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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
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.

References

[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
23 Oct 2023
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The Moa the Merrier: Resolving When the Dinornithiformes Went Extinct

Are Moas ancient Lazarus species?

Recommended by ORCID_LOGO based on reviews by Tim Coulson and Richard Holdaway

Ancient human colonisation often had catastrophic consequences for native fauna. The North American Megafauna went extinct shortly after humans entered the scene and Madagascar suffered twice, before 1500 CE and around 1700 CE after the Malayan and European colonisation. Maoris colonised New Zealand by about 1300 and a century later the giant Moa birds (Dinornithiformes) sharply declined. But did they went extinct or are they an ancient example of Lazarus species, species thought to be extinct but still alive? Scattered anecdotes of late sightings of living Moas even up to the 20th century seem to suggest the latter. The quest for later survival has also a criminal aspect. Who did it, the Maoris or the white colonisers in the late 18th century?

The present work by Floe Foxon (2023) tries to settle this question. It uses a survival modelling approach and an assessment of the reliability of nearly 100 alleged sightings. The model favours the so-called overkill hypothesis, that Moas probably went extinct in the 15th century shortly after Maori colonisation. A small but still remarkable probability remained for survival up to 1770. Later sightings turned out to be highly unreliable.

The paper is important as it does not rely on subjective discussions of late sightings but on a probabilistic modelling approach with sensitivity testing prior applied to marsupials. As common in probabilistic approaches, the study does not finally settle the case. A probability of as much as 20% remained for late survival after 1450 CE. This is not improbable as New Zealand was sufficiently unexplored in those days to harbour a few refuges for late survivors. However, in this respect, it is a bit unfortunate that at the end of the discussion, the paper cites Heuvelmans, the founder of cryptozoology, and it mentions the ivory-billed woodpecker, which has recently been redetected. No Moa remains were found after 1450.

References

Foxon F (2023) The Moa the Merrier: Resolving When the Dinornithiformes Went Extinct. bioRxiv, 2023.08.07.552261, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2023.08.07.552261

The Moa the Merrier: Resolving When the Dinornithiformes Went ExtinctFloe Foxon<p style="text-align: justify;">The Moa (Aves: Dinornithiformes) are an extinct group of the ratite clade from New Zealand. The overkill hypothesis asserts that the first New Zealand settlers hunted the Moa to extinction by 1450 CE, whereas the st...Conservation biology, Human impact, Statistical ecology, ZoologyWerner Ulrich Tim Coulson, Richard Holdaway2023-08-08 17:14:30 View
22 Apr 2021
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The hidden side of the Allee effect: correlated demographic traits and extinction risk in experimental populations

Allee effects under the magnifying glass

Recommended by ORCID_LOGO based on reviews by Tom Van Dooren, Dani Oro and 1 anonymous reviewer

For decades, the effect of population density on individual performance has been studied by ecologists using both theoretical, observational, and experimental approaches. The generally accepted definition of the Allee effect is a positive correlation between population density and average individual fitness that occurs at low population densities, while individual fitness is typically decreased through intraspecific competition for resources at high population densities.  Allee effects are very relevant in conservation biology because species at low population densities would then be subjected to much higher extinction risks. 

However, due to all kinds of stochasticity, low population numbers are always more vulnerable to extinction than larger population sizes. This effect by itself cannot be necessarily ascribed to lower individual performance at low densities, i.e, Allee effects. Vercken and colleagues (2021) address this challenging question and measure the extent to which average individual fitness is affected by population density analyzing 30 experimental populations. As a model system, they use populations of parasitoid wasps of the genus Trichogramma. They report Allee effect in 8 out 30 experimental populations. Vercken and colleagues's work has several strengths. 

First of all, it is nice to see that they put theory at work. This is a very productive way of using theory in ecology. As a starting point, they look at what simple theoretical population models say about Allee effects (Lewis and Kareiva 1993; Amarasekare 1998; Boukal and Berec 2002). These models invariably predict a one-humped relation between population-density and per-capita growth rate. It is important to remark that pure logistic growth, the paradigm of density-dependence, would never predict such qualitative behavior. It is only when there is a depression of per-capita growth rates at low densities that true Allee effects arise. Second, these authors manage to not only experimentally test this main prediction but also report additional demographic traits that are consistently affected by population density. 

