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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 ORCID_LOGO 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
20 Aug 2024
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Bayesian reinforcement learning models reveal how great-tailed grackles improve their behavioral flexibility in serial reversal learning experiments

Changes in behavioral flexibility to cope with environment instability: theoretical and empirical insights from serial reversal learning experiments

Recommended by ORCID_LOGO based on reviews by Maxime Dahirel and 1 anonymous reviewer

Behavioral flexibility, i.e. the “ability to adapt behavior to new circumstances through packaging information and making it available to other cognitive processes” (Logan et al. 2023), appears as one of the crucial elements of responses of animal species to changing environments. Behavioral flexibility can change within the life of individuals, depending on their experience on the degree of variability and predictability of their surrounding environment. But little is known on the cognitive processes involved in these temporal changes in behavioral flexibility within individuals.

This is what Lukas et al. (2024) investigated very thoroughly, using the framework of serial reversal learning experiments on great-tailed grackles to study different aspects of the question. Behavioral flexibility as involved in serial reversal learning experiments was previously modeled as being made of two primary parameters: the rate of updating associations, phi (i.e. how fast individuals learn the associations between a cue and its associated reward or danger); and the sensitivity to the learned associations, lambda (i.e. how strong do individuals make their choices based on the associations they learned). 

Lukas et al. (2024)* used a Bayesian reinforcement model to infer phi and lambda in individuals going through serial reversal learning experiments, to understand which of these two parameters explains most of the variation in grackle performance in serial reversal learning, how correlated they are, how they can change along time depending on an individual’s experience, how variable they can be among individuals, and whether they can predict performance in other contexts. But beforehand, the authors used an individual-based model to assess the ability of the Bayesian reinforcement model to correctly assess phi and lambda in their experimental design. They also used the Bayesian model to infer the range of values of phi and lambda an individual needs to exhibit to reduce errors in the serial reversal learning experiment.

Among other results, this study shows that in a context of rapidly changing but strongly reliable cues, the variation in the success of grackles is more associated with the rate of updating associations (phi) than the sensitivity to learned associations (lambda). Besides, phi increased within individuals along the serial reversal learning experiment, while lambda only slightly decreased. However, it is very interesting to note that different approaches could be adopted by different individuals through the training, leading them eventually to the same final performance: slightly different combinations of changes in lambda and phi lead to different behaviours but compensate each other in the end in the final success rate. 
This study provides exciting insights into the cognitive processes involved in how changes in behavioral flexibility of individuals can happen in this type of serial learning experiments. But it also offers interesting openings to understand the mechanisms by which behavioral flexibility can change in the wild, helping individuals to cope with rapidly changing environments.
 
* Lukas et al. (2024) 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). 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

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  

Dieter Lukas, Kelsey B. McCune, Aaron P. Blaisdell, Zoe Johnson-Ulrich, Maggie MacPherson, Benjamin M. Seitz, Augustus Sevchik, Corina J. Logan (2024) Bayesian reinforcement learning models reveal how great-tailed grackles improve their behavioral flexibility in serial reversal learning experiments. ecoevoRxiv, ver.4 peer-reviewed and recommended by Peer Community in Ecology https://doi.org/10.32942/osf.io/4ycps

Bayesian reinforcement learning models reveal how great-tailed grackles improve their behavioral flexibility in serial reversal learning experimentsDieter Lukas, Kelsey B. McCune, Aaron P. Blaisdell, Zoe Johnson-Ulrich, Maggie MacPherson, Benjamin M. Seitz, Augustus Sevchik, Corina J. Logan<p>Environments can change suddenly and unpredictably and animals might benefit from being able to flexibly adapt their behavior through learning new associations. Serial (repeated) reversal learning experiments have long been used to investigate ...Behaviour & Ethology, Phenotypic plasticity, Preregistrations, ZoologyAurélie Coulon2022-08-15 21:04:14 View
24 Jan 2023
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Four decades of phenology in an alpine amphibian: trends, stasis, and climatic drivers

