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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.

References

[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.

References

[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.

References

[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
15 Jun 2020
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Investigating the rare behavior of male parental care in great-tailed grackles

Studying a rare behavior in a polygamous bird: male parental care in great-tailed grackles

Recommended by based on reviews by Matthieu Paquet and André C Ferreira

The Great-tailed grackle (Quiscalus mexicanus) is a polygamous bird species that is originating from Central America and rapidly expanding its geographic range toward the North, and in which females were long thought to be the sole nest builders and caretakers of the young. In their pre-registration [1], Folsom and collaborators report repeated occurrences of male parental care and develop hypotheses aiming at better understanding the occurrence and the fitness consequences of this very rarely observed male behavior. They propose to assess if male parental care correlates with the circulating levels of several relevant hormones, increases offspring survival, is a local adaptation, and is a mating strategy, in surveying three populations located in Arizona (middle of the geographic range expansion), California (northern edge of the geographic range), and in Central America (core of the range). This study is part of a 5-year bigger project.
Both reviewers and I strongly value Folsom and collaborators’ commitment to program a study, in natural field conditions, of a rare, yet likely evolutionary-important behavior, namely parental care by males of the great-tailed grackle. Yet, we all also recognized that it is a risky endeavor, and as a consequence, we wondered about the authors’ ability to reach a sufficient sample size to statistically test (all) hypotheses and predictions with enough confidence (e.g. risk of type I errors, also known as false positives).
Folsom and collaborators acknowledged these limitations in their pre-registration. (i) They made the exploratory nature of their research work clear to readers. (ii) They adapted their analysis plan in running prior power analyses and in focusing on effect sizes (estimates and confidence intervals). (iii) Last and not least, Folsom and collaborators clearly exposed a priori hypotheses, their associated predictions and alternatives, and ranked the latter based on their plausibility according to knowledge in the current and other study systems. Developing theory about male parental care behavior more generally with regard to a polygamous species that is rapidly expanding its geographic range and that is considered not to provide male parental care is without any doubt an added value to this study.
In summary, while this study will likely be insufficient to fully understand male parental care behavior of great-tailed grackles, it is much needed because it will definitely allow rejecting some predictions (e.g., if this behavior is present in all the studied populations, it would be common across range against expectation; finding only one male providing care to an unrelated offspring would lead to reject the prediction that males only care for their own offspring) and thus it will help laying the foundation of future research directions.
I strongly support the pre-registration system and thank all the contributors for producing a fruitful discussion throughout the review process, which in fine improved the clarity and logic of this pre-registration. Given the positive and encouraging reviews, the detailed and thorough answers to all comments by Folsom and collaborators, and their satisfactory and interesting revisions, I am happy to recommend this pre-registration and I look forward to seeing its outcomes.

References

[1] Folsom MA, MacPherson M, Lukas D, McCune KB, Bergeron L, Bond A, Blackwell A, Rowney C, Logan CJ. 2020. Investigating the rare behavior of male parental care in great-tailed grackles. corinalogan.com/Preregistrations/gmalecare.html In principle acceptance by PCI Ecology of the version on 15 June 2020 corinalogan/grackles/blob/master/Files/Preregistrations/gmalecare.Rmd.

Investigating the rare behavior of male parental care in great-tailed gracklesFolsom MA, MacPherson M, Lukas D, McCune KB, Bergeron L, Bond A, Blackwell A, Rowney C, Logan CJThis is a PREREGISTRATION submitted for pre-study peer review. Our planned data collection START DATE is May 2020, therefore it would be ideal if the peer review process could be completed before then. Abstract: Great-tailed grackles (Quiscalus...Behaviour & Ethology, Biological invasions, Preregistrations, ZoologyMarie-Jeanne Holveck2019-12-05 17:38:47 View
26 Mar 2019
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Is behavioral flexibility linked with exploration, but not boldness, persistence, or motor diversity?

