, 181(S1), S46-S57. doi: 10.1086/668078
[17] Bolnick, D. I., Amarasekare, P., Araújo, M. S., Bürger, R., Levine, J. M., Novak, M., ... & Vasseur, D. A. (2011). Why intraspecific trait variation matters in community ecology. Trends in ecology & evolution, 26(4), 183-192. doi: 10.1016/j.tree.2011.01.009
[18] Drès, M., & Mallet, J. (2002). Host races in plant–feeding insects and their importance in sympatric speciation. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 357(1420), 471-492. doi: 10.1098/rstb.2002.1059
[19] Magalhães, S., Forbes, M. R., Skoracka, A., Osakabe, M., Chevillon, C., & McCoy, K. D. (2007). Host race formation in the Acari. Experimental and Applied Acarology, 42(4), 225-238. doi: 10.1007/s10493-007-9091-0
[20] Sentis, A., Bertram, R., Dardenne, N., Simon, J.-C., Magro, A., Pujol, B., Danchin, E. and J.-L. Hemptinne (2020) Intraspecific difference among herbivore lineages and their host-plant specialization drive the strength of trophic cascades. bioRxiv, 722140, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/722140

Intraspecific difference among herbivore lineages and their host-plant specialization drive the strength of trophic cascadesArnaud Sentis, Raphaël Bertram, Nathalie Dardenne, Jean-Christophe Simon, Alexandra Magro, Benoit Pujol, Etienne Danchin and Jean-Louis Hemptinne<p>Trophic cascades, the indirect effect of predators on non-adjacent lower trophic levels, are important drivers of the structure and dynamics of ecological communities. However, the influence of intraspecific trait variation on the strength of t...Community ecology, Eco-evolutionary dynamics, Food webs, Population ecologySara Magalhães2019-08-02 09:11:03 View
21 Oct 2020
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Why scaling up uncertain predictions to higher levels of organisation will underestimate change

Uncertain predictions of species responses to perturbations lead to underestimate changes at ecosystem level in diverse systems

Recommended by based on reviews by Carlos Melian and 1 anonymous reviewer

Different sources of uncertainty are known to affect our ability to predict ecological dynamics (Petchey et al. 2015). However, the consequences of uncertainty on prediction biases have been less investigated, especially when predictions are scaled up to higher levels of organisation as is commonly done in ecology for instance. The study of Orr et al. (2020) addresses this issue. It shows that, in complex systems, the uncertainty of unbiased predictions at a lower level of organisation (e.g. species level) leads to a bias towards underestimation of change at higher level of organisation (e.g. ecosystem level). This bias is strengthened by larger uncertainty and by higher dimensionality of the system.
This general result has large implications for many fields of science, from economics to energy supply or demography. In ecology, as discussed in this study, these results imply that the uncertainty of predictions of species’ change increases the probability of underestimation of changes of diversity and stability at community and ecosystem levels, especially when species richness is high. The uncertainty of predictions of species’ change also increases the probability of underestimation of change when multiple ecosystem functions are considered at once, or when the combined effect of multiple stressors is considered.
The consequences of species diversity on ecosystem functions and stability have received considerable attention during the last decades (e.g. Cardinale et al. 2012, Kéfi et al. 2019). However, since the bias towards underestimation of change increases with species diversity, future studies will need to investigate how the general statistical effect outlined by Orr et al. might affect our understanding of the well-known relationships between species diversity and ecosystem functioning and stability in response to perturbations.


Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S (2012) Biodiversity loss and its impact on humanity. Nature, 486, 59–67.
Kéfi S, Domínguez‐García V, Donohue I, Fontaine C, Thébault E, Dakos V (2019) Advancing our understanding of ecological stability. Ecology Letters, 22, 1349–1356.
Orr JA, Piggott JJ, Jackson A, Arnoldi J-F (2020) Why scaling up uncertain predictions to higher levels of organisation will underestimate change. bioRxiv, 2020.05.26.117200.
Petchey OL, Pontarp M, Massie TM, Kéfi S, Ozgul A, Weilenmann M, Palamara GM, Altermatt F, Matthews B, Levine JM, Childs DZ, McGill BJ, Schaepman ME, Schmid B, Spaak P, Beckerman AP, Pennekamp F, Pearse IS (2015) The ecological forecast horizon, and examples of its uses and determinants. Ecology Letters, 18, 597–611.