Alpine ecology and their dynamics under climate change

Recommended by based on reviews by Nigel Yoccoz and 1 anonymous reviewer

​​Research about the effects of climate change on ecological communities has been abundant in the last decades. In particular, studies about the effects of climate change on mountain ecosystems have been key for understanding and communicating the consequences of this global phenomenon. Alpine regions show higher increases in warming in comparison to low-altitude ecosystems and this trend is likely to continue. This warming has caused reduced snowfall and/or changes in the duration of snow cover. For example, Notarnicola (2020) reported that 78% of the world’s mountain areas have experienced a snow cover decline since 2000. In the same vein, snow cover has decreased by 10% compared with snow coverage in the late 1960s (Walther et al., 2002) and snow cover duration has decreased at a rate of 5 days/decade (Choi et al., 2010). These changes have impacted the dynamics of high-altitude plant and animal populations. Some impacts are changes in the hibernation of animals, the length of the growing season for plants and the soil microbial composition (Chávez et al. 2021).

Lenzi et al. (2023), give us an excellent study using long-term data on alpine amphibian populations. Authors show how climate change has impacted the reproductive phenology of Bufo bufo, especially the breeding season starts 30 days earlier than ~40 years ago. This earlier breeding is associated with the increasing temperatures and reduced snow cover in these alpine ecosystems. However, these changes did not occur in a linear trend but a marked acceleration was observed until mid-1990s with a later stabilization. Authors associated these nonlinear changes with complex interactions between the global trend of seasonal temperatures and site-specific conditions. 

Beyond the earlier breeding season, changes in phenology can have important impacts on the long-term viability of alpine populations. Complex interactions could involve positive and negative effects like harder environmental conditions for propagules, faster development of juveniles, or changes in predation pressure. This study opens new research opportunities and questions like the urgent assessment of the global impact of climate change on animal fitness. This study provides key information for the conservation of these populations.

References

Chávez RO, Briceño VF, Lastra JA, Harris-Pascal D, Estay SA (2021) Snow Cover and Snow Persistence Changes in the Mocho-Choshuenco Volcano (Southern Chile) Derived From 35 Years of Landsat Satellite Images. Frontiers in Ecology and Evolution, 9. https://doi.org/10.3389/fevo.2021.643850

Choi G, Robinson DA, Kang S (2010) Changing Northern Hemisphere Snow Seasons. Journal of Climate, 23, 5305–5310. https://doi.org/10.1175/2010JCLI3644.1

Lenzi O, Grossenbacher K, Zumbach S, Lüscher B, Althaus S, Schmocker D, Recher H, Thoma M, Ozgul A, Schmidt BR (2022) Four decades of phenology in an alpine amphibian: trends, stasis, and climatic drivers.bioRxiv, 2022.08.16.503739, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.08.16.503739

Notarnicola C (2020) Hotspots of snow cover changes in global mountain regions over 2000–2018. Remote Sensing of Environment, 243, 111781. https://doi.org/10.1016/j.rse.2020.111781

Four decades of phenology in an alpine amphibian: trends, stasis, and climatic driversOmar Lenzi, Kurt Grossenbacher, Silvia Zumbach, Beatrice Luescher, Sarah Althaus, Daniela Schmocker, Helmut Recher, Marco Thoma, Arpat Ozgul, Benedikt R. Schmidt<p style="text-align: justify;">Strong phenological shifts in response to changes in climatic conditions have been reported for many species, including amphibians, which are expected to breed earlier. Phenological shifts in breeding are observed i...Climate change, Population ecology, ZoologySergio EstayAnonymous, Nigel Yoccoz2022-08-18 08:25:21 View
24 May 2023
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Evolutionary determinants of reproductive seasonality: a theoretical approach

When does seasonal reproduction evolve?

Recommended by ORCID_LOGO based on reviews by Francois-Xavier Dechaume-Moncharmont, Nigel Yoccoz and 1 anonymous reviewer

Have you ever wondered why some species breed seasonally while others do not? You might think it is all down to lattitude and the harshness of winters but it turns out it is quite a bit more complicated than that. A consequence of this is that climate change may result in the evolution of the degree of seasonal reproduction, with some species perhaps becoming less seasonal and others more so even in the same habitat. 

