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03 Oct 2023
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Integrating biodiversity assessments into local conservation planning: the importance of assessing suitable data sources

Biodiversity databases are ever more numerous, but can they be used reliably for Species Distribution Modelling?

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

Proposing efficient guidelines for biodiversity conservation often requires the use of forecasting tools. Species Distribution Models (SDM) are more and more used to predict how the distribution of a species will react to environmental change, including any large-scale management actions that could be implemented. Their use is also boosted by the increase of publicly available biodiversity databases[1]. The now famous aphorism by George Box "All models are wrong but some are useful"[2] very well summarizes that the outcome of a model must be adjusted to, and will depend on, the data that are used to parameterize it. The question of the reliability of using biodiversity databases to parameterize biodiversity models such as SDM –but the question would also apply to other kinds of biodiversity models, e.g. Population Viability Analysis models[3]– is key to determine the confidence that can be placed in model predictions. This point is often overlooked by some categories of biodiversity conservation stakeholders, in particular the fact that some data were collected using controlled protocols while others are opportunistic. 

In this study[4], the authors use a collection of databases covering a range of species as well as of geographic scales in France and using different data collection and validation approaches as a case study to evaluate the impact of data quality when performing Strategic Environmental Assessment (SEA). Among their conclusions, the fact that a large-scale database (what they call the “country” level) is necessary to reliably parameterize SDM. Besides this and other conclusions of their study, which are likely to be in part specific to their case study –unfortunately for its conservation, biodiversity is complex and varies a lot–, the merit of this work lies in the approach used to test the impact of data on model predictions.

References

1.  Feng, X. et al. A review of the heterogeneous landscape of biodiversity databases: Opportunities and challenges for a synthesized biodiversity knowledge base. Global Ecology and Biogeography 31, 1242–1260 (2022). https://doi.org/10.1111/geb.13497

2.  Box, G. E. P. Robustness in the Strategy of Scientific Model Building. in Robustness in Statistics (eds. Launer, R. L. & Wilkinson, G. N.) 201–236 (Academic Press, 1979). https://doi.org/10.1016/B978-0-12-438150-6.50018-2.

3.  Beissinger, S. R. & McCullough, D. R. Population Viability Analysis. (The University of Chicago Press, 2002).

4.  Ferraille, T., Kerbiriou, C., Bigard, C., Claireau, F. & Thompson, J. D. (2023) Integrating biodiversity assessments into local conservation planning: the importance of assessing suitable data sources. bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Ecology.  https://doi.org/10.1101/2023.05.09.539999

Integrating biodiversity assessments into local conservation planning: the importance of assessing suitable data sourcesThibaut Ferraille, Christian Kerbiriou, Charlotte Bigard, Fabien Claireau, John D. Thompson<p>Strategic Environmental Assessment (SEA) of land-use planning is a fundamental tool to minimize environmental impacts of artificialization. In this context, Systematic Conservation Planning (SCP) tools based on Species Distribution Models (SDM)...Biodiversity, Conservation biology, Species distributions, Terrestrial ecologyNicolas Schtickzelle2023-05-11 09:41:05 View
12 Jan 2024
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Methods for tagging an ectoparasite, the salmon louse Lepeophtheirus salmonis

Marking invertebrates using RFID tags

Recommended by ORCID_LOGO based on reviews by Simon Blanchet and 1 anonymous reviewer

Guiding and monitoring the efficiency of conservation efforts needs robust scientific background information, of which one key element is estimating wildlife abundance and its spatial and temporal variation. As raw counts are by nature incomplete counts of a population, correcting for detectability is required (Clobert, 1995; Turlure et al., 2018). This can be done with Capture-Mark-Recapture protocols (Iijima, 2020). Techniques for marking individuals are diverse, e.g. writing on butterfly wings, banding birds, or using natural specific patterns in the individual’s body such as leopard fur or whale tail. Advancement in technology opens new opportunities for developing marking techniques, including strategies to limit mark identification errors (Burchill & Pavlic, 2019), and for using active marks that can transmit data remotely or be read automatically.

The details of such methodological developments frequently remain unpublished, the method being briefly described in studies that use it. For a few years, there has been however a renewed interest in proper publishing of methods for ecology and evolution. This study by Folk & Mennerat (2023) fits in this context, offering a nice example of detailed description and testing of a method to mark salmon ectoparasites using RFID tags. Such tags are extremely small, yet easy to use, even with automatic recording procedure. The study provides a very good basis protocol that should help researchers working for small species, in particular invertebrates. The study is complemented by a video illustrating the placement of the tag so the reader who would like to replicate the procedure can get a very precise idea of it.

References

Burchill, A. T., & Pavlic, T. P. (2019). Dude, where’s my mark? Creating robust animal identification schemes informed by communication theory. Animal Behaviour, 154, 203–208. https://doi.org/10.1016/j.anbehav.2019.05.013

Clobert, J. (1995). Capture-recapture and evolutionary ecology: A difficult wedding ? Journal of Applied Statistics, 22(5–6), 989–1008.

