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26 May 2023
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Using repeatability of performance within and across contexts to validate measures of behavioral flexibility

Do reversal learning methods measure behavioral flexibility?

Recommended by based on reviews by Maxime Dahirel and Aparajitha Ramesh

Assessing the reliability of the methods we use in actually measuring the intended trait should be one of our first priorities when designing a study – especially when the trait in question is not directly observable and is measured through a proxy. 

This is the case for cognitive traits, which are often quantified through measures of behavioral performance. Behavioral flexibility is of particular interest in the context of great environmental changes that a lot of populations have to experiment. This type of behavioral performance is often measured through reversal learning experiments (Bond 2007). In these experiments, individuals first learn a preference, for example for an object of a certain type of form or color, associated with a reward such as food. The characteristics of the rewarded object then change, and the individuals hence have to learn these new characteristics (to get the reward). The time needed by the individual to make this change in preference has been considered a measure of behavioral flexibility.

Although reversal learning experiments have been widely used, their construct validity to assess behavioral flexibility has not been thoroughly tested. This was the aim of McCune and collaborators' (2023) study, through the test of the repeatability of individual performance within and across contexts of reversal learning, in the great-tailed grackle.

This manuscript presents a post-study of the preregistered study* (Logan et al. 2019) that was peer-reviewed and received an In Principle Recommendation for PCI Ecology (Coulon 2019; the initial preregistration was split into 3 post-studies).
Using 34 great-tailed grackles wild-caught in Tempe, Arizona (USA), the authors tested in aviaries 2 hypotheses:

  • First, that the behavioral flexibility measured by reversal learning is repeatable within individuals across sessions of the same experiment;
  • Second, that there is repeatability of the measured behavioral flexibility (within individuals) across different types of reversal learning experiments (context).

The first hypothesis was tested by measuring the repeatability of the time needed by individuals to switch color preference in a color reversal learning task (colored tubes), over serial sessions of this task. The second one was tested by measuring the time needed by individuals to switch solutions, within 3 different contexts: (1) colored tubes, (2) plastic and (3) wooden multi-access boxes involving several ways to access food.

Despite limited sample sizes, the results of these experiments suggest that there is both temporal and contextual repeatability of behavioral flexibility performance of great-tailed grackles, as measured by reversal learning experiments.

Those results are a first indication of the construct validity of reversal learning experiments to assess behavioral flexibility. As highlighted by McCune and collaborators, it is now necessary to assess the discriminant validity of these experiments, i.e. checking that a different performance is obtained with tasks (experiments) that are supposed to measure different cognitive abilities.
 
* A pre-registered study is a study in which context, aims, hypotheses and methodologies have been written down as an empirical paper, peer-reviewed and pre-accepted before research is undertaken. Pre-registrations are intended to reduce publication bias and reporting bias.
 
REFERENCES
 
Bond, A. B., Kamil, A. C., & Balda, R. P. (2007). Serial reversal learning and the evolution of behavioral
flexibility in three species of north american corvids (Gymnorhinus cyanocephalus, Nucifraga columbiana,
Aphelocoma californica). Journal of Comparative Psychology, 121 (4), 372. https://doi.org/10.1037/0735-7036.121.4.372

Coulon, A. (2019) Can context changes improve behavioral flexibility? Towards a better understanding of species adaptability to environmental changes. Peer Community in Ecology, 100019. https://doi.org/10.24072/pci.ecology.100019

Logan, CJ, Lukas D, Bergeron L, Folsom M, & McCune, K. (2019).  Is behavioral flexibility related to foraging and social behavior in a rapidly expanding species? In Principle Acceptance by PCI Ecology of the Version on 6 Aug 2019. http://corinalogan.com/Preregistrations/g_flexmanip.html

McCune KB, Blaisdell AP, Johnson-Ulrich Z, Lukas D, MacPherson M, Seitz BM, Sevchik A, Logan CJ (2023) Using repeatability of performance within and across contexts to validate measures of behavioral flexibility. EcoEvoRxiv, ver. 5 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.32942/X2R59K

Using repeatability of performance within and across contexts to validate measures of behavioral flexibilityMcCune KB, Blaisdell AP, Johnson-Ulrich Z, Lukas D, MacPherson M, Seitz BM, Sevchik A, Logan CJ<p style="text-align: justify;">Research into animal cognitive abilities is increasing quickly and often uses methods where behavioral performance on a task is assumed to represent variation in the underlying cognitive trait. However, because thes...Behaviour & Ethology, Evolutionary ecology, Preregistrations, ZoologyAurélie Coulon2022-08-15 20:56:42 View
30 Jan 2020
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Diapause is not selected as a bet-hedging strategy in insects: a meta-analysis of reaction norm shapes

When to diapause or not to diapause? Winter predictability is not the answer

Recommended by based on reviews by Kévin Tougeron, Md Habibur Rahman Salman and 1 anonymous reviewer

