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08 Aug 2020
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Trophic cascade driven by behavioural fine-tuning as naïve prey rapidly adjust to a novel predator

While the quoll’s away, the mice will play… and the seeds will pay

Recommended by based on reviews by 2 anonymous reviewers

A predator can strongly influence the demography of its prey, which can have profound carryover effects on the trophic network; so-called density-mediated indirect interactions (DMII; Werner and Peacor 2003; Schmitz et al. 2004; Trussell et al. 2006). Furthermore, a novel predator can alter the phenotypes of its prey for traits that will change prey foraging efficiency. These trait-mediated indirect interactions may in turn have cascading effects on the demography and features of the basal resources consumed by the intermediate consumer (TMIII; Werner and Peacor 2003; Schmitz et al. 2004; Trussell et al. 2006), but very few studies have looked for these effects (Trusell et al. 2006). The study “Trophic cascade driven by behavioural fine-tuning as naïve prey rapidly adjust to a novel predator”, by Jolly et al. (2020) is therefore a much-needed addition to knowledge in this field. The authors have profited from a rare introduction of Northern quolls (Dasyurus hallucatus) on an Australian island, to examine both the density-mediated and trait-mediated indirect interactions with grassland melomys (Melomys burtoni) and the vegetation of their woodland habitat.
Jolly et al. (2020) compared melomys populations in four quoll-invaded and three quoll-free sites on the same island. Using capture-mark-recapture methods, they found a lower survival and decreased population size in quoll-invaded sites compared to quoll-free sites. Although they acknowledge that this decline could be attributable to either the direct effects of the predator or to a wildfire that occurred early in the experiment in the quoll-invaded sites, the authors argue that the wildfire alone cannot explain all of their results.
Beyond demographic effects, Jolly et al. (2020) also examined risk taking, foraging behaviour, and predator avoidance in melomys. Quoll presence was first associated with a strong decrease in risk taking in melomys, but the difference disappeared over the three years of study, indicating a possible adjustment by the prey. In quoll-invaded sites, though, melomys continued to be more neophobic than in the quoll-free sites throughout the study. Furthermore, in a seed (i.e. wheat) removal experiment, Jolly et al. (2020) measured how melomys harvested seeds in the presence or absence of predator scents. In both quoll-invaded and quoll-free sites, melomys density increased seed harvest efficiency. Melomys also removed less seeds in quoll-invaded sites than in quoll-free sites, supporting both the DMII and TMII hypotheses. However, in the quoll-invaded sites only, melomys foraged less on predator-scented seed patches than on unscented ones, trading foraging efficiency for an increased safety against predators, and this effect increased across the years. This last result indicates that predators can indirectly influence seed consumption through the trade-off between foraging and predator avoidance, strongly supporting the TMII hypothesis.
Ideally, the authors would have run a nice before-after, impact-control design, but nature does not always allow for ideal experimental designs. Regardless, the results of such an “experiment in the wild” predation study are still valuable, as they are very rare (Trussell et al. 2006), and they provide crucial information on the direct and indirect interactions along a trophic cascade. Furthermore, the authors have effectively addressed any concerns about potential confounding factors, and thus have a convincing argument that their results represent predator-driven demographic and behavioural changes.
One important question remains from an evolutionary ecology standpoint: do the responses of melomys to the presence of quolls represent phenotypically plastic changes or rapid evolutionary changes caused by novel selection pressures? Classically, TMII are assumed to be mostly caused by phenotypic plasticity (Werner and Peacor 2003), and this might be the case when the presence of the predator is historical. Phenotypic plasticity allows quick and reversible adjustments of the prey population to changes in the predator density. When the predator population declines, such rapid phenotypic changes can be reversed, reducing the cost associated with anti-predator behaviour (e.g., lower foraging efficiency) in the absence of predators. In the case of a novel predator, however, short-term evolutionary responses by the prey may play role in the TMII, as they would allow a phenotypic shift in prey’s traits along the trade-off between foraging efficiency and anti-predator response that will probably more advantageous over the longer term, if the predator does not disappear. The authors state that they could not rule out one or the other of these hypotheses. However, future work estimating the relative importance of phenotypic plasticity and evolutionary changes in the quoll-melomys system would be valuable. Phenotypic selection analysis, for example, by estimating the link between survival and the traits measured, might help test for a fitness advantage to altered behaviour in the presence of a predator. Common garden experiments, comparing the quoll-invaded and the quoll-free melomys populations, might also provide information on any potential evolutionary changes caused by predation. More work could also analyse the potential effects on the seed populations. Not only might the reduction in seed predation have consequences on the landscape in the future, as the authors mention, but it may also mean that the seeds themselves could be subject to novel selection pressures, which may affect their phenology, physiology or life history. Off course, the authors will have to switch from wheat to a more natural situation, and evaluate the effects of changes in the melomys population on the feature of the local vegetation and the ecosystem.
Finally, the authors have not yet found that the observed changes in the traits have translated into a demographic rebound for melomys. Here again, I can see an interesting potential for further studies. Should we really expect an evolutionary rescue (Bell and Gonzalez 2009) in this system? Alternatively, should the changes in behaviour be accompanied by permanent changes in life history, such as a slower pace-of-life (Réale et al. 2010) that could possibly lead to lower melomys density?
This paper provides nice in natura evidence for density- and trait-mediated indirect interactions hypotheses. I hope it will be the first of a long series of work on this interesting quoll-melomys system, and that the authors will be able to provide more information on the eco-evolutionary consequences of a novel predator on a trophic network.