Folk, A., & Mennerat, A. (2023). Methods for tagging an ectoparasite, the salmon louse Lepeophtheirus salmonis (p. 2023.08.31.555695). bioRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2023.08.31.555695

Iijima, H. (2020). A Review of Wildlife Abundance Estimation Models: Comparison of Models for Correct Application. Mammal Study, 45(3), 177–188. https://doi.org/10.3106/ms2019-0082

Turlure, C., Pe’er, G., Baguette, M., & Schtickzelle, N. (2018). A simplified mark–release–recapture protocol to improve the cost effectiveness of repeated population size quantification. Methods in Ecology and Evolution, 9(3), 645–656. https://doi.org/10.1111/2041-210X.12900

 

Methods for tagging an ectoparasite, the salmon louse *Lepeophtheirus salmonis*Alexius Folk, Adele Mennerat<p style="text-align: justify;">Monitoring individuals within populations is a cornerstone in evolutionary ecology, yet individual tracking of invertebrates and particularly parasitic organisms remains rare. To address this gap, we describe here a...Dispersal & Migration, Evolutionary ecology, Host-parasite interactions, Marine ecology, Parasitology, Terrestrial ecology, ZoologyNicolas Schtickzelle2023-09-04 15:25:08 View
14 Nov 2022
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Estimating abundance of a recovering transboundary brown bear population with capture-recapture models

A new and efficient approach to estimate, from protocol and opportunistic data, the size and trends of populations: the case of the Pyrenean brown bear

Recommended by based on reviews by Tim Coulson, Romain Pigeault and ?

In this study, the authors report a new method for estimating the abundance of the Pyrenean brown bear population. Precisely, the methodology involved aims to apply Pollock's closed robust design (PCRD) capture-recapture models to estimate population abundance and trends over time. Overall, the results encourage the use of PCRD to study populations' demographic rates, while minimizing biases due to inter-individual heterogeneity in detection probabilities.

Estimating the size and trends of animal population over time is essential for informing conservation status and management decision-making (Nichols & Williams 2006). This is particularly the case when the population is small, geographically scattered, and threatened. Although several methods can be used to estimate population abundance, they may be difficult to implement when individuals are rare, elusive, solitary, largely nocturnal, highly mobile, and/or occupy large home ranges in remote and/or rugged habitats. Moreover, in such standard methods,

  • the population is assumed to be closed both geographically (no immigration nor emigration) and demographically (no births nor deaths) and
  • all individuals are assumed to have identical detection probabilities regardless of their individual attributes (e.g., age, body mass, social status) and habitat features (home-range location and composition) (Otis et al. 1978).

However, these conditions are rarely met in real populations, such as wild mammals (e.g., Bellemain et al. 2005; Solbert et al. 2006), and therefore the risk of underestimating population size can rapidly increase because the assumption of perfect detection of all individuals in the population is violated.

Focusing on the critically endangered Pyrenean brown bear that was close to extinction in the mid-1990s, the study by Vanpe et al. (2022), uses protocol and opportunistic data to describe a statistical modeling exercise to construct mark-recapture histories from 2008 to 2020. Among the data, the authors collected non-invasive samples such as a mixture of hair and scat samples used for genetic identification, as well as photographic trap data of recognized individuals. These data are then analyzed in RMark to provide detection and survival estimates. The final model (i.e. PCRD capture-recapture) is then used to provide Bayesian population estimates. Results show a five-fold increase in population size between 2008 and 2020, from 13 to 66 individuals. Thus, this study represents the first published annual abundance and temporal trend estimates of the Pyrenean brown bear population since 2008.

Then, although the results emphasize that the PCRD estimates were broadly close to the MRS counts and had reasonably narrow associated 95% Credibility Intervals, they also highlight that the sampling effort is different according to individuals. Indeed, as expected, the detection of an individual depends on

  • the intraspecific home range size variation that results in individuals that move the most being most likely to be detected and
  • the mortality rate which is higher on cubs than on adults and subadults (due to infanticide by males, predation, death of the mother, or abandonment).

Overall, the PCRD capture-recapture modelling approach, involved in this study, provides robust estimates of abundance and demographic rates of the Pyrenean brown bear population (with associated uncertainty) while minimizing and considering bias due to inter-individual heterogeneity in detection probabilities.

The authors conclude that mark-recapture provides useful population estimates and urge wildlife ecologists and managers to use robust approaches, such as the RDPC capture-recapture model, when studying large mammal populations. This information is essential to inform management decisions and assess the conservation status of populations.

 

References

Bellemain, E.V.A., Swenson, J.E., Tallmon, D., Brunberg, S. and Taberlet, P. (2005). Estimating population size of elusive animals with DNA from hunter-collected feces: four methods for brown bears. Cons. Biol. 19(1), 150-161. https://doi.org/10.1111/j.1523-1739.2005.00549.x

Nichols, J.D. and Williams, B.K. (2006). Monitoring for conservation. Trends Ecol. Evol. 21(12), 668-673. https://doi.org/10.1016/j.tree.2006.08.007

Otis, D.L., Burnham, K.P., White, G.C. and Anderson, D.R. (1978). Statistical inference from capture data on closed animal populations. Wildlife Monographs (62), 3-135.