Burtschell et al. (2023) investigated how various factors influence seasonal breeding by building an individual-based model of a baboon population from which they calculated the degree of seasonality for the fittest reproductive strategy. They then altered key aspects of their model to examine how these changes impacted the degree of seasonality in the reproductive strategy. What they found is fascinating. 

The degree of seasonality in reproductive strategy is expected to increase with increased seasonality in the environment, decreased food availability, increased energy expenditure, and how predictable resource availability is. Interestingly, neither female cycle length nor extrinsic infant mortality influenced the degree of seasonality in reproduction.

What this means in reality for seasonal species is more challenging to understand. Some environments appear to be becoming more seasonal yet less predictable, and some species appear to be altering their daily energy budgets in response to changing climate in quite complex ways. As with pretty much everything in biology, Burtschell et al.'s work reveals much nuance and complexity, and that predicting how species might alter their reproductive timing is fraught with challenges.

The paper is very well written. With a simpler model it may have proven possible to achieve analytical solutions, but this is a very minor gripe. The reviewers were positive about the paper, and I have little doubt it will be well-cited. 

REFERENCES

Burtschell L, Dezeure J, Huchard E, Godelle B (2023) Evolutionary determinants of reproductive seasonality: a theoretical approach. bioRxiv, 2022.08.22.504761, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.08.22.504761

Evolutionary determinants of reproductive seasonality: a theoretical approachLugdiwine Burtschell, Jules Dezeure, Elise Huchard, Bernard Godelle<p style="text-align: justify;">Reproductive seasonality is a major adaptation to seasonal cycles and varies substantially among organisms. This variation, which was long thought to reflect a simple latitudinal gradient, remains poorly understood ...Evolutionary ecology, Life history, Theoretical ecologyTim Coulson Nigel Yoccoz2022-08-23 21:37:28 View
20 Sep 2024
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Body mass change over winter is consistently sex-specific across roe deer (Capreolus capreolus) populations

Is it sexual mass dimorphism season?

Recommended by based on reviews by Patrick Bergeron, Philip McLoughlin and Achaz von Hardenberg

Polygyny is assumed to have led to the evolution of strong sexual size dimorphism (SSD) in mammals, males often being heavier or showing more developed armaments than females (Weckerly 1998; Loison et al. 1999; Pérez‐Barbería et al. 2002).  SSD generally increases with the degree of polygyny of the species. However, the degree of SSD, and particularly of sexual mass dimorphism, is not fixed for each species, and differences exist between populations (Blanckenhorn et al. 2006; Cox & Calsbeek 2010) or even between seasons within populations (Rughetti & Festa‐Bianchet 2011).

In this study, Hewison et al. propose that studying seasonal variation in sexual mass dimorphism and how this can be affected by winter harshness and latitude allows us to better assess the energetic costs associated with the eco-evolutionary constraints acting on each sex. To achieve their goal, Hewison et al. use a formidable, long-term dataset of over 7,000 individuals, in five roe deer populations (Capreolus capreolus), from south-west France and Sweden.

According to the authors, sexual mass dimorphism should be at its lowest in early spring in this species due to a stronger trade-off between antler growth and body weight maintenance in males over winter than in females. Furthermore, harsher conditions, varying both in time and space (i.e., Sweden vs. France), should increase winter weight loss, and thus, mass change differences between the sexes should be stronger and show more variation in Sweden than in France.


Their results support their hypotheses. In the two Swedish populations, males lost more mass than females. In the three French populations, males maintain their body mass while females gain some over the winter. Because of these sex-dependent loss/gain in body mass, sexual dimorphism was stronger early in the winter and null at the onset of spring. Furthermore, sexual dimorphism was stronger in southern than in northern populations. In France, males weighed about 10% more than females, while they weighed about 5% more in Sweden. Roe deer, however, do not show any dimorphism early in the spring, when males start defending their territory. 


The authors also found more variation in mass change among years in Swedish than in French roe deer, suggesting a stronger effect of winter severity on the dynamics of mass change in northern than in southern populations. The authors interpret the decrease in sexual dimorphism throughout the winter by the fact that, during this period, the energetic cost paid by males associated with the growth of their antlers and the effort of establishing their mating territory. They thus attribute the greater mass change in males to the competitive allocation of resources to antler growth or body mass. They also discuss the low probability that such sex differences in mass change could be caused by females’ gestation in this species.