Why scaling up uncertain predictions to higher levels of organisation will underestimate changeJames Orr, Jeremy Piggott, Andrew Jackson, Jean-François Arnoldi<p>Uncertainty is an irreducible part of predictive science, causing us to over- or underestimate the magnitude of change that a system of interest will face. In a reductionist approach, we may use predictions at the level of individual system com...Community ecology, Ecosystem functioning, Theoretical ecologyElisa ThebaultAnonymous2020-06-02 15:41:12 View
19 Dec 2020
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Hough transform implementation to evaluate the morphological variability of the moon jellyfish (Aurelia spp.)

A new member of the morphometrics jungle to better monitor vulnerable lagoons

Recommended by based on reviews by Julien Claude and 1 anonymous reviewer

In the recent years, morphometrics, the quantitative description of shape and its covariation [1] gained considerable momentum in evolutionary ecology. Using the form of organisms to describe, classify and try to understand their diversity can be traced back at least to Aristotle. More recently, two successive revolutions rejuvenated this idea [1–3]: first, a proper mathematical refoundation of the theory of shape, then a technical revolution in the apparatus able to acquire raw data. By using a feature extraction method and planning its massive use on data acquired by aerial drones, the study by Lacaux and colleagues [4] retraces this curse of events.
The radial symmetry of Aurelia spp. jelly fish, a common species complex, is affected by stress and more largely by environmental variations, such as pollution exposition. Aurelia spp. normally present four gonads so that the proportion of non-tetramerous individuals in a population has been proposed as a biomarker [5,6].
In this study, the authors implemented the Hough transform to largely automate the detection of the gonads in Aurelia spp. Such use of the Hough transform, a long-used approach to identify shapes through edge detection, is new to morphometrics. Here, the Aurelia spp. gonads are identified as ellipses from which aspect descriptors can be derived, and primarily counted and thus can be used to quantify the proportion of individuals presenting body plans disorders.

The sample sizes studied here were too low to allow finer-grained ecophysiological investigations. That being said, the proof-of-concept is convincing and this paper paths the way for an operational and innovative approach to the ecological monitoring of sensible aquatic ecosystems.


[1] Kendall, D. G. (1989). A survey of the statistical theory of shape. Statistical Science, 87-99. doi:
[2] Rohlf, F. J., and Marcus, L. F. (1993). A revolution morphometrics. Trends in ecology & evolution, 8(4), 129-132. doi:
[3] Adams, D. C., Rohlf, F. J., and Slice, D. E. (2004). Geometric morphometrics: ten years of progress following the ‘revolution’. Italian Journal of Zoology, 71(1), 5-16. doi:
[4] Lacaux, C., Desolneux, A., Gadreaud, J., Martin-Garin, B. and Thiéry, A. (2020) Hough transform implementation to evaluate the morphological variability of the moon jellyfish (Aurelia spp.). bioRxiv, 2020.03.11.986984, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. doi:
[5] Gershwin, L. A. (1999). Clonal and population variation in jellyfish symmetry. Journal of the Marine Biological Association of the United Kingdom, 79(6), 993-1000. doi:
[6] Gadreaud, J., Martin-Garin, B., Artells, E., Levard, C., Auffan, M., Barkate, A.-L. and Thiéry, A. (2017) The moon jellyfish as a new bioindicator: impact of silver nanoparticles on the morphogenesis. In: Mariottini GL, editor. Jellyfish: ecology, distribution patterns and human interactions. Nova Science Publishers; 2017. pp. 277–292.