References

-Bell G, Gonzalez A (2009) Evolutionary rescue can prevent extinction following environmental change. Ecology letters, 12(9), 942-948. https://doi.org/10.1111/j.1461-0248.2009.01350.x
-Jolly CJ, Smart AS, Moreen J, Webb JK, Gillespie GR, Phillips BL (2020) Trophic cascade driven by behavioural fine-tuning as naïve prey rapidly adjust to a novel predator. bioRxiv, 856997, ver. 6 peer-reviewed and recommended by PCI Ecology. https://doi.org/ 10.1101/856997
-Matassa C, Ewanchuk P, Trussell G (2018) Cascading effects of a top predator on intraspecific competition at intermediate and basal trophic levels. Functional Ecology, 32(9), 2241-2252. https://doi.org/10.1111/1365-2435.13131
-Réale D, Garant D, Humphries MM, Bergeron P, Careau V, Montiglio PO (2010) Personality and the emergence of the pace-of-life syndrome concept at the population level. Philosophical Transactions of the Royal Society B: Biological Sciences, 365(1560), 4051-4063. https://doi.org/10.1098/rstb.2010.0208
-Schmitz O, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait‐mediated indirect interactions. Ecology Letters 7(2), 153-163. https://doi.org/10.1111/j.1461-0248.2003.00560.x
-Trussell G, Ewanchuk P, Matassa C (2006). Habitat effects on the relative importance of trait‐ and density‐mediated indirect interactions. Ecology Letters, 9(11), 1245-1252. https://doi.org/10.1111/j.1461-0248.2006.00981.x
-Werner EE, Peacor SD (2003) A review of trait‐mediated indirect interactions in ecological communities. Ecology, 84(5), 1083-1100. https://doi.org/10.1890/0012-9658(2003)084[1083:AROTII]2.0.CO;2

Trophic cascade driven by behavioural fine-tuning as naïve prey rapidly adjust to a novel predatorChris J Jolly, Adam S Smart, John Moreen, Jonathan K Webb, Graeme R Gillespie and Ben L Phillips<p>The arrival of novel predators can trigger trophic cascades driven by shifts in prey numbers. Predators also elicit behavioural change in prey populations, via phenotypic plasticity and/or rapid evolution, and such changes may also contribute t...Behaviour & Ethology, Biological invasions, Evolutionary ecology, Experimental ecology, Foraging, Herbivory, Population ecology, Terrestrial ecology, Tropical ecologyDenis Réale2019-11-27 21:39:44 View
12 Aug 2021
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A study on the role of social information sharing leading to range expansion in songbirds with large vocal repertoires: Enhancing our understanding of the Great-Tailed Grackle (Quiscalus mexicanus) alarm call

Does the active vocabulary in Great-tailed Grackles supports their range expansion? New study will find out

Recommended by Jan Oliver Engler based on reviews by Guillermo Fandos and 2 anonymous reviewers

Alarm calls are an important acoustic signal that can decide the life or death of an individual. Many birds are able to vary their alarm calls to provide more accurate information on e.g. urgency or even the type of a threatening predator. According to the acoustic adaptation hypothesis, the habitat plays an important role too in how acoustic patterns get transmitted. This is of particular interest for range-expanding species that will face new environmental conditions along the leading edge. One could hypothesize that the alarm call repertoire of a species could increase in newly founded ranges to incorporate new habitats and threats individuals might face. Hence selection for a larger active vocabulary might be beneficial for new colonizers. Using the Great-Tailed Grackle (Quiscalus mexicanus) as a model species, Samantha Bowser from Arizona State University and Maggie MacPherson from Louisiana State University want to find out exactly that. 

The Great-Tailed Grackle is an appropriate species given its high vocal diversity. Also, the species consists of different subspecies that show range expansions along the northern range edge yet to a varying degree. Using vocal experiments and field recordings the researchers have a high potential to understand more about the acoustic adaptation hypothesis within a range dynamic process. 

Over the course of this assessment, the authors incorporated the comments made by two reviewers into a strong revision of their research plans. With that being said, the few additional comments made by one of the initial reviewers round up the current stage this interesting research project is in. 

To this end, I can only fully recommend the revised research plan and am much looking forward to the outcomes from the author’s experiments, modeling, and field data. With the suggestions being made at such an early stage I firmly believe that the final outcome will be highly interesting not only to an ornithological readership but to every ecologist and biogeographer interested in drivers of range dynamic processes.

References

Bowser, S., MacPherson, M. (2021). A study on the role of social information sharing leading to range expansion in songbirds with large vocal repertoires: Enhancing our understanding of the Great-Tailed Grackle (Quiscalus mexicanus) alarm call. In principle recommendation by PCI Ecology. https://doi.org/10.17605/OSF.IO/2UFJ5. Version 3

A study on the role of social information sharing leading to range expansion in songbirds with large vocal repertoires: Enhancing our understanding of the Great-Tailed Grackle (Quiscalus mexicanus) alarm call Samantha Bowser, Maggie MacPherson<p>The acoustic adaptation hypothesis posits that animal sounds are influenced by the habitat properties that shape acoustic constraints (Ey and Fischer 2009, Morton 2015, Sueur and Farina 2015).Alarm calls are expected to signal important habitat...Biogeography, Biological invasions, Coexistence, Dispersal & Migration, Habitat selection, Landscape ecologyJan Oliver Engler Darius Stiels, Anonymous2020-12-01 18:11:02 View
29 Jan 2020
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Stoichiometric constraints modulate the effects of temperature and nutrients on biomass distribution and community stability

On the importance of stoichiometric constraints for understanding global change effects on food web dynamics

Recommended by based on reviews by 2 anonymous reviewers

The constraints associated with the mass balance of chemical elements (i.e. stoichiometric constraints) are critical to our understanding of ecological interactions, as outlined by the ecological stoichiometry theory [1]. Species in ecosystems differ in their elemental composition as well as in their level of elemental homeostasis [2], which can determine the outcome of interactions such as herbivory or decomposition on species coexistence and ecosystem functioning [3, 4].
Despite their importance, stoichiometric constraints are still often ignored in theoretical studies exploring the consequences of environmental perturbations on food web stability. Meanwhile, drivers of global change strongly alter biochemical cycles and the balance of chemical elements in ecosystems [5]. An important challenge is thus to understand how stoichiometric constraints affect food web responses to global changes.
The study of Sentis et al. [6] makes a step in that direction. This article investigates how stoichiometric constraints affect the response of consumer-resource dynamics to increasing temperature and nutrient inputs. It shows that the stoichiometric flexibility of the resource, coupled with lower consumer assimilation efficiency when stoichiometric unbalance between the resource and the consumer is higher, dampens the destabilizing effects of nutrient enrichment on species dynamics but reduces consumer persistence at extreme temperatures. Interestingly, these effects of stoichiometric constraints arise not only from changes in species assimilation efficiencies and carrying capacities but also from stoichiometric negative feedback loops on resource and consumer populations.
The results of this study are a call to further include stoichiometric constraints into food web models to better understand and predict the consequences of global changes on ecological communities. Many perspectives exist on that issue. For instance, it would be interesting to assess the effects of other stoichiometric mechanisms (e.g. changes in the element limiting growth [3]) on food web stability and its response to nutrient enrichment, as well as the effects of other global change drivers associated with altered biochemical cycles (e.g. carbon dioxide increase).

