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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.

References

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. https://doi.org/10.1002/edn3.117

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. https://doi.org/10.1126/science.1212928

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. https://doi.org/10.1111/mec.14734

Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends in Ecology & Evolution, 23, 202–210. https://doi.org/10.1016/j.tree.2008.01.003

McCauley DJ, Pinsky ML, Palumbi SR, Estes JA, Joyce FH, Warner RR (2015) Marine defaunation: Animal loss in the global ocean. Science, 347, 1255641. https://doi.org/10.1126/science.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. https://doi.org/10.3389/fmars.2017.00277

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. https://doi.org/10.1101/2020.10.30.360289

Votier SC, Sherley RB (2017) Seabirds. Current Biology, 27, R448–R450. https://doi.org/10.1016/j.cub.2017.01.042

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
12 May 2020
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On the efficacy of restoration in stream networks: comments, critiques, and prospective recommendations

A stronger statistical test of stream restoration experiments

Recommended by based on reviews by Eric Harvey and Mariana Perez Rocha

The metacommunity framework acknowledges that local sites are connected to other sites through dispersal, and that these connectivity patterns can influence local dynamics [1]. This framework is slowly moving from a framework that guides fundamental research to being actively applied in for instance a conservation context (e.g. [2]). Swan and Brown [3,4] analyzed the results of a suite of experimental manipulations in headwater and mainstem streams on invertebrate community structure in the context of the metacommunity concept. This was an important contribution to conservation ecology.
However, David Murray-Stoker [5] was not satisfied with their statistical analyses, and recreated, and more importantly, improved their original analyses in the peer-reviewed article. The new analyses are based on a combination of a more consistent site selection, checking the model assumptions, using different estimation procedures, and focusing more on effect size calculations versus statistical significance. This peer-reviewed article is thus the perfect example of the advantages of open research: the original authors making available both the data and their R script files, initially first updating the analyses and results themselves, followed by more in-depth analyses of the original data and question.
This peer reviewed went through a very in-depth process itself, with several rounds of questions and feedback that addressed both the statistical analyses, the interpretation of the results, and the conclusions. It also, however, addressed something that is often harder to provide feedback on, for instance the tone of the argument. I hope that scientists interested in these issues will not only read the final manuscript, but also the different steps of the peer review processes. These are very informative, I think, and provide a more complete picture of mainly the raison for certain decisions.
Not only does this provide the reader interested in stream conservation with the opportunity to make up their own mind on the appropriateness of these decisions, but it could potentially lead to more analyses of this important data set. For instance, maybe a formal meta-analysis that starts with the effect sizes of all the original studies might bring some new insights into this question?

References

[1] Leibold, M. A., Holyoak, M., Mouquet, N. et al. (2004). The metacommunity concept: a framework for multi‐scale community ecology. Ecology letters, 7(7), 601-613. doi: 10.1111/j.1461-0248.2004.00608.x
[2] Heino, J. (2013). The importance of metacommunity ecology for environmental assessment research in the freshwater realm. Biological Reviews, 88(1), 166-178. doi: 10.1111/j.1469-185X.2012.00244.x
[3] Swan, C. M., and Brown, B. L. (2017). Metacommunity theory meets restoration: isolation may mediate how ecological communities respond to stream restoration. Ecological Applications, 27(7), 2209-2219. doi: 10.1002/eap.1602
[4] Swan, C. M., and Brown, B. L. (2018). Erratum for: Metacommunity theory meets restoration: isolation may mediate how ecological communities respond to stream restoration. Ecological Applications 28:1370–1371. doi: 10.1002/eap.1738
[5] Murray-Stoker, D. (2020). On the efficacy of restoration in stream networks: comments, critiques, and prospective recommendations. bioRxiv, 611939, ver. 7 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/611939

On the efficacy of restoration in stream networks: comments, critiques, and prospective recommendationsDavid Murray-Stoker<p>Swan and Brown (2017) recently addressed the effects of restoration on stream communities under the meta-community framework. Using a combination of headwater and mainstem streams, Swan and Brown (2017) evaluated how position within a stream ne...Community ecology, Freshwater ecology, Spatial ecology, Metacommunities & MetapopulationsKarl Cottenie2019-09-21 22:12:57 View
02 Aug 2021
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Dynamics of Fucus serratus thallus photosynthesis and community primary production during emersion across seasons: canopy dampening and biochemical acclimation