In these wasps, individual performance can be measured in terms of the average number of individuals every adult is able to put into the next generation ---the lambda parameter in their analysis. The first panel in figure 3 shows that the per-capita growth rates are lower in populations presenting Allee effects, the ones showing a one-humped behavior in the relation between per-capita growth rates and population densities (see figure 2). Also other population traits, such maximum population size and exitinction probability, change in a correlated and consistent manner. 

In sum, Vercken and colleagues's results are experimentally solid and based on theory expectations. However, they are very intriguing. They find the signature of Allee effects in only 8 out 30 populations, all from the same genus Trichogramma, and some populations belonging to the same species (from different sampling sites) do not show consistently Allee effects. Where does this population variability comes from? What are the reasons underlying this within- and between-species variability? What are the individual mechanisms driving Allee effects in these populations? Good enough, this piece of work generates more intriguing questions than the question is able to clearly answer. Science is not a collection of final answers but instead good questions are the ones that make science progress. 

References

Amarasekare P (1998) Allee Effects in Metapopulation Dynamics. The American Naturalist, 152, 298–302. https://doi.org/10.1086/286169

Boukal DS, Berec L (2002) Single-species Models of the Allee Effect: Extinction Boundaries, Sex Ratios and Mate Encounters. Journal of Theoretical Biology, 218, 375–394. https://doi.org/10.1006/jtbi.2002.3084

Lewis MA, Kareiva P (1993) Allee Dynamics and the Spread of Invading Organisms. Theoretical Population Biology, 43, 141–158. https://doi.org/10.1006/tpbi.1993.1007

Vercken E, Groussier G, Lamy L, Mailleret L (2021) The hidden side of the Allee effect: correlated demographic traits and extinction risk in experimental populations. HAL, hal-02570868, ver. 4 peer-reviewed and recommended by Peer community in Ecology. https://hal.archives-ouvertes.fr/hal-02570868

The hidden side of the Allee effect: correlated demographic traits and extinction risk in experimental populationsVercken Elodie, Groussier Géraldine, Lamy Laurent, Mailleret Ludovic<p style="text-align: justify;">Because Allee effects (i.e., the presence of positive density-dependence at low population size or density) have major impacts on the dynamics of small populations, they are routinely included in demographic models ...Demography, Experimental ecology, Population ecologyDavid Alonso2020-09-30 16:38:29 View
14 Jun 2024
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Hierarchizing multi-scale environmental effects on agricultural pest population dynamics: a case study on the annual onset of Bactrocera dorsalis population growth in Senegalese orchards

Uncovering the ecology in big-data by hierarchizing multi-scale environmental effects

Recommended by based on reviews by Kévin Tougeron and Jianqiang Sun

Along with the generalization of open-access practices, large, heterogeneous datasets are becoming increasingly available to ecologists (Farley et al. 2018). While such data offer exciting opportunities for unveiling original patterns and trends, they also raise new challenges regarding how to extract relevant information and actually improve our knowledge of complex ecological systems, beyond purely descriptive correlations (Dietze 2017, Farley et al. 2018).

In this work, Caumette et al. (2024) develop an original ecoinformatics approach to relate multi-scale environmental factors to the temporal dynamics of a major pest in mango orchards. Their method relies on the recent tree-boosting method GPBoost (Sigrist 2022) to hierarchize the influence of environmental factors of heterogeneous nature (e.g., orchard composition and management; landscape structure; climate) on the emergence date of the oriental fruit fly, Bactrocera dorsalis. As boosting methods allows the analysis of high-dimensional data, they are particularly adapted to the exploration of such datasets, to uncover unexpected, potentially complex dependencies between ecological dynamics and multiple environmental factors (Farley et al. 2018). In this article, Caumette et al. (2024) make a special effort to guide the reader step by step through their complex analysis pipeline to make it broadly understandable to the average ecologist, which is no small feat. I particularly welcome this commitment, as making new, cutting-edge analytical methods accessible to a large community of science practitioners with varying degrees of statistical or programming expertise is a major challenge for the future of quantitative ecology. 