Interestingly, Hewison et al. found that individual differences represented more than 70% of the total variation in body mass, and the low estimated among-individual variance in slopes with time might indicate that, despite a lower SSD, selection pressures on body mass can still be maintained at times when body mass may play an important role, such as in spring with territorial defense or later during mating (Vanpé et al. 2010). 


I recommend this article because it produces strong results, which show, without a shadow of a doubt, sex differences in their seasonal mass changes, resulting in a marked seasonal variation in SSD. The differences observed between southern and northern populations confirm the idea that the severity of the winters endured by these populations acts as a constraint on the deer's patterns of mass change. I hope this study will encourage more examinations of how eco-evolutionary constraints affect the sexual size dimorphism.

References

Blanckenhorn, W. U., Stillwell, R. C., Young, K. A., Fox, C. W., & Ashton, K. G. (2006). When Rensch meets Bergmann: does sexual size dimorphism change systematically with latitude? Evolution, 60(10), 2004-2011. https://doi.org/10.1554/06-110.1

Cox, R. M., & Calsbeek, R. (2010). Sex-specific selection and intraspecific variation in sexual size dimorphism. Evolution, 64(3), 798-809. https://doi.org/10.1111/j.1558-5646.2009.00851.x

Hewison M, Bonnot N, Gaillard JM, Kjellander P, Lemaitre J-F, Morellet N. and Pellerin M (2024) Body mass change over winter is consistently sex-specific across roe deer (Capreolus capreolus) populations. bioRxiv, ver.4 peer-reviewed and recommended by PCI Ecology https://doi.org/10.1101/2022.09.09.507329

Loison, A., Gaillard, J. M., Pélabon, C., & Yoccoz, N. G. (1999). What factors shape sexual size dimorphism in ungulates? Evolutionary Ecology Research, 1(5), 611-633. https://www.evolutionary-ecology.com/issues/v01n05/jjar1019.pdf

Pérez‐Barbería, F. J., Gordon, I. J., & Pagel, M. (2002). The origins of sexual dimorphism in body size in ungulates. Evolution, 56(6), 1276-1285. https://doi.org/10.1111/j.0014-3820.2002.tb01438.x

Rughetti, M., & Festa‐Bianchet, M. (2011). Seasonal changes in sexual size dimorphism in northern chamois. Journal of Zoology, 284(4), 257-264. https://doi.org/10.1111/j.1469-7998.2011.00800.x

Vanpé, C., Gaillard, J. M., Kjellander, P., Liberg, O., Delorme, D., & Hewison, A. M. (2010). Assessing the intensity of sexual selection on male body mass and antler length in roe deer Capreolus capreolus: is bigger better in a weakly dimorphic species? Oikos, 119(9), 1484-1492. https://doi.org/10.1111/j.1600-0706.2010.18312.x

Weckerly, F. W. (1998). Sexual-size dimorphism: influence of mass and mating systems in the most dimorphic mammals. Journal of Mammalogy, 79(1), 33-52. https://doi.org/10.2307/1382840

Body mass change over winter is consistently sex-specific across roe deer (*Capreolus capreolus*) populationsMark Hewison, Nadège Bonnot, Jean-Michel Gaillard, Petter Kjellander, Jean-François Lemaitre, Nicolas Morellet & Maryline Pellerin<p>In most polygynous vertebrates, males must allocate energy to growing secondary sexual characteristics, such as ornaments or weapons, that they require to attract and defend potential mates, impacting body condition and potentially entailing fi...Behaviour & Ethology, Life historyDenis Réale2022-09-16 15:41:53 View
31 May 2023
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Conservation networks do not match the ecological requirements of amphibians

Amphibians under scrutiny - When human-dominated landscape mosaics are not in full compliance with their ecological requirements

Recommended by ORCID_LOGO based on reviews by Peter Vermeiren and 1 anonymous reviewer

Among vertebrates, amphibians are one of the most diverse groups with more than 7,000 known species. Amphibians occupy various ecosystems, including forests, wetlands, and freshwater habitats. Amphibians are known to be highly sensitive to changes in their environment, particularly to water quality and habitat degradation, so that monitoring abundance of amphibian populations can provide early warning signs of ecosystem disturbances that may also affect other organisms including humans (Bishop et al., 2012). Accordingly, efforts in habitat preservation and sustainable land and water management are necessary to safeguard amphibian populations.