Winter is a harsh season for many organisms that have to cope with food shortage and potentially lethal temperatures. Many species have evolved avoidance strategies. Among them, diapause is a resistance stage many insects use to overwinter. For an insect, it is critical to avoid lethal winter temperatures and thus to initiate diapause before winter comes, while making the most of autumn suitable climatic conditions [1,2]. Several cues can be used to appreciate that winter is coming, including day length and temperature [3]. But climate changes, temperatures rise and become more variable from year to year, which imposes strong pressure upon insect phenology [4]. How can insects adapt to changes in the mean and variance of winter onset?
In this paper, Jens Joschinski and Dries Bonte [5] address this question by using a well conducted meta-analysis of 458 diapause reaction norms obtained from 60 primary studies. They first ask first if insect mean diapause timing is tuned to match winter onset. They further ask if insects adapt to climatic unpredictability through a bet-hedging strategy by playing it safe and avoid risk (conservative bet-hedging) or on the contrary by avoiding to put all their eggs in one basket and spread the risk among their offspring (diversified bet-hedging). From published papers, the authors extracted data on mean diapause timing and information on latitude from which they retrieved day length inducing diapause, the date of winter onset and the day length at winter onset.
They found a positive correlation between latitude and the day length inducing diapause. On the contrary they found positive but (very) weak correlation between the date of winter onset and the date of diapause, thus indicating that diapause timing is not as optimally adapted to local environments as expected, particularly at high latitudes. They only found weak correlations between climate unpredictability and variability in diapause timing, and no correlation between climate unpredictability and deviation from optimal diapause timing. Together, these findings go against the hypothesis that insects use diversified or conservative bet-hedging strategies to cope with uncertainty in climatic conditions.
This is what makes the study thought provoking: the results do not match the theory well. Not because of a lack of data or a narrow scope, but because diapause is a complex trait that is determined by a large array of physiological and ecological factors [3]. Determining what are these factors is of particular interest in the face of the current climate change. This study shows what does not determine the timing of insect diapause. Researchers now know where to look at to improve our understanding of this key aspect of insect adaptation to climatic conditions.

References

[1] Dyck, H. V., Bonte, D., Puls, R., Gotthard, K., and Maes, D. (2015). The lost generation hypothesis: could climate change drive ectotherms into a developmental trap? Oikos, 124(1), 54–61. doi: 10.1111/oik.02066
[2] Gallinat, A. S., Primack, R. B., and Wagner, D. L. (2015). Autumn, the neglected season in climate change research. Trends in Ecology & Evolution, 30(3), 169–176. doi: 10.1016/j.tree.2015.01.004
[3] Tougeron, K. (2019). Diapause research in insects: historical review and recent work perspectives. Entomologia Experimentalis et Applicata, 167(1), 27–36. doi: 10.1111/eea.12753
[4] Bale, J. S., and Hayward, S. a. L. (2010). Insect overwintering in a changing climate. Journal of Experimental Biology, 213(6), 980–994. doi: 10.1242/jeb.037911
[5] Joschinski, J., and Bonte, D. (2020). Diapause is not selected as a bet-hedging strategy in insects: a meta-analysis of reaction norm shapes. BioRxiv, 752881, ver. 3 recommended and peer-reviewed by PCI Ecology. doi: 10.1101/752881

Diapause is not selected as a bet-hedging strategy in insects: a meta-analysis of reaction norm shapesJens Joschinski and Dries BonteMany organisms escape from lethal climatological conditions by entering a resistant resting stage called diapause, and it is essential that this strategy remains optimally timed with seasonal change. Climate change therefore exerts selection press...Maternal effects, Meta-analyses, Phenotypic plasticity, Terrestrial ecologyBastien Castagneyrol2019-09-20 11:47:47 View
12 Aug 2021
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A study on the role of social information sharing leading to range expansion in songbirds with large vocal repertoires: Enhancing our understanding of the Great-Tailed Grackle (Quiscalus mexicanus) alarm call

Does the active vocabulary in Great-tailed Grackles supports their range expansion? New study will find out

Recommended by Jan Oliver Engler based on reviews by Guillermo Fandos and 2 anonymous reviewers

Alarm calls are an important acoustic signal that can decide the life or death of an individual. Many birds are able to vary their alarm calls to provide more accurate information on e.g. urgency or even the type of a threatening predator. According to the acoustic adaptation hypothesis, the habitat plays an important role too in how acoustic patterns get transmitted. This is of particular interest for range-expanding species that will face new environmental conditions along the leading edge. One could hypothesize that the alarm call repertoire of a species could increase in newly founded ranges to incorporate new habitats and threats individuals might face. Hence selection for a larger active vocabulary might be beneficial for new colonizers. Using the Great-Tailed Grackle (Quiscalus mexicanus) as a model species, Samantha Bowser from Arizona State University and Maggie MacPherson from Louisiana State University want to find out exactly that. 