Probing behaviors correlated with behavioral flexibility

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

Behavioral plasticity, which is a subset of phenotypic plasticity, is an important component of foraging, defense against predators, mating, and many other behaviors. More specifically, behavioral flexibility, in this study, captures how quickly individuals adapt to new circumstances. In cases where individuals disperse to new environments, which often occurs in range expansions, behavioral flexibility is likely crucial to the chance that individuals can establish in these environments. Thus, it is important to understand how best to measure behavioral flexibility and how measures of such flexibility might vary across individuals and behavioral contexts and with other measures of learning and problem solving.
In this preregistration, Logan and colleagues propose to use a long-term study of the great-tailed grackle to measure how much they can manipulate behavioral flexibility in a reversal learning task, how much behavioral flexibility in one task predicts flexibility in another task and in problem solving a new task, and how robust these patterns are within individuals and across tasks. Logan and colleagues lay out their hypotheses and predictions for each experiment in a clear and concise manner. They also are very clear about the details of their study system, such as how they determined the number of trials they use in their learning reversal experiments, and how those details have influenced their experimental design. Further, given that the preregistration uses RMarkdown and is stored on GitHub (as are other studies in the larger project), their statistical code and its history of modification are easily available. This is a crucial component of making research more reproducible, which is a recent emphasis in behavioral sciences more broadly.
Reviewers of this preregistration found the study of substantial merit. The authors have responded to the reviewers' comments and their revisions have made the preregistration much clearer and cogent. I am happy to recommend this preregistration.

Is behavioral flexibility linked with exploration, but not boldness, persistence, or motor diversity?Kelsey McCune, Carolyn Rowney, Luisa Bergeron, Corina LoganThis 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_exploration.Rmd, which is easily accessible at GitHub at https://github.com/cor...Behaviour & Ethology, Preregistrations, ZoologyJeremy Van Cleve2018-09-27 03:35:12 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
12 Oct 2019
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Investigating the use of learning mechanisms in a species that is rapidly expanding its geographic range

How would variation in environmental predictability affect the use of different learning mechanisms in a social bird?

Recommended by based on reviews by Matthew Petelle and 1 anonymous reviewer

In their pre-registered paper [1], McCune and colleagues propose a field-based study of social versus individual learning mechanisms in an avian species (great-tailed grackles) that has been expanding its geographic range. The study forms part of a longer-term project that addresses various aspects of this species’ behaviour and biology, and the experience of the team is clear from the preprint. Assessing variation in learning mechanisms in different sections of the grackles’ distribution range, the researchers will investigate how individual learning and social transmission may impact learning about novel challenges in the environment. Considering that this is a social species, the authors expect both individual learning and social transmission to occur, when groups of grackles encounter new challenges/ opportunities in the wild. This in itself is not a very unusual idea to test [2, 3], but the authors are rigorously distinguishing between imitation, emulation, local enhancement, and social enhancement. Such rigour is certainly valuable in studies of cognition in the wild.
Further, the authors predict that the contribution of individual versus social learning could vary between populations, as the core may contain fewer unfamiliar/novel stimuli than the edge, where artificial sources of water (for example) may be more common. They make an argument that the core, middle, and edge populations would experience differing levels of environmental predictability. If true, their field experiments could yield very novel results on how changes in environmental predictability affect social/individual learning in a single study species. Their data would then give unusual insights into the ecological value of individual learning and distinct forms of social learning – something that is not easy to test in wild animals. The authors consider a variety of alternative hypotheses that may ultimately explain their findings, and clarify their methods and analyses in fine detail. The authors also set out limitations clearly, and give a thorough account of their approaches and thinking.
The reviewers and I have a still-unanswered question, which is central to the study: what is the predictability or unpredictability of the core versus edge environments? Although the authors have explained similarities and distinctions between the different sections of the grackles’ range, their description feels a bit vague -- it's not as rigorous or well-defined as the rest of the paper. Such a lack of definition may be inevitable in the limitations of a preprint, but ultimately it does suggest that there may be real uncertainty about the qualitative differences between the core, edge, and middle environments. The authors do explain that a lack of variation in individual responses to the field experiments would preclude the testing of further hypothesis, but do not mention how a salient lack of variation in novelty/ predictability between the environments could impact their hypotheses.
An assessment/quantification of the rate at which the different populations of grackles encounter novel stimuli would be a cornerstone of the success of this proposed study. Certainly, the authors cannot address this in much more detail during the preprint stage, but they need to consider how to best assess/describe differences before starting the full study. Such an assessment could take the form of either a GIS desktop study (comparing, for example, rates of dam/canal construction in core versus edge sections of the distribution range), or observational/ movement data contrasting how frequently members of core versus edge populations encounter artificial sources of water/food in a given month/year. Considering the long-term nature of the larger project, it is possible that these data are already available, but I am speculating. I would highly recommend that such an assessment be undertaken, beyond the mere mention of expected differences. This would solidify the central idea that there are concrete differences between the environments.
Despite this concern, the authors attended well to the comments and recommendations of the two reviewers – both experts in cognitive ecology. It is a preprint showing clear thinking and a consideration of most of the challenges that may be encountered during the course of the study. My own opinion and the estimations of the two reviewers all underscore the originality and value of this project – this should be a very valuable and potentially novel study. I look forward to seeing the outcomes of the research.