The main result of Caumette et al. (2024) is that temperature and humidity conditions both at the local and regional scales are the main predictors of B. dorsalis emergence date, while orchard management practices seem to have relatively little influence. This suggests that favourable climatic conditions may allow the persistence of small populations of B. dorsalis over the dry season, which may then act as a propagule source for early re-infestations. However, as the authors explain, the resulting regression model is not designed for predictive purposes and should not at this stage be used for decision-making in pest management. Its main interest rather resides in identifying potential key factors favoring early infestations of B. dorsalis, and help focusing future experimental field studies on the most relevant levers for integrated pest management in mango orchards.

In a wider perspective, this work also provides a convincing proof-of-concept for the use of boosting methods to identify the most influential factors in large, multivariate datasets in a variety of ecological systems. It is also crucial to keep in mind that the current exponential growth in high-throughput environmental data (Lucivero 2020) could quickly come into conflict with the need to reduce the environmental footprint of research (Mariette et al. 2022). In this context, robust and accessible methods for extracting and exploiting all the information available in already existing datasets might prove essential to a sustainable pursuit of science.

References
 
Caumette C, Diatta P, Piry S, Chapuis M-P, Faye E, Sigrist F, Martin O, Papaïx J, Brévault T, Berthier K. 2024. Hierarchizing multi-scale environmental effects on agricultural pest population dynamics: a case study on the annual onset of Bactrocera dorsalis population growth in Senegalese orchards. bioRxiv 2023.11.10.566583, ver. 3 peer-reviewed and recommended by Peer Community in Ecology.  https://doi.org/10.1101/2023.11.10.566583

Dietze MC. 2017. Ecological Forecasting. Princeton University Press
 
Farley SS, Dawson A, Goring SJ, Williams JW. 2018. Situating Ecology as a Big-Data Science: Current Advances, Challenges, and Solutions. BioScience, 68, 563–576, https://doi.org/10.1093/biosci/biy068
 
Lucivero F. 2020. Big Data, Big Waste? A Reflection on the Environmental Sustainability of Big Data Initiatives. Science and Engineering Ethics 26, 1009–1030. https://doi.org/10.1007/s11948-019-00171-7

Mariette J, Blanchard O, Berné O, Aumont O, Carrey J, Ligozat A-L, Lellouch E, Roche P-E, Guennebaud G, Thanwerdas J, Bardou P, Salin G, Maigne E, Servan S, Ben-Ari T 2022. An open-source tool to assess the carbon footprint of research. Environmental Research: Infrastructure and Sustainability, 2022. https://dx.doi.org/10.1088/2634-4505/ac84a4
 
Sigrist F. 2022. Gaussian process boosting. The Journal of Machine Learning Research, 23, 10565-10610. https://jmlr.org/papers/v23/20-322.html
 

Hierarchizing multi-scale environmental effects on agricultural pest population dynamics: a case study on the annual onset of *Bactrocera dorsalis* population growth in Senegalese orchardsCécile Caumette, Paterne Diatta, Sylvain Piry, Marie-Pierre Chapuis, Emile Faye, Fabio Sigrist, Olivier Martin, Julien Papaïx, Thierry Brévault, Karine Berthier<p>Implementing integrated pest management programs to limit agricultural pest damage requires an understanding of the interactions between the environmental variability and population demographic processes. However, identifying key environmental ...Demography, Landscape ecology, Statistical ecologyElodie Vercken2023-12-11 17:02:08 View
18 Mar 2019
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Evaluating functional dispersal and its eco-epidemiological implications in a nest ectoparasite

Limited dispersal in a vector on territorial hosts

Recommended by based on reviews by Shelly Lachish and 1 anonymous reviewer

Parasitism requires parasites and hosts to meet and is therefore conditioned by their respective dispersal abilities. While dispersal has been studied in a number of wild vertebrates (including in relation to infection risk), we still have poor knowledge of the movements of their parasites. Yet we know that many parasites, and in particular vectors transmitting pathogens from host to host, possess the ability to move actively during at least part of their lives.
So... how far does a vector go – and is this reflected in the population structure of the pathogens they transmit? This is the question addressed by Rataud et al. [1], who provide the first attempt at using capture-mark-recapture to estimate not only functional dispersal, but also detection probability and survival in a wild parasite that is also a vector for other pathogens.
The authors find that (i) functional dispersal of soft ticks within a gull colony is very limited. Moreover, they observe unexpected patterns: (ii) experimental displacement of ticks does not induce homing behaviour, and (iii) despite lower survival, tick dispersal was lower in nests not containing hosts than in successful nests.
These results contrast with expectations based on the distribution of infectious agents. Low tick dispersal within the colony, combined with host territoriality during breeding and high site fidelity between years should result in a spatially structured distribution of infectious agents carried by ticks. This is not the case here. One possible explanation could be that soft ticks live for much longer than a breeding season, and that they disperse at other times of year to a larger extent than usually assumed.
This study represents one chapter of a story that will likely keep unfolding. It raises fascinating questions, and illustrates the importance of basic knowledge of parasite ecology and behaviour to better understand pathogen dynamics in the wild.