Towards a better understanding of the effects of self-shading on Fucus serratus populations

Recommended by ORCID_LOGO based on reviews by Gwenael Abril, Francesca Rossi and 1 anonymous reviewer

The importance of the vertical structure of vegetation cover for the functioning, management and conservation of ecosystems has received particular attention from ecologists in the last decades. Canopy architecture has many implications for light extinction coefficient, temperature variation reduction, self-shading which are all key parameters for the structuring and functioning of different ecosystems such as grasslands [1,2], forests [3,4], phytoplankton communities [5, 6], macroalgal populations [7] and even underwater animal forests such as octocoral communities [8].

This research topic, therefore, benefits from a large body of literature and the facilitative role of self-shadowing is no longer in question. However, it is always puzzling to note that some of the most common ecosystems turn out to be amongst the least known. This is precisely the case of the Fucus serratus communities which are widespread in Northeast Atlantic along the Atlantic coast of Europe from Svalbard to Portugal, as well as Northwest Atlantic & Gulf of St. Lawrence, easily accessible at low tide, but which have comparatively received less attention than more emblematic macro-algal communities such as Laminariales.

The lack of attention paid to these most common Fucales is particularly critical as some species such as F. serratus are proving to be particularly vulnerable to environmental change, leading to a predicted northward retreat from its current southern boundary [9].

In the present study [10], the authors showed the importance of the vegetation cover in resisting tide-induced environmental stresses. The canopy of F. serratus mitigates stress levels experienced in the lower layers during emersion, while various acclimation strategies take over to maintain the photosynthetic apparatus in optimal conditions.

They hereby highlight adaptation mechanisms to the extreme environment represented by the intertidal zone. These adaptation strategies were expected and similar mechanisms had been shown at the cellular level previously [11]. The earliest studies on the subject have shown that the structure of the bottom, the movement of water, and light availability all "influence the distribution of Fucaceae and disturb the regularity of their fine zonation, which itself is caused by the most important factor, desiccation", as Zaneveld states in his review [12]. He observed that the causes of the zonal distribution of marine algae are numerous, and identified several points of interest such as the relative period of emersion, the rapidity of desiccation, the loss of water, and the thickness of the cell walls.

The present study thus highlights the existence of facilitative mechanisms associated with F. serratus canopy and nicely confirms previous work with in situ observations. It also highlights the importance of the vegetative cover in combating desiccation and introduces the dampening effect as a facilitating mechanism.

The effect of the vegetation cover can sometimes even be felt beyond its immediate area of influence. A recent study shows that ground-level ozone is significantly reduced by the combined effects of canopy shading and turbulence [4]. Below the canopy, the light intensity becomes sufficiently low which inhibits ozone formation due to the decrease in the rates of hydroxyl radical formation and the rates of conversion of nitrogen dioxide to nitrogen oxide by photolysis. In addition, reductions in light levels associated with foliage promote ozone-destroying reactions between plant-emitted species, such as nitric oxide and/or alkenes, and ozone itself. The reduction in diffusivity slows the upward transport of surface emitted species, partially decoupling the area under the canopy from the rest of the atmosphere.

By analogy with the work of Makar et al [4], and in the light of the results provided by the authors of this study, one may wonder whether the canopy dampening of F. serratus communities (and other common fucoids widely distributed on our coasts) might not also influence atmospheric chemistry, both at the Earth's surface and in the atmospheric boundary layer. The lack of accumulation of reactive oxygen species under the canopy found by the authors is consistent with this hypothesis and suggests that the damping effect of F. serratus may well have much wider consequences than expected.

References

[1] Jurik TW, Kliebenstein H (2000) Canopy Architecture, Light Extinction and Self-Shading of a Prairie Grass, Andropogon Gerardii. The American Midland Naturalist, 144, 51–65. http://www.jstor.org/stable/3083010

[2] Mitchley J, Willems JH (1995) Vertical canopy structure of Dutch chalk grasslands in relation to their management. Vegetatio, 117, 17–27. https://doi.org/10.1007/BF00033256

[3] Kane VR, Gillespie AR, McGaughey R, Lutz JA, Ceder K, Franklin JF (2008) Interpretation and topographic compensation of conifer canopy self-shadowing. Remote Sensing of Environment, 112, 3820–3832. https://doi.org/10.1016/j.rse.2008.06.001