Hough transform implementation to evaluate the morphological variability of the moon jellyfish (Aurelia spp.)Céline Lacaux, Agnès Desolneux, Justine Gadreaud, Bertrand Martin-Garin and Alain Thiéry<p>Variations of the animal body plan morphology and morphometry can be used as prognostic tools of their habitat quality. The potential of the moon jellyfish (Aurelia spp.) as a new model organism has been poorly tested. However, as a tetramerous...MorphometricsVincent Bonhomme2020-03-18 17:40:51 View
28 Dec 2022
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Deleterious effects of thermal and water stresses on life history and physiology: a case study on woodlouse

An experimental approach for understanding how terrestrial isopods respond to environmental stressors

Recommended by based on reviews by Aaron Yilmaz and Michael Morris

​​In this article, the authors discuss the results of their study investigating the effects of heat stress and moisture stress on a terrestrial isopod Armadilldium vulgare, the common woodlouse [1]. Specifically, the authors have assessed how increased temperature or decreased moisture affects life history traits (such as growth, survival, and reproduction) as well as physiological traits (immune cell parameters and \( beta \)-galactosidase activity). This article quantitatively evaluates the effects of the two stressors on woodlouse. Terrestrial isopods like woodlouse are sensitive to thermal and moisture stress [2; 3] and are therefore good models to test hypotheses in global change biology and for monitoring ecosystem health.

​An important feature of this study is the combination of experimental, laboratory, and analytical techniques. Experiments were conducted under controlled conditions in the laboratory by modulating temperature and moisture, life history and physiological traits were measured/analyzed and then tested using models. Both stressors had negative impacts on survival and reproduction of woodlouse, and result in premature ageing. Although thermal stress did not affect survival, it slowed woodlouse growth. Moisture stress did not have a detectable effect on woodlouse growth but decreased survival and reproductive success. An important insight from this study is that effects of heat and moisture stressors on woodlouse are not necessarily linear, and experimental approaches can be used to better elucidate the mechanisms and understand how these organisms respond to environmental stress.

​This article is timely given the increasing attention on biological monitoring and ecosystem health.​


[1] Depeux C, Branger A, Moulignier T, Moreau J, Lemaître J-F, Dechaume-Moncharmont F-X, Laverre T, Pauhlac H, Gaillard J-M, Beltran-Bech S (2022) Deleterious effects of thermal and water stresses on life history and physiology: a case study on woodlouse. bioRxiv, 2022.09.26.509512., ver. 3 peer-reviewd and recommended by PCI Ecology.

[2] ​Warburg MR, Linsenmair KE, Bercovitz K (1984) The effect of climate on the distribution and abundance of isopods. In: Sutton SL, Holdich DM, editors. The Biology of Terrestrial Isopods. Oxford: Clarendon Press. pp. 339–367.​

[3] Hassall M, Helden A, Goldson A, Grant A (2005) Ecotypic differentiation and phenotypic plasticity in reproductive traits of Armadillidium vulgare (Isopoda: Oniscidea). Oecologia 143: 51–60.​

Deleterious effects of thermal and water stresses on life history and physiology: a case study on woodlouseCharlotte Depeux, Angele Branger, Theo Moulignier, Jérôme Moreau, Jean-Francois Lemaitre, Francois-Xavier Dechaume-Moncharmont, Tiffany Laverre, Hélène Paulhac, Jean-Michel Gaillard, Sophie Beltran-Bech<p>We tested independently the influences of increasing temperature and decreasing moisture on life history and physiological traits in the arthropod <em>Armadillidium vulgare</em>. Both increasing temperature and decreasing moisture led individua...Biodiversity, Evolutionary ecology, Experimental ecology, Life history, Physiology, Terrestrial ecology, ZoologyAniruddha Belsare2022-09-28 13:13:47 View
22 May 2019
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Sex makes them sleepy: host reproductive status induces diapause in a parasitoid population experiencing harsh winters