References

[1] Sterner, R. W. and Elser, J. J. (2017). Ecological Stoichiometry, The Biology of Elements from Molecules to the Biosphere. doi: 10.1515/9781400885695
[2] Elser, J. J., Sterner, R. W., Gorokhova, E., Fagan, W. F., Markow, T. A., Cotner, J. B., Harrison, J.F., Hobbie, S.E., Odell, G.M., Weider, L. W. (2000). Biological stoichiometry from genes to ecosystems. Ecology Letters, 3(6), 540–550. doi: 10.1111/j.1461-0248.2000.00185.x
[3] Daufresne, T., and Loreau, M. (2001). Plant–herbivore interactions and ecological stoichiometry: when do herbivores determine plant nutrient limitation? Ecology Letters, 4(3), 196–206. doi: 10.1046/j.1461-0248.2001.00210.x
[4] Zou, K., Thébault, E., Lacroix, G., and Barot, S. (2016). Interactions between the green and brown food web determine ecosystem functioning. Functional Ecology, 30(8), 1454–1465. doi: 10.1111/1365-2435.12626
[5] Peñuelas, J., Poulter, B., Sardans, J., Ciais, P., van der Velde, M., Bopp, L., Boucher, O., Godderis, Y., Hinsinger, P., Llusia, J., Nardin, E., Vicca, S., Obersteiner, M., Janssens, I. A. (2013). Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe. Nature Communications, 4(1), 1–10. doi: 10.1038/ncomms3934
[6] Sentis, A., Haegeman, B. & Montoya, J.M. (2020). Stoichiometric constraints modulate the effects of temperature and nutrients on biomass distribution and community stability. bioRxiv, 589895, ver. 7 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/589895

Stoichiometric constraints modulate the effects of temperature and nutrients on biomass distribution and community stability Arnaud Sentis, Bart Haegeman, and José M. Montoya<p>Temperature and nutrients are two of the most important drivers of global change. Both can modify the elemental composition (i.e. stoichiometry) of primary producers and consumers. Yet their combined effect on the stoichiometry, dynamics, and s...Climate change, Community ecology, Food webs, Theoretical ecology, Thermal ecologyElisa Thebault2019-08-08 12:20:08 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
11 Mar 2022
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Comment on “Information arms race explains plant-herbivore chemical communication in ecological communities”

Does information theory inform chemical arms race communication?

Recommended by based on reviews by Claudio Ramirez and 2 anonymous reviewers

One of the long-standing questions in evolutionary ecology is on the mechanisms involved in arms race coevolution. One way to address this question is to understand the conditions under which one species evolves traits in response to the presence of a second species and so on. However, specialized pairwise interactions are by far less common in nature than interactions involving a higher number of interacting species (Bascompte, Jordano 2013). While interactions between large sets of species are the norm rather than the exception in mutualistic (pollination, seed dispersal), and antagonist (herbivory, parasitism) relationships, few is known on the way species identify, process, and respond to information provided by other interacting species under field conditions (Schaefer, Ruxton 2011). 

Zu et al. (2020) addressed this general question by developing an interesting information theory-based approach that hypothesized conditional entropy in chemical communication plays a role as proxy of fitness in plant-herbivore communities. More specifically, plant fitness was assumed to be related to the efficiency to code signals by plant species, and herbivore fitness to the capacity to decode plant signals. In this way, from the plant perspective, the elaboration of plant signals that elude decoding by herbivores is expected to be favored, as herbivores are expected to attack plants with simple chemical signals. The empirical observation upon which the model was tested was the redundancy in volatile organic compounds (VOC) found across plant species in a plant-herbivore community. Interestingly, Zu et al.’s model predicted successfully that VOC redundancy in the plant community associates with increased conditional entropy, which conveys herbivore confusion and plant protection against herbivory. In this way, plant species that evolve VOCs already present in the community might be benefitted, ultimately leading to the patterns of VOC redundancy commonly observed in nature.

Bass & Kessler performed a series of interesting observations on Zu et al. (2020), that can be organized along three lines of reasoning. First, from an evolutionary perspective, Bass & Kessler note the important point that accepting that conditional information entropy, estimated from the contribution of every plant species to volatile redundancy implies that average plant fitness seems to depend on community-level properties (i.e., what the other species in the community are doing) rather than on population-level characteristics (I.e., what the individuals belonging a population are doing). While the level at which selection acts upon is a longstanding debate (e.g., Goodnight, 1990; Williams, 1992), the model seems to contradict one of the basic tenets of Darwinian evolution. The extent to which this important observation invalidates the contribution of Zu et al. (2020) is open to scrutiny. However, one can indulge the evolutionary criticism by arguing that every theoretical model performs a number of assumptions to preserve the simplicity of analyses. Furthermore, even accepting the criticism, the overall information-based framework is valuable as it provides a fresh perspective to the way coding and decoding chemical information in plant-herbivore interactions may result in arm race coevolution. The question to be assessed by members of the scientific community is how strong the evolutionary assumptions are to be acceptable. A second line of reasoning involves consideration of additional routes of chemical information transfer. If chemical volatiles are involved in another ecological function unrelated to arm race (as they are) such as toxicity, crypsis, aposematism, etc., the conditional information indices considered as proxy to plant and herbivore fitness may be only secondarily related to arms race. This is an interesting observation, which suggests that VOC production may have more than one ecological function, as it often happens in “pleiotropic” traits (Strauss, Irwin 2004). This is an exciting avenue for future research. Finally, a third category of comments involves the relationship between conditional information entropy and plant and herbivore fitness. Bass & Kessler developed a Bayesian treatment of the community-level information developed by Zu et al. (2020) that permitted to estimate fitness on a species rather than community level. Their results revealed that community conditional entropies fail to align with species-level indices, suggesting that conclusions of Strauss & Irwin (2004) are not commensurate with fitness at the species level, where the analysis seems to be pertinent. In general, I strongly recommend Bass & Kessler’s contribution as it provides a series of observations and new perspectives to Zu et al. (2020). Rather than restricting their manuscript to blind criticisms, Bass & Kessler provides new interesting perspectives, which is always welcome as it improves the value and scope of the original work.