[4] Makar PA, Staebler RM, Akingunola A, Zhang J, McLinden C, Kharol SK, Pabla B, Cheung P, Zheng Q (2017) The effects of forest canopy shading and turbulence on boundary layer ozone. Nature Communications, 8, 15243. https://doi.org/10.1038/ncomms15243

[5] Shigesada N, Okubo A (1981) Analysis of the self-shading effect on algal vertical distribution in natural waters. Journal of Mathematical Biology, 12, 311–326. https://doi.org/10.1007/BF00276919

[6] Barros MP, Pedersén M, Colepicolo P, Snoeijs P (2003) Self-shading protects phytoplankton communities against H2O2-induced oxidative damage. Aquatic Microbial Ecology, 30, 275–282. https://doi.org/10.3354/ame030275

[7] Ørberg SB, Krause-Jensen D, Mouritsen KN, Olesen B, Marbà N, Larsen MH, Blicher ME, Sejr MK (2018) Canopy-Forming Macroalgae Facilitate Recolonization of Sub-Arctic Intertidal Fauna and Reduce Temperature Extremes. Frontiers in Marine Science, 5. https://doi.org/10.3389/fmars.2018.00332

[8] Nelson H, Bramanti L (2020) From Trees to Octocorals: The Role of Self-Thinning and Shading in Underwater Animal Forests. In: Perspectives on the Marine Animal Forests of the World (eds Rossi S, Bramanti L), pp. 401–417. Springer International Publishing, Cham. https://doi.org/10.1007/978-3-030-57054-5_12

[9] Jueterbock A, Kollias S, Smolina I, Fernandes JMO, Coyer JA, Olsen JL, Hoarau G (2014) Thermal stress resistance of the brown alga Fucus serratus along the North-Atlantic coast: Acclimatization potential to climate change. Marine Genomics, 13, 27–36. https://doi.org/10.1016/j.margen.2013.12.008

[10] Migné A, Duong G, Menu D, Davoult D, Gévaert F (2021) Dynamics of Fucus serratus thallus photosynthesis and community primary production during emersion across seasons: canopy dampening and biochemical acclimation. HAL, hal-03079617, ver. 4 peer-reviewed and recommended by Peer community in Ecology. https://hal.archives-ouvertes.fr/hal-03079617

[11] Lichtenberg M, Kühl M (2015) Pronounced gradients of light, photosynthesis and O2 consumption in the tissue of the brown alga Fucus serratus. New Phytologist, 207, 559–569. https://doi.org/10.1111/nph.13396

[12] Zaneveld JS (1937) The Littoral Zonation of Some Fucaceae in Relation to Desiccation. Journal of Ecology, 25, 431–468. https://doi.org/10.2307/2256204

Dynamics of Fucus serratus thallus photosynthesis and community primary production during emersion across seasons: canopy dampening and biochemical acclimationAline Migné, Gwendoline Duong, Dominique Menu, Dominique Davoult & François Gévaert<p style="text-align: justify;">The brown alga <em>Fucus serratus</em> forms dense stands on the sheltered low intertidal rocky shores of the Northeast Atlantic coast. In the southern English Channel, these stands have proved to be highly producti...Marine ecologyCédric Hubas2021-01-05 16:24:02 View
24 May 2022
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Controversy over the decline of arthropods: a matter of temporal baseline?

Don't jump to conclusions on arthropod abundance dynamics without appropriate data

Recommended by ORCID_LOGO based on reviews by Gabor L Lovei and 1 anonymous reviewer

Humans are dramatically modifying many aspects of our planet via increasing concentrations of carbon dioxide in the atmosphere, patterns of land-use change, and unsustainable exploitation of the planet’s resources. These changes impact the abundance of species of wild organisms, with winners and losers. Identifying how different species and groups of species are influenced by anthropogenic activity in different biomes, continents, and habitats, has become a pressing scientific question with many publications reporting analyses of disparate data on species population sizes. Many conclusions are based on the linear analysis of rather short time series of organismal abundances.
 
There has been particular interest in how arthropods are impacted by environmental change, with several recent papers reporting contradictory results. To investigate why these contradictions might arise, Duchenne et al. (2022) conducted an analysis of four published data sets along with a series of experimental analyses of simulated time series to examine the power of widely used statistical analyses to gain inference on temporal trends. Their important paper reveals that accurate inference on dynamics, particularly of species that exhibit large temporal fluctuations in abundance, requires time series that are substantially longer than are typically collected, as well as careful thought as to whether linear models are appropriate. Linear analyses of short time series are susceptible to providing unreliable inference as trends can be strongly influenced by points at either end of the time series. 
 