Solberg, K.H., Bellemain, E., Drageset, O.M., Taberlet, P. and Swenson, J.E. (2006). An evaluation of field and non-invasive genetic methods to estimate brown bear (Ursus arctos) population size. Biol. Conserv. 128(2), 158-168. https://doi.org/10.1016/j.biocon.2005.09.025

Vanpé C, Piédallu B, Quenette P-Y, Sentilles J, Queney G, Palazón S, Jordana IA, Jato R, Elósegui Irurtia MM, de la Torre JS, and Gimenez O (2022) Estimating abundance of a recovering transboundary brown bear population with capture-recapture models. bioRxiv, 2021.12.08.471719, ver. 4 recommended and peer-reviewed by PCI Ecology. https://doi.org/10.1101/2021.12.08.471719

Estimating abundance of a recovering transboundary brown bear population with capture-recapture modelsCécile Vanpé, Blaise Piédallu, Pierre-Yves Quenette, Jérôme Sentilles, Guillaume Queney, Santiago Palazón, Ivan Afonso Jordana, Ramón Jato, Miguel Mari Elósegui Irurtia, Jordi Solà de la Torre, Olivier Gimenez<p>Estimating the size of small populations of large mammals can be achieved via censuses, or complete counts, of recognizable individuals detected over a time period: minimum detected (population) size (MDS). However, as a population grows larger...Conservation biology, Demography, Population ecologyNicolas BECH2022-01-20 10:49:59 View
30 May 2024
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Disentangling the effects of eutrophication and natural variability on macrobenthic communities across French coastal lagoons

Untangling Eutrophication Effects on Coastal Lagoon Ecosystems

Recommended by ORCID_LOGO based on reviews by Kaylee P. Smit, Matthew J. Pruden and Kendyl Wright

Disentangling the effects on ecosystem structure and functioning of natural and human-induced impacts in transitional waters is a great challenge in coast ecology. This is due to the observation that the ecosystems of transitional waters are naturally dynamic systems with characteristics of stressed systems. For example, the benthic communities present low species richness and high abundance of species with a high tolerance to variations, e.g., salinity. This general observation is known as the paradigm of the “Transitional Waters Quality Paradox” (Zaldívar et al., 2008) derived from the previously described “Estuarine Quality Paradox” (Elliott and Quintino, 2007). 

In Jones et al. (2024) “Disentangling the effects of eutrophication and natural variability on macrobenthic communities across French coastal lagoons”, a great diversity of lagoons is analyzed to disentangle the effects of eutrophication from those of natural environmental variability on benthic macroinvertebrates and understanding the links between environmental variables affecting benthic macroinvertebrates. These authors use a very elegant set of numerical approaches, including correlograms, linear models and variance partitioning. They apply this suite to a dataset of macrobenthic invertebrate abundances and environmental variables from 29 Mediterranean coastal lagoons in France.

Through this suite of analyses, they demonstrate the strong complexity of the mechanisms interplaying in a situation of eutrophication on lagoon macrobenthos. The mechanisms involved are direct, like toxicity, or indirect, for example, through modifications of the sediment's biogeochemistry. Such a result on the different interactions involved is very important in the context of the search for indicators to define ecosystem status. Improving the definition of metrics is essential in environmental management decisions.

References

Elliott, M. and Quintino, V. (2007) The estuarine quality paradox, environmental homeostasis and the difficulty of detecting anthropogenic stress in naturally stressed areas. Marine Pollution Bulletin 54, 640–645. https://doi.org/10.1016/j.marpolbul.2007.02.003

Jones et al. (2024) Disentangling the effects of eutrophication and natural variability on macrobenthic communities across French coastal lagoons bioRxiv, 2022.08.18.504439, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.08.18.504439

Zaldívar, J. (2008). Eutrophication in transitional waters: an overview. https://doi.org/10.1285/I18252273V2N1P1

Disentangling the effects of eutrophication and natural variability on macrobenthic communities across French coastal lagoonsAuriane G. Jones, Gauthier Schaal, Aurélien Boyé, Marie Creemers, Valérie Derolez, Nicolas Desroy, Annie Fiandrino, Théophile L. Mouton, Monique Simier, Niamh Smith, Vincent Ouisse<p style="text-align: justify;">Coastal lagoons are transitional ecosystems that host a unique diversity of species and support many ecosystem services. Owing to their position at the interface between land and sea, they are also subject to increa...Biodiversity, Community ecology, Ecosystem functioning, Marine ecologyNathalie Niquil Matthew J. Pruden2023-09-08 11:26:01 View
11 May 2020
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Interplay between historical and current features of the cityscape in shaping the genetic structure of the house mouse (Mus musculus domesticus) in Dakar (Senegal, West Africa)