References
[1] Rataud A., Dupraz M., Toty C., Blanchon T., Vittecoq M., Choquet R. & McCoy K.D. (2019). Evaluating functional dispersal and its eco-epidemiological implications in a nest ectoparasite. Zenodo, 2592114. Ver. 3 peer-reviewed and recommended by PCI Ecology. doi: 10.5281/zenodo.2592114

Evaluating functional dispersal and its eco-epidemiological implications in a nest ectoparasiteAmalia Rataud, Marlène Dupraz, Céline Toty, Thomas Blanchon, Marion Vittecoq, Rémi Choquet, Karen D. McCoy<p>Functional dispersal (between-site movement, with or without subsequent reproduction) is a key trait acting on the ecological and evolutionary trajectories of a species, with potential cascading effects on other members of the local community. ...Dispersal & Migration, Epidemiology, Parasitology, Population ecologyAdele Mennerat2018-11-05 11:44:58 View
12 Jan 2024
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Methods for tagging an ectoparasite, the salmon louse Lepeophtheirus salmonis

Marking invertebrates using RFID tags

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

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

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

References

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

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

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

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

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

 

Methods for tagging an ectoparasite, the salmon louse *Lepeophtheirus salmonis*Alexius Folk, Adele Mennerat<p style="text-align: justify;">Monitoring individuals within populations is a cornerstone in evolutionary ecology, yet individual tracking of invertebrates and particularly parasitic organisms remains rare. To address this gap, we describe here a...Dispersal & Migration, Evolutionary ecology, Host-parasite interactions, Marine ecology, Parasitology, Terrestrial ecology, ZoologyNicolas Schtickzelle2023-09-04 15:25:08 View
27 Jan 2023
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Spatial heterogeneity of interaction strength has contrasting effects on synchrony and stability in trophic metacommunities

How does spatial heterogeneity affect stability of trophic metacommunities?

Recommended by ORCID_LOGO based on reviews by Phillip P.A. Staniczenko, Ludek Berec and Diogo Provete

The temporal or spatial variability in species population sizes and interaction strength of animal and plant communities has a strong impact on aggregate community properties (for instance biomass), community composition, and species richness (Kokkoris et al. 2002). Early work on spatial and temporal variability strongly indicated that asynchronous population and environmental fluctuations tend to stabilise community structures and diversity (e.g. Holt 1984, Tilman and Pacala 1993, McCann et al. 1998, Amarasekare and Nisbet 2001). Similarly, trophic networks might be stabilised by spatial heterogeneity (Hastings 1977) and an asymmetry of energy flows along food chains (Rooney et al. 2006). The interplay between temporal, spatial, and trophic heterogeneity within the meta-community concept has got much less interest. In the recent preprint in PCI Ecology, Quévreux et al. (2023) report that Spatial heterogeneity of interaction strength has contrasting effects on synchrony and stability in trophic metacommunities. These authors rightly notice that the interplay between trophic and spatial heterogeneity might induce contrasting effects depending on the internal dynamics of the system. Their contribution builds on prior work (Quévreux et al. 2021a, b) on perturbed trophic cascades.

I found this paper particularly interesting because it is in the, now century-old, tradition to show that ecological things are not so easy. Since the 1930th, when Nicholson and Baily and others demonstrated that simple deterministic population models might generate stability and (pseudo-)chaos ecologists have realised that systems triggered by two or more independent processes might be intrinsically unpredictable and generate different outputs depending on the initial parameter settings. This resembles the three-body problem in physics. The present contribution of Quévreux et al. (2023) extends this knowledge to an example of a spatially explicit trophic model. Their main take-home message is that asymmetric energy flows in predator–prey relationships might have contrasting effects on the stability of metacommunities receiving localised perturbations. Stability is context dependent.