In this context, Matutini et al. (2023) compared ecological requirements of amphibian species with the quality of agricultural landscape mosaics. Doing so, they identified critical gaps in existing conservation tools that include protected areas, green infrastructures, and inventoried sites. Matutini et al. (2023) focused on nine amphibian species in the Pays-de-la-Loire region where the landscape has been fashioned over the years by human activities. Three of the chosen amphibian species are living in a dense hedgerow mosaic landscape, while five others are more generalists.

Matutini et al. (2023) established multi-species habitat suitability maps, together with their levels of confidence, by combining single species maps with a probabilistic stacking method at 500-m resolution. From these maps, habitats were classified in five categories, from not suitable to highly suitable. Then, the circuit theory was used to map the potential connections between each highly suitable patch at the regional scale. Finally, comparing suitability maps with existing conservation tools, Matutini et al. (2023) were able to assess their coverage and efficiency.

Whatever their species status (endangered or not), Matutini et al. (2023) highlighted some discrepancies between the ecological requirements of amphibians in terms of habitat quality and the conservation tools of the landscape mosaic within which they are evolving. More specifically, Matutini et al. (2023) found that protected areas and inventoried sites covered only a small proportion of highly suitable habitats, while green infrastructures covered around 50% of the potential habitat for amphibian species. Such a lack of coverage and efficiency of protected areas brings to light that geographical sites with amphibian conservation challenges are known but not protected. Regarding the landscape fragmentation, Matutini et al. (2023) found that generalist amphibian species have a more homogeneous distribution of suitable habitats at the regional scale. They also identified two bottlenecks between two areas of suitable habitats, a situation that could prove critical to amphibian movements if amphibians were forced to change habitats to global change.

In conclusion, Matutini et al. (2023) bring convincing arguments in support of land-use species-conservation planning based on a better consideration of human-dominated landscape mosaics in full compliance with ecological requirements of the species that inhabit the regions concerned.

References

Bishop, P.J., Angulo, A., Lewis, J.P., Moore, R.D., Rabb, G.B., Moreno, G., 2012. The Amphibian Extinction Crisis - what will it take to put the action into the Amphibian Conservation Action Plan? Sapiens - Surveys and Perspectives Integrating Environment and Society 5, 1–16. http://journals.openedition.org/sapiens/1406

Matutini, F., Baudry, J., Fortin, M.-J., Pain, G., Pithon, J., 2023. Conservation networks do not match ecological requirements of amphibians. bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.07.18.500425

Conservation networks do not match the ecological requirements of amphibiansMatutini Florence, Jacques Baudry, Marie-Josée Fortin, Guillaume Pain, Joséphine Pithon<p style="text-align: justify;">1. Amphibians are among the most threatened taxa as they are highly sensitive to habitat degradation and fragmentation. They are considered as model species to evaluate habitats quality in agricultural landscapes. I...Biodiversity, Biogeography, Human impact, Landscape ecology, Macroecology, Spatial ecology, Metacommunities & Metapopulations, Species distributions, Terrestrial ecologySandrine Charles2022-09-20 14:40:03 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
28 Dec 2022
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Deleterious effects of thermal and water stresses on life history and physiology: a case study on woodlouse

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

Recommended by ORCID_LOGO based on reviews by Aaron Yilmaz and Michael Morris

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

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

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

References:

[1] Depeux C, Branger A, Moulignier T, Moreau J, Lemaître J-F, Dechaume-Moncharmont F-X, Laverre T, Pauhlac H, Gaillard J-M, Beltran-Bech S (2022) Deleterious effects of thermal and water stresses on life history and physiology: a case study on woodlouse. bioRxiv, 2022.09.26.509512., ver. 3 peer-reviewd and recommended by PCI Ecology. https://doi.org/10.1101/2022.09.26.509512