Urban past predicts contemporary genetic structure in city rats

Recommended by based on reviews by Torsti Schulz, ? and 1 anonymous reviewer

Urban areas are expanding worldwide, and have become a dominant part of the landscape for many species. Urbanization can fragment pre-existing populations of vulnerable species leading to population declines and the loss of connectivity. On the other hand, expansion of urban areas can also facilitate the spread of human commensals including pests. Knowledge of the features of cityscapes that facilitate gene flow and maintain diversity of pests is thus key to their management and eradication.
Cities are complex mosaics of natural and manmade surfaces, and habitat quality is not only influenced by physical aspects of the cityscape but also by socioeconomic factors and human behaviour. Constant development means that cities also change rapidly in time; contemporary urban life reflects only a snapshot of the environmental conditions faced by populations. It thus remains a challenge to identify the features that actually drive ecology and evolution of populations in cities [1]. While several studies have highlighted strong urban clines in genetic structure and adaption [2], few have considered the influence of factors beyond physical aspects of the cityscape or historical processes.
In this paper, Stragier et al. [3] sought to identify the current and past features of the cityscape and socioeconomic factors that shape genetic structure and diversity of the house mouse (Mus musculus domesticus) in Dakar, Senegal. The authors painstakingly digitized historical maps of Dakar from the time of European settlement in 1862 to present. The authors found that the main spatial genetic cline was best explained by historical cityscape features, with higher apparent gene flow and genetic diversity in areas that were connected earlier to initial European settlements. Beyond the main trend of spatial genetic structure, they found further evidence that current features of the cityscape were important. Specifically, areas with low vegetation and poor housing conditions were found to support large, genetically diverse populations. The authors demonstrate that their results are reproducible using several statistical approaches, including modeling that explicitly accounts for spatial autocorrelation.
The work of Stragier et al. [3] thus highlights that populations of city-dwelling species are the product of both past and present cityscapes. Going forward, urban evolutionary ecologists should consider that despite the potential for rapid evolution in urban landscapes, the signal of a species’ colonization can remain for generations.

References

[1] Rivkin, L. R., Santangelo, J. S., Alberti, M. et al. (2019). A roadmap for urban evolutionary ecology. Evolutionary Applications, 12(3), 384-398. doi: 10.1111/eva.12734
[2] Miles, L. S., Rivkin, L. R., Johnson, M. T., Munshi‐South, J. and Verrelli, B. C. (2019). Gene flow and genetic drift in urban environments. Molecular ecology, 28(18), 4138-4151. doi: 10.1111/mec.15221
[3] Stragier, C., Piry, S., Loiseau, A., Kane, M., Sow, A., Niang, Y., Diallo, M., Ndiaye, A., Gauthier, P., Borderon, M., Granjon, L., Brouat, C. and Berthier, K. (2020). Interplay between historical and current features of the cityscape in shaping the genetic structure of the house mouse (Mus musculus domesticus) in Dakar (Senegal, West Africa). bioRxiv, 557066, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/557066

Interplay between historical and current features of the cityscape in shaping the genetic structure of the house mouse (Mus musculus domesticus) in Dakar (Senegal, West Africa)Claire Stragier, Sylvain Piry, Anne Loiseau, Mamadou Kane, Aliou Sow, Youssoupha Niang, Mamoudou Diallo, Arame Ndiaye, Philippe Gauthier, Marion Borderon, Laurent Granjon, Carine Brouat, Karine Berthier<p>Population genetic approaches may be used to investigate dispersal patterns of species living in highly urbanized environment in order to improve management strategies for biodiversity conservation or pest control. However, in such environment,...Biological invasions, Landscape ecology, Molecular ecologyMichelle DiLeo2019-02-22 08:36:13 View
21 Jan 2025
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Exploring Rubiaceae fungal endophytes across contrasting tropical forests, tree tissues, and developmental stages

The hidden diversity of fungal endophytes, associated with Rubiaceae of Costa Rican old-growth forests

Recommended by based on reviews by Marion Boisseaux and 1 anonymous reviewer

Endophytic fungi are expected to be hyperdiverse in tropical forests, and here is an article exploring their diversity, hidden in Rubiaceae leaves, in two old-growth forests of Costa Rica. Humberto Castillo-González et al. not only described their diversity, but also test for the impact of leaf development stage, tissue origin, and site location. They distinguish the different fungal lineages and do identify distinct indicators, showing that specialization of endophytic fungi could be related to other factors in tropical forests.

This article is a great example of fungal ecology in the tropics, interacting at fine and large scale with a diversity of hosts. It also invites to discuss the high specialization observed in the tropics, and the ecology of old-growth forests in Costa Rica.