Duchenne et al.’s paper provides important insight on the conditions when strong inference on temporal trends of arthropod (and other species) abundances can be made, and when they should be treated with caution. They do not doubt that many insect and arachnid species are changing their abundances, and that patterns in these changes may vary spatially. What their results do say is that we should treat grand claims of population recovery or rapid declines apparently to extinction with caution when they are based on short time series, particularly of species that show significant boom and bust dynamics. In many ways, these results are not unexpected, but it is nice to see such careful and thoughtful analyses and interpretation. More data are required for most arthropod species before clear assessments of abundance trends can be made. Given our reliance on many arthropods for food, pollination, and numerous ecosystem services, and the ability of other species to spread devastating human diseases such as dengue and malaria, it is advisable that we slow our modification of their habitats while additional data are collected to allow us to better characterise the trajectory of arthropod populations to understand what the consequences of our actions on the natural world are likely to be.  
 
References

Duchenne F, Porcher E, Mihoub J-B, Loïs G, Fontaine C (2022) Controversy over the decline of arthropods: a matter of temporal baseline? bioRxiv, 2022.02.09.479422, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.02.09.479422

Controversy over the decline of arthropods: a matter of temporal baseline?François Duchenne, Emmanuelle Porcher, Jean-Baptiste Mihoub, Grégoire Loïs, Colin Fontaine<p style="text-align: justify;">Recently, a number of studies have reported somewhat contradictory patterns of temporal trends in arthropod abundance, from decline to increase. Arthropods often exhibit non-monotonous variation in abundance over ti...Conservation biologyTim Coulson2022-02-11 15:44:44 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.

References
[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
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
01 Mar 2019
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Parasite intensity is driven by temperature in a wild bird

The global change of species interactions

Recommended by based on reviews by 2 anonymous reviewers

What kinds of studies are most needed to understand the effects of global change on nature? Two deficiencies stand out: lack of long-term studies [1] and lack of data on species interactions [2]. The paper by Mennerat and colleagues [3] is particularly valuable because it addresses both of these shortcomings. The first one is obvious. Our understanding of the impact of climate on biota improves with longer times series of observations. Mennerat et al. [3] analysed an impressive 18-year series from multiple sites to search for trends in parasitism rates across a range of temperatures. The second deficiency (lack of species interaction data) is perhaps not yet fully appreciated, despite studies pointing this out ten years ago [2,4]. The focus is often on species range limits and how taking species interactions into account changes species range predictions based on climate alone (climate envelope models; [5]). But range limits are not everything, as the function of a species (or community, network, etc.) ultimately depends on the strengths of species interactions and not only on the presence or absence of a given species [2,4]. Mennerat et al. [3] show that in the case of birds and their nest parasites, it is the strength of the interaction that has changed, while the species involved stayed the same. Mennerat et al. [3] found nest parasitism to increase with temperature at the nestling stage. They have also searched for trends of parasitism dynamics dependence on the host, but did not find any, probably because the nest parasites are generalists and attack other bird species within the study sites. This study thus draws attention to wider networks of interacting species, and we urgently need more data to predict how interaction networks will rewire with progressing environmental change [6,7].