The Great-Tailed Grackle is an appropriate species given its high vocal diversity. Also, the species consists of different subspecies that show range expansions along the northern range edge yet to a varying degree. Using vocal experiments and field recordings the researchers have a high potential to understand more about the acoustic adaptation hypothesis within a range dynamic process. 

Over the course of this assessment, the authors incorporated the comments made by two reviewers into a strong revision of their research plans. With that being said, the few additional comments made by one of the initial reviewers round up the current stage this interesting research project is in. 

To this end, I can only fully recommend the revised research plan and am much looking forward to the outcomes from the author’s experiments, modeling, and field data. With the suggestions being made at such an early stage I firmly believe that the final outcome will be highly interesting not only to an ornithological readership but to every ecologist and biogeographer interested in drivers of range dynamic processes.

References

Bowser, S., MacPherson, M. (2021). A study on the role of social information sharing leading to range expansion in songbirds with large vocal repertoires: Enhancing our understanding of the Great-Tailed Grackle (Quiscalus mexicanus) alarm call. In principle recommendation by PCI Ecology. https://doi.org/10.17605/OSF.IO/2UFJ5. Version 3

A study on the role of social information sharing leading to range expansion in songbirds with large vocal repertoires: Enhancing our understanding of the Great-Tailed Grackle (Quiscalus mexicanus) alarm call Samantha Bowser, Maggie MacPherson<p>The acoustic adaptation hypothesis posits that animal sounds are influenced by the habitat properties that shape acoustic constraints (Ey and Fischer 2009, Morton 2015, Sueur and Farina 2015).Alarm calls are expected to signal important habitat...Biogeography, Biological invasions, Coexistence, Dispersal & Migration, Habitat selection, Landscape ecologyNone Darius Stiels, Anonymous2020-12-01 18:11:02 View
05 Mar 2019
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Are the more flexible great-tailed grackles also better at inhibition?

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

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

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

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

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

Recommended by ORCID_LOGO and 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
06 Mar 2020
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Interplay between the paradox of enrichment and nutrient cycling in food webs

New insights into the role of nutrient cycling in food web dynamics

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

Understanding the factors that govern the relationship between structure, stability and functioning of food webs has been a central problem in ecology for many decades. Historically, apart from microbial and soil food webs, the role of nutrient cycling has largely been ignored in theoretical and empirical food web studies. A prime example of this is the widespread use of Lotka-Volterra type models in theoretical studies; these models per se are not designed to capture the effect of nutrients being released back into the system by interacting populations. Thus overall, we still lack a general understanding of how nutrient cycling affects food web dynamics.
A new study by Quévreux, Barot and Thébault [1] tackles this problem by building a new food web model. This model features some important biological details: trophic interactions and vital rates constrained by species' body masses (using Ecological Metabolic Theory), adaptive foraging, and stoichiometric rules to ensure meaningful conversion between carbon and nutrient flows. The authors analyze the model through detailed simulations combined with thorough sensitivity analyses of model assumptions and parametrizations (including of allometric scaling relationships). I am happy to recommend this preprint because of the novelty of the work and it's technical quality.
The study yields interesting and novel findings. Overall, nutrient cycling does have a strong effect on community dynamics. Nutrient recycling is driven mostly by consumers at low mineral nutrient inputs, and by primary producers at high inputs. The extra nutrients made available through recycling increases species' persistence at low nutrient input levels, but decreases persistence at higher input levels by increasing population oscillations (a new, nuanced perspective on the classical "paradox of enrichment"). Also, for the same level of nutrient input, food webs with nutrient recycling show more fluctuations in primary producer biomass (and less at higher trophic levels) than those without recycling, with this effect weakening in more complex food webs.
Overall, these results provide new insights, suggesting that nutrient cycling may enhance the positive effects of species richness on ecosystem stability, and point at interesting new directions for future theoretical and empirical studies.

References

[1] Quévreux, P., Barot, S. and E. Thébault (2020) Interplay between the paradox of enrichment and nutrient cycling in food webs. bioRxiv, 276592, ver. 7 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/276592

Interplay between the paradox of enrichment and nutrient cycling in food websPierre Quévreux, Sébastien Barot and Élisa Thébault<p>Nutrient cycling is fundamental to ecosystem functioning. Despite recent major advances in the understanding of complex food web dynamics, food web models have so far generally ignored nutrient cycling. However, nutrient cycling is expected to ...Biodiversity, Community ecology, Ecosystem functioning, Food webs, Interaction networks, Theoretical ecologySamraat Pawar2018-11-03 21:47:37 View
18 Dec 2019
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Validating morphological condition indices and their relationship with reproductive success in great-tailed grackles

Are condition indices positively related to each other and to fitness?: a test with grackles

Recommended by based on reviews by Javier Seoane and Isabel López-Rull

Reproductive succes, as a surrogate of individual fitness, depends both on extrinsic and intrinsic factors [1]. Among the intrinsic factors, resource level or health are considered important potential drivers of fitness but exceedingly difficult to measure directly. Thus, a host of proxies have been suggested, known as condition indices [2]. The question arises whether all condition indices consistently measure the same "inner state" of individuals and whether all of them similarly correlate to individual fitness. In this preregistration, Berens and colleagues aim to answer this question for two common condition indices, fat score and scaled mass index (Fig. 1), using great-tailed grackles as a model system. Although this question is not new, it has not been satisfactorily solved and both reviewers found merit in the attempt to clarify this matter.