References

Humberto Castillo-González, Jason C. Slot, Stephanie Yarwood, Priscila Chaverri (2025) Exploring Rubiaceae fungal endophytes across contrasting tropical forests, tree tissues, and developmental stages. bioRxiv, ver.3 peer-reviewed and recommended by PCI Ecology https://doi.org/10.1101/2024.02.13.580172

Exploring Rubiaceae fungal endophytes across contrasting tropical forests, tree tissues, and developmental stagesHumberto Castillo-González, Jason C. Slot, Stephanie Yarwood, Priscila Chaverri<p>Fungal endophytes play a pivotal role in tropical forest dynamics, influencing plant fitness through growth stimulation, disease suppression, stress tolerance, and nutrient mobilization. This study investigates the effects of region, leaf devel...Agroecology, Biodiversity, Community ecology, Microbial ecology & microbiology, Mycology, SymbiosisMelanie Roy2024-02-15 22:42:10 View
13 Jul 2020
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Preregistration - The effect of dominance rank on female reproductive success in social mammals

Why are dominant females not always showing higher reproductive success? A preregistration of a meta-analysis on social mammals

Recommended by ORCID_LOGO based on reviews by Bonaventura Majolo and 1 anonymous reviewer

In social species conflicts among group members typically lead to the formation of dominance hierarchies with dominant individuals outcompeting other groups members and, in some extreme cases, suppressing reproduction of subordinates. It has therefore been typically assumed that dominant individuals have a higher breeding success than subordinates. However, previous work on mammals (mostly primates) revealed high variation, with some populations showing no evidence for a link between female dominance reproductive success, and a meta-analysis on primates suggests that the strength of this relationship is stronger for species with a longer lifespan [1]. Therefore, there is now a need to understand 1) whether dominance and reproductive success are generally associated across social mammals (and beyond) and 2) which factors explains the variation in the strength (and possibly direction) of this relationship.
In their preregistration, Shivani et al. [2] plan to perform a meta-analysis on 86 social mammal species to address these two points. More specifically, they will investigate whether the relationship between female dominance and reproductive success vary according to life history traits (e.g. stronger for species with large litter size), ecological conditions (e.g. stronger when resources are limited) and the social environment (e.g. stronger for cooperative breeders than for plural breeders).
The two reviewers and I were particularly positive and enthusiastic about this preregistration and only had minor comments that were nicely addressed by the authors. We found the background well-grounded in the existing literature and that the predictions were therefore clear and well-motivated. The methods were particularly transparent with a nicely annotated R script and the authors even simulated a dataset with the same structure as the actual data in order to make sure that the coding of the data handling and statistical analyses were appropriate (without being tempted to look at model outputs from the true dataset).
Perhaps one limitation to keep in mind once we will have the chance to look at the outcome of this study if that the dataset may not be fully representative of social species with dominance hierarchies. For example, the current dataset contains only one aquatic mammal (Mirounga angustirostris) as far as I can see, which is likely due to a lack of knowledge on such systems. Furthermore, not only mammals exhibit dominance hierarchies and it will be interesting to see if the results of the proposed study hold for other social taxa (and if not, what may explain their differences).
That being said, the proposed study will already offer a much broader overview of the relationship between dominance and reproductive success in animal societies and a better understanding for its variation. The reviewers and I believe it will make an important contribution to the fields of socio-ecology and evolutionary ecology. I therefore strongly recommend this preregistration and we are particularly looking forward to seeing the outcome of this exciting study.

References

[1] Majolo, B., Lehmann, J., de Bortoli Vizioli, A., & Schino, G. (2012). Fitness‐related benefits of dominance in primates. American journal of physical anthropology, 147(4), 652-660. doi: 10.1002/ajpa.22031
[2] Shivani, Huchard, E., Lukas, D. (2020). Preregistration - The effect of dominance rank on female reproductive success in social mammals In principle acceptance by PCI Ecology of the version 1.2 on 07 July 2020. https://github.com/dieterlukas/FemaleDominanceReproductionMetaAnalysis/blob/trunk/PreregistrationMetaAnalysis_RankSuccess.Rmd

Preregistration - The effect of dominance rank on female reproductive success in social mammalsShivani, Elise Huchard, Dieter Lukas<p>Life in social groups, while potentially providing social benefits, inevitably leads to conflict among group members. In many social mammals, such conflicts lead to the formation of dominance hierarchies, where high-ranking individuals consiste...Behaviour & Ethology, Meta-analyses, Preregistrations, Social structure, ZoologyMatthieu Paquet Bonaventura Majolo, Anonymous2020-04-06 17:42:37 View
02 Aug 2022
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The effect of dominance rank on female reproductive success in social mammals

When do dominant females have higher breeding success than subordinates? A meta-analysis across social mammals.

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

In this meta-analysis, Shivani et al. [1] investigate 1) whether dominance and reproductive success are generally associated across social mammals and 2) whether this relationship varies according to a) life history traits (e.g., stronger for species with large litter size), b) ecological conditions (e.g., stronger when resources are limited) and c) the social environment (e.g., stronger for cooperative breeders than for plural breeders). Generally, the results are consistent with their predictions, except there was no clear support for this relationship to be conditional on the ecological conditions. considered

As I have previously recommended the preregistration of this study [2,3], I do not have much to add here, as such recommendation should not depend on the outcome of the study. What I would like to recommend is the whole scientific process performed by the authors, from preregistration sent for peer review, to preprint submission and post-study peer review. It is particularly recommendable to notice that this project was a Masters student project, which shows that it is possible and worthy to preregister studies, even for such rather short-term projects. I strongly congratulate the authors for choosing this process even for an early career short-term project. I think it should be made possible for short-term students to conduct a preregistration study as a research project, without having to present post-study results. I hope this study can encourage a shift in the way we sometimes evaluate students’ projects.