References

[1] Lindenmayer, D.B., Likens, G.E., Andersen, A., Bowman, D., Bull, C.M., Burns, E., et al. (2012). Value of long-term ecological studies. Austral Ecology, 37(7), 745–57. doi: 10.1111/j.1442-9993.2011.02351.x
[2] Tylianakis, J.M., Didham, R.K., Bascompte, J. & Wardle, D.A. (2008). Global change and species interactions in terrestrial ecosystems. Ecology Letters, 11(12), 1351–63. doi: 10.1111/j.1461-0248.2008.01250.x
[3] Mennerat, A., Charmantier, A., Hurtrez-Bousses, S., Perret, P. & Lambrechts, M.M. (2019). Parasite intensity is driven by temperature in a wild bird. bioRxiv, 323311. Ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/323311
[4] Gilman, S.E., Urban, M.C., Tewksbury, J., Gilchrist, G.W. & Holt, R.D. (2010). A framework for community interactions under climate change. Trends in Ecology & Evolution, 25(6), 325–31. doi: 10.1016/j.tree.2010.03.002
[5] Louthan, A.M., Doak, D.F. & Angert, A.L. (2015). Where and when do species interactions set range limits? Trends in Ecology & Evolution, 30(12), 780–92. doi: 10.1016/j.tree.2015.09.011
[6] Bartley, T.J., McCann, K.S., Bieg, C., Cazelles, K., Granados, M., Guzzo, M.M., et al. (2019). Food web rewiring in a changing world. Nature Ecology & Evolution, 3(3), 345–54. doi: 10.1038/s41559-018-0772-3
[7] Staniczenko, P.P.A., Lewis, O.T., Jones, N.S. & Reed-Tsochas, F. (2010). Structural dynamics and robustness of food webs. Ecology Letters, 13(7), 891–9. doi: 10.1111/j.1461-0248.2010.01485.x

Parasite intensity is driven by temperature in a wild birdAdèle Mennerat, Anne Charmantier, Sylvie Hurtrez-Boussès, Philippe Perret, Marcel M Lambrechts<p>Increasing awareness that parasitism is an essential component of nearly all aspects of ecosystem functioning, as well as a driver of biodiversity, has led to rising interest in the consequences of climate change in terms of parasitism and dise...Climate change, Evolutionary ecology, Host-parasite interactions, Parasitology, ZoologyJan Hrcek2018-05-17 14:37:14 View
05 Nov 2019
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Crown defoliation decreases reproduction and wood growth in a marginal European beech population.

Defoliation induces a trade-off between reproduction and growth in a southern population of Beech

Recommended by based on reviews by 3 anonymous reviewers

Individuals ability to withstand abiotic and biotic stresses is crucial to the maintenance of populations at climate edge of tree species distribution. We start to have a detailed understanding of tree growth response and to a lesser extent mortality response in these populations. In contrast, our understanding of the response of tree fecundity and recruitment remains limited because of the difficulty to monitor it at the individual tree level in the field. Tree recruitment limitation is, however, crucial for tree population dynamics [1-2].
In their study Oddou-Muratorio et al. [3] use a new method that they recently developed that jointly estimate male and female effective fecundity in natural populations using naturally established seedlings [4]. Their method uses a spatially explicit Bayesian analysis based on molecular markers and parentage analyses (MEMM program [4]). They apply this method to an unmanaged Beech forest at the southern edge of Beech distribution, where tree defoliation – taken as an integrative indicator of tree abiotic and biotic stress – and growth have been monitored for all adult trees.
This allows the authors to explore alternative hypothesis about tree fecundity response to stress. In one hand, biotic and abiotic stresses are thought to negatively impact tree fecundity. In the other hand, management and studies of orchard fruit tree support the idea that stress could trigger a compensatory increase of fecundity at the cost of other performances such as growth and survival.
They show that both growth and female fecundity are negatively affected by defoliation. There was no evidence that stresses trigger a compensatory increase of fecundity. Yet, they also found that, for large highly defoliated trees, there was a trade-off between growth and female fecundity. Some individuals are able to mitigate stress impact on fecundity by decreasing their growth. It is difficult to understand with available data what is driving such divergent responses between defoliated individuals. This could be related to differences in micro-environmental conditions or genetic background of individual trees. Such individual-level difference in response to stress could be crucial to understand tree populations response to ongoing climate change. This study clearly opens exciting new perspectives to apply such new methods to understand the role of fecundity on tree population dynamics. For instance, could we apply this method across the species distribution to understand how effective fecundity and its response to abiotic stress change between southern edge populations, core populations, and northern edge populations? Using time-series retrieved from such analysis can we disentangle the effect of different climatic drivers? It would also be interesting to see how such results can contribute to analyses covering the full tree life cycle to understand the contribution of fecundity response to population and evolutionary.