Of course, the work is merely a theoretical exercise using a simplistic trophic model. It demands verification with field data. Nevertheless, we might expect even stronger unpredictability in more realistic multitrophic situations. Therefore, it should be seen as a proof of concept. Remember that increasing trophic connectance tends to destabilise food webs (May 1972). In this respect, I found the final outlook to bioconservation ambitious but substantiated. Biodiversity management needs a holistic approach focusing on all aspects of ecological functioning. I would add the need to see stability and biodiversity within an evolutionary perspective.        

References

Amarasekare P, Nisbet RM (2001) Spatial Heterogeneity, Source‐Sink Dynamics, and the Local Coexistence of Competing Species. The American Naturalist, 158, 572–584. https://doi.org/10.1086/323586

Hastings A (1977) Spatial heterogeneity and the stability of predator-prey systems. Theoretical Population Biology, 12, 37–48. https://doi.org/10.1016/0040-5809(77)90034-X

Holt RD (1984) Spatial Heterogeneity, Indirect Interactions, and the Coexistence of Prey Species. The American Naturalist, 124, 377–406. https://doi.org/10.1086/284280

Kokkoris GD, Jansen VAA, Loreau M, Troumbis AY (2002) Variability in interaction strength and implications for biodiversity. Journal of Animal Ecology, 71, 362–371. https://doi.org/10.1046/j.1365-2656.2002.00604.x

May RM (1972) Will a Large Complex System be Stable? Nature, 238, 413–414. https://doi.org/10.1038/238413a0

McCann K, Hastings A, Huxel GR (1998) Weak trophic interactions and the balance of nature. Nature, 395, 794–798. https://doi.org/10.1038/27427

Quévreux P, Barbier M, Loreau M (2021) Synchrony and Perturbation Transmission in Trophic Metacommunities. The American Naturalist, 197, E188–E203. https://doi.org/10.1086/714131

Quévreux P, Pigeault R, Loreau M (2021) Predator avoidance and foraging for food shape synchrony and response to perturbations in trophic metacommunities. Journal of Theoretical Biology, 528, 110836. https://doi.org/10.1016/j.jtbi.2021.110836

Quévreux P, Haegeman B, Loreau M (2023) Spatial heterogeneity of interaction strength has contrasting effects on synchrony and stability in trophic metacommunities. hal-03829838, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://hal.science/hal-03829838

Rooney N, McCann K, Gellner G, Moore JC (2006) Structural asymmetry and the stability of diverse food webs. Nature, 442, 265–269. https://doi.org/10.1038/nature04887

Tilman D, Pacala S (1993) The maintenance of species richness in plant communities. In: Ricklefs, R.E., Schluter, D. (eds) Species Diversity in Ecological Communities: Historical and Geographical Perspectives. University of Chicago Press, pp. 13–25.

Spatial heterogeneity of interaction strength has contrasting effects on synchrony and stability in trophic metacommunitiesPierre Quévreux, Bart Haegeman and Michel Loreau<p>&nbsp;Spatial heterogeneity is a fundamental feature of ecosystems, and ecologists have identified it as a factor promoting the stability of population dynamics. In particular, differences in interaction strengths and resource supply between pa...Dispersal & Migration, Food webs, Interaction networks, Spatial ecology, Metacommunities & Metapopulations, Theoretical ecologyWerner Ulrich2022-10-26 13:38:34 View
16 Jun 2020
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Environmental perturbations and transitions between ecological and evolutionary equilibria: an eco-evolutionary feedback framework

Stasis and the phenotypic gambit

Recommended by based on reviews by Jacob Johansson, Katja Räsänen and 1 anonymous reviewer

