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06 Mar 2020
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The persistence in time of distributional patterns in marine megafauna impacts zonal conservation strategies

The importance of spatio-temporal dynamics on MPA's design

Recommended by based on reviews by Ana S. L. Rodrigues and 1 anonymous reviewer

Marine protected areas (MPA) have arisen as the main approach for conservation of marine species. Fishes, marine mammals and birds can be conservation targets that justify the implementation of these areas. However, MPAs undergo many of the problems faced by their terrestrial equivalent. One of the major concerns is that these conservation areas are spatially constrained, by logistic reasons, and many times these constraints caused that key areas for the species (reproductive sites, refugees, migration) fall outside the limits, making conservation efforts even more difficult. Lambert et al. [1] evaluate at what point the Bay of Biscay MPA contains key ecological areas for several emblematic species. The evaluation incorporated a spatio-temporal dimension. To evaluate these ideas, authors evaluate two population descriptors: aggregation and persistence of several species of cetaceans and seabirds.
The authors determined that despite the MPA contains key areas for some species, for many others the key areas fall outside the MPA (aggregation sites) or observed aggregation sites are poorly persistent in time. They found that aggregation and persistence behave as two uncorrelated descriptors of the spatio-temporal distribution of populations. Variability of both characteristics was species-specific, but in all cases the message is clear: both features must be taken into account to evaluate the effectiveness of MPAs. Both conclusions pointed out to the difficulties that a strategy based on MPAs could face when the target are those species with low aggregation or those where key sites show low persistence in time.
Conceptually, the manuscript and its conclusions are very interesting, specially its recommendation of including temporal variability of species abundances and aggregation in the design of MPAs. However, despite the clear biological importance of persistence and aggregation of the conservation targets for the design of a MPA, its implementation will still be an extremely complex task. A first constraint is that important areas for one species could not be relevant for others, making the design of the MPA difficult because the more target species we include the larger the area needed for the MPA. As a consequence, the management of the MPA turns difficult and expensive as the area increases. These increased costs could be a key point for accepting/rejecting the implementation of these MPAs for governments. Also larger areas could imply highest level of conflict with local communities or stakeholders. In many the inclusion inside MPAs of areas with traditional social or economic use will be a major source of conflict with the people.
Despite these difficulties, the results of Lambert et al. [1] give us a key message for improving MPA’s design. The best strategy for including their conclusions in the effective implementation of these areas will be the next target in conservation research.


[1] Lambert, C., Dorémus, G. and V. Ridoux (2020) The persistence in time of distributional patterns in marine megafauna impacts zonal conservation strategies. bioRxiv, 790634, ver. 3 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/790634

The persistence in time of distributional patterns in marine megafauna impacts zonal conservation strategiesCharlotte Lambert, Ghislain Dorémus, Vincent Ridoux<p>The main type of zonal conservation approaches corresponds to Marine Protected Areas (MPAs), which are spatially defined and generally static entities aiming at the protection of some target populations by the implementation of a management pla...Conservation biology, Habitat selection, Species distributionsSergio Estay2019-10-03 08:47:17 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.


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.

Choi G, Robinson DA, Kang S (2010) Changing Northern Hemisphere Snow Seasons. Journal of Climate, 23, 5305–5310.

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.

Notarnicola C (2020) Hotspots of snow cover changes in global mountain regions over 2000–2018. Remote Sensing of Environment, 243, 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
20 Feb 2019
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Differential immune gene expression associated with contemporary range expansion of two invasive rodents in Senegal

Are all the roads leading to Rome?