Figure 1. Hypothesized relationships between two condition indices and reproductive success. Single arrow heads indicate causal relationships; double arrow heads indicate only correlation. In a best case scenario, all relationships should be positive and linear.
A problem in adressing this question with grackles is limited population, ergo sample, size and limited possibilites of recapture individuals. Some relationships can be missed due to low statistical power. Unfortunately, existing tools for power analysis fall behind complex designs and the one planned for this study. Thus, any potentially non significant relationship has to be taken cautiously. Nevertheless, even if grackles will not provide a definitive answer (they never meant to do it), this preregistration can inspire broader explorations of matches and mismatches across condition indices and species, as well as uncover non-linear relationships with reproductive success.

References

[1] Roff, D. A. (2001). Life history evolution. Oxford University Press, Oxford.
[2] Labocha, M. K.; Hayes, J. P. (2012). Morphometric indices of body condition in birds: a review. Journal of Ornithology 153: 1–22. doi: 10.1007/s10336-011-0706-1

Validating morphological condition indices and their relationship with reproductive success in great-tailed gracklesJennifer M. Berens, Corina J. Logan, Melissa Folsom, Luisa Bergeron, Kelsey B. McCuneMorphological variation among individuals has the potential to influence multiple life history characteristics such as dispersal, migration, reproductive fitness, and survival (Wilder, Raubenheimer, and Simpson (2016)). Theoretically, individuals ...Behaviour & Ethology, Conservation biology, Demography, Morphometrics, Preregistrations, ZoologyMarcos Mendez2019-08-05 20:05:56 View
21 Nov 2023
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Pathogen community composition and co-infection patterns in a wild community of rodents

Reservoirs of pestilence: what pathogen and rodent community analyses can tell us about transmission risk

Recommended by ORCID_LOGO based on reviews by Adrian Diaz, Romain Pigeault and 1 anonymous reviewer

Rodents are well known as one of the main animal groups responsible for human-transmitted pathogens. As such, it seems logical to try and survey what kinds of pathogenic microbes might be harboured by wild rodents, in order to establish some baseline surveillance and prevent future zoonotic outbreaks (Bernstein et al., 2022). This is exactly what Abbate et al. (2023) endeavoured and their findings are intimidating. Based on quite a large sampling effort, they collected more than 700 rodents of seven species around two villages in northeastern France. They looked for molecular markers indicative of viral and bacterial infections and proceeded to analyze their pathogen communities using multivariate techniques.

Variation in the prevalence of the different pathogens was found among host species, with e.g. signs of CPXV more prevalent in Cricetidae while some Mycoplasma strains were more prevalent in Muridae. Co-circulation of pathogens was found in all species, with some evidencing signs of up to 12 different pathogen taxa. The diversity of co-circulating pathogens was markedly different between host species and higher in adult hosts, but not affected by sex. The dataset also evinced some slight differences between habitats, with meadows harbouring a little more diversity of rodent pathogens than forests. Less intuitively, some pathogen associations seemed quite repeatable, such as the positive association of Bartonella spp. with CPXV in the montane water vole. The study allowed the authors to test several associations already described in the literature, including associations between different hemotropic Mycoplasma species.

I strongly invite colleagues interested in zoonoses, emerging pandemics and more generally One Health to read the paper of Abbate et al. (2023) and try to replicate them across the world. To prevent the next sanitary crises, monitoring rodents, and more generally vertebrates, population demographics is a necessary and enlightening step (Johnson et al., 2020), but insufficient. Following the lead of colleagues working on rodent ectoparasites (Krasnov et al., 2014), we need more surveys like the one described by Abbate et al. (2023) to understand the importance of the dilution effect in the prevalence and transmission of microbial pathogens (Andreazzi et al., 2023) and the formation of epidemics. We also need other similar studies to assess the potential of different rodent species to carry pathogens more or less capable of infecting other mammalian species (Morand et al., 2015), in other places in the world.

