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12 Jan 2022
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No Evidence for Long-range Male Sex Pheromones in Two Malaria Mosquitoes

The search for sex pheromones in malaria mosquitoes

Recommended by based on reviews by Marcelo Lorenzo and 1 anonymous reviewer

Pheromones are used by many insects to find the opposite sex for mating. Especially for nocturnal mosquitoes it seems logical that such pheromones exist as they can only partly rely on visual cues when flying at night. The males of many mosquito species form swarms and conspecific females fly into these swarms to mate. The two sibling species of malaria mosquitoes Anopheles gambiae s.s. and An. coluzzii coexist and both form swarms consisting of only one species. Although hybrids can be produced, these hybrids are rarely found in nature. In the study presented by Poda and colleagues (2022) it was tested if long-range sex pheromones exist in these two mosquito sibling species.

In a previous study by Mozūraites et al. (2020), five compounds (acetoin, sulcatone, octanal, nonanal and decanal) were identified that induced male swarming and increase mating success. Interestingly these compounds are frequently found in nature and have been shown to play a role in sugar feeding or host finding of An. gambiae. In the recommended study performed by Poda et al. (2022) no evidence of long-range sex pheromones in A. gambiae s.s. and An. coluzzii was found. The discrepancy between the two studies is difficult to explain but some of the methods varied between studies. Mozūraites et al. (2020) for example, collected odours from mosquitoes in small 1l glass bottles, where swarming is questionable, while in the study of Poda et al. (2022) 50 x 40 x 40 cm cages were used and swarming observed, although most swarms are normally larger. On the other hand, some of the analytical techniques used in the Mozūraites et al. (2020) study were more sensitive while others were more sensitive in the Poda et al. (2022) study. Because it is difficult to prove that something does not exist, the authors nicely indicate that “an absence of evidence is not an evidence of absence” (Poda et al., 2022). Nevertheless, recently colonized species were tested in large cage setups where swarming was observed and various methods were used to try to detect sex pheromones. No attraction to the volatile blend from male swarms was detected in an olfactometer, no antenna-electrophysiological response of females to male swarm volatile compounds was detected and no specific male swarm volatile was identified.

This study will open the discussion again if (sex) pheromones play a role in swarming and mating of malaria mosquitoes. Future studies should focus on sensitive real-time volatile analysis in mating swarms in large cages or field settings. In comparison to moths for example that are very sensitive to very specific pheromones and attract from a large distance, such a long-range specific pheromone does not seem to exist in these mosquito species. Acoustic and visual cues have been shown to be involved in mating (Diabate et al., 2003; Gibson and Russell, 2006) and especially at long distances, visual cues are probably important for the detection of these swarms.


Diabate A, Baldet T, Brengues C, Kengne P, Dabire KR, Simard F, Chandre F, Hougard JM, Hemingway J, Ouedraogo JB, Fontenille D (2003) Natural swarming behaviour of the molecular M form of Anopheles gambiae. Transactions of The Royal Society of Tropical Medicine and Hygiene, 97, 713–716.

Gibson G, Russell I (2006) Flying in Tune: Sexual Recognition in Mosquitoes. Current Biology, 16, 1311–1316.

Mozūraitis, R., Hajkazemian, M., Zawada, J.W., Szymczak, J., Pålsson, K., Sekar, V., Biryukova, I., Friedländer, M.R., Koekemoer, L.L., Baird, J.K., Borg-Karlson, A.-K., Emami, S.N. (2020) Male swarming aggregation pheromones increase female attraction and mating success among multiple African malaria vector mosquito species. Nature Ecology & Evolution, 4, 1395–1401.

Poda, S.B., Buatois, B., Lapeyre, B., Dormont, L., Diabate, A., Gnankine, O., Dabire, R.K.,  Roux, O. (2022) No evidence for long-range male sex pheromones in two malaria mosquitoes. bioRxiv, 2020.07.05.187542, ver. 6 peer-reviewed and recommended by Peer Community in Ecology.