The preprint "Environmental perturbations and transitions between ecological and evolutionary equilibria: an eco-evolutionary feedback framework" by Coulson (2020) presents a general framework for evolutionary ecology, useful to interpret patterns of selection and evolutionary responses to environmental transitions. The paper is written in an accessible and intuitive manner. It reviews important concepts which are at the heart of evolutionary ecology. Together, they serve as a worldview which you can carry with you to interpret patterns in data or observations in nature. I very much appreciate it that Coulson (2020) presents his personal intuition laid bare, the framework he uses for his research and how several strong concepts from theoretical ecology fit in there. Overviews as presented in this paper are important to understand how we as researchers put the pieces together.
A main message of the paper is that resource detection and acquisition traits, broadly called "resource accrual traits" are at the core of evolutionary dynamics. These traits and the processes they are involved in often urge some degree of individual specialization. Not all traits are resource accrual traits all the time. Guppies are cited as an example, which have traits in high predation environments that make foraging easier for them, such as being less conspicuous to predators. In the absence of predators, these same traits might be neutral. Their colour pattern might then contribute much less to the odds of obtaining resources.
"Resource accrual" reminds me of discussions of resource holding potential (Parker 1974), which can be for example the capacity to remain on a bird feeder without being dislodged. However, the idea is much broader and aggression does not need to be important for the acquisition of resources. Evolutionary success is reserved for those steadily obtaining resources. This recalls the pessimization principle of Metz et al. (2008), which applies in a restricted set of situations and where the strategy which persists at the lowest resource levels systematically wins evolutionary contests. If this principle would apply universally, the world then inherently become the worst possible. Resources determine energy budgets and different life history strategies allocate these differently to maximize fitness. The fine grain of environments and the filtration by individual histories generate a lot of variation in outcomes. However, constraint-centered approaches (Kempes et al. 2019, Kooijman 2010) are mentioned but are not at the core of this preprint. Evolution is rather seen as dynamic programming optimization with interactions within and between species. Coulson thus extends life history studies such as for example Tonnabel et al. (2012) with eco-evolutionary feedbacks. Examples used are guppies, algae-rotifer interactions and others. Altogether, this makes for an optimistic paper pushing back the pessimization principle.
Populations are expected to spend most of the time in quasi-equilibrium states where the long run stochastic growth rate is close to zero for all genotypes, alleles or other chosen classes. In the preprint, attention is given to reproductive value calculus, another strong tool in evolutionary dynamics (Grafen 2006, Engen et al. 2009), which tells us how classes within a population contribute to population composition in the distant future. The expected asymptotic fitness of an individual is equated to its expected reproductive value, but this might require particular ways of calculating reproductive values (Coulson 2020). Life history strategies can also be described by per generation measures such as R0 (currently on everyone's radar due to the coronavirus pandemic), generation time etc. Here I might disagree because I believe that this focus in per generation measures can lead to an incomplete characterization of plastic and other strategies involved in strategies such as bet-hedging. A property at quasi-equilibrium states is precise enough to serve as a null hypothesis which can be falsified: all types must in the long run leave equal numbers of descendants. If there is any property in evolutionary ecology which is useful it is this one and it rightfully merits attention.
However, at quasi-equilibrium states, directional selection has been observed, often without the expected evolutionary response. The preprint aims to explain this and puts forward the presence of non-additive gene action as a mechanism. I don't believe that it is the absence of clonal inheritance which matters very much in itself (Van Dooren 2006) unless genes with major effect are present in protected polymorphisms. The preprint remains a bit unclear on how additive gene action is broken, and here I add from the sphere in which I operate. Non-additive gene action can be linked to non-linear genotype-phenotype maps (Van Dooren 2000, Gilchrist and Nijhout 2001) and if these maps are non-linear enough to create constraints on phenotype determination, by means of maximum or minimum phenotypes which cannot be surpassed for any combination of the underlying traits, then they create additional evolutionary quasi-equilibrium states, with directional selection on a phenotype such as body size. I believe Coulson hints at this option (Coulson et al. 2006), but also at a different one: if body size is mostly determined by variation in resource accrual traits, then the resource accrual traits can be under stabilizing selection while body size is not. This requires that all resource accrual traits affect other phenotypic or demographic properties next to body size. In both cases, microevolutionary outcomes cannot be inferred from inspecting body sizes alone, either resource accrual traits need to be included explicitly, or non-linearities, or both when the map between resource accrual and body size is non-linear (Van Dooren 2000).
The discussion of the phenotypic gambit (Grafen 1984) leads to another long-standing issue in evolutionary biology. Can predictions of adaptation be made by inspecting and modelling individual phenotypes alone? I agree that with strongly non-linear genotype-phenotype maps they cannot and for multivariate sets of traits, genetic and phenotypic correlations can be very different (Hadfield et al. 2007). However, has the phenotypic gambit ever claimed to be valid globally or should it rather be used locally for relatively small amounts of variation? Grafen (1984) already contained caveats which are repeated here. As a first approximation, additivity might produce quite correct predictions and thus make the gambit operational in many instances. When important individual traits are omitted, it may just be misspecified. I am interested to see cases where the framework Coulson (2020) proposes is used for very large numbers of phenotypic and genotypic attributes. In the end, these highly dimensional trait distributions might basically collapse to a few major axes of variation due to constraints on resource accrual.
I highly recommend reading this preprint and I am looking forward to the discussion it will generate.