References

Abbate, J. L., Galan, M., Razzauti, M., Sironen, T., Voutilainen, L., Henttonen, H., Gasqui, P., Cosson, J.-F. & Charbonnel, N. (2023) Pathogen community composition and co-infection patterns in a wild community of rodents. BioRxiv, ver.4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2020.02.09.940494 

Andreazzi, C. S., Martinez-Vaquero, L. A., Winck, G. R., Cardoso, T. S., Teixeira, B. R., Xavier, S. C. C., Gentile, R., Jansen, A. M. & D'Andrea, P. S. (2023) Vegetation cover and biodiversity reduce parasite infection in wild hosts across ecological levels and scales. Ecography, 2023, e06579.
https://doi.org/10.1111/ecog.06579
 
Bernstein, A. S., Ando, A. W., Loch-Temzelides, T., Vale, M. M., Li, B. V., Li, H., Busch, J., Chapman, C. A., Kinnaird, M., Nowak, K., Castro, M. C., Zambrana-Torrelio, C., Ahumada, J. A., Xiao, L., Roehrdanz, P., Kaufman, L., Hannah, L., Daszak, P., Pimm, S. L. & Dobson, A. P. (2022) The costs and benefits of primary prevention of zoonotic pandemics. Science Advances, 8, eabl4183.
https://doi.org/10.1126/sciadv.abl4183
 
Johnson, C. K., Hitchens, P. L., Pandit, P. S., Rushmore, J., Evans, T. S., Young, C. C. W. & Doyle, M. M. (2020) Global shifts in mammalian population trends reveal key predictors of virus spillover risk. Proceedings of the Royal Society B: Biological Sciences, 287, 20192736.
https://doi.org/10.1098/rspb.2019.2736
 
Krasnov, B. R., Pilosof, S., Stanko, M., Morand, S., Korallo-Vinarskaya, N. P., Vinarski, M. V. & Poulin, R. (2014) Co-occurrence and phylogenetic distance in communities of mammalian ectoparasites: limiting similarity versus environmental filtering. Oikos, 123, 63-70.
https://doi.org/10.1111/j.1600-0706.2013.00646.x
 
Morand, S., Bordes, F., Chen, H.-W., Claude, J., Cosson, J.-F., Galan, M., Czirjak, G. Á., Greenwood, A. D., Latinne, A., Michaux, J. & Ribas, A. (2015) Global parasite and Rattus rodent invasions: The consequences for rodent-borne diseases. Integrative Zoology, 10, 409-423.
https://doi.org/10.1111/1749-4877.12143

Pathogen community composition and co-infection patterns in a wild community of rodentsJessica Lee Abbate, Maxime Galan, Maria Razzauti, Tarja Sironen, Liina Voutilainen, Heikki Henttonen, Patrick Gasqui, Jean-François Cosson, Nathalie Charbonnel<p style="text-align: justify;">Rodents are major reservoirs of pathogens that can cause disease in humans and livestock. It is therefore important to know what pathogens naturally circulate in rodent populations, and to understand the factors tha...Biodiversity, Coexistence, Community ecology, Eco-immunology & Immunity, Epidemiology, Host-parasite interactions, Population ecology, Species distributionsFrancois Massol2020-02-11 12:42:28 View
14 Jan 2021
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Consistent variations in personality traits and their potential for genetic improvement of biocontrol agents: Trichogramma evanescens as a case study

Tell us how you can be, and we’ll make you better: exploiting genetic variability in personality traits to improve top-down control of agricultural pests

Recommended by based on reviews by Bart A Pannebakker, François Dumont, Joshua Patrick Byrne and Ana Pimenta Goncalves Pereira

Agriculture in the XXI century faces the huge challenge of having to provide food to a rapidly growing human population, which is expected to reach 10.9 billion in 2100 (UUNN 2019), by means of practices and methods that guarantee crop sustainability, human health safety, and respect to the environment (UUNN 2015). Such regulation by the United Nations ultimately entails that agricultural scientists are urged to design strategies and methods that effectively minimize the use of harmful chemical products to control pest populations and to improve soil quality.
One of the most, if not the most, sustainable, safe, and environmentally friendly approach to apply against pests is Biological Pest Control (BPC, hereafter), that is, the use of natural enemies to control the populations of pest organisms. The concept of BPC is by no means new: long back to the 300 AC, Chinese farmers built bamboo bridges between citrus trees to facilitate the foraging of the ant species Oecophylla smaragdina to control lepidopteran citrus pests (Konishi and Ito, 1973); It is also nice to use this recommendation letter to recall and quote the words written in 1752 by the famous Swedish taxonomist, botanist and zoologist, Carl Linnaeus: "Every insect has its predator which follows and destroys it. Such predatory insects should be caught and used for disinfecting crop-plants" (Hörstadius (1974) apud Linnaeus 1752).
Acknowledging the many cases of successes from BPC along our recent history, it is also true that application of BPC strategies during the XX century suffered from wrong-doings, mainly when the introduced biological control agent (BCA, hereafter) was of exotic origin and with a generalist diet-breath; in some cases the release of exotic species resulted on global extinction, reduction in the range of distribution, reduction in the population abundance, and partial displacement, of native and functionally similar species, and interbreeding with them (reviewed in van Lenteren et al. 2006). One of the most famous cases is that of Harmonia axyridis, a coccinellid predator of Asian origin that caused important environmental damage in North America (reviewed in Koch & Galvan, 2008).
Fortunately, after the implementation of the Nagoya protocol (CBD, 2011) importation of exotic species for BPC use was severely restricted and controlled, worldwide. Consequently, companies and agricultural scientist were driven to reinforce their focus and interest on the exploitation of native natural enemies, via the mass-rearing and release of native candidates (augmentative BPC), the conservation of landscapes near the crops to provide resources for natural enemies (i.e. conservation biological pest control), or via the exploitation of the genetic variability of BCAs, to create strains performing better at regulating pest populations under specific biotic or abiotic negative circumstances. Some of these cases are cited in Lartigue et al. (2020). The genetic improvement of BCAs is a strategy still in its infancy, but there is no doubt that the interest for it has significantly increased over the last 5 years (Lommen et al 2017, Bielza 2020, Leung et al 2020).
In my humble opinion, what makes the paper of Lartigue et al. (2020) a remarkable contribution to the field of genetic breeding of BCAs is that it opens a new window of opportunities to the field, by exploring the possibilities for artificial selection of behavioral traits (Réale et al. 2007) to "create" strains of natural enemies displaying behavioral syndromes (Sih et al. 2004) that makes them better at regulating pest populations. The behavioral approach for breeding BCAs can then be extended by crossing it with known abiotic and/or biotic hostile environments (e.g. warm and drought environments, presence of predators/competitors to the BCA, respectively) and engineer strains more prompt to display particular behavioral syndromes to help them to overcome the overall hostility of specific environments. I strongly believe that the approach proposed in Lartigue et al. (2020) will influence the future management of agricultural systems, where strategies including the genetic breeding of BCAs’ behavior will contribute to create better guards and protectors of our crops.