I also recommend the readers to look into the whole pre- and post- study reviewing history of this manuscript and the associated preregistration, as it provides a better understanding of the process and a good example of the associated challenges and benefits [4]. It was a really enriching experience and I encourage others to submit and review preregistrations and registered reports!

 

References

[1] Shivani, Huchard, E., Lukas, D. (2022). The effect of dominance rank on female reproductive success in social mammals. EcoEvoRxiv, rc8na, ver. 10 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.32942/osf.io/rc8na

[2] Shivani, Huchard, E., Lukas, D. (2020). Preregistration - The effect of dominance rank on female reproductive success in social mammals In principle acceptance by PCI Ecology of the version 1.2 on 07 July 2020. https://dieterlukas.github.io/Preregistration_MetaAnalysis_RankSuccess.html

[3] Paquet, M. (2020) Why are dominant females not always showing higher reproductive success? A preregistration of a meta-analysis on social mammals. Peer Community in Ecology, 100056. https://doi.org/10.24072/pci.ecology.100056

[4] Parker, T., Fraser, H., & Nakagawa, S. (2019). Making conservation science more reliable with preregistration and registered reports. Conservation Biology, 33(4), 747-750. https://doi.org/10.1111/cobi.13342

The effect of dominance rank on female reproductive success in social mammalsShivani, Elise Huchard, Dieter Lukas<p>Life in social groups, while potentially providing social benefits, inevitably leads to conflict among group members. In many social mammals, such conflicts lead to the formation of dominance hierarchies, where high-ranking individuals consiste...Behaviour & Ethology, Meta-analysesMatthieu Paquet2021-10-13 18:26:42 View
31 May 2022
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Sexual coercion in a natural mandrill population

Rare behaviours can have strong effects: evidence for sexual coercion in mandrills

Recommended by ORCID_LOGO based on reviews by Micaela Szykman Gunther and 1 anonymous reviewer

Sexual coercion can be defined as the use by a male of force, or threat of force, which increases the chances that a female will mate with him at a time when she is likely to be fertile, and/or decrease the chances that she will mate with other males, at some cost to the female (Smuts & Smuts 1993). It has been evidenced in a wide range of species and may play an important role in the evolution of sexual conflict and social systems. However, identifying sexual coercion in natural systems can be particularly challenging. Notably, while male behaviour may have immediate consequences on mating success (“harassment”), the mating benefits may be delayed in time (“intimidation”), and in such cases, evidencing coercion requires detailed temporal data at the individual level. Moreover, in some species male aggressive behaviours may be subtle or rare and hence hardly observed, yet still have important effects on female mating probability and fitness. Therefore, investigating the occurrence and consequences of sexual coercion in such species is particularly relevant but studying it in a statistically robust way is likely to require a considerable amount of time spent observing individuals.

In this paper, Smit et al. (2022) test three clear predictions of the sexual coercion hypothesis in a natural population of Mandrills, where severe male aggression towards females is rare: (1) male aggression is more likely on sexually receptive females than on females in other reproductive states, (2) receptive females are more likely to be injured and (3) male aggression directed towards females is positively related to subsequent probability of copulation between those dyads. They also tested an alternative hypothesis, the “aggressive male phenotype” under which the correlation between male aggression towards females and subsequent mating could be statistically explained by male overall aggressivity. In agreement with the three predictions of the sexual coercion hypothesis, (1) male aggression was on average 5 times more likely, and (2) injuries twice as likely, to be observed on sexually receptive females than on females in other reproductive states and (3) copulation between males and sexually receptive females was twice more likely to be observed when aggression by this male was observed on the female before sexual receptivity. There was no support for the aggressive male hypothesis.

The reviewers and I were highly positive about this study, notably regarding the way it is written and how the predictions are carefully and clearly stated, tested, interpreted, and discussed.

This study is a good illustration of a case where some behaviours may not be common or obvious yet have strong effects and likely important consequences and thus be clearly worth studying. More generally, it shows once more the importance of detailed long-term studies at the individual level for our understanding of the ecology and evolution of wild populations.

It is also a good illustration of the challenges faced, when comparing the likelihood of contrasting hypotheses means we need to alter sample sizes and/or the likelihood to observe at all some behaviours. For example, observing copulation within minutes after aggression (and therefore, showing statistical support for “harassment”) is inevitably less likely than observing copulations on the longer-term (and therefore showing statistical support for “intimidation”, when of course effort is put into recording such behavioural data on the long-term). Such challenges might partly explain some apparently intriguing results. For example, why are swollen females more aggressed by males if only aggression before the swollen period seems associated with more chances of mating? Here, the authors systematically provide effect sizes (and confidence intervals) and often describe the effects in an intuitive biological way (e.g., “Swollen females were, on average, about five times more likely to become injured”). This clearly helps the reader to not merely compare statistical significances but also the biological strengths of the estimated effects and the uncertainty around them. They also clearly acknowledge limits due to sample size when testing the harassment hypothesis, yet they provide precious information on the probability of observing mating (a rare behaviour) directly after aggression (already a rare behaviour!), that is, 3 times out of 38 aggressions observed between a male and a swollen female. Once again, this highlights how important it is to be able to pursue the enormous effort put so far into closely and continuously monitoring this wild population.