References

[1] McCune, K. B., McElreath, R., and Logan, C. J. (2019). Investigating the use of learning mechanisms in a species that is rapidly expanding its geographic range. In principle recommendation by Peer Community In Ecology. corinalogan.com/Preregistrations/g_sociallearning.html
[2] Benson-Amram, S. and Holekamp, K. E. (2012). Innovative problem solving by wild spotted hyenas. Proceedings of the Royal Society B: Biological Sciences, 279(1744), 4087–4095. doi: 10.1098/rspb.2012.1450
[3] Federspiel, I. G., Boeckle, M., von Bayern, A. M. P. and Emery, N. J. (2019). Exploring individual and social learning in jackdaws (Corvus monedula). Learning & Behavior, 47(3), 258–270. doi: 10.3758/s13420-019-00383-8

Investigating the use of learning mechanisms in a species that is rapidly expanding its geographic rangeKelsey McCune, Richard McElreath, Corina LoganThis is one of many studies planned for our long-term research on the role of behavior and learning in rapid geographic range expansions. Project background: Behavioral flexibility, the ability to change behavior when circumstances change based on...Behaviour & Ethology, Eco-evolutionary dynamics, Foraging, Preregistrations, Social structure, Spatial ecology, Metacommunities & Metapopulations, ZoologyAliza le Roux2019-07-23 18:45:20 View
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
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
31 Jan 2019
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Do the more flexible individuals rely more on causal cognition? Observation versus intervention in causal inference in great-tailed grackles

From cognition to range dynamics: advancing our understanding of macroecological patterns

Recommended by based on reviews by 2 anonymous reviewers

Understanding the distribution of species on earth is one of the fundamental challenges in ecology and evolution. For a long time, this challenge has mainly been addressed from a correlative point of view with a focus on abiotic factors determining a species abiotic niche (classical bioenvelope models; [1]). It is only recently that researchers have realized that behaviour and especially plasticity in behaviour may play a central role in determining species ranges and their dynamics [e.g., 2-5]. Blaisdell et al. propose to take this even one step further and to analyse how behavioural flexibility and possibly associated causal cognition impacts range dynamics.
The current preregistration is integrated in an ambitious long-term research plan that aims at addressing the above outlined question and focuses specifically on investigating whether more behaviourally flexible individuals are better at deriving causal inferences. The model system the authors plan on using are Great-tailed Grackles which have expanded their range into North America during the last century. The preregistration by Blaisdell et al. is a great example of the future of scientific research: it includes conceptual models, alternative hypotheses and testable predictions along with a sound sampling and analysis plan and embraces the principles of Open Science. Overall, the research the authors propose is fascinating and of highest relevance, as it aims at bridging scales from the microscopic mechanisms that underlie animal behaviour to macroscopic, macroecological consequences (see also [3]). I am very much looking forward to the results the authors will report.

References
[1] Elith, J. & Leathwick, J. R. 2009. Species distribution models: ecological explanation and prediction across space and time. Annu. Rev. Ecol. Evol. Syst. 40: 677-697. doi: 10.1146/annurev.ecolsys.110308.120159
[2] Kubisch, A.; Degen, T.; Hovestadt, T. & Poethke, H. J. (2013) Predicting range shifts under global change: the balance between local adaptation and dispersal. Ecography 36: 873-882. doi: 10.1111/j.1600-0587.2012.00062.x
[3] Keith, S. A. & Bull, J. W. (2017) Animal culture impacts species' capacity to realise climate-driven range shifts. Ecography, 40: 296-304. doi: 10.1111/ecog.02481
[4] Sullivan, L. L.; Li, B.; Miller, T. E.; Neubert, M. G. & Shaw, A. K. (2017) Density dependence in demography and dispersal generates fluctuating invasion speeds. Proc. Natl. Acad. Sci. USA, 114: 5053-5058. doi: 10.1073/pnas.1618744114
[5] Fronhofer, E. A.; Nitsche, N. & Altermatt, F. (2017) Information use shapes the dynamics of range expansions into environmental gradients. Glob. Ecol. Biogeogr. 26: 400-411. doi: 10.1111/geb.12547

Do the more flexible individuals rely more on causal cognition? Observation versus intervention in causal inference in great-tailed gracklesAaron Blaisdell, Zoe Johnson-Ulrich, Luisa Bergeron, Carolyn Rowney, Benjamin Seitz, Kelsey McCune, Corina LoganThis PREREGISTRATION has undergone one round of peer reviews. We have now revised the preregistration and addressed reviewer comments. The DOI was issued by OSF and refers to the whole GitHub repository, which contains multiple files. The specific...Behaviour & Ethology, Preregistrations, ZoologyEmanuel A. Fronhofer2018-08-20 11:09:48 View