References

Bielza, P., Balanza, V., Cifuentes, D. and Mendoza, J. E. (2020). Challenges facing arthropod biological control: Identifying traits for genetic improvement of predators in protected crops. Pest Manag Sci. doi: https://doi.org/10.1002/ps.5857
CBD - Convention on Biological Diversity, 2011. The Nagoya Protocol on Access and Benefit-sharing, https://www.cbd.int/abs/doc/protocol/nagoya-protocol-en.pdf
Hörstadius, S. (1974). Linnaeus, animals and man. Biological Journal of the Linnaean Society, 6, 269-275. doi: https://doi.org/10.1111/j.1095-8312.1974.tb00725.x
Koch, R.L. and Galvan, T.L. (2008). Bad side of a good beetle: the North American experience with Harmonia axyridis. BioControl 53, 23–35. doi: https://doi.org/10.1007/978-1-4020-6939-0_3
Konishi, M. and Ito, Y. (1973). Early entomology in East Asia. In: Smith, R.F., Mittler, T.E., Smith, C.N. (Eds.), History of Entomology, Annual Reviews Inc., Palo Alto, California, pp. 1-20.
Lartigue, S., Yalaoui, M., Belliard, J., Caravel, C., Jeandroz, L., Groussier, G., Calcagno, V., Louâpre, P., Dechaume-Moncharmont, F.-X., Malausa, T. and Moreau, J. (2020). Consistent variations in personality traits and their potential for genetic improvement of biocontrol agents: Trichogramma evanescens as a case study. bioRxiv, 2020.08.21.257881, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: https://doi.org/10.1101/2020.08.21.257881
Leung et al. (2020). Next-generation biological control: the need for integrating genetics and genomics. Biological Reviews, 95(6), 1838–1854. doi: https://doi.org/10.1111/brv.12641
Lommen, S. T. E., de Jong, P. W. and Pannebakker, B. A. (2017). It is time to bridge the gap between exploring and exploiting: prospects for utilizing intraspecific genetic variation to optimize arthropods for augmentative pest control – a review. Entomologia Experimentalis et Applicata, 162: 108-123. doi: https://doi.org/10.1111/eea.12510
Réale, D., Reader, S. M., Sol, D., McDougall, P. T. and Dingemanse, N. J. (2007). Integrating animal temperament within ecology and evolution. Biological Reviews, 82: 291-318. doi: https://doi.org/10.1111/j.1469-185X.2007.00010.x
Sih, A., Bell, A. and Johnson, J. C. (2004). Behavioral syndromes: an ecological and evolutionary overview. Trends in Ecology and Evolution, 19(7), 372–378. doi: https://doi.org/10.1016/j.tree.2004.04.009
UUNN. 2015. Transforming our world: the 2030 Agenda for Sustainable Development. report of the Open Working Group of the General Assembly on Sustainable Development Goals (A/68/970 and Corr.1; see also A/68/970/Add.1–3).
UUNN. 2019. World population prospects 2019. United Nations, Department of Economic and Social Affairs, Population Division: Highlights. ST/ESA/SER.A/423.
van Lenteren, J. C., Bale, J., Bigler, F., Hokkanen, H. M. T. and Loomans A. J. M. (2006). Assessing risks of releasing exotic biological control agents of arthropod pests. Annual Review of Entomology, 51: 609-634. doi: https://doi.org/10.1146/annurev.ento.51.110104.151129