References

[1] Coulson, T. (2020) Environmental perturbations and transitions between ecological and evolutionary equilibria: an eco-evolutionary feedback framework. bioRxiv, 509067, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/509067
[2] Coulson, T., Benton, T. G., Lundberg, P., Dall, S. R. X., and Kendall, B. E. (2006). Putting evolutionary biology back in the ecological theatre: a demographic framework mapping genes to communities. Evolutionary Ecology Research, 8(7), 1155-1171.
[3] Engen, S., Lande, R., Sæther, B. E. and Dobson, F. S. (2009) Reproductive value and the stochastic demography of age-structured populations. The American Naturalist 174: 795-804. doi: 10.1086/647930
[4] Gilchrist, M. A. and Nijhout, H. F. (2001). Nonlinear developmental processes as sources of dominance. Genetics, 159(1), 423-432.
[5] Grafen, A. (1984) Natural selection, kin selection and group selection. In: Behavioural Ecology: An Evolutionary Approach,2nd edn (JR Krebs & NB Davies eds), pp. 62–84. Blackwell Scientific, Oxford.
[6] Grafen, A. (2006). A theory of Fisher's reproductive value. Journal of mathematical biology, 53(1), 15-60. doi: 10.1007/s00285-006-0376-4
[7] Hadfield, J. D., Nutall, A., Osorio, D. and Owens, I. P. F. (2007). Testing the phenotypic gambit: phenotypic, genetic and environmental correlations of colour. Journal of evolutionary biology, 20(2), 549-557. doi: 10.1111/j.1420-9101.2006.01262.x
[8] Kempes, C. P., West, G. B., and Koehl, M. (2019). The scales that limit: the physical boundaries of evolution. Frontiers in Ecology and Evolution, 7, 242. doi: 10.3389/fevo.2019.00242
[9] Kooijman, S. A. L. M. (2010) Dynamic Energy Budget theory for metabolic organisation. University Press, third edition.
[10] Metz, J. A. J., Mylius, S.D. and Diekman, O. (2008) When does evolution optimize?. Evolutionary Ecology Research 10: 629-654.
[11] Parker, G. A. (1974). Assessment strategy and the evolution of fighting behaviour. Journal of theoretical Biology, 47(1), 223-243. doi: 10.1016/0022-5193(74)90111-8
[12] Tonnabel, J., Van Dooren, T. J. M., Midgley, J., Haccou, P., Mignot, A., Ronce, O., and Olivieri, I. (2012). Optimal resource allocation in a serotinous non‐resprouting plant species under different fire regimes. Journal of Ecology, 100(6), 1464-1474. doi: 10.1111/j.1365-2745.2012.02023.x
[13] Van Dooren, T. J. M. (2000). The evolutionary dynamics of direct phenotypic overdominance: emergence possible, loss probable. Evolution, 54(6), 1899-1914. doi: 10.1111/j.0014-3820.2000.tb01236.x
[14] Van Dooren, T. J. M. (2006). Protected polymorphism and evolutionary stability in pleiotropic models with trait‐specific dominance. Evolution, 60(10), 1991-2003. doi: 10.1111/j.0014-3820.2006.tb01837.x

Environmental perturbations and transitions between ecological and evolutionary equilibria: an eco-evolutionary feedback frameworkTim Coulson<p>I provide a general framework for linking ecology and evolution. I start from the fact that individuals require energy, trace molecules, water, and mates to survive and reproduce, and that phenotypic resource accrual traits determine an individ...Eco-evolutionary dynamics, Evolutionary ecologyTom Van Dooren2019-01-03 10:05:16 View
05 Jun 2024
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Attracting pollinators vs escaping herbivores: eco-evolutionary dynamics of plants confronted with an ecological trade-off