Recommended by based on reviews by Nadia Aubin-Horth and 1 anonymous reviewer

Identifying the factors which favour the establishment and spread of non-native species in novel environments is one of the keys to predict - and hence prevent or control - biological invasions. This includes biological factors (i.e. factors associated with the invasive species themselves), and one of the prevailing hypotheses is that some species traits may explain their impressive success to establish and spread in novel environments [1]. In animals, most research studies have focused on traits associated with fecundity, age at maturity, level of affiliation to humans or dispersal ability for instance. The “composite picture” of the perfect (i.e. successful) invader that has gradually emerged is a small-bodied animal strongly affiliated to human activities with high fecundity, high dispersal ability and a super high level of plasticity. Of course, the story is not that simple, and actually a perfect invader sometimes – if not often- takes another form… Carrying on to identify what makes a species a successful invader or not is hence still an important research axis with major implications.
In this manuscript, Charbonnel and collaborators [2] provide an interesting opportunity to gain novel insights into our understanding of (the) traits underlying invasion success. They nicely combine the power of Next-Generation Sequencing (NGS) with a clever comparative approach of two closely-related invasive rodents (the house mouse Mus musculus and the black rat Rattus rattus) in a common environment. They use this experimental design to test the appealing hypothesis that pathogens may be actors of the story, and may indirectly explain why some non-native species are so successful in invading novel habitats.
It is generally assumed that the community of pathogens encountered by non-native species in novel environments is different from that of their native area. On the one hand (the enemy-release hypothesis), it can be hypothesized that non-native species, when they arrive into a novel environment, will be relaxed from the pressure imposed by their native pathogens because local pathogens are not adapted (and hence do not infect) to this novel host. Because immune defence against pathogens is highly costly, non-native species establishing into a novel environment could hence reallocate these costs to other functions such as fecundity or dispersal apparatus. This scenario has been termed the “evolution of increased competitive ability” (EICA) hypothesis [3]. On the other hand (the EICA-refined hypothesis [4]), one can assume that invaders will encounter new pathogens in newly established areas, and will allocate energy toward cost-effective immune pathways to permit allocating a non-negligible amount of energy toward other functions. Finally, a last hypothesis (the “immune protection” hypothesis) assumes major changes in pathogen composition between native and invaded areas, which should lead to an overall increase in immune investment by the native species to successfully invade novel environments [4]. This last hypothesis suggests that only non-native species being able to take up the associated costs of immunity will be successful invaders.
The role of immunity in invasion success has yet been poorly investigated, mainly because of the difficulty to simultaneously analyse multiple immune pathways [4]. Charbonnel and collaborators [2] overpass this difficulty by screening all genes expressed (using a whole RNA sequencing approach) in an immune tissue: the spleen. They do so along the invasion routes of two sympatric invasive rodents in Africa and compare anciently and newly invaded areas (respectively). For one of the two species (the house mouse), they found a high number of immune-related genes to be up-regulated in newly invaded areas compared to anciently invaded areas. All categories of immune pathways (costly and cost-effective) were up-regulated, suggesting an overall increase in immune investment in the mouse, which corroborates the “immune protection” hypothesis. For the black rat, patterns of gene expression were somewhat different, with much less pronounced differentiation in gene expression between newly and anciently invaded areas. Among the few differentiated genes, a few were associated to immune responses and some of theses genes were even down-regulated in the newly invaded areas. This pattern may actually corroborate the EICA hypothesis, although it could alternatively suggest that stochastic processes (drift) associated to recent decrease in population size (which is expected during a colonisation event) are more important than selection imposed by pathogens in shaping patterns of immune gene expression.
Overall, this study [2] suggests (i) that immune-related traits are important in predicting invasion success and (ii) that two successful species with a similar invasion history and living in similar environments can use different life-history strategies to reach the same success. This later finding is particularly relevant and intriguing as it suggests that the traits and strategies deployed by species to colonise new habitats might actually be idiosyncratic, and that, if general trends actually emerge in regards of traits predicting the success of invaders, the devil might actually be into the details. Comparative studies are extremely important to identify the general rules and the specificities sustaining actual patterns, but these approaches are yet poorly used in biological invasions (at least empirically). The work presented by Charbonnel and colleagues [2] calls for future comparative studies performed at multiple spatial scales (native vs. non-native areas, anciently vs. recently invaded areas), multiple taxonomic resolutions and across multiple traits (to search for trade-offs), so that the success of invasive species can be properly understood and predicted.


[1] Jeschke, J. M., & Strayer, D. L. (2006). Determinants of vertebrate invasion success in Europe and North America. Global Change Biology, 12(9), 1608-1619. doi: 10.1111/j.1365-2486.2006.01213.x
[2] Blossey, B., & Notzold, R. (1995). Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. Journal of Ecology, 83(5), 887-889. doi: 10.2307/2261425
[3] Charbonnel, N., Galan, M., Tatard, C., Loiseau, A., Diagne, C. A., Dalecky, A., Parrinello, H., Rialle, S., Severac, D., & Brouat, C. (2019). Differential immune gene expression associated with contemporary range expansion of two invasive rodents in Senegal. bioRxiv, 442160, ver. 5 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/442160
[4] Lee, K. A., & Klasing, K. C. (2004). A role for immunology in invasion biology. Trends in Ecology & Evolution, 19(10), 523-529. doi: 10.1016/j.tree.2004.07.012

Differential immune gene expression associated with contemporary range expansion of two invasive rodents in SenegalNathalie Charbonnel, Maxime Galan, Caroline Tatard, Anne Loiseau, Christophe Diagne, Ambroise Dalecky, Hugues Parrinello, Stephanie Rialle, Dany Severac and Carine Brouat<p>Background: Biological invasions are major anthropogenic changes associated with threats to biodiversity and health. What determines the successful establishment of introduced populations still remains unsolved. Here we explore the appealing as...Biological invasions, Eco-immunology & Immunity, Population ecologySimon Blanchet2018-10-14 12:21:52 View
11 Mar 2021
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Size-dependent eco-evolutionary feedbacks in fisheries

“Hidden” natural selection and the evolution of body size in harvested stocks

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

Humans are exploiting biological resources since thousands of years. Exploitation of biological resources has become particularly intense since the beginning of the 20th century and the steep increase in the worldwide human population size. Marine and freshwater fishes are not exception to that rule, and they have been (and continue to be) strongly harvested as a source of proteins for humans. For some species, fishery has been so intense that natural stocks have virtually collapsed in only a few decades. The worst example begin that of the Northwest Atlantic cod that has declined by more than 95% of its historical biomasses in only 20-30 years of intensive exploitation (Frank et al. 2005). These rapid and steep changes in biomasses have huge impacts on the entire ecosystems since species targeted by fisheries are often at the top of trophic chains (Frank et al. 2005). 