The response of interacting species to biotic seasonal cues

Recommended by and based on reviews by Anne Duplouy and 1 anonymous reviewer

In temperate regions, food abundance and quality vary greatly throughout the year, and the ability of organisms to synchronise their phenology to these changes is a key determinant of their reproductive success. Successful synchronisation requires that cues are perceived prior to change, leaving time for physiological adjustments.
But what are the cues used to anticipate seasonal changes? Abiotic factors like temperature and photoperiod are known for their driving role in the phenology of a wide range of plant an animal species [1,2] . Arguably though, biotic cues directly linked to upcoming changes in food abundance could be as important as abiotic factors, but the response of organisms to these cues remains relatively unexplored.
Biotic cues may be particularly important for higher trophic levels because of their tight interaction with the hosts or preys they depend on. In this study Tougeron and colleagues [3] address this topic using interacting insects, namely herbivorous aphids and the parasitic wasps (or parasitoids) that feed on them. The key finding of the study by Tougeron et al. [3] is that the host morph in which parasitic wasp larvae develop is a major driver of diapause induction. More importantly, the aphid morph that triggers diapause in the wasp is the one that will lay overwintering eggs in autumn at the onset of harsh winter conditions. Its neatly designed experimental setup also provides evidence that this response may vary across populations as host-dependent diapause induction was only observed in a wasp population that originated from a cold area. As the authors suggests, this may be caused by local adaptation to environmental conditions because, relative to warmer regions, missing the time window to enter diapause in colder regions may have more dramatic consequences. The study also shows that different aphid morphs differ greatly in their chemical composition, and points to particular types of metabolites like sugars and polyols as specific cues for diapause induction.
This study provides a nice example of the complexity of biological interactions, and of the importance of phenological synchrony between parasites and their hosts. The authors provide evidence that phenological synchrony is likely to be achieved via chemical cues derived from the host. A similar approach was used to demonstrate that the herbivorous beetle Leptinotarsa decemlineata uses plant chemical cues to enter diapause [4]. Beetles fed on plants exposed to pre-wintering conditions entered diapause in higher proportions than those fed on control plants grown at normal conditions. As done by Tougeron et al. [3], in [4] the authors associated diapause induction to changes in the composition of metabolites in the plant. In both studies, however, the missing piece is to unveil the particular chemical involved, an answer that may be provided by future experiments.
Latitudinal clines in diapause induction have been described in a number of insect species [5]. Correlative studies, in which the phenology of different trophic levels has been monitored, suggest that these clines may in part be governed by lower trophic levels. For example, Phillimore et al. [6] explored the relative contribution of temperature and of host plant phenology on adult flight periods of the butterfly Anthocharis cardamines. Tougeron et al. [3], by using aphids and their associated parasitoids, take the field further by moving from observational studies to experiments. Besides, aphids are not only a tractable host-parasite system in the laboratory, they are important agricultural pests. Improving our basic knowledge of their ecological interactions may ultimately contribute to improving pest control techniques. The study by Tougeron et al. [3] exemplifies the multiple benefits that can be gained from addressing fundamental questions in species that are also directly relevant to society.


[1] Tauber, M. J., Tauber, C. A., and Masaki, S. (1986). Seasonal Adaptations of Insects. Oxford, New York: Oxford University Press.
[2] Bradshaw, W. E., and Holzapfel, C. M. (2007). Evolution of Animal Photoperiodism. Annual Review of Ecology, Evolution, and Systematics, 38(1), 1–25. doi: 10.1146/annurev.ecolsys.37.091305.110115
[3] Tougeron, K., Brodeur, J., Baaren, J. van, Renault, D., and Lann, C. L. (2019b). Sex makes them sleepy: host reproductive status induces diapause in a parasitoid population experiencing harsh winters. bioRxiv, 371385, ver. 6 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/371385
[4] Izzo, V. M., Armstrong, J., Hawthorne, D., and Chen, Y. (2014). Time of the season: the effect of host photoperiodism on diapause induction in an insect herbivore, Leptinotarsa decemlineata. Ecological Entomology, 39(1), 75–82. doi: 10.1111/een.12066
[5] Hut Roelof A., Paolucci Silvia, Dor Roi, Kyriacou Charalambos P., and Daan Serge. (2013). Latitudinal clines: an evolutionary view on biological rhythms. Proceedings of the Royal Society B: Biological Sciences, 280(1765), 20130433. doi: 10.1098/rspb.2013.0433
[6] Phillimore, A. B., Stålhandske, S., Smithers, R. J., and Bernard, R. (2012). Dissecting the Contributions of Plasticity and Local Adaptation to the Phenology of a Butterfly and Its Host Plants. The American Naturalist, 180(5), 655–670. doi: 10.1086/667893