References

Bascompte J, Jordano P (2013) Mutualistic Networks. Princeton University Press. https://doi.org/10.23943/princeton/9780691131269.001.0001

Bass E, Kessler A (2022) Comment on “Information arms race explains plant-herbivore chemical communication in ecological communities.” EcoEvoRxiv, ver. 8 peer-reviewed and recommended by Peer Community in Ecology.  https://doi.org/10.32942/osf.io/xsbtm

Goodnight CJ (1990) Experimental Studies of Community Evolution I: The Response to Selection at the Community Level. Evolution, 44, 1614–1624. https://doi.org/10.1111/j.1558-5646.1990.tb03850.x

Schaefer HM, Ruxton GD (2011) Plant-Animal Communication. Oxford University Press, Oxford. https://doi.org/10.1093/acprof:osobl/9780199563609.001.0001

Strauss SY, Irwin RE (2004) Ecological and Evolutionary Consequences of Multispecies Plant-Animal Interactions. Annual Review of Ecology, Evolution, and Systematics, 35, 435–466. https://doi.org/10.1146/annurev.ecolsys.35.112202.130215

Williams GC (1992) Natural Selection: Domains, Levels, and Challenges. Oxford University Press, Oxford, New York.

Zu P, Boege K, del-Val E, Schuman MC, Stevenson PC, Zaldivar-Riverón A, Saavedra S (2020) Information arms race explains plant-herbivore chemical communication in ecological communities. Science, 368, 1377–1381. https://doi.org/10.1126/science.aba2965

Comment on “Information arms race explains plant-herbivore chemical communication in ecological communities”Ethan Bass, André Kessler<p style="text-align: justify;">Zu et al (Science, 19 Jun 2020, p. 1377) propose that an ‘information arms-race’ between plants and herbivores explains plant-herbivore communication at the community level. However, the analysis presented here show...Chemical ecology, Community ecology, Eco-evolutionary dynamics, Evolutionary ecology, Herbivory, Interaction networks, Theoretical ecologyRodrigo Medel2021-10-02 06:06:07 View
20 Oct 2021
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Eco-evolutionary dynamics further weakens mutualistic interaction and coexistence under population decline

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

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

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

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

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

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

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

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

References

Goh BS (1979) Stability in Models of Mutualism. The American Naturalist, 113, 261–275. http://www.jstor.org/stable/2460204.

Holland JN, DeAngelis DL (2010) A consumer–resource approach to the density-dependent population dynamics of mutualism. Ecology, 91, 1286–1295. https://doi.org/10.1890/09-1163.1

Weinbach A, Loeuille N, Rohr RP (2021) Eco-evolutionary dynamics further weakens mutualistic interaction and coexistence under population decline. bioRxiv, 570580, ver. 5 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/570580

Eco-evolutionary dynamics further weakens mutualistic interaction and coexistence under population declineAvril Weinbach, Nicolas Loeuille, Rudolf P. Rohr<p style="text-align: justify;">With current environmental changes, evolution can rescue declining populations, but what happens to their interacting species? Mutualistic interactions can help species sustain each other when their environment wors...Coexistence, Eco-evolutionary dynamics, Evolutionary ecology, Interaction networks, Pollination, Theoretical ecologySylvain Billiard2019-09-05 11:29:45 View
01 Mar 2024
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Cities as parasitic amplifiers? Malaria prevalence and diversity in great tits along an urbanization gradient

Exploring the Impact of Urbanization on Avian Malaria Dynamics in Great Tits: Insights from a Study Across Urban and Non-Urban Environments

Recommended by based on reviews by Ana Paula Mansilla and 2 anonymous reviewers

Across the temporal expanse of history, the impact of human activities on global landscapes has manifested as a complex interplay of ecological alterations. From the advent of early agricultural practices to the successive waves of industrialization characterizing the 18th and 19th centuries, anthropogenic forces have exerted profound and enduring transformations upon Earth's ecosystems. Indeed, by 2017, more than 80% of the terrestrial biosphere was transformed by human populations and land use, and just 19% remains as wildlands (Ellis et al. 2021).
 
Urbanization engenders profound alterations in environmental conditions, exerting substantial impacts on biological communities. The expansion of built infrastructure, modification of land use patterns, and the introduction of impervious surfaces and habitat fragmentation are key facets of urbanization (Faeth et al. 2011). These alterations generate biodiversity loss, changes in the composition of biological communities, disruptions in access and availability of food and nutrients, and a loss of efficiency in the immune system's control of infections, etc. (Reyes et al. 2013).
 
In this study, Caizergues et al. (2023) investigated the prevalence and diversity of avian malaria parasites (Plasmodium/Haemoproteus sp. and Leucocytozoon sp.) in great tits (Parus major) living across an urbanization gradient. The study reveals nuanced patterns of avian malaria prevalence and lineage diversity in great tits across urban and non-urban environments. While overall parasite diversity remains consistent, there are marked differences in prevalence between life stages and habitats. They observed a high prevalence in adult birds (from 95% to 100%), yet lower prevalence in fledglings (from 0% to 38%). Notably, urban nestlings exhibit higher parasite prevalence than their non-urban counterparts, suggesting a potential link between early malaria infection and the urban heat island effect. This finding underscores the importance of considering both spatial and temporal aspects of urbanization in understanding disease dynamics. Parasite lineages were not habitat-specific. The results suggest a potential parasitic burden in more urbanized areas, with a marginal but notable effect of nest-level urbanization on Plasmodium prevalence. This challenges the common perception of lower parasitic prevalence in urban environments and highlights the need for further investigation into the factors influencing parasite prevalence at finer spatial scales.
 
The discussion emphasizes the significance of examining vector distributions, abundance, and diversity in urban areas, which may be influenced by ecological niches and the presence of suitable habitats such as marshes. The identification of habitat-specific Haemosporidian lineages, particularly those occurring more frequently in urban areas, raises intriguing questions about the factors influencing parasite diversity. The presence of rare lineages in urban environments, such as AFR065, DELURB4, and YWT4, suggests a potential connection between urban bird communities and specific parasite strains.
 