Beyond demographic impacts, fisheries also have evolutionary impacts on populations, which can also indirectly alter ecosystems (Uusi-Heikkilä et al. 2015; Palkovacs et al. 2018). Fishermen generally focus on the largest specimens, and hence exert a strong selective pressure against these largest fish (which is called “harvest selection”). There is now ample evidence that harvest selection can lead to rapid evolutionary changes in natural populations toward small individuals (Kuparinen & Festa-Bianchet 2017). These evolutionary changes are of course undesirable from a human perspective, and have attracted many scientific questions. Nonetheless, the consequence of harvest selection is not always observable in natural populations, and there are cases in which no phenotypic change (or on the contrary an increase in mean body size) has been observed after intense harvest pressures. In a conceptual Essay, Edeline and Loeuille (Edeline & Loeuille 2020) propose novel ideas to explain why the evolutionary consequences of harvest selection can be so diverse, and how a cross talk between ecological and evolutionary dynamics can explain patterns observed in natural stocks.

 The general and novel concept proposed by Edeline and Loeuille is actually as old as Darwin’s book; The Origin of Species (Darwin 1859). It is based on the simple idea that natural selection acting on harvested populations can actually be strong, and counter-balance (or on the contrary reinforce) the evolutionary consequence of harvest selection. Although simple, the idea that natural and harvest selection are jointly shaping contemporary evolution of exploited populations lead to various and sometimes complex scenarios that can (i) explain unresolved empirical patterns and (ii) refine predictions regarding the long-term viability of exploited populations. 

The Edeline and Loeuille’s crafty inspiration is that natural selection acting on exploited populations is itself an indirect consequence of harvest (Edeline & Loeuille 2020). They suggest that, by modifying the size structure of populations (a key parameter for ecological interactions), harvest indirectly alters interactions between populations and their biotic environment through competition and predation, which changes the ecological theatre and hence the selective pressures acting back to populations. They named this process “size-dependent eco-evolutionary feedback loops” and develop several scenarios in which these feedback loops ultimately deviate the evolutionary outcome of harvest selection from expectation. The scenarios they explore are based on strong theoretical knowledge, and range from simple ones in which a single species (the harvest species) is evolving to more complex (and realistic) ones in which multiple (e.g. the harvest species and its prey) species are co-evolving.

I will not come into the details of each scenario here, and I will let the readers (re-)discovering the complex beauty of biological life and natural selection. Nonetheless, I will emphasize the importance of considering these eco-evolutionary processes altogether to fully grasp the response of exploited populations. Edeline and Loeuille convincingly demonstrate that reduced body size due to harvest selection is obviously not the only response of exploited fish populations when natural selection is jointly considered (Edeline & Loeuille 2020). On the contrary, they show that –under some realistic ecological circumstances relaxing exploitative competition due to reduced population densities- natural selection can act antagonistically, and hence favour stable body size in exploited populations. Although this seems further desirable from a human perspective than a downsizing of exploited populations, it is actually mere window dressing as Edeline and Loeuille further showed that this response is accompanied by an erosion of the evolvability –and hence a lowest probability of long-term persistence- of these exploited populations.

Humans, by exploiting biological resources, are breaking the relative equilibrium of complex entities, and the response of populations to this disturbance is itself often complex and heterogeneous. In this Essay, Edeline and Loeuille provide –under simple terms- the theoretical and conceptual bases required to improve predictions regarding the evolutionary responses of natural populations to exploitation by humans (Edeline & Loeuille 2020). An important next step will be to generate data and methods allowing confronting the empirical reality to these novel concepts (e.g. (Monk et al. 2021), so as to identify the most likely evolutionary scenarios sustaining biological responses of exploited populations, and hence to set the best management plans for the long-term sustainability of these populations.


Darwin, C. (1859). On the Origin of Species by Means of Natural Selection. John Murray, London.

Edeline, E. & Loeuille, N. (2021) Size-dependent eco-evolutionary feedbacks in fisheries. bioRxiv, 2020.04.03.022905, ver. 4 peer-reviewed and recommended by PCI Ecology. doi:

Frank, K.T., Petrie, B., Choi, J. S. & Leggett, W.C. (2005). Trophic Cascades in a Formerly Cod-Dominated Ecosystem. Science, 308, 1621–1623. doi:

Kuparinen, A. & Festa-Bianchet, M. (2017). Harvest-induced evolution: insights from aquatic and terrestrial systems. Philos. Trans. R. Soc. B Biol. Sci., 372, 20160036. doi:

Monk, C.T., Bekkevold, D., Klefoth, T., Pagel, T., Palmer, M. & Arlinghaus, R. (2021). The battle between harvest and natural selection creates small and shy fish. Proc. Natl. Acad. Sci., 118, e2009451118. doi: 

Palkovacs, E.P., Moritsch, M.M., Contolini, G.M. & Pelletier, F. (2018). Ecology of harvest-driven trait changes and implications for ecosystem management. Front. Ecol. Environ., 16, 20–28. doi:

Uusi-Heikkilä, S., Whiteley, A.R., Kuparinen, A., Matsumura, S., Venturelli, P.A., Wolter, C., et al. (2015). The evolutionary legacy of size-selective harvesting extends from genes to populations. Evol. Appl., 8, 597–620. doi:

Size-dependent eco-evolutionary feedbacks in fisheriesEric Edeline and Nicolas Loeuille<p>Harvesting may drive body downsizing along with population declines and decreased harvesting yields. These changes are commonly construed as direct consequences of harvest selection, where small-bodied, early-reproducing individuals are immedia...Biodiversity, Community ecology, Competition, Eco-evolutionary dynamics, Evolutionary ecology, Food webs, Interaction networks, Life history, Population ecology, Theoretical ecologySimon Blanchet2020-04-03 16:14:05 View
06 Mar 2020
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A community perspective on the concept of marine holobionts: current status, challenges, and future directions