References

[1] Clark, J. S. et al. (1999). Interpreting recruitment limitation in forests. American Journal of Botany, 86(1), 1-16. doi: 10.2307/2656950
[2] Petit, R. J., and Hampe, A. (2006). Some evolutionary consequences of being a tree. Annu. Rev. Ecol. Evol. Syst., 37, 187-214. doi: 10.1146/annurev.ecolsys.37.091305.110215
[3] Oddou-Muratorio, S., Petit, C., Journe, V., Lingrand, M., Magdalou, J. A., Hurson, C., Garrigue, J., Davi, H. and Magnanou, E. (2019). Crown defoliation decreases reproduction and wood growth in a marginal European beech population. bioRxiv, 474874, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/474874
[4] Oddou‐Muratorio, S. and Klein, E. K. (2008). Comparing direct vs. indirect estimates of gene flow within a population of a scattered tree species. Molecular Ecology, 17(11), 2743-2754. doi: 10.1111/j.1365-294X.2008.03783.x

Crown defoliation decreases reproduction and wood growth in a marginal European beech population.Sylvie Oddou-Muratorio, Cathleen Petit-Cailleux, Valentin Journé, Matthieu Lingrand, Jean-André Magdalou, Christophe Hurson, Joseph Garrigue, Hendrik Davi, Elodie Magnanou.<p>1. Although droughts and heatwaves have been associated to increased crown defoliation, decreased growth and a higher risk of mortality in many forest tree species, their impact on tree reproduction and forest regeneration still remains underst...Climate change, Eco-evolutionary dynamics, Molecular ecology, Physiology, Population ecologyGeorges Kunstler2018-11-20 13:29:42 View
25 Nov 2022
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Positive fitness effects help explain the broad range of Wolbachia prevalences in natural populations

Population dynamics of Wolbachia symbionts playing Dr. Jekyll and Mr. Hyde

Recommended by based on reviews by 3 anonymous reviewers

"Good and evil are so close as to be chained together in the soul"
Robert Louis Stevenson, Dr. Jekyll and Mr. Hyde


Maternally inherited symbionts—microorganisms that pass from a female host to her progeny—have two main ways of increasing their own fitness. First, they can increase the fecundity or viability of infected females. This “positive fitness effects” strategy is the one commonly used by mutualistic symbionts, such as Buchnera aphidicola—the bacterial endosymbiont of the pea aphid, Acyrthosiphon pisum [4]. Second, maternally inherited symbionts can manipulate the reproduction of infected females in a way that enhances symbiont transmission at the expense of host fitness. A famous example of this “reproductive parasitism” strategy is the cytoplasmic incompatibility (CI) [3] induced by bacteria of the genus Wolbachia in their arthropod and nematode hosts. CI works as a toxin-antidote system, whereby the sperm of infected males is modified in a lethal way (toxin) that can only be reverted if the egg is also infected (antidote) [1]. As a result, CI imposes a kind of conditional sterility on their hosts: while infected females are compatible with both infected and uninfected males, uninfected females experience high offspring mortality if (and only if) they mate with infected males [7].

These two symbiont strategies (positive fitness effects versus reproductive parasitism) have been traditionally studied separately, both empirically and theoretically. However, it has become clear that the two strategies are not mutually exclusive, and that a reproductive parasite can simultaneously act as a mutualist—an infection type that has been dubbed “Jekyll and Hyde” [6], after the famous novella by Robert Louis Stevenson about kind scientist Dr. Jekyll and his evil alter ego, Mr. Hyde. In important previous work, Zug and Hammerstein [7] analyzed the consequences of positive fitness effects on the dynamics of different kind of infections, including “Jekyll and Hyde” infections characterized by CI and other reproductive parasitism strategies. Building on this and related modeling framework, Karisto et al. [2] re-investigate and expand on the interplay between positive fitness effects and reproductive parasitism in Wolbachia infections by focusing on CI in both diplodiploid and haplodiploid populations, and by paying particular attention to the mathematical assumption structure underlying their results.

Karisto et al. begin by reviewing classic models of Wolbachia infections in diplodiploid populations that assume a “negative fitness effect” (modeled as a fertility penalty on infected females), characteristic of a pure strategy of reproductive parasitism. Together with the positive frequency-dependent effects due to CI (whereby the fitness benefits to symbionts infecting females increase with the proportion of infected males in the population) this results in population dynamics characterized by two stable equilibria (the Wolbachia-free state and an interior equilibrium with a high frequency of Wolbachia-carrying hosts) separated by an unstable interior equilibrium. Wolbachia can then spread once the initial frequency is above a threshold or an invasion barrier, but is prevented from fixing by a proportion of infections failing to be passed on to offspring. Karisto et al. show that, given the assumption of negative fitness effects, the stable interior equilibrium can never feature a Wolbachia prevalence below one-half. Moreover, they convincingly argue that a prevalence greater than but close to one-half is difficult to maintain in the presence of stochastic fluctuations, as in these cases the high-prevalence stable equilibrium would be too close to the unstable equilibrium signposting the invasion barrier.