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

[3] Hassall M, Helden A, Goldson A, Grant A (2005) Ecotypic differentiation and phenotypic plasticity in reproductive traits of Armadillidium vulgare (Isopoda: Oniscidea). Oecologia 143: 51–60.​ https://doi.org/10.1007/s00442-004-1772-3

Deleterious effects of thermal and water stresses on life history and physiology: a case study on woodlouseCharlotte Depeux, Angele Branger, Theo Moulignier, Jérôme Moreau, Jean-Francois Lemaitre, Francois-Xavier Dechaume-Moncharmont, Tiffany Laverre, Hélène Paulhac, Jean-Michel Gaillard, Sophie Beltran-Bech<p>We tested independently the influences of increasing temperature and decreasing moisture on life history and physiological traits in the arthropod <em>Armadillidium vulgare</em>. Both increasing temperature and decreasing moisture led individua...Biodiversity, Evolutionary ecology, Experimental ecology, Life history, Physiology, Terrestrial ecology, ZoologyAniruddha Belsare2022-09-28 13:13:47 View
01 Oct 2023
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Seasonality of host-seeking Ixodes ricinus nymph abundance in relation to climate

Assessing seasonality of tick abundance in different climatic regions

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

Tick-borne pathogens are considered as one of the major threats to public health – Lyme borreliosis being a well-known example of such disease. Global change – from climate change to changes in land use or invasive species – is playing a role in the increased risk associated with these pathogens. An important aspect of our knowledge of ticks and their associated pathogens is seasonality – one component being the phenology of within-year tick occurrences. This is important both in terms of health risk – e.g., when is the risk of encountering ticks high – and ecological understanding, as tick dynamics may depend on the weather as well as different hosts with their own dynamics and habitat use.

Hoch et al. (2023) provide a detailed data set on the phenology of one species of tick, Ixodes ricinus, in 6 different locations of France. Whereas relatively cool sites showed a clear peak in spring-summer, warmer sites showed in addition relatively high occurrences in fall-winter, with a minimum in late summer-early fall. Such results add robust data to the existing evidence of the importance of local climatic patterns for explaining tick phenology.

Recent analyses have shown that the phenology of Lyme borreliosis has been changing in northern Europe in the last 25 years, with seasonal peaks in cases occurring now 6 weeks earlier (Goren et al. 2023). The study by Hoch et al. (2023) is of too short duration to establish temporal changes in phenology (“only” 8 years, 2014-2021, see also Wongnak et al 2021 for some additional analyses; given the high year-to-year variability in weather, establishing phenological changes often require longer time series), and further work is needed to get better estimates of these changes and relate them to climate, land-use, and host density changes. Moreover, the phenology of ticks may also be related to species-specific tick phenology, and different tick species do not respond to current changes in identical ways (see for example differences between the two Ixodes species in Finland; Uusitalo et al. 2022). An efficient surveillance system requires therefore an adaptive monitoring design with regard to the tick species as well as the evolving causes of changes.

References

Goren, A., Viljugrein, H., Rivrud, I. M., Jore, S., Bakka, H., Vindenes, Y., & Mysterud, A. (2023). The emergence and shift in seasonality of Lyme borreliosis in Northern Europe. Proceedings of the Royal Society B: Biological Sciences, 290(1993), 20222420. https://doi.org/10.1098/rspb.2022.2420

Hoch, T., Madouasse, A., Jacquot, M., Wongnak, P., Beugnet, F., Bournez, L., . . . Agoulon, A. (2023). Seasonality of host-seeking Ixodes ricinus nymph abundance in relation to climate. bioRxiv, ver.4 peer-reviewed and recommended by Peer Community In Ecology. https://doi.org/10.1101/2022.07.25.501416

Uusitalo, R., Siljander, M., Lindén, A., Sormunen, J. J., Aalto, J., Hendrickx, G., . . . Vapalahti, O. (2022). Predicting habitat suitability for Ixodes ricinus and Ixodes persulcatus ticks in Finland. Parasites & Vectors, 15(1), 310. https://doi.org/10.1186/s13071-022-05410-8