Marine holobiont in the high throughput sequencing era

Recommended by and based on reviews by Sophie Arnaud-Haond and Aurélie Tasiemski

The concept of holobiont dates back to more than thirty years, it was primarily coined to hypothesize the importance of symbiotic associations to generate significant evolutionary novelties. Quickly adopted to describe the now well-studied system formed by zooxanthella associated corals, this concept expanded much further after the emergence of High-Throughput Sequencing and associated progresses in metabarcoding and metagenomics.
Holobionts – defined as the association between an individual host and its microbiota - are now increasingly described at sea and on land. The opinion article by Dittami et al. [1] provides a synthetic overview of marine holobionts. It retraces the history of the holobiont concept, recalls the main mechanisms underlying the association between hosts and microbial communities, highlights the influence of these symbioses on marine ecosystem functioning, and outlines current tools and future lines of research.
In particular, the article discusses some particularities of marine systems, such as the strong connectivity allowing an exchange of microorganisms and chemical signals between and within holobionts.
The authors advocate the need to bridge the gap between large scale exploration studies and smaller scale mechanistic studies, by conducting interdisciplinary research (combining physiology, biochemistry, ecology, experimentation and computational modeling) on some keystone holobionts.
Finally, one strength of the paper by Dittami et al. [1] is that it places the concept of the holobiont in an applied research framework. Several possible applications of knowledge on host-microbiota interactions are suggested, both in the field of aquaculture and that of monitoring the health of marine ecosystems. This article contains all the necessary elements for someone who would like to jump into the study of the holobionths in the marine world.

[1] Dittami SM, Arboleda E, Auguet J, Bigalke A, Briand E, Cardenas P, Cardini U, Decelle J, Engelen AH, Eveillard D, Gachon CMM, Griffiths SM, Harder T, Kayal E, Kazamia E, Lallier FH, Medina M, Marzinelli E, Morganti T, Núñez Pons L, Prado S, Pintado J, Saha M, Selosse M, Skillings D, Stock W, Sunagawa S, Toulza E, Vorobev A, Leblanc C, Not F. (2020). A community perspective on the concept of marine holobionts: current status, challenges, and future directions. Zenodo, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.5281/zenodo.3696771

A community perspective on the concept of marine holobionts: current status, challenges, and future directionsSimon M. Dittami, Enrique Arboleda, Jean-Christophe Auguet, Arite Bigalke, Enora Briand, Paco Cárdenas, Ulisse Cardini, Johan Decelle, Aschwin Engelen, Damien Eveillard, Claire M.M. Gachon, Sarah Griffiths, Tilmann Harder, Ehsan Kayal, Elena Kazam...Host-microbe interactions play crucial roles in marine ecosystems. However, we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. T...Marine ecology, Microbial ecology & microbiology, SymbiosisSophie Arnaud-Haond2019-02-05 17:57:11 View
02 Dec 2021
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Metabarcoding faecal samples to investigate spatiotemporal variation in the diet of the endangered Westland petrel (Procellaria westlandica)

The promise and limits of DNA based approach to infer diet flexibility in endangered top predators

Recommended by based on reviews by Francis John Burdon and Babett Günther

There is growing evidence of worldwide decline of populations of top predators, including marine ones (Heithaus et al, 2008, Mc Cauley et al., 2015), with cascading effects expected at the ecosystem level, due to global change and human activities, including habitat loss or fragmentation, the collapse or the range shifts of their preys. On a global scale, seabirds are among the most threatened group of birds, about one-third of them being considered as threatened or endangered (Votier& Sherley, 2017). The large consequences of the decrease of the populations of preys they feed on (Cury et al, 2011) points diet flexibility as one important element to understand for effective management (McInnes et al, 2017).  Nevertheless, morphological inventory of preys requires intrusive protocols, and the differential digestion rate of distinct taxa may lead to a large bias in morphological-based diet assessments. The use of DNA metabarcoding on feces (or diet DNA, dDNA) now allows non-invasive approaches facilitating the recollection of samples and the detection of multiple preys independently of their digestion rates (Deagle et al., 2019). Although no gold standard exists yet to avoid bias associated with metabarcoding (primer bias, gaps in reference databases, inability to differentiate primary from secondary predation…), the use of these recent techniques has already improved the knowledge of the foraging behaviour and diet of many animals (Ando et al., 2020).

Both promise and shortcomings of this approach are illustrated in the article “Metabarcoding faecal samples to investigate spatiotemporal variation in the diet of the endangered Westland petrel (Procellaria westlandica)” by Quereteja et al. (2021). In this work, the authors assessed the nature and spatio-temporal flexibility of the foraging behaviour and consequent diet of the endangered petrel Procellaria westlandica from New-Zealand through metabarcoding of faeces samples.

The results of this dDNA, non-invasive approach, identify some expected and also unexpected prey items, some of which require further investigation likely due to large gaps in the reference databases. They also reveal the temporal (before and after hatching) and spatial (across colonies only 1.5km apart) flexibility of the foraging behaviour, additionally suggesting a possible influence of fisheries activities in the surroundings of the colonies. This study thus both underlines the power of the non-invasive metabarcoding approach on faeces, and the important results such analysis can deliver for conservation, pointing a potential for diet flexibility that may be essential for the resilience of this iconic yet endangered species.