Sex makes them sleepy: host reproductive status induces diapause in a parasitoid population experiencing harsh wintersTougeron K., Brodeur J., van Baaren J., Renault D. and Le Lann C.<p>When organisms coevolve, any change in one species can induce phenotypic changes in traits and ecology of the other species. The role such interactions play in ecosystems is central, but their mechanistic bases remain underexplored. Upper troph...Coexistence, Evolutionary ecology, Experimental ecology, Host-parasite interactions, PhysiologyAdele Mennerat2018-07-18 18:51:03 View
21 Feb 2019
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Photosynthesis of Laminaria digitata during the immersion and emersion periods of spring tidal cycles during hot, sunny weather

Evaluating physiological responses of a kelp to environmental changes at its vulnerable equatorward range limit

Recommended by based on reviews by 2 anonymous reviewers

Understanding processes at species’ range limits is of paramount importance in an era of global change. For example, the boreal kelp Laminaria digitata, which dominates low intertidal and shallow subtidal rocky reefs in northwestern Europe, is declining in the equatorward portion of its range [1]. In this contribution, Migné and colleagues [2] focus on L. digitata near its southern range limit on the coast of France and use a variety of techniques to paint a complete picture of the physiological responses of the kelp to environmental changes. Importantly, and in contrast to earlier work on the species which focused on subtidal individuals (e.g. [3]), Migné et al. [2] describe responses not only in the most physiologically stressful portion of the species’ range but also in the most stressful portion of its local environment: the upper portion of its zone on the shoreline, where it is periodically exposed to aerial conditions and associated thermal and desiccation stresses.
The authors show that whereas L. digitata possesses mechanisms to protect it from irradiance stress at low tide, these mechanisms are not sufficient to prevent damage to photosynthetic pathways (e.g., reduction in optimal quantum yields of photosystem II). This species experiences severe heat stress associated with mid-day low tides during the summer, and the cumulative damage associated with these stresses is likely associated with the range contraction that is currently underway. Given the important role that L. digitata plays as food and habitat for other organisms, its loss will have cascading impacts on community structure and ecosystem functioning. Understanding the mechanisms underlying these declines is essential to understanding the impacts of climate change on species, communities, and ecosystems.


[1] Raybaud, V., Beaugrand, G., Goberville, E., Delebecq, G., Destombe, C., Valero, M., Davoult, D., Morin, P. & Gevaert, F. (2013). Decline in kelp in west Europe and climate. PloS one, 8(6), e66044. doi: 10.1371/journal.pone.0066044
[2] Delebecq, G., Davoult, D., Menu, D., Janquin, M. A., Migné, A., Dauvin, J. C., & Gevaert, F. (2011). In situ photosynthetic performance of Laminaria digitata (Phaeophyceae) during spring tides in Northern Brittany. CBM-Cahiers de Biologie Marine, 52(4), 405. doi: 10.21411/CBM.A.C9EE91F
[3] Migné, A., Delebecq, G., Davoult, D., Spilmont, N., Menu, D., Janquin, M.-A., and Gevaert, F. (2019). Photosynthesis of Laminaria digitata during the immersion and emersion periods of spring tidal cycles during hot, sunny weather. Hal, 01827565, ver. 4 peer-reviewed and recommended by PCI Ecology. hal-01827565