Wongnak, P., Bord, S., Jacquot, M., Agoulon, A., Beugnet, F., Bournez, L., . . . Chalvet-Monfray, K. (2022). Meteorological and climatic variables predict the phenology of Ixodes ricinus nymph activity in France, accounting for habitat heterogeneity. Scientific Reports, 12(1), 7833. https://doi.org/10.1038/s41598-022-11479-z

Seasonality of host-seeking *Ixodes ricinus* nymph abundance in relation to climateThierry Hoch, Aurélien Madouasse, Maude Jacquot, Phrutsamon Wongnak, Fréderic Beugnet, Laure Bournez, Jean-François Cosson, Frédéric Huard, Sara Moutailler, Olivier Plantard, Valérie Poux, Magalie René-Martellet, Muriel Vayssier-Taussat, Hélène Ve...<p style="text-align: justify;">There is growing concern about climate change and its impact on human health. Specifically, global warming could increase the probability of emerging infectious diseases, notably because of changes in the geographic...Climate change, Population ecology, Statistical ecologyNigel Yoccoz2022-10-14 18:43:56 View
29 May 2023
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Using integrated multispecies occupancy models to map co-occurrence between bottlenose dolphins and fisheries in the Gulf of Lion, French Mediterranean Sea

Mapping co-occurence of human activities and wildlife from multiple data sources

Recommended by based on reviews by Mason Fidino and 1 anonymous reviewer

Two fields of research have grown considerably over the past twenty years: the investigation of human-wildlife conflicts (e.g. see Treves & Santiago-Ávila 2020), and multispecies occupancy modelling (Devarajan et al. 2020). In their recent study, Lauret et al. (2023) combined both in an elegant methodological framework, applied to the study of the co-occurrence of fishing activities and bottlenose dolphins in the French Mediterranean.

A common issue with human-wildlife conflicts (and, in particular, fishery by-catch) is that data is often only available from those conflicts or interactions, limiting the validity of the predictions (Kuiper et al. 2022). Lauret et al. use independent data sources informing the occurrence of fishing vessels and dolphins, combined in a Bayesian multispecies occupancy model where vessels are "the other species". I particularly enjoyed that approach, as integration of human activities in ecological models can be extremely complex, but can also translate in phenomena that can be captured as one would of individuals of a species, as long as the assumptions are made clearly. Here, the model is made more interesting by accounting for environmental factors (seabed depth) borrowing an approach from Generalized Additive Models in the Bayesian framework. While not pretending to provide (yet) practical recommendations to help conserve bottlenose dolphins (and other wildlife conflicts), this study and the associated code are a promising step in that direction.

REFERENCES

Devarajan, K., Morelli, T.L. & Tenan, S. (2020), Multi-species occupancy models: review, roadmap, and recommendations. Ecography, 43: 1612-1624. https://doi.org/10.1111/ecog.04957

Kuiper, T., Loveridge, A.J. and Macdonald, D.W. (2022), Robust mapping of human–wildlife conflict: controlling for livestock distribution in carnivore depredation models. Anim. Conserv., 25: 195-207. https://doi.org/10.1111/acv.12730

Lauret V, Labach H, David L, Authier M, & Gimenez O (2023) Using integrated multispecies occupancy models to map co-occurrence between bottlenose dolphins and fisheries in the Gulf of Lion, French Mediterranean Sea. Ecoevoarxiv, ver. 2 peer-reviewed and recommended by PCI Ecology. https://doi.org/10.32942/osf.io/npd6u

Treves, A. & Santiago-Ávila, F.J. (2020). Myths and assumptions about human-wildlife conflict and coexistence. Conserv. Biol. 34, 811–818.  https://doi.org/10.1111/cobi.13472

Using integrated multispecies occupancy models to map co-occurrence between bottlenose dolphins and fisheries in the Gulf of Lion, French Mediterranean SeaValentin Lauret, Hélène Labach, Léa David, Matthieu Authier, Olivier Gimenez<p style="text-align: justify;">In the Mediterranean Sea, interactions between marine species and human activities are prevalent. The coastal distribution of bottlenose dolphins (<em>Tursiops truncatus</em>) and the predation pressure they put on ...Marine ecology, Population ecology, Species distributionsPaul Caplat2022-10-21 11:13:36 View