No Evidence for Long-range Male Sex Pheromones in Two Malaria MosquitoesSerge Bèwadéyir Poda, Bruno Buatois, Benoit Lapeyre, Laurent Dormont, Abdoulaye Diabaté, Olivier Gnankiné, Roch K. Dabiré, Olivier Roux<p style="text-align: justify;">Cues involved in mate seeking and recognition prevent hybridization and can be involved in speciation processes. In malaria mosquitoes, females of the two sibling species <em>Anopheles gambiae</em> s.s. and <em>An. ...Behaviour & Ethology, Chemical ecologyNiels Verhulst2021-04-26 12:28:36 View
06 Sep 2019
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Assessing metacommunity processes through signatures in spatiotemporal turnover of community composition

On the importance of temporal meta-community dynamics for our understanding of assembly processes

Recommended by ORCID_LOGO based on reviews by Joaquín Hortal and 2 anonymous reviewers

The processes that trigger community assembly are still in the centre of ecological interest. While prior work mostly focused on spatial patterns of co-occurrence within a meta-community framework [reviewed in 1, 2] recent studies also include temporal patterns of community composition [e.g. 3, 4, 5, 6]. In this preprint [7], Franck Jabot and co-workers extend they prior approaches to quasi neutral community assembly [8, 9, 10] and develop an analytical framework of spatial and temporal diversity turnover. A simple and heuristic path model for beta diversity and an extended ecological drift model serve as starting points. The model can be seen as a counterpart to Ulrich et al. [5]. These authors implemented competitive hierarchies into their neutral meta-community model while the present paper focuses on environmental filtering. Most important, the model and parameterization of four empirical data sets on aquatic plant and animal meta-communities used by Jabot et al. returned a consistent high influence of environmental stochasticity on species turnover. Of course, this major result does not come to a surprise. As typical for this kind of models it depends also to a good deal on the initial model settings. It nevertheless makes a strong conceptual point for the importance of environmental variability over dispersal and richness effects. One interesting side effect regards the impact of richness differences (ΔS). Jabot et al. interpret this as a ‘nuisance variable’ as they do not have a stringent explanation. Of course, it might be a pure statistical bias introduced by the Soerensen metric of turnover that is normalized by richness. However, I suspect that there is more behind the ΔS effect. Richness differences are generally associated with respective differences in total abundances and introduce source – sink dynamics that inevitably shape subsequent colonization – extinction processes. It would be interesting to see whether ΔS alone is able to trigger observed patterns of community assembly and community composition. Such an analysis would require partitioning of species turnover into richness and nestedness effects [11]. I encourage Jabot et al. to undertake such an effort.
The present paper is also another call to include temporal population variability into metapopulation models for a better understanding of the dynamics and triggering of community assembly. In a next step, competitive interactions should be included into the model to infer the relative importance of both factors.


[1] Götzenberger, L. et al. (2012). Ecological assembly rules in plant communities—approaches, patterns and prospects. Biological reviews, 87(1), 111-127. doi: 10.1111/j.1469-185X.2011.00187.x
[2] Ulrich, W., & Gotelli, N. J. (2013). Pattern detection in null model analysis. Oikos, 122(1), 2-18. doi: 10.1111/j.1600-0706.2012.20325.x
[3] Grilli, J., Barabás, G., Michalska-Smith, M. J., & Allesina, S. (2017). Higher-order interactions stabilize dynamics in competitive network models. Nature, 548(7666), 210. doi: 10.1038/nature23273
[4] Nuvoloni, F. M., Feres, R. J. F., & Gilbert, B. (2016). Species turnover through time: colonization and extinction dynamics across metacommunities. The American Naturalist, 187(6), 786-796. doi: 10.1086/686150
[5] Ulrich, W., Jabot, F., & Gotelli, N. J. (2017). Competitive interactions change the pattern of species co‐occurrences under neutral dispersal. Oikos, 126(1), 91-100. doi: 10.1111/oik.03392
[6] Dobramysl, U., Mobilia, M., Pleimling, M., & Täuber, U. C. (2018). Stochastic population dynamics in spatially extended predator–prey systems. Journal of Physics A: Mathematical and Theoretical, 51(6), 063001. doi: 10.1088/1751-8121/aa95c7
[7] Jabot, F., Laroche, F., Massol, F., Arthaud, F., Crabot, J., Dubart, M., Blanchet, S., Munoz, F., David, P., and Datry, T. (2019). Assessing metacommunity processes through signatures in spatiotemporal turnover of community composition. bioRxiv, 480335, ver. 3 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/480335
[8] Jabot, F., & Chave, J. (2011). Analyzing tropical forest tree species abundance distributions using a nonneutral model and through approximate Bayesian inference. The American Naturalist, 178(2), E37-E47. doi: 10.1086/660829
[9] Jabot, F., & Lohier, T. (2016). Non‐random correlation of species dynamics in tropical tree communities. Oikos, 125(12), 1733-1742. doi: 10.1111/oik.03103
[10] Datry, T., Bonada, N., & Heino, J. (2016). Towards understanding the organisation of metacommunities in highly dynamic ecological systems. Oikos, 125(2), 149-159. doi: 10.1111/oik.02922
[11] Baselga, A. (2010). Partitioning the turnover and nestedness components of beta diversity. Global ecology and biogeography, 19(1), 134-143. doi: 10.1111/j.1466-8238.2009.00490.x