Photosynthesis of Laminaria digitata during the immersion and emersion periods of spring tidal cycles during hot, sunny weatherAline Migné, Gaspard Delebecq, Dominique Davoult, Nicolas Spilmont, Dominique Menu, Marie-Andrée Janquin and François GévaertThe boreal kelp Laminaria digitata dominates the low intertidal and upper subtidal zones of moderately exposed rocky shores in north-western Europe. Due to ocean warming, this foundation species is predicted to disappear from French coasts in the ...Marine ecologyMatthew Bracken2018-07-02 18:03:11 View
02 Oct 2018
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How optimal foragers should respond to habitat changes? On the consequences of habitat conversion.

Optimal foraging in a changing world: old questions, new perspectives

Recommended by ORCID_LOGO based on reviews by Frederick Adler, Andrew Higginson and 1 anonymous reviewer

Marginal value theorem (MVT) is an archetypal model discussed in every behavioural ecology textbook. Its popularity is largely explained but the fact that it is possible to solve it graphically (at least in its simplest form) with the minimal amount of equations, which is a sensible strategy for an introductory course in behavioural ecology [1]. Apart from this heuristic value, one may be tempted to disregard it as a naive toy model. After a burst of interest in the 70's and the 80's, the once vivid literature about optimal foraging theory (OFT) has lost its momentum [2]. Yet, OFT and MVT have remained an active field of research in the parasitoidologists community, mostly because the sampling strategy of a parasitoid in patches of hosts and its resulting fitness gain are straightforward to evaluate, which eases both experimental and theoretical investigations [3].
This preprint [4] is in line with the long-established literature on OFT. It follows two theoretical articles [5,6] in which Vincent Calcagno and co-authors assessed the effect of changes in the environmental conditions on optimal foraging strategy. This time, they did not modify the shape of the gain function (describing the diminishing return of the cumulative intake as a function of the residency time in a patch) but the relative frequencies of good and bad patches. At first sight, that sounds like a minor modification of their earlier models. Actually, even the authors initially were fooled by the similarities before spotting the pitfalls. Here, they genuinely point out the erroneous verbal prediction in their previous paper in which some non-trivial effects of the change in patch frequencies have been overlooked. The present study indeed provides a striking example of ecological fallacy, and more specifically of Simpson's paradox which occurs when the aggregation of subgroups modifies the apparent pattern at the scale of the entire population [7,8]. In the case of MVT under constraints of habitat conversion, the increase of the residency times in both bad and good patches can result in a decrease of the average residency time at the level of the population. This apparently counter-intuitive property can be observed, for instance, when the proportion of bad quality patches strongly increases, which increases the probability that the individual forages on theses quickly exploited patches, and thus decreases its average residency time on the long run.
The authors thus put the model on the drawing board again. Proper assessment of the effect of change in the frequency of patch quality is more mathematically challenging than when one considers only changes in the shape of the gain function. The expected gain must be evaluated at the scale of the entire habitat instead of single patch. Overall, this study, which is based on a rigorous formalism, stands out as a warning against too rapid interpretations of theoretical outputs. It is not straightforward to generalize the predictions of previous models without careful evaluating their underlying hypotheses. The devil is in the details: some slight, seemingly minor, adjustments of the assumptions may have some major consequences.
The authors discussed the general conditions leading to changes in residency times or movement rates. Yet, it is worth pointing out again that it would be a mistake to blindly consider these theoretical results as forecasts for the foragers' behaviour in natura. OFT models has for a long time been criticized for sweeping under the carpet the key questions of the evolutionary dynamics and the maintenance of the optimal strategy in a population [9,10]. The distribution of available options is susceptible to change rapidly due to modifications of the environmental conditions or, even more simply, the presence of competitors which continuously remove the best options from the pool of available options [11]. The key point here is that the constant monitoring of available options implies cognitive (neural tissue is one of the most metabolically expensive tissues) and ecological costs: assessment and adjustment to the environmental conditions requires time, energy, and occasional mistakes (cost of naiveté, [12]). While rarely considered in optimal analyses, these costs should severely constraint the evolution of the subtle decision rules. Under rapidly fluctuating conditions, it could be more profitable to maintain a sub-optimal strategy (but performing reasonably well on the long run) than paying the far from negligible costs implied by the pursuit of optimal strategies [13,14]. For instance, in the analysis presented in this preprint, it is striking how close the fitness gains of the plastic and the non-plastic forager are, particularly if one remembers that the last-mentioned cognitive and ecological costs have been neglected in these calculations.
Yet, even if one can arguably question its descriptive value, such models are worth more than a cursory glance. They still have normative value insofar that they provide upper bounds for the response to modifications of the environmental conditions. Such insights are precious to design future experiments on the question. Being able to compare experimentally measured behaviours with the extremes of the null model (stubborn non-plastic forager) and the optimal strategy (only achievable by an omniscient daemon) informs about the cognitive bias or ecological costs experienced by real life foragers. I thus consider that this model, and more generally most OFT models, are still a valuable framework which deserves further examination.