Future research should empirically demonstrate these relationships to enhance our understanding of urban parasitology. This finding has broader implications for wildlife epidemiology, especially when introducing or keeping exotic wildlife in contact with native species. The study highlights the importance of considering not only the prevalence but also the specific lineages of parasites in understanding the dynamics of avian malaria in urban and non-urban habitats. This preprint contributes valuable insights to the ongoing discourse on the intricate interplay between ecological repercussions of human-induced changes (urbanization), biological communities, and the prevalence of vector-borne diseases.
 
References

Caizergues AE, Robira B, Perrier C, Jeanneau M, Berthomieu A, Perret S, Gandon S, Charmantier A (2023) Cities as parasitic amplifiers? Malaria prevalence and diversity in great tits along an urbanization gradient. bioRxiv, 2023.05.03.539263, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2023.05.03.539263

Ellis EC, Gauthier N, Klein Goldewijk K, Bliege Bird R, Boivin N, Díaz S, Fuller DQ, Gill JL, Kaplan JO, Kingston N, Locke H, McMichael CNH, Ranco D, Rick TC, Shaw MR, Stephens L, Svenning JC, Watson JEM. People have shaped most of terrestrial nature for at least 12,000 years. Proc Natl Acad Sci U S A. 2021 Apr 27;118(17):e2023483118. https://doi.org/10.1073/pnas.2023483118

Faeth  SH, Bang  C, Saari  S (2011) Urban biodiversity: Patterns and mechanisms. Ann N Y Acad Sci 1223:69–81. https://doi.org/10.1111/j.1749-6632.2010.05925.x

Faeth  SH, Bang  C, Saari  S (2011) Urban biodiversity: Patterns and mechanisms. Ann N Y Acad Sci 1223:69–81. https://doi.org/10.1111/j.1749-6632.2010.05925.x

Reyes  R, Ahn  R, Thurber  K, Burke  TF (2013) Urbanization and Infectious Diseases: General Principles, Historical Perspectives, and Contemporary Challenges. Challenges Infect Dis 123. https://doi.org/10.1007/978-1-4614-4496-1_4

Cities as parasitic amplifiers? Malaria prevalence and diversity in great tits along an urbanization gradientAude E. Caizergues, Benjamin Robira, Charles Perrier, Melanie Jeanneau, Arnaud Berthomieu, Samuel Perret, Sylvain Gandon, Anne Charmantier<p style="text-align: justify;">Urbanization is a worldwide phenomenon that modifies the environment. By affecting the reservoirs of pathogens and the body and immune conditions of hosts, urbanization alters the epidemiological dynamics and divers...Epidemiology, Host-parasite interactions, Human impactAdrian DiazAnonymous, Gauthier Dobigny, Ana Paula Mansilla2023-09-11 20:24:44 View
26 Apr 2021
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Experimental test for local adaptation of the rosy apple aphid (Dysaphis plantaginea) during its recent rapid colonization on its cultivated apple host (Malus domestica) in Europe

A planned experiment on local adaptation in a host-parasite system: is adaptation to the host linked to its recent domestication?

Recommended by based on reviews by Sharon Zytynska, Alex Stemmelen and 1 anonymous reviewer

Local adaptation shall occur whenever selective pressures vary across space and overwhelm the effects of gene flow and local extinctions (Kawecki and Ebert 2004). Because the intimate interaction that characterizes their relationship exerts a strong selective pressure on both partners, host-parasite systems represent a classical example in which local adaptation is expected from rapidly evolving parasites adapting to more evolutionary constrained hosts (Kaltz and Shykoff 1998). Such systems indeed represent a large proportion of the study-cases in local adaptation research (Runquist et al. 2020). Biotic interactions intervene in many environment-related societal challenges, so that understanding when and how local adaptation arises is important not only for understanding evolutionary dynamics but also for more applied questions such as the control of agricultural pests, biological invasions, or pathogens (Parker and Gilbert 2004).

The exact conditions under which local adaptation does occur and can be detected is however still the focus of many theoretical, methodological and empirical studies (Blanquart et al. 2013, Hargreaves et al. 2020, Hoeksema and Forde 2008, Nuismer and Gandon 2008, Richardson et al. 2014). A recent review that evaluates investigations that examined the combined influence of biotic and abiotic factors on local adaptation reaches partial conclusions about their relative importance in different contexts and underlines the many traps that one has to avoid in such studies (Runquist et al. 2020). The authors of this review emphasize that one should evaluate local adaptation using wild-collected strains or populations and over multiple generations, on environmental gradients that span natural ranges of variation for both biotic and abiotic factors, in a theory-based hypothetico-deductive framework that helps interpret the outcome of experiments. These multiple targets are not easy to reach in each local adaptation experiment given the diversity of systems in which local adaptation may occur. Improving research practices may also help better understand when and where local adaptation does occur by adding controls over p-hacking, HARKing or publication bias, which is best achieved when hypotheses, date collection and analytical procedures are known before the research begins (Chambers et al. 2014). In this regard, the route taken by Olvera-Vazquez et al. (2021) is interesting. They propose to investigate whether the rosy aphid (Dysaphis plantaginea) recently adapted to its cultivated host, the apple tree (Malus domestica), and chose to pre-register their hypotheses and planned experiments on PCI Ecology (Peer Community In 2020). Though not fulfilling all criteria mentioned by Runquist et al. (2020), they clearly state five hypotheses that all relate to the local adaptation of this agricultural pest to an economically important fruit tree, and describe in details a powerful, randomized experiment, including how data will be collected and analyzed. The experimental set-up includes comparisons between three sites located along a temperature transect that also differ in local edaphic and biotic factors, and contrasts wild and domesticated apple trees that originate from the three sites and were both planted in the local, sympatric site, and transplanted to allopatric sites. Beyond enhancing our knowledge on local adaptation, this experiment will also test the general hypothesis that the rosy aphid recently adapted to Malus sp. after its domestication, a question that population genetic analyses was not able to answer (Olvera-Vazquez et al. 2020).