Finally, this study raises exciting new questions, notably regarding to what extent females exhibit “counter-strategies” in response to sexual coercion, notably whether there is still scope for female mate choice under such conditions, and what are the fitness consequences of these dynamic conflicting sexual interactions. No doubt these questions will sooner than later be addressed by the authors, and I am looking forward to reading their upcoming work.

References

Smit N, Baniel A, Roura-Torres B, Amblard-Rambert P, Charpentier MJE, Huchard E (2022) Sexual coercion in a natural mandrill population. bioRxiv, 2022.02.07.479393, ver. 5 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.02.07.479393

Smuts BB, Smuts R w. (1993) Male Aggression and Sexual Coercion of Females in Nonhuman Primates and Other Mammals: Evidence and Theoretical Implications. In: Advances in the Study of Behavior (eds Slater PJB, Rosenblatt JS, Snowdon CT, Milinski M), pp. 1–63. Academic Press. https://doi.org/10.1016/S0065-3454(08)60404-0

Sexual coercion in a natural mandrill populationNikolaos Smit, Alice Baniel, Berta Roura-Torres, Paul Amblard-Rambert, Marie J. E. Charpentier, Elise Huchard<p style="text-align: justify;">Increasing evidence indicates that sexual coercion is widespread. While some coercive strategies are conspicuous, such as forced copulation or sexual harassment, less is known about the ecology and evolution of inti...Behaviour & EthologyMatthieu Paquet2022-02-11 09:32:49 View
11 Mar 2024
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Sex differences in the relationship between maternal and neonate cortisol in a free-ranging large mammal

Stress and stress hormones’ transmission from mothers to offspring

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

Individuals can respond to environmental changes that they undergo directly (within-generation plasticity) but also through transgenerational plasticity, providing lasting effects that are transmitted to the next generations (Donelson et al. 2012; Munday et al. 2013; Kuijper & Hoyle 2015; Auge et al. 2017, Tariel et al. 2020). These parental effects can affect offspring via various mechanisms, notably via maternal transmission of hormones to the eggs or growing embryos (Mousseau & Fox 1998). While the effects of environmental quality may simply carry-over to the next generation (e.g., females in stressful environments give birth to offspring in poorer condition), parental effects may also be a mechanism that adjusts offspring phenotype in response to environmental variation and predictability, and thereby match offspring's phenotype to future environmental conditions (Gluckman et al. 2005; Marshall & Uller 2007; Dey et al. 2016; Yin et al. 2019), for example by preparing their offspring to an expected stressful environment.

When females experience stress during gestation or egg formation, elevations in glucocorticoids (GC) are expected to affect offspring phenotype in many ways, from the offspring's own GC levels, to their growth and survival (Sheriff et al. 2017). This is a well established idea, but how strong is the evidence for this? A meta-analysis on birds found no clear effect of corticosterone manipulation on offspring traits (38 studies on 9 bird species for corticosterone manipulation; Podmokła et al. 2018). Another meta-analysis including 14 vertebrate species found no clear effect of prenatal stress on offspring GC (Thayer et al. 2018). Finally, a meta-analysis on wild vertebrates (23 species) found no clear effect of GC-mediated maternal effects on offspring traits (MacLeod et al. 2021). As often when facing such inconclusive results, context dependence has been suggested as one potential reason for such inconsistencies, for exemple sex specific effects (Groothuis et al. 2019, 2020). However, sex specific measures on offspring are scarce (Podmokła et al. 2018). Moreover, the literature available is still limited to a few, mostly “model” species.

With their study, Amin et al. (2024) show the way to improve our understanding on GC transmission from mother to offspring and its effects in several aspects. First they used innovative non-invasive methods (which could broaden the range of species available to study) by quantifying cortisol metabolites from faecal samples collected from pregnant females, as proxy for maternal GC level, and relating it to GC levels from hairs of their neonate offspring. Second they used a free ranging large mammal (taxa from which literature is missing): the fallow deer (Dama dama). Third, they provide sex specific measures of GC levels. And finally but importantly, they are exemplary in their transparency regarding 1) the exploratory nature of their study, 2) their statistical thinking and procedure, and 3) the study limitations (e.g., low sample size and high within individual variation of measurements). I hope this study will motivate more research (on the fallow deer, and on other species) to broaden and strengthen our understanding of sex specific effects of maternal stress and CG levels on offspring phenotype and fitness.