[1] Fawcett, T. W. & Higginson, A. D. 2012 Heavy use of equations impedes communication among biologists. Proc. Natl. Acad. Sci. 109, 11735–11739. doi: 10.1073/pnas.1205259109
[2] Owens, I. P. F. 2006 Where is behavioural ecology going? Trends Ecol. Evol. 21, 356–361. doi: 10.1016/j.tree.2006.03.014
[3] Louâpre, P., Fauvergue, X., van Baaren, J. & Martel, V. 2015 The male mate search: an optimal foraging issue? Curr. Opin. Insect Sci. 9, 91–95. doi: 10.1016/j.cois.2015.02.012
[4] Calcagno, V., Hamelin, F., Mailleret, L., & Grognard, F. (2018). How optimal foragers should respond to habitat changes? On the consequences of habitat conversion. bioRxiv, 273557, ver. 4 peer-reviewed and recommended by PCI Ecol. doi: 10.1101/273557
[5] Calcagno, V., Grognard, F., Hamelin, F. M., Wajnberg, É. & Mailleret, L. 2014 The functional response predicts the effect of resource distribution on the optimal movement rate of consumers. Ecol. Lett. 17, 1570–1579. doi: 10.1111/ele.12379
[6] Calcagno, V., Mailleret, L., Wajnberg, É. & Grognard, F. 2013 How optimal foragers should respond to habitat changes: a reanalysis of the Marginal Value Theorem. J. Math. Biol. 69, 1237–1265. doi: 10.1007/s00285-013-0734-y
[7] Galipaud, M., Bollache, L., Wattier, R., Dechaume-Moncharmont, F.-X. & Lagrue, C. 2015 Overestimation of the strength of size-assortative pairing in taxa with cryptic diversity: a case of Simpson's paradox. Anim. Behav. 102, 217–221. doi: 10.1016/j.anbehav.2015.01.032
[8] Kievit, R. A., Frankenhuis, W. E., Waldorp, L. J. & Borsboom, D. 2013 Simpson's paradox in psychological science: a practical guide. Front. Psychol. 4, 513. doi: 10.3389/fpsyg.2013.00513
[9] Bolduc, J.-S. & Cézilly, F. 2012 Optimality modelling in the real world. Biol. Philos. 27, 851–869. doi: 10.1007/s10539-012-9333-3
[10] Pierce, G. J. & Ollason, J. G. 1987 Eight reasons why optimal foraging theory is a complete waste of time. Oikos 49, 111–118. doi: 10.2307/3565560
[11] Dechaume-Moncharmont, F.-X., Brom, T. & Cézilly, F. 2016 Opportunity costs resulting from scramble competition within the choosy sex severely impair mate choosiness. Anim. Behav. 114, 249–260. doi: 10.1016/j.anbehav.2016.02.019
[12] Snell-Rood, E. C. 2013 An overview of the evolutionary causes and consequences of behavioural plasticity. Anim. Behav. 85, 1004–1011. doi: 10.1016/j.anbehav.2012.12.031
[13] Fawcett, T. W., Fallenstein, B., Higginson, A. D., Houston, A. I., Mallpress, D. E. W., Trimmer, P. C. & McNamara, J. M. 2014 The evolution of decision rules in complex environments. Trends Cogn. Sci. 18, 153–161. doi: 10.1016/j.tics.2013.12.012
[14] Marshall, J. A. R., Trimmer, P. C., Houston, A. I. & McNamara, J. M. 2013 On evolutionary explanations of cognitive biases. Trends Ecol. Evol. 28, 469-473. doi: 10.1016/j.tree.2013.05.013