Karisto et al. then relax the assumption of negative fitness effects and allow for positive fitness effects (modeled as a fertility premium on infected females) in a diplodiploid population. They show that positive fitness effects may result in situations where the original invasion threshold is now absent, the bistable coexistence dynamics are transformed into purely co-existence dynamics, and Wolbachia symbionts can now invade when rare. Karisto et al. conclude that positive fitness effects provide a plausible and potentially testable explanation for the low frequencies of symbiont-carrying hosts that are sometimes observed in nature, which are difficult to reconcile with the assumption of negative fitness effects. 

Finally, Karisto et al. extend their analysis to haplodiploid host populations (where all fertilized eggs develop as females). Here, they investigate two types of cytoplasmic incompatibility: a female-killing effect, similar to the CI effect studied in diplodiploid populations (the “Leptopilina type” of Vavre et al. [5]) and a masculinization effect, where CI leads to the loss of paternal chromosomes and to the development of the offspring as a male (the “Nasonia type” of Vavre et al. [5]). The models are now two-sex, which precludes a complete analytical treatment, in particular regarding the stability of fixed points. Karisto et al. compensate by conducting large numerical analyses that support their claims. Importantly, all main conclusions regarding the interplay between positive fitness effects and reproductive parasitism continue to hold under haplodiploidy. 

All in all, the analysis and results by Karisto et al. suggest that it is not necessary to resort to classical (but depending on the situation, unlikely) mechanisms, such as ongoing invasion or source-sink dynamics, to explain arthropod populations featuring low-prevalent Wolbachia infections. Instead, low-frequency equilibria might be simply due to reproductive parasites conferring beneficial fitness effects, or Wolbachia symbionts playing Dr. Jekyll (positive fitness effects) and Mr. Hyde (cytoplasmatic incompatibility). 

References

[1] Beckmann JF, Bonneau M, Chen H, Hochstrasser M, Poinsot D, Merçot H, Weill M, Sicard M, Charlat S (2019) The Toxin–Antidote Model of Cytoplasmic Incompatibility: Genetics and Evolutionary Implications. Trends in Genetics, 35, 175–185. https://doi.org/10.1016/j.tig.2018.12.004

[2] Karisto P, Duplouy A, Vries C de, Kokko H (2022) Positive fitness effects help explain the broad range of Wolbachia prevalences in natural populations. bioRxiv, 2022.04.11.487824, ver. 5 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.04.11.487824

[3] Laven H (1956) Cytoplasmic Inheritance in Culex. Nature, 177, 141–142. https://doi.org/10.1038/177141a0

[4] Perreau J, Zhang B, Maeda GP, Kirkpatrick M, Moran NA (2021) Strong within-host selection in a maternally inherited obligate symbiont: Buchnera and aphids. Proceedings of the National Academy of Sciences, 118, e2102467118. https://doi.org/10.1073/pnas.2102467118

[5] Vavre F, Fleury F, Varaldi J, Fouillet P, Bouletreau M (2000) Evidence for Female Mortality in Wolbachia-Mediated Cytoplasmic Incompatibility in Haplodiploid Insects: Epidemiologic and Evolutionary Consequences. Evolution, 54, 191–200. https://doi.org/10.1111/j.0014-3820.2000.tb00019.x

[6] Zug R, Hammerstein P (2015) Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biological Reviews, 90, 89–111. https://doi.org/10.1111/brv.12098

[7] Zug R, Hammerstein P (2018) Evolution of reproductive parasites with direct fitness benefits. Heredity, 120, 266–281. https://doi.org/10.1038/s41437-017-0022-5

Positive fitness effects help explain the broad range of Wolbachia prevalences in natural populationsPetteri Karisto, Anne Duplouy, Charlotte de Vries, Hanna Kokko<p style="text-align: justify;">The bacterial endosymbiont <em>Wolbachia</em> is best known for its ability to modify its host’s reproduction by inducing cytoplasmic incompatibility (CI) to facilitate its own spread. Classical models predict eithe...Host-parasite interactions, Population ecologyJorge Peña2022-04-12 12:52:55 View