Ando H, Mukai H, Komura T, Dewi T, Ando M, Isagi Y (2020) Methodological trends and perspectives of animal dietary studies by noninvasive fecal DNA metabarcoding. Environmental DNA, 2, 391–406.

Cury PM, Boyd IL, Bonhommeau S, Anker-Nilssen T, Crawford RJM, Furness RW, Mills JA, Murphy EJ, Österblom H, Paleczny M, Piatt JF, Roux J-P, Shannon L, Sydeman WJ (2011) Global Seabird Response to Forage Fish Depletion—One-Third for the Birds. Science, 334, 1703–1706.

Deagle BE, Thomas AC, McInnes JC, Clarke LJ, Vesterinen EJ, Clare EL, Kartzinel TR, Eveson JP (2019) Counting with DNA in metabarcoding studies: How should we convert sequence reads to dietary data? Molecular Ecology, 28, 391–406.

Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends in Ecology & Evolution, 23, 202–210.

McCauley DJ, Pinsky ML, Palumbi SR, Estes JA, Joyce FH, Warner RR (2015) Marine defaunation: Animal loss in the global ocean. Science, 347, 1255641.

McInnes JC, Jarman SN, Lea M-A, Raymond B, Deagle BE, Phillips RA, Catry P, Stanworth A, Weimerskirch H, Kusch A, Gras M, Cherel Y, Maschette D, Alderman R (2017) DNA Metabarcoding as a Marine Conservation and Management Tool: A Circumpolar Examination of Fishery Discards in the Diet of Threatened Albatrosses. Frontiers in Marine Science, 4, 277.

Querejeta M, Lefort M-C, Bretagnolle V, Boyer S (2021) Metabarcoding faecal samples to investigate spatiotemporal variation in the diet of the endangered Westland petrel (Procellaria westlandica). bioRxiv, 2020.10.30.360289, ver. 4 peer-reviewed and recommended by Peer Community in Ecology.

Votier SC, Sherley RB (2017) Seabirds. Current Biology, 27, R448–R450.

Metabarcoding faecal samples to investigate spatiotemporal variation in the diet of the endangered Westland petrel (Procellaria westlandica)Marina Querejeta, Marie-Caroline Lefort, Vincent Bretagnolle, Stéphane Boyer<p style="text-align: justify;">As top predators, seabirds can be indirectly impacted by climate variability and commercial fishing activities through changes in marine communities. However, high mobility and foraging behaviour enables seabirds to...Conservation biology, Food webs, Marine ecology, Molecular ecologySophie Arnaud-Haond2020-10-30 20:14:50 View
29 Nov 2019
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Investigating sex differences in genetic relatedness in great-tailed grackles in Tempe, Arizona to infer potential sex biases in dispersal

Investigate fine scale sex dispersal with spatial and genetic analyses

Recommended by ORCID_LOGO based on reviews by Sylvine Durand and 1 anonymous reviewer

The preregistration "Investigating sex differences in genetic relatedness in great-tailed grackles in Tempe, Arizona to infer potential sex biases in dispersal" [1] presents the analysis plan that will be used to genetically and spatially investigate sex-biased dispersal in great-tailed grackles (Quiscalus mexicanus).
Several hypotheses implying mating systems, intrasexual competition or sex-related handicaps have been proposed to explain the diversity of dispersal patterns between or within species according to their ecological requirements, environmental factors such as seasonality [2], or individual characteristics such as age [3] or sex [4].
In birds, females are classically the dispersing sex, while males remain close to the place they were hatched [5], with potential benefits that males derive from knowing the local environment to establish territories [6].
In great-tailed grackles the males hold territories and the females choose which territory to place their nest in [7]. In this context, the main hypothesis is that females are the dispersing sex in this species. The authors of this preregistration plan to investigate this hypothesis and its 3 alternatives ((i) the males are the dispersing sex, (ii) both sexes disperse or (iii) neither of the two sexes disperse), investigating the spatial distribution of genetic relatives.
The authors plan to measure the genetic relatedness (using SNP markers) and geographic distances among all female dyads and among all male dyads in the fine geographic scale (Tempe campus, Arizona). If females disperse away from relatives, the females will be less likely to be found geographically close to genetic relatives.
This pre-registration shows that the authors are well aware of the possible limitations of their study, particularly in relation to their population of 57 individuals, on a small scale. But they will use methods that should be able to detect a signal. They were very good at incorporating the reviewers' comments and suggestions, which enabled them to produce a satisfactory and interesting version of the manuscript presenting their hypotheses, limitations and the methods they plan to use. Another point I would like to stress is that this pre-registration practice is a very good one that makes it possible to anticipate the challenges and the type of analyses to be carried out, in particular by setting out the working hypotheses and confronting them (as well as the methods envisaged) with peers from this stage. I therefore recommend this manuscript and thank all the contributors (authors and reviewers) for their work. I look forward to seeing the outcomes of this study.