Consistent variations in personality traits and their potential for genetic improvement of biocontrol agents: Trichogramma evanescens as a case studySilène Lartigue, Myriam Yalaoui, Jean Belliard, Claire Caravel, Louise Jeandroz, Géraldine Groussier, Vincent Calcagno, Philippe Louâpre, François-Xavier Dechaume-Moncharmont, Thibaut Malausa and Jérôme Moreau<p>Improvements in the biological control of agricultural pests require improvements in the phenotyping methods used by practitioners to select efficient biological control agent (BCA) populations in industrial rearing or field conditions. Consist...Agroecology, Behaviour & Ethology, Biological control, Evolutionary ecology, Life historyMarta Montserrat2020-08-24 10:40:03 View
28 Apr 2023
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Most diverse, most neglected: weevils (Coleoptera: Curculionoidea) are ubiquitous specialized brood-site pollinators of tropical flora

Pollination-herbivory by weevils claiming for recognition: the Cinderella among pollinators

Recommended by based on reviews by Susan Kirmse, Carlos Eduardo Nunes and 2 anonymous reviewers

Since Charles Darwin times, and probably earlier, naturalists have been eager to report the rarest pollinators being discovered, and this still happens even in recent times; e.g., increased evidence of lizards, cockroaches, crickets or earwigs as pollinators (Suetsugu 2018, Komamura et al. 2021, de Oliveira-Nogueira et al. 2023), shifts to invasive animals as pollinators, including passerine birds and rats (Pattemore & Wilcove 2012), new amazing cases of mimicry in pollination, such as “bleeding” flowers that mimic wounded insects (Heiduk et al., 2023) or even the possibility that a tree frog is reported for the first time as a pollinator (de Oliveira-Nogueira et al. 2023). This is in part due to a natural curiosity of humans about rarity, which pervades into scientific insight (Gaston 1994). Among pollinators, the apparent rarity of some interaction types is sometimes a symptom of a lack of enough inquiry. This seems to be the case of weevil pollination, given that these insects are widely recognized as herbivores, particularly those that use plant parts to nurse their breed and never were thought they could act also as mutualists, pollinating the species they infest. This is known as a case of brood site pollination mutualism (BSPM), which also involves an antagonistic counterpart (herbivory) to which plants should face. This is the focus of the manuscript (Haran et al. 2023) we are recommending here. There is wide treatment of this kind of pollination in textbooks, albeit focused on yucca-yucca moth and fig-fig wasp interactions due to their extreme specialization (Pellmyr 2003, Kjellberg et al. 2005), and more recently accompanied by Caryophyllaceae-moth relationship (Kephart et al. 2006). 

Here we find a detailed review that shows that the most diverse BSPM, in terms of number of plant and pollinator species involved, is that of weevils in the tropics. The mechanism of BSPM does not involve a unique morphological syndrome, as it is mostly functional and thus highly dependent on insect biology (Fenster & al. 2004), whereas the flower phenotypes are highly divergent among species. Probably, the inconspicuous nature of the interaction, and the overwhelming role of weevils as seed predators, even as pests, are among the causes of the neglection of weevils as pollinators, as it could be in part the case of ants as pollinators (de Vega et al. 2014). The paper by Haran et al (2023) comes to break this point.

Thus, the rarity of weevil pollination in former reports is not a consequence of an anecdotical nature of this interaction, even for the BSPM, according to the number of cases the authors are reporting, both in terms of plant and pollinator species involved. This review has a classical narrative format which involves a long text describing the natural history behind the cases. It is timely and fills the gap for this important pollination interaction for biodiversity and also for economic implications for fruit production of some crops. Former reviews have addressed related topics on BSPM but focused on other pollinators, such as those mentioned above. Besides, the review put much effort into the animal side of the interaction, which is not common in the pollination literature. Admittedly, the authors focus on the detailed description of some paradigmatic cases, and thereafter suggest that these can be more frequently reported in the future, based on varied evidence from morphology, natural history, ecology, and distribution of alleged partners. This procedure was common during the development of anthecology, an almost missing term for floral ecology (Baker 1983), relying on accumulative evidence based on detailed observations and experiments on flowers and pollinators. Currently, a quantitative approach based on the tools of macroecological/macroevolutionary analyses is more frequent in reviews. However, this approach requires a high amount of information on the natural history of the partnership, which allows for sound hypothesis testing. By accumulating this information, this approach allows the authors to pose specific questions and hypotheses which can be tested, particularly on the efficiency of the systems and their specialization degree for both the plants and the weevils, apparently higher for the latter. This will guarantee that this paper will be frequently cited by floral ecologists and evolutionary biologists and be included among the plethora of floral syndromes already described, currently based on more explicit functional grounds (Fenster et al. 2004). In part, this is one of the reasons why the sections focused on future prospects is so large in the review. 