References

Blanquart F, Kaltz O, Nuismer SL, Gandon S (2013) A practical guide to measuring local adaptation. Ecology Letters, 16, 1195–1205. https://doi.org/10.1111/ele.12150

Briscoe Runquist RD, Gorton AJ, Yoder JB, Deacon NJ, Grossman JJ, Kothari S, Lyons MP, Sheth SN, Tiffin P, Moeller DA (2019) Context Dependence of Local Adaptation to Abiotic and Biotic Environments: A Quantitative and Qualitative Synthesis. The American Naturalist, 195, 412–431. https://doi.org/10.1086/707322

Chambers CD, Feredoes E, Muthukumaraswamy SD, Etchells PJ, Chambers CD, Feredoes E, Muthukumaraswamy SD, Etchells PJ (2014) Instead of “playing the game” it is time to change the rules: Registered Reports at <em>AIMS Neuroscience</em> and beyond. AIMS Neuroscience, 1, 4–17. https://doi.org/10.3934/Neuroscience.2014.1.4

Hargreaves AL, Germain RM, Bontrager M, Persi J, Angert AL (2019) Local Adaptation to Biotic Interactions: A Meta-analysis across Latitudes. The American Naturalist, 195, 395–411. https://doi.org/10.1086/707323

Hoeksema JD, Forde SE (2008) A Meta‐Analysis of Factors Affecting Local Adaptation between Interacting Species. The American Naturalist, 171, 275–290. https://doi.org/10.1086/527496

Kaltz O, Shykoff JA (1998) Local adaptation in host–parasite systems. Heredity, 81, 361–370. https://doi.org/10.1046/j.1365-2540.1998.00435.x

Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecology Letters, 7, 1225–1241. https://doi.org/10.1111/j.1461-0248.2004.00684.x

Nuismer SL, Gandon S (2008) Moving beyond Common‐Garden and Transplant Designs: Insight into the Causes of Local Adaptation in Species Interactions. The American Naturalist, 171, 658–668. https://doi.org/10.1086/587077

Olvera-Vazquez SG, Remoué C, Venon A, Rousselet A, Grandcolas O, Azrine M, Momont L, Galan M, Benoit L, David G, Alhmedi A, Beliën T, Alins G, Franck P, Haddioui A, Jacobsen SK, Andreev R, Simon S, Sigsgaard L, Guibert E, Tournant L, Gazel F, Mody K, Khachtib Y, Roman A, Ursu TM, Zakharov IA, Belcram H, Harry M, Roth M, Simon JC, Oram S, Ricard JM, Agnello A, Beers EH, Engelman J, Balti I, Salhi-Hannachi A, Zhang H, Tu H, Mottet C, Barrès B, Degrave A, Razmjou J, Giraud T, Falque M, Dapena E, Miñarro M, Jardillier L, Deschamps P, Jousselin E, Cornille A (2020) Large-scale geographic survey provides insights into the colonization history of a major aphid pest on its cultivated apple host in Europe, North America and North Africa. bioRxiv, 2020.12.11.421644. https://doi.org/10.1101/2020.12.11.421644

Olvera-Vazquez S.G., Alhmedi A., Miñarro M., Shykoff J. A., Marchadier E., Rousselet A., Remoué C., Gardet R., Degrave A. , Robert P. , Chen X., Porcher J., Giraud T., Vander-Mijnsbrugge K., Raffoux X., Falque M., Alins, G., Didelot F., Beliën T., Dapena E., Lemarquand A. and Cornille A. (2021) Experimental test for local adaptation of the rosy apple aphid (Dysaphis plantaginea) to its host (Malus domestica) and to its climate in Europe. In principle recommendation by Peer Community In Ecology. https://forgemia.inra.fr/amandine.cornille/local_adaptation_dp, ver. 4.

Parker IM, Gilbert GS (2004) The Evolutionary Ecology of Novel Plant-Pathogen Interactions. Annual Review of Ecology, Evolution, and Systematics, 35, 675–700. https://doi.org/10.1146/annurev.ecolsys.34.011802.132339

Peer Community In. (2020, January 15). Submit your preregistration to Peer Community In for peer review. https://peercommunityin.org/2020/01/15/submit-your-preregistration-to-peer-community-in-for-peer-review/

Richardson JL, Urban MC, Bolnick DI, Skelly DK (2014) Microgeographic adaptation and the spatial scale of evolution. Trends in Ecology & Evolution, 29, 165–176. https://doi.org/10.1016/j.tree.2014.01.002

Experimental test for local adaptation of the rosy apple aphid (Dysaphis plantaginea) during its recent rapid colonization on its cultivated apple host (Malus domestica) in EuropeOlvera-Vazquez S.G., Alhmedi A., Miñarro M., Shykoff J. A., Marchadier E., Rousselet A., Remoué C., Gardet R., Degrave A. , Robert P. , Chen X., Porcher J., Giraud T., Vander-Mijnsbrugge K., Raffoux X., Falque M., Alins, G., Didelot F., Beliën T.,...<p style="text-align: justify;">Understanding the extent of local adaptation in natural populations and the mechanisms enabling populations to adapt to their environment is a major avenue in ecology research. Host-parasite interaction is widely se...Evolutionary ecology, PreregistrationsEric Petit2020-07-26 18:31:42 View
15 Nov 2023
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The challenges of independence: ontogeny of at-sea behaviour in a long-lived seabird

On the road to adulthood: exploring progressive changes in foraging behaviour during post-fledging immaturity using remote tracking

Recommended by based on reviews by Juliet Lamb and 1 anonymous reviewer

In most vertebrate species, the period of life spanning from departure from the growing site until reaching a more advanced life stage (immature or adult) is critical. During this period, juveniles are often highly vulnerable because they have not reached the morphological, physiological and behavioural maturity levels of adults yet and are therefore at high risk of mortality, e.g. through starvation, depredation or competition (e.g. Marchetti & Price 1989, Wunderle 1991, Naef-Daenzer & Grüebler 2016). In line with this, juvenile survival is most often far lower than adult survival (e.g. Wooller et al. 1992). In species with parental care, juveniles have to acquire behavioural independence from their parents and possibly establish their own territory during this period of life. Very often, this is also the period that is least well-known in the life cycle (Cox et al. 2014, Naef-Daenzer & Grüebler 2016) because of reduced accessibility to individuals and/or adoption of low conspicuous behaviours. Therefore, our understanding of how juveniles acquire typical adult behaviours and how this progressively increases their survival prospects is still very limited (Naef-Daenzer & Grüebler 2016), and questions such as the length of this transition period or the cognitive (e.g. learning, memorization) mechanisms involved remain largely unresolved. This is particularly true regarding the acquisition of independent foraging behaviour (Marchetti & Price 1989).