References

Amin, B., Fishman, R., Quinn, M., Matas, D., Palme, R., Koren, L., & Ciuti, S. (2024). Sex differences in the relationship between maternal and foetal glucocorticoids in a free-ranging large mammal. bioRxiv, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2023.05.04.538920 

Auge, G.A., Leverett, L.D., Edwards, B.R. & Donohue, K. (2017). Adjusting phenotypes via within-and across-generational plasticity. New Phytologist, 216, 343–349. https://doi.org/10.1111/nph.14495

Dey, S., Proulx, S.R. & Teotonio, H. (2016). Adaptation to temporally fluctuating environments by the evolution of maternal effects. PLoS biology, 14, e1002388. https://doi.org/10.1371/journal.pbio.1002388

Donelson, J.M., Munday, P.L., McCormick, M.I. & Pitcher, C.R. (2012). Rapid transgenerational acclimation of a tropical reef fish to climate change. Nature Climate Change, 2, 30. https://doi.org/10.1038/nclimate1323

Gluckman, P.D., Hanson, M.A. & Spencer, H.G. (2005). Predictive adaptive responses and human evolution. Trends in ecology & evolution, 20, 527–533. https://doi.org/10.1016/j.tree.2005.08.001

Groothuis, Ton GG, Bin-Yan Hsu, Neeraj Kumar, and Barbara Tschirren. "Revisiting mechanisms and functions of prenatal hormone-mediated maternal effects using avian species as a model." Philosophical Transactions of the Royal Society B 374, no. 1770 (2019): 20180115. https://doi.org/10.1098/rstb.2018.0115

Groothuis, Ton GG, Neeraj Kumar, and Bin-Yan Hsu. "Explaining discrepancies in the study of maternal effects: the role of context and embryo." Current Opinion in Behavioral Sciences 36 (2020): 185-192. https://doi.org/10.1016/j.cobeha.2020.10.006 

Kuijper, B. & Hoyle, R.B. (2015). When to rely on maternal effects and when on phenotypic plasticity? Evolution, 69, 950–968. https://doi.org/10.1111/evo.12635   

MacLeod, Kirsty J., Geoffrey M. While, and Tobias Uller. "Viviparous mothers impose stronger glucocorticoid‐mediated maternal stress effects on their offspring than oviparous mothers." Ecology and Evolution 11, no. 23 (2021): 17238-17259.

Marshall, D.J. & Uller, T. (2007). When is a maternal effect adaptive? Oikos, 116, 1957–1963. https://doi.org/10.1111/j.2007.0030-1299.16203.x       

Mousseau, T.A. & Fox, C.W. (1998). Maternal effects as adaptations. Oxford University Press.

Munday, P.L., Warner, R.R., Monro, K., Pandolfi, J.M. & Marshall, D.J. (2013). Predicting evolutionary responses to climate change in the sea. Ecology Letters, 16, 1488–1500. https://doi.org/10.1111/ele.12185

Podmokła, Edyta, Szymon M. Drobniak, and Joanna Rutkowska. "Chicken or egg? Outcomes of experimental manipulations of maternally transmitted hormones depend on administration method–a meta‐analysis." Biological Reviews 93, no. 3 (2018): 1499-1517. https://doi.org/10.1111/brv.12406 

Sheriff, M. J., Bell, A., Boonstra, R., Dantzer, B., Lavergne, S. G., McGhee, K. E., MacLeod, K. J., Winandy, L., Zimmer, C., & Love, O. P. (2017). Integrating ecological and evolutionary context in the study of maternal stress. Integrative and Comparative Biology, 57(3), 437–449. https://doi.org/10.1093/icb/icx105

Tariel, Juliette, Sandrine Plénet, and Émilien Luquet. "Transgenerational plasticity in the context of predator-prey interactions." Frontiers in Ecology and Evolution 8 (2020): 548660. https://doi.org/10.3389/fevo.2020.548660 

Thayer, Zaneta M., Meredith A. Wilson, Andrew W. Kim, and Adrian V. Jaeggi. "Impact of prenatal stress on offspring glucocorticoid levels: A phylogenetic meta-analysis across 14 vertebrate species." Scientific Reports 8, no. 1 (2018): 4942. https://doi.org/10.1038/s41598-018-23169-w 

Yin, J., Zhou, M., Lin, Z., Li, Q.Q. & Zhang, Y.-Y. (2019). Transgenerational effects benefit offspring across diverse environments: a meta-analysis in plants and animals. Ecology letters, 22, 1976–1986. https://doi.org/10.1111/ele.13373

Sex differences in the relationship between maternal and neonate cortisol in a free-ranging large mammalAmin, B., Fishman, R., Quinn, M., Matas, D., Palme, R., Koren, L., Ciuti, S.<p style="text-align: justify;">Maternal phenotypes can have long-term effects on offspring phenotypes. These maternal effects may begin during gestation, when maternal glucocorticoid (GC) levels may affect foetal GC levels, thereby having an orga...Evolutionary ecology, Maternal effects, Ontogeny, Physiology, ZoologyMatthieu Paquet2023-06-05 09:06:56 View