I foresee that this mutualistic/antagonistic relationship will provide excellent study cases for the relative weight of these contrary interactions among the same partners and its relationship with pollination specialization-generalization and patterns of diversification in the plants and/or the weevils. As new studies are coming, it is possible that BSPM by weevils appears more common in non-tropical biogeographical regions. In fact, other BSPM are not so uncommon in other regions (Prieto-Benítez et al. 2017). In the future, it would be desirable an appropriate testing of the actual effect of phylogenetic niche conservatism, using well known and appropriately selected BSPM cases and robust phylogenies of both partners in the mutualism. Phylogenetic niche conservatism is a central assumption by the authors to report as many cases as possible in their review, and for that they used taxonomic relatedness. As sequence data and derived phylogenies for large numbers of vascular plant species are becoming more frequent (Jin & Quian 2022), I would recommend the authors to perform a comparative analysis using this phylogenetic information. At least, they have included information on phylogenetic relatedness of weevils involved in BSPM which allow some inferences on the multiple origins of this interaction. This is a good start to explore the drivers of these multiple origins through the lens of comparative biology.

References

Baker HG (1983) An Outline of the History of Anthecology, or Pollination Biology. In: L Real (ed). Pollination Biology. Academic Press.

de-Oliveira-Nogueira CH, Souza UF, Machado TM, Figueiredo-de-Andrade CA, Mónico AT, Sazima I, Sazima M, Toledo LF (2023). Between fruits, flowers and nectar: The extraordinary diet of the frog Xenohyla truncate. Food Webs 35: e00281. https://doi.org/10.1016/j.fooweb.2023.e00281

Fenster CB W, Armbruster S, Wilson P, Dudash MR, Thomson JD (2004). Pollination syndromes and floral specialization. Annu. Rev. Ecol. Evol. Syst. 35: 375–403. https://doi.org/10.1146/annurev.ecolsys.34.011802.132347

Gaston KJ (1994). What is rarity? In KJ Gaston (ed): Rarity. Population and Community Biology Series, vol 13. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-0701-3_1

Haran J, Kergoat GJ, Bruno, de Medeiros AS (2023) Most diverse, most neglected: weevils (Coleoptera: Curculionoidea) are ubiquitous specialized brood-site pollinators of tropical flora. hal. 03780127, version 2 peer-reviewed and recommended by Peer Community in Ecology. https://hal.inrae.fr/hal-03780127

Heiduk A, Brake I, Shuttleworth A, Johnson SD (2023) ‘Bleeding’ flowers of Ceropegia gerrardii (Apocynaceae-Asclepiadoideae) mimic wounded insects to attract kleptoparasitic fly pollinators. New Phytologist. https://doi.org/10.1111/nph.18888

Jin, Y., & Qian, H. (2022). V. PhyloMaker2: An updated and enlarged R package that can generate very large phylogenies for vascular plants. Plant Diversity, 44(4), 335-339. https://doi.org/10.1016/j.pld.2022.05.005

Kjellberg F, Jousselin E, Hossaert-Mckey M, Rasplus JY (2005). Biology, ecology, and evolution of fig-pollinating wasps (Chalcidoidea, Agaonidae). In: A. Raman et al (eds) Biology, ecology and evolution of gall-inducing arthropods 2, 539-572. Science Publishers, Enfield.

Komamura R, Koyama K, Yamauchi T, Konno Y, Gu L (2021). Pollination contribution differs among insects visiting Cardiocrinum cordatum flowers. Forests 12: 452. https://doi.org/10.3390/f12040452

Pattemore DE, Wilcove DS (2012) Invasive rats and recent colonist birds partially compensate for the loss of endemic New Zealand pollinators. Proc. R. Soc. B 279: 1597–1605. https://doi.org/10.1098/rspb.2011.2036

Pellmyr O (2003) Yuccas, yucca moths, and coevolution: a review. Ann. Missouri Bot. Gard. 90: 35-55. https://doi.org/10.2307/3298524

Prieto-Benítez S, Yela JL, Giménez-Benavides L (2017) Ten years of progress in the study of Hadena-Caryophyllaceae nursery pollination. A review in light of new Mediterranean data. Flora, 232, 63-72. https://doi.org/10.1016/j.flora.2017.02.004

Suetsugu K (2019) Social wasps, crickets and cockroaches contribute to pollination of the holoparasitic plant Mitrastemon yamamotoi (Mitrastemonaceae) in southern Japan. Plant Biology 21 176–182. https://doi.org/10.1111/plb.12889

Most diverse, most neglected: weevils (Coleoptera: Curculionoidea) are ubiquitous specialized brood-site pollinators of tropical floraJulien Haran, Gael J. Kergoat, Bruno A. S. de Medeiros<p style="text-align: justify;">In tropical environments, and especially tropical rainforests, a major part of pollination services is provided by diverse insect lineages. Unbeknownst to most, beetles, and more specifically hyperdiverse weevils (C...Biodiversity, Evolutionary ecology, Pollination, Tropical ecologyJuan Arroyo2022-09-28 11:54:37 View