Assessing metacommunity processes through signatures in spatiotemporal turnover of community compositionFranck Jabot, Fabien Laroche, Francois Massol, Florent Arthaud, Julie Crabot, Maxime Dubart, Simon Blanchet, Francois Munoz, Patrice David, Thibault Datry<p>Although metacommunity ecology has been a major field of research in the last decades, with both conceptual and empirical outputs, the analysis of the temporal dynamics of metacommunities has only emerged recently and still consists mostly of r...Biodiversity, Coexistence, Community ecology, Spatial ecology, Metacommunities & MetapopulationsWerner Ulrich2018-11-29 14:58:54 View
06 Nov 2023
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Influence of mimicry on extinction risk in Aculeata: a theoretical approach

Mullerian and Batesian mimicry can influence population and community dynamics

Recommended by based on reviews by Jesus Bellver and 1 anonymous reviewer

Mimicry between species has long attracted the attention of scientists. Over a century ago, Bates first proposed that palatable species should gain a benefit by resembling unpalatable species (Bates 1862). Not long after, Müller suggested that there could also be a mutual advantage for two unpalatable species to mimic one another to reduce predator error (Müller 1879). These forms of mimicry, Batesian and Müllerian, are now widely studied, providing broad insights into behaviour, ecology and evolution.

Numerous taxa, including both invertebrates and vertebrates, show examples of Batesian or Müllerian mimicry. Bees and wasps provide a particularly interesting case due to the differences in defence between females and males of the same species. While both males and females may display warning colours, only females can sting and inject venom to cause pain and allow escape from predators. Therefore, males are palatable mimics and can resemble females of their own species or females of another species (dual sex-limited mimicry). This asymmetry in defence could have impacts on both population structure and community assembly, yet research into mimicry largely focuses on systems without sex differences.

Here, Boutin and colleagues (2023) use a differential equations model to explore the effect of mimicry on population structure and community assembly for sex-limited defended species. Specifically, they address three questions, 1) how do female noxiousness and sex-ratio influence the extinction risk of a single species?; 2) what is the effect of mimicry on species co-existence? and 3) how does dual sex-limited mimicry influence species co-existence? Their results reveal contexts in which populations with undefended males can persist, the benefit of Müllerian mimicry for species coexistence and that dual sex-limited mimicry can have a destabilising impact on species coexistence.

The results not only contribute to our understanding of how mimicry is maintained in natural systems but also demonstrate how changes in relative abundance or population structure of one species could impact another species. Further insight into the population and community dynamics of insects is particularly important given the current population declines (Goulson 2019; Seibold et al 2019).


Bates, H. W. 1862. Contributions to the insect fauna of the Amazon Valley, Lepidoptera: Heliconidae. Trans. Linn. Soc. Lond. 23:495- 566.

Boutin, M., Costa, M., Fontaine, C., Perrard, A., Llaurens, V. 2022 Influence of sex-limited mimicry on extinction risk in Aculeata: a theoretical approach. bioRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Ecology.

Goulson, D. 2019. The insect apocalypse, and why it matters. Curr. Biol. 29: R967-R971.

Müller, F. 1879. Ituna and Thyridia; a remarkable case of mimicry in butterflies. Trans. Roy. Entom. Roc. 1879:20-29.

Seibold, S., Gossner, M. M., Simons, N. K., Blüthgen, N., Müller, J., Ambarlı, D., ... & Weisser, W. W. 2019. Arthropod decline in grasslands and forests is associated with landscape-level drivers. Nature, 574: 671-674.