[1] Sevchik A., Logan C. J., Folsom M., Bergeron L., Blackwell A., Rowney C., and Lukas D. (2019). Investigating sex differences in genetic relatedness in great-tailed grackles in Tempe, Arizona to infer potential sex biases in dispersal. In principle recommendation by Peer Community In Ecology.
[2] Fies, M. L., Puckett, K. M., and Larson-Brogdon, B. (2002). Breeding season movements and dispersal of Northern Bobwhites in fragmented habitats of Virginia. Vol. 5 , Article 35. Available at:
[3] Marvá, M., and San Segundo, F. (2018). Age-structure density-dependent fertility and individuals dispersal in a population model. Mathematical biosciences, 300, 157-167. doi: 10.1016/j.mbs.2018.03.029
[4] Trochet, A., Courtois, E. A., Stevens, V. M., Baguette, M., Chaine, A., Schmeller, D. S., Clobert, J., and Wiens, J. J. (2016). Evolution of sex-biased dispersal. The Quarterly Review of Biology, 91(3), 297-320. doi: 10.1086/688097
[5] Greenwood, P. J., and Harvey, P. H. (1982). The natal and breeding dispersal of birds. Annual review of ecology and systematics, 13(1), 1-21. doi: 10.1146/
[6] Greenwood, P. J. (1980). Mating systems, philopatry and dispersal in birds and mammals. Animal behaviour, 28(4), 1140-1162. doi: 10.1016/S0003-3472(80)80103-5
[7] Johnson, K., DuVal, E., Kielt, M., and Hughes, C. (2000). Male mating strategies and the mating system of great-tailed grackles. Behavioral Ecology, 11(2), 132-141. doi: 10.1093/beheco/11.2.132

Investigating sex differences in genetic relatedness in great-tailed grackles in Tempe, Arizona to infer potential sex biases in dispersalAugust Sevchik, Corina Logan, Melissa Folsom, Luisa Bergeron, Aaron Blackwell, Carolyn Rowney, Dieter LukasIn most bird species, females disperse prior to their first breeding attempt, while males remain close to the place they were hatched for their entire lives (Greenwood and Harvey (1982)). Explanations for such female bias in natal dispersal have f...Behaviour & Ethology, Life history, Preregistrations, Social structure, ZoologySophie Beltran-Bech2019-07-24 12:47:07 View
04 Sep 2019
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Gene expression plasticity and frontloading promote thermotolerance in Pocillopora corals

Transcriptomics of thermal stress response in corals

Recommended by based on reviews by Mar Sobral

Climate change presents a challenge to many life forms and the resulting loss of biodiversity will critically depend on the ability of organisms to timely respond to a changing environment. Shifts in ecological parameters have repeatedly been attributed to global warming, with the effectiveness of these responses varying among species [1, 2]. Organisms do not only have to face a global increase in mean temperatures, but a complex interplay with another crucial but largely understudied aspect of climate change: thermal fluctuations. Understanding the mechanisms underlying adaptation to thermal fluctuations is thus a timely and critical challenge.
Coral reefs are among the most threaten ecosystems in the context of current global changes [3]. Brener-Raffalli and colleagues [4] provided a very complete study digging into the physiological, symbiont-based and transcriptomic mechanisms underlying response of corals to temperature changes. They used an experimental approach, following the heat stress response of coral colonies from different species of the genus Pocillopora. While the symbiont community composition did not significantly change facing exposure to warmer temperatures, the authors provided evidence for transcriptomic changes especially linked to stress response genes that may underlie plastic responses to heat stress.
The authors furthermore investigated the thermal stress response of corals originating from two sites differing in their natural thermal regimes, and found that they differ in the extent and nature of plastic response, including the expression of gene regulation factors and the basal expression level of some genes. These two sites also differ in a variety of aspects, including the focal coral species, which precludes from concluding about the role of thermal regime adaptation into the differences observed. However, these results still highlight a very interesting and important direction deserving further investigation [5], and point out the importance of variability in thermal stress response among localities [6] that might potentially mediate global warming consequences on coral reefs.


[1] Parmesan, C., & Yohe, G. (2003). A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421(6918), 37–42. doi: 10.1038/nature01286
[2] Menzel, A., Sparks, T. H., Estrella, N., Koch, E., Aasa, A., Ahas, R., … Zust, A. (2006). European phenological response to climate change matches the warming pattern. Global Change Biology, 12(10), 1969–1976. doi: 10.1111/j.1365-2486.2006.01193.x
[3] Bellwood, D. R., Hughes, T. P., Folke, C., & Nyström, M. (2004). Confronting the coral reef crisis. Nature, 429(6994), 827–833. doi: 10.1038/nature02691
[4] Brener-Raffalli, K., Vidal-Dupiol, J., Adjeroud, M., Rey, O., Romans, P., Bonhomme, F., Pratlong, M., Haguenauer, A., Pillot, R., Feuillassier, L., Claereboudt, M., Magalon, H., Gélin, P., Pontarotti, P., Aurelle, D., Mitta, G. and Toulza, E. (2019). Gene expression plasticity and frontloading promote thermotolerance in Pocillopora corals. BioRxiv, 398602, ver 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/398602
[5] Kenkel, Carly D., and Matz, M. V. (2017). Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nature Ecology and Evolution, 1(1), 0014. doi: 10.1038/s41559-016-0014
[6] Kenkel, C. D., Meyer, E., and Matz, M. V. (2013). Gene expression under chronic heat stress in populations of the mustard hill coral (Porites astreoides) from different thermal environments. Molecular Ecology, 22(16), 4322–4334. doi: 10.1111/mec.12390