How optimal foragers should respond to habitat changes? On the consequences of habitat conversion.Vincent Calcagno, Frederic Hamelin, Ludovic Mailleret, Frederic GrognardThe Marginal Value Theorem (MVT) provides a framework to predict how habitat modifications related to the distribution of resources over patches should impact the realized fitness of individuals and their optimal rate of movement (or patch residen...Behaviour & Ethology, Dispersal & Migration, Foraging, Landscape ecology, Spatial ecology, Metacommunities & Metapopulations, Theoretical ecologyFrancois-Xavier Dechaume-Moncharmont2018-03-05 10:42:11 View
16 Oct 2018
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Impact of group management and transfer on individual sociality in Highland cattle (Bos Taurus)

How empirical sciences may improve livestock welfare and help their management

Recommended by based on reviews by Alecia CARTER and 1 anonymous reviewer

Understanding how livestock management is a source of social stress and disturbances for cattle is an important question with potential applications for animal welfare programs and sustainable development. In their article, Sosa and colleagues [1] first propose to evaluate the effects of individual characteristics on dyadic social relationships and on the social dynamics of four groups of cattle. Using network analyses, the authors provide an interesting and complete picture of dyadic interactions among groupmates. Although shown elsewhere, the authors demonstrate that individuals that are close in age and close in rank form stronger dyadic associations than other pairs. Second, the authors take advantage of some transfers of animals between groups -for management purposes- to assess how these transfers affect the social dynamics of groupmates. Their central finding is that the identity of transferred animals is a key-point. In particular, removing offspring strongly destabilizes the social relationships of mothers while adding a bull into a group also profoundly impacts female-female social relationships, as social networks before and after transfer of these key-animals are completely different. In addition, individuals, especially the young ones, that are transferred without familiar conspecifics take more time to socialize with their new group members than individuals transferred with familiar groupmates, generating a potential source of stress. Interestingly, the authors end up their article with some thoughts on the implications of their findings for animal welfare and ethics. This study provides additional evidence that empirical science has a major role to play in providing recommendations regarding societal questions such as livestock management and animal wellbeing.


[1] Sosa, S., Pelé, M., Debergue, E., Kuntz, C., Keller, B., Robic, F., Siegwalt-Baudin, F., Richer, C., Ramos, A., & Sueur C. (2018). Impact of group management and transfer on individual sociality in Highland cattle (Bos Taurus). arXiv:1805.11553v4 [q-bio.PE] peer-reviewed and recommended by PCI Ecol.

Impact of group management and transfer on individual sociality in Highland cattle (Bos Taurus)Sebastian Sosa, Marie Pelé, Elise Debergue, Cedric Kuntz, Blandine Keller, Florian Robic, Flora Siegwalt-Baudin, Camille Richer, Amandine Ramos, Cédric SueurThe sociality of cattle facilitates the maintenance of herd cohesion and synchronisation, making these species the ideal choice for domestication as livestock for humans. However, livestock populations are not self-regulated, and farmers transfer ...Behaviour & Ethology, Social structureMarie Charpentier2018-05-30 14:05:39 View