Because direct observations of juvenile behaviours are usually very difficult except in specific situations or at the cost of an enormous effort, the use of remote tracking devices can be particularly appealing in this context (e.g. Ponchon et al. 2013, Kays et al. 2015). Over the past decades, technical advances have allowed the monitoring of not only individuals’ movements at both large and small spatial scales but also their activities and behaviours based on different parameters recording e.g. speed of movement or diving depth (Whitford & Klimley 2019). Device miniaturization has in particular allowed smaller species to be equipped and/or longer periods of time to be monitored (e.g. Naef-Daenzer et al. 2005). This has opened up whole fields of research, and has been particularly used on marine seabirds. In these species, individuals are most often inaccessible when at sea, representing most of the time outside (and even within) the breeding season, and the life cycle of these long-lived species can include an extended immature period (up to many years) during which most of them will remain unseen, until they come back as breeders or pre-breeders (e.g. Wooller et al. 1992, Oro & Martínez-Abraín 2009). Survival has been found to increase gradually with age in these species before reaching high values characteristic of the adult stage. However, the mechanisms underlying this increase are still to be deciphered.

The study by Delord et al. (2023) builds upon the hypothesis that juveniles gradually learn foraging techniques and movement strategies, improving their foraging efficiency, as previous data on flight parameters seemed to show in different long-lived bird species. Yet, these previous studies obtained data over a limited period of time, i.e. a few months at best. Whether these data could capture the whole dynamics of the progressive acquisition of foraging and movement skills can only be assessed by measuring behaviour over a longer time period and comparing it to similar data in adults, to account for seasonal variation in relation to both resource availability and energetic demands, e.g. due to molt.

The present study (Delord et al. 2023) addresses these questions by taking advantage of longer-lasting recordings of the location and activity of juvenile, immature and adult birds obtained simultaneously to investigate changes over time in juvenile behaviour and thereby provide hints about how young progressively acquire foraging skills. This study is performed on Amsterdam albatrosses, a highly endangered long-lived sea bird, with obvious conservation issues (Thiebot et al. 2015). The results show progressive changes in foraging effort over the first two months after departure from the birth colony, but large differences remain between life stages over a much longer time frame. They also reveal strong variations between sexes and over time in the year. Overall, this study, therefore, confirms the need for very long-term data to be collected in order to address the question of progressive behavioural maturation and associated survival consequences in such species with strongly deferred maturity. Ideally, the same individuals should be monitored over different life stages, from the juvenile period up to adulthood, but this would require further technical development to release the issue of powering duration limitation.

As reviewers emphasized in the first review round, one main challenge now remains to ascertain the outcome of the observed behavioural changes in foraging behaviour: we expect them to reflect improvement in foraging skills and thus performance of juveniles over time, but this would need to be tested. Collecting data on foraging efficiency is yet another challenge, that future technical developments may also help overcome. Importantly also, data were available only for individuals that could be caught again because the tracking device had to be retrieved from the bird. Here, a substantial fraction of the loggers (one-fifth) could not be found again (Delord et al. 2023). To what extent the birds for which no data could be obtained are a random sample of the equipped birds would also need to be assessed. The further development of remote tracking techniques allowing data to be downloaded from a long distance should help further exploration of behavioural ontogeny of juveniles while maturing and its survival consequences. Because the maturation process explored here is likely to show very different characteristics (e.g. timing and speed) in smaller / shorter-lived species (see Cox et al. 2014, Naef-Daenzer & Grüebler 2016), the development of miniaturization is also expected to allow further investigation of post-fledging behavioural maturation in a wider range of bird species. Our understanding of this crucial life phase in different types of species should thus continue to progress in the coming years.

References

Cox W. A., Thompson F. R. III, Cox A. S. & Faaborg J. 2014. Post-fledging survival in passerine birds and the value of post-fledging studies to conservation. Journal of Wildlife Management, 78: 183-193. https://doi.org/10.1002/jwmg.670

Delord K., Weimerskirch H. & Barbraud C. 2023. The challenges of independence: ontogeny of at-sea behaviour in a long-lived seabird. bioRxiv, ver. 6 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2021.10.23.465439

Kays R., Crofoot M. C., Jetz W. & Wikelski M. 2015. Terrestrial animal tracking as an eye on life and planet. Science, 348 (6240). https://doi.org/10.1126/science.aaa2478

Marchetti K: & Price T. 1989. Differences in the foraging of juvenile and adult birds: the importance of developmental constraints. Biological Reviews, 64: 51-70. https://doi.org/10.1111/j.1469-185X.1989.tb00638.x

Naef-Daenzer B., Fruh D., Stalder M., Wetli P. & Weise E. 2005. Miniaturization (0.2 g) and evaluation of attachment techniques of telemetry transmitters. The Journal of Experimental Biology, 208: 4063–4068. https://doi.org/10.1242/jeb.01870

Naef-Daenzer B. & Grüebler M. U. 2016. Post-fledging survival of altricial birds: ecological determinants and adaptation. Journal of Field Ornithology, 87: 227-250. https://doi.org/10.1111/jofo.12157

Oro D. & Martínez-Abraín A. 2009. Ecology and behavior of seabirds. Marine Ecology, pp.364-389.

Ponchon A., Grémillet D., Doligez B., Chambert T., Tveera T., Gonzàles-Solìs J & Boulinier T. 2013. Tracking prospecting movements involved in breeding habitat selection: insights, pitfalls and perspectives. Methods in Ecology and Evolution, 4: 143-150. https://doi.org/10.1111/j.2041-210x.2012.00259.x

Thiebot J.-B., Delord K., Barbraud C., Marteau C. & Weimerskirch H. 2015. 167 individuals versus millions of hooks: bycatch mitigation in longline fisheries underlies conservation of Amsterdam albatrosses. Aquatic Conservation 26: 674-688. https://doi.org/10.1002/aqc.2578

Whitford M & Klimley A. P. An overview of behavioral, physiological, and environmental sensors used in animal biotelemetry and biologging studies. Animal Biotelemetry, 7: 26. https://doi.org/10.1186/s40317-019-0189-z

Wooller R.D., Bradley J. S. & Croxall J. P. 1992. Long-term population studies of seabirds. Trends in Ecology and Evolution, 7: 111-114. https://doi.org/10.1016/0169-5347(92)90143-y

Wunderle J. M. 1991. Age-specific foraging proficiency in birds. Current Ornithology, 8: 273-324.