Gene expression plasticity and frontloading promote thermotolerance in Pocillopora coralsK. Brener-Raffalli, J. Vidal-Dupiol, M. Adjeroud, O. Rey, P. Romans, F. Bonhomme, M. Pratlong, A. Haguenauer, R. Pillot, L. Feuillassier, M. Claereboudt, H. Magalon, P. Gélin, P. Pontarotti, D. Aurelle, G. Mitta, E. Toulza<p>Ecosystems worldwide are suffering from climate change. Coral reef ecosystems are globally threatened by increasing sea surface temperatures. However, gene expression plasticity provides the potential for organisms to respond rapidly and effect...Climate change, Evolutionary ecology, Marine ecology, Molecular ecology, Phenotypic plasticity, SymbiosisStaffan Jacob2018-08-29 10:46:55 View
05 Feb 2020
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A flexible pipeline combining clustering and correction tools for prokaryotic and eukaryotic metabarcoding

A flexible pipeline combining clustering and correction tools for prokaryotic and eukaryotic metabarcoding

Recommended by ORCID_LOGO based on reviews by Tiago Pereira and 1 anonymous reviewer

High-throughput sequencing-based techniques such as DNA metabarcoding are increasingly advocated as providing numerous benefits over morphology‐based identifications for biodiversity inventories and ecosystem biomonitoring [1]. These benefits are particularly apparent for highly-diversified and/or hardly accessible aquatic and marine environments, where simple water or sediment samples could already produce acceptably accurate biodiversity estimates based on the environmental DNA present in the samples [2,3]. However, sequence-based characterization of biodiversity comes with its own challenges. A major one resides in the capacity to disentangle true biological diversity (be it taxonomic or genetic) from artefactual diversity generated by sequence-errors accumulation during PCR and sequencing processes, or from the amplification of non-target genes (i.e. pseudo-genes). On one hand, the stringent elimination of sequence variants might lead to biodiversity underestimation through the removal of true species, or the clustering of closely-related ones. On the other hand, a more permissive sequence filtering bears the risks of biodiversity inflation. Recent studies have outlined an excellent methodological framework for addressing this issue by proposing bioinformatic tools that allow the amplicon-specific error-correction as alternative or as complement to the more arbitrary approach of clustering into Molecular Taxonomic Units (MOTUs) based on sequence dissimilarity [4,5]. But to date, the relevance of amplicon-specific error-correction tools has been demonstrated only for a limited set of taxonomic groups and gene markers.
The study of Brandt et al. [6] successfully builds upon existing methodological frameworks for filling this gap in current literature. By proposing a bioinformatic pipeline combining Amplicon Sequence Variants (ASV) curation with MOTU clustering and additional post-clustering curation, the authors show that contrary to previous recommendations, ASV-based curation alone does not represent an adequate approach for DNA metabarcoding-based inventories of metazoans. Metazoans indeed, do exhibit inherently higher intra-specific and intra-individual genetic variability, necessarily leading to biased biodiversity estimates unbalanced in favor of species with higher intraspecific diversity in the absence of MOTU clustering. Interestingly, the positive effect of additional clustering showed to be dependent on the target gene region. Additional clustering had proportionally higher effect on the more polymorphic mitochondrial COI region (as compared to the 18S ribosomal gene). Thus, the major advantage of the study lies in the provision of optimal curation parameters that reflect the best possible balance between minimizing the impact of PCR/sequencing errors and the loss of true biodiversity across markers with contrasting levels of intragenomic variation. This is important as combining multiple markers is increasingly considered for improving the taxonomic coverage and resolution of data in DNA metabarcoding studies.
Another critical aspect of the study is the taxonomic assignation of curated OTUs (which is also the case for the majority of DNA metabarcoding-based biodiversity assessments). Facing the double challenge of focusing on taxonomic groups that are both highly diverse and poorly represented in public sequence reference databases, the authors failed to obtain high-resolution taxonomic assignments for several of the most closely-related species. As a result, taxa with low divergence levels were clustered as single taxonomic units, subsequently leading to underestimation of true biodiversity present. This finding adds to the argument that in order to be successful, sequence-based techniques still require the availability of comprehensive, high-quality reference databases.
Perhaps the only regret we might have with the study is the absence of mock community validation for the prokaryotes compartment. Even though the analyses of natural samples seem to suggest a positive effect of the curation pipeline, the concept of intra- versus inter-species variation in naturally occurring prokaryote communities remains at best ambiguous. Of course, constituting a representative sample of taxonomically-resolved prokaryote taxa from deep-sea habitats does not come without difficulties but has the benefit of opening opportunities for further studies on the matter.


[1] Porter, T. M., and Hajibabaei, M. (2018). Scaling up: A guide to high-throughput genomic approaches for biodiversity analysis. Molecular Ecology, 27(2), 313–338. doi: 10.1111/mec.14478
[2] Valentini, A., Taberlet, P., Miaud, C., Civade, R., Herder, J., Thomsen, P. F., … Dejean, T. (2016). Next-generation monitoring of aquatic biodiversity using environmental DNA metabarcoding. Molecular Ecology, 25(4), 929–942. doi: 10.1111/mec.13428
[3] Leray, M., and Knowlton, N. (2015). DNA barcoding and metabarcoding of standardized samples reveal patterns of marine benthic diversity. Proceedings of the National Academy of Sciences, 112(7), 2076–2081. doi: 10.1073/pnas.1424997112
[4] Callahan, B. J., McMurdie, P. J., and Holmes, S. P. (2017). Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. The ISME Journal, 11(12), 2639–2643. doi: 10.1038/ismej.2017.119
[5] Edgar, R. C. (2016). UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. BioRxiv, 081257. doi: 10.1101/081257
[6] Brandt, M. I., Trouche, B., Quintric, L., Wincker, P., Poulain, J., and Arnaud-Haond, S. (2020). A flexible pipeline combining clustering and correction tools for prokaryotic and eukaryotic metabarcoding. BioRxiv, 717355, ver. 3 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/717355