Plant-herbivore-pollinator ménage-à-trois: tell me how well they match, and I'll tell you if it's made to last

Recommended by ORCID_LOGO based on reviews by Marcos Mendez and Yaroslav Ispolatov

How would a plant trait evolve if it is involved in interacting with both a pollinator and an herbivore species? The answer by Yacine and Loeuille is straightforward: it is not trivial, but it can explain many situations found in natural populations.

Yacine and Loeuille applied the well-known Adaptive Dynamics framework to a system with three interacting protagonists: a herbivore, a pollinator, and a plant. The evolution of a plant trait is followed under the assumption that it regulates the frequency of interaction with the two other species. As one can imagine, that is where problems begin: interacting more with pollinators seems good, but what if at the same time it implies interacting more with herbivores? And that's not a silly idea, as there are many cases where herbivores and pollinators share the same cues to detect plants, such as colors or chemical compounds.

They found that depending on the trade-off between the two types of interactions and their density-dependent effects on plant fitness, the possible joint ecological and evolutionary outcomes are numerous. When herbivory prevails, evolution can make the ménage-à-trois ecologically unstable, as one or even two species can go extinct, leaving the plant alone. Evolution can also make the coexistence of the three species more stable when pollination services prevail, or lead to the appearance of a second plant species through branching diversification of the plant trait when herbivory and pollination are balanced.

Yacine and Loeuille did not only limit themselves to saying "it is possible," but they also did much work evaluating when each evolutionary outcome would occur. They numerically explored in great detail the adaptive landscape of the plant trait for a large range of parameter values. They showed that the global picture is overall robust to parameter variations, strengthening the plausibility that the evolution of a trait involved in antagonistic interactions can explain many of the correlations between plant and animal traits or phylogenies found in nature.

Are we really there yet? Of course not, as some assumptions of the model certainly limit its scope. Are there really cases where plants' traits evolve much faster than herbivores' and pollinators' traits? Certainly not, but the model is so general that it can apply to any analogous system where one species is caught between a mutualistic and a predator species, including potential species that evolve much faster than the two others. And even though this limitation might cast doubt on the generality of the model's predictions, studying a system where a species' trait and a preference trait coevolve is possible, as other models have already been studied (see Fritsch et al. 2021 for a review in the case of evolution in food webs). We can bet this is the next step taken by Yacine and Loeuille in a similar framework with the same fundamental model, promising fascinating results, especially regarding the evolution of complex communities when species can accumulate after evolutionary branchings.

Relaxing another assumption seems more challenging as it would certainly need to change the model itself: interacting species generally do not play fixed roles, as being mutualistic or antagonistic might generally be density-dependent (Holland and DeAngelis 2010). How would the exchange of resources between three interacting species evolve? It is an open question.

References

Fritsch, C., Billiard, S., & Champagnat, N. (2021). Identifying conversion efficiency as a key mechanism underlying food webs adaptive evolution: a step forward, or backward? Oikos, 130(6), 904-930.
https://doi.org/10.1111/oik.07421
 
Holland, J. N., & DeAngelis, D. L. (2010). A consumer-resource approach to the density‐dependent population dynamics of mutualism. Ecology, 91(5), 1286-1295.
https://doi.org/10.1890/09-1163.1

Yacine, Y., & Loeuille, N. (2024) Attracting pollinators vs escaping herbivores: eco-evolutionary dynamics of plants confronted with an ecological trade-off. bioRxiv 2021.12.02.470900; doi: https://doi.org/10.1101/2021.12.02.470900

Attracting pollinators vs escaping herbivores: eco-evolutionary dynamics of plants confronted with an ecological trade-offYoussef Yacine, Nicolas Loeuille<p style="text-align: justify;">Many plant traits are subject to an ecological trade-off between attracting pollinators and escaping herbivores. The interplay of both plant-animal interaction types determines their evolution. As most studies focus...Eco-evolutionary dynamics, Herbivory, Pollination, Theoretical ecologySylvain Billiard2023-03-21 14:23:12 View