The challenges of independence: ontogeny of at-sea behaviour in a long-lived seabirdKarine Delord, Henri Weimerskirch, Christophe Barbraud<p style="text-align: justify;">The transition to independent foraging represents an important developmental stage in the life cycle of most vertebrate animals. Juveniles differ from adults in various life history traits and tend to survive less w...Behaviour & Ethology, Foraging, OntogenyBlandine Doligez2021-10-26 07:51:49 View
06 May 2021
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Trophic niche of the invasive gregarious species Crepidula fornicata, in relation to ontogenic changes

A lack of clear dietary differences between ontogenetic stages of invasive slippersnails provides important insights into resource use and potential inter- and intra-specific competition

Recommended by based on reviews by 2 anonymous reviewers

The slippersnail (Crepidula fornicata), originally from the eastern coast of North America, has invaded European coastlines from Norway to the Mediterranean Sea [1]. This species is capable of achieving incredibly high densities (up to several thousand individuals per square meter) and likely has major impacts on a variety of community- and ecosystem-level processes, including alteration of carbon and nitrogen fluxes and competition with native suspension feeders [2].

Given this potential for competition, it is important to understand the diet of C. fornicata and its potential overlap with native species. However, previous research on the diet of C. fornicata and related species suggests that the types of food consumed may change with age [3, 4]. This species has an unusual reproductive strategy. It is a sequential hermaphrodite, which begins life as a somewhat mobile male but eventually slows down to become sessile. Sessile individuals form stacks of up to 10 or more individuals, with larger individuals on the bottom of the stack, and decreasingly smaller individuals piled on top. Snails at the bottom of the stack are female, whereas snails at the top of the stack are male; when the females die, the largest males become female [5]. Thus, understanding these potential ontogenetic dietary shifts has implications for both intraspecific (juvenile vs. male vs. female) and interspecific competition associated with an abundant, invasive species.

To this end, Androuin and colleagues evaluated the stable-isotope (d13C and d15N) and fatty-acid profiles of food sources and different life-history stages of C. fornicata [6]. Based on previous work highlighting the potential for life-history changes in the diet of this species [3,4], they hypothesized that C. fornicata would shift its diet as it aged and predicted that this shift would be reflected in changes in its stable-isotope and fatty-acid profiles. The authors found that potential food sources (biofilm, suspended particulate organic matter, and superficial sedimentary organic matter) differed substantially in both stable-isotope and fatty-acid signatures. However, whereas fatty-acid profiles changed substantially with age, there was no shift in the stable-isotope signatures. Because stable-isotope differences between food sources were not reflected in differences between life-history stages, the authors conservatively concluded that there was insufficient evidence for a diet shift with age. The ontogenetic shifts in fatty-acid profiles were intriguing, but the authors suggested that these reflected age-related physiological changes rather than changes in diet.

The authors’ work highlights the need to consider potential changes in the roles of invasive species with age, especially when evaluating interactions with native species. In this case, C. fornicata consumed a variety of food sources, including both benthic and particulate organic matter, regardless of age. The carbon stable-isotope signature of C. fornicata overlaps with those of several native suspension- and deposit-feeding species in the region [7], suggesting the possibility of resource competition, especially given the high abundances of this invader. This contribution demonstrates the potential difficulty of characterizing the impacts of an abundant invasive species with a complex life-history strategy. Like many invasive species, C. fornicata appears to be a dietary generalist, which likely contributes to its success in establishing and thriving in a variety of locations [8].

 

References

[1] Blanchard M (1997) Spread of the slipper limpet Crepidula fornicata (L. 1758) in Europe. Current state dans consequences. Scientia Marina, 61, 109–118. Open Access version : https://archimer.ifremer.fr/doc/00423/53398/54271.pdf

[2] Martin S, Thouzeau G, Chauvaud L, Jean F, Guérin L, Clavier J (2006) Respiration, calcification, and excretion of the invasive slipper limpet, Crepidula fornicata L.: Implications for carbon, carbonate, and nitrogen fluxes in affected areas. Limnology and Oceanography, 51, 1996–2007. https://doi.org/10.4319/lo.2006.51.5.1996

[3] Navarro JM, Chaparro OR (2002) Grazing–filtration as feeding mechanisms in motile specimens of Crepidula fecunda (Gastropoda: Calyptraeidae). Journal of Experimental Marine Biology and Ecology, 270, 111–122. https://doi.org/10.1016/S0022-0981(02)00013-8

[4] Yee AK, Padilla DK (2015) Allometric Scaling of the Radula in the Atlantic Slippersnail Crepidula fornicata. Journal of Shellfish Research, 34, 903–907. https://doi.org/10.2983/035.034.0320

[5] Collin R (1995) Sex, Size, and Position: A Test of Models Predicting Size at Sex Change in the Protandrous Gastropod Crepidula fornicata. The American Naturalist, 146, 815–831. https://doi.org/10.1086/285826

[6] Androuin T, Dubois SF, Hubas C, Lefebvre G, Grand FL, Schaal G, Carlier A (2021) Trophic niche of the invasive gregarious species Crepidula fornicata, in relation to ontogenic changes. bioRxiv, 2020.07.30.229021, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2020.07.30.229021

[7] Dauby P, Khomsi A, Bouquegneau J-M (1998) Trophic Relationships within Intertidal Communities of the Brittany Coasts: A Stable Carbon Isotope Analysis. Journal of Coastal Research, 14, 1202–1212. Retrieved May 4, 2021, from http://www.jstor.org/stable/4298880

[8] Machovsky-Capuska GE, Senior AM, Simpson SJ, Raubenheimer D (2016) The Multidimensional Nutritional Niche. Trends in Ecology & Evolution, 31, 355–365. https://doi.org/10.1016/j.tree.2016.02.009

 

Trophic niche of the invasive gregarious species Crepidula fornicata, in relation to ontogenic changesThibault Androuin, Stanislas F. Dubois, Cédric Hubas, Gwendoline Lefebvre, Fabienne Le Grand, Gauthier Schaal, Antoine Carlier<p style="text-align: justify;">The slipper limpet Crepidula fornicata is a common and widespread invasive gregarious species along the European coast. Among its life-history traits, well-documented ontogenic changes in behavior (i.e., motile male...Food webs, Life history, Marine ecologyMatthew Bracken2020-08-01 23:55:57 View