A flexible pipeline combining clustering and correction tools for prokaryotic and eukaryotic metabarcoding Miriam I Brandt, Blandine Trouche, Laure Quintric, Patrick Wincker, Julie Poulain, Sophie Arnaud-Haond<p>Environmental metabarcoding is an increasingly popular tool for studying biodiversity in marine and terrestrial biomes. With sequencing costs decreasing, multiple-marker metabarcoding, spanning several branches of the tree of life, is becoming ...Biodiversity, Community ecology, Marine ecology, Molecular ecologyStefaniya Kamenova2019-08-02 20:52:45 View
20 Oct 2021
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Eco-evolutionary dynamics further weakens mutualistic interaction and coexistence under population decline

Doomed by your partner: when mutualistic interactions are like an evolutionary millstone around a species’ neck

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

Mutualistic interactions are the weird uncles of population and community ecology. They are everywhere, from the microbes aiding digestion in animals’ guts to animal-pollination services in ecosystems; They increase productivity through facilitation; They fascinate us when small birds pick the teeth of a big-mouthed crocodile. Yet, mutualistic interactions are far less studied and understood than competition or predation. Possibly because we are naively convinced that there is no mystery here: isn’t it obvious that mutualistic interactions necessarily facilitate species coexistence? Since mutualistic species benefit from one another, if one species evolves, the other should just follow, isn’t that so?

It is not as simple as that, for several reasons. First, because simple mutualistic Lotka-Volterra models showed that most of the time mutualistic systems should drift to infinity and be unstable (e.g. Goh 1979). This is not what happens in natural populations, so something is missing in simple models. At a larger scale, that of communities, this is even worse, since we are still far from understanding the link between the topology of mutualistic networks and the stability of a community. Second, interactions are context-dependent: mutualistic species exchange resources, and thus from the point of view of one species the interaction is either beneficial or not, depending on the net gain of energy (e.g. Holland and DeAngelis 2010). In other words, considering interactions as mutualistic per se is too caricatural. Third, since evolution is blind, the evolutionary response of a species to an environmental change can have any effect on its mutualistic partner, and not necessarily a neutral or positive effect. This latter reason is particularly highlighted by the paper by A. Weinbach et al. (2021).

Weinbach et al. considered a simple two-species mutualistic Lotka-Volterra model and analyzed the evolutionary dynamics of a trait controlling for the rate of interaction between the two species by using the classical Adaptive Dynamics framework. They showed that, depending on the form of the trade-off between this interaction trait and its effect on the intrinsic growth rate, several situations can occur at evolutionary equilibrium: species can stably coexist and maintain their interaction, or the interaction traits can evolve to zero where species can coexist without any interactions.

Weinbach et al. then investigated the fate of the two-species system if a partner species is strongly affected by environmental change, for instance, a large decrease of its growth rate. Because of the supposed trade-off between the interaction trait and the growth rate, the interaction trait in the focal species tends to decrease as an evolutionary response to the decline of the partner species. If environmental change is too large, the interaction trait can evolve to zero and can lead the partner species to extinction. An “evolutionary murder”.

Even though Weinbach et al. interpreted the results of their model through the lens of plant-pollinators systems, their model is not specific to this case. On the contrary, it is very general, which has advantages and caveats. By its generality, the model is informative because it is a proof of concept that the evolution of mutualistic interactions can have unexpected effects on any category of mutualistic systems. Yet, since the model lacks many specificities of plant-pollinator interactions, it is hard to evaluate how their result would apply to plant-pollinators communities.

I wanted to recommend this paper as a reminder that it is certainly worth studying the evolution of mutualistic interactions, because i) some unexpected phenomenons can occur, ii) we are certainly too naive about the evolution and ecology of mutualistic interactions, and iii) one can wonder to what extent we will be able to explain the stability of mutualistic communities without accounting for the co-evolutionary dynamics of mutualistic species.


Goh BS (1979) Stability in Models of Mutualism. The American Naturalist, 113, 261–275.

Holland JN, DeAngelis DL (2010) A consumer–resource approach to the density-dependent population dynamics of mutualism. Ecology, 91, 1286–1295.

Weinbach A, Loeuille N, Rohr RP (2021) Eco-evolutionary dynamics further weakens mutualistic interaction and coexistence under population decline. bioRxiv, 570580, ver. 5 peer-reviewed and recommended by Peer Community in Ecology.

Eco-evolutionary dynamics further weakens mutualistic interaction and coexistence under population declineAvril Weinbach, Nicolas Loeuille, Rudolf P. Rohr<p style="text-align: justify;">With current environmental changes, evolution can rescue declining populations, but what happens to their interacting species? Mutualistic interactions can help species sustain each other when their environment wors...Coexistence, Eco-evolutionary dynamics, Evolutionary ecology, Interaction networks, Pollination, Theoretical ecologySylvain Billiard2019-09-05 11:29:45 View