Influence of mimicry on extinction risk in Aculeata: a theoretical approachMaxime Boutin, Manon Costa, Colin Fontaine, Adrien Perrard, Violaine Llaurens<p style="text-align: justify;">Positive ecological interactions, such as mutualism, can play a role in community structure and species co-existence. A well-documented case of mutualistic interaction is Mullerian mimicry, the convergence of colour...Biodiversity, Coexistence, Eco-evolutionary dynamics, Evolutionary ecology, Facilitation & MutualismAmanda Franklin2022-10-25 19:11:55 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.


[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
03 Apr 2020
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Body temperatures, life history, and skeletal morphology in the nine-banded armadillo (Dasypus novemcinctus)

Is vertebral count in mammals influenced by developmental temperature? A study with Dasypus novemcinctus

Recommended by based on reviews by Darin Croft and ?

Mammals show a very low level of variation in vertebral count, both among and within species, in comparison to other vertebrates [1]. Jordan’s rule for fishes states that the vertebral number among species increases with latitude, due to ambient temperatures during development [2]. Temperature has also been shown to influence vertebral count within species in fish [3], amphibians [4], and birds [5]. However, in mammals the count appears to be constrained, on the one hand, by a possible relationship between the development of the skeleton and the proliferations of cell lines with associated costs (neural malformations, cancer etc., [6]), and on the other by the cervical origin of the diaphragm [7].
Knight et al. [8] investigate the effect of intrauterine temperature variation on skeletal morphology during development, and focus on a particular mammal, Dasypus novemcinctus, or nine-banded armadillo. Armadillos (Xenarthra) and are characterized by relatively low body temperatures and low basal rates of metabolism. Dasypus novemcinctus is the only xenarthran mammal to have naturally expanded its range into the middle latitudes of the U.S., and one of the few mammals that invaded North America from South America. It is one of few placentals that withstand considerable decrease of body temperature without torpor. It presents a resting body temperature that is low and variable for a placental mammal of its size [9] and is the only vertebrate that gives birth to monozygotic quadruplets. Among 42 monotreme, marsupial and placental genera, Dasypus novemcinctus shows the highest variation of thoracolumbar vertebral count [10].
The particularities of Dasypus novemcinctus regarding vertebral count variation and ability to withstand variable temperature qualify it as a target organism for study of the relationship between skeleton morphology and temperature in mammals.
Knight et al. [8] explored variability in vertebral count within Dasypus novemcinctus to understand whether temperature during development determines skeleton morphology. To this end they experimented with 22 armadillos (19 with data) and litters from 12 pregnant females, in two environments, for three years — an impressive effort and experimental setup. Moreover, they used a wide variety of advanced experimental and analytical techniques. For example, they implanted intra-abdominal, long-term temperature recorders, which recorded data every 6 to 120 minutes for up to several months. They analysed body temperature periodicity by approximation of the recordings with Fourier series, and they CT-scanned fetuses.
All 19 individuals (from which data could be gathered) exhibited substantial daily variation in body temperature. Several intriguing results emerged such as the counter-intuitive finding that the mammals’ body temperature fluctuates more indoors than outdoors. Furthermore, three females (out of 12) were found to have offspring with atypical skeletons, and two of these mothers presented an extremely low internal temperature early in pregnancy. Additionally, genetically identical quadruplets differed skeletally among themselves within two litters.
Results are not yet definitive about the relationship of temperature during development and vertebral count in Dasypus novemcinctus. However, Knight et al. [8] demonstrated that nine-banded armadillos survive with high daily internal temperature fluctuations and successfully bring to term offspring which vary in skeletal morphology among and within genetically identical litters despite major temperature extremes.


[1] Hautier L, Weisbecker V, Sánchez-Villagra MR, Goswami A, Asher RJ (2010) Skeletal development in sloths and the evolution of mammalian vertebral patterning. Proceedings of the National Academy of Sciences, 107, 18903–18908. doi: 10.1073/pnas.1010335107
[2] Jordan, D.S. (1892) Relations of temperature to vertebrae among fishes. Proceedings of the United States National Museum, 1891, 107-120. doi: 10.5479/si.00963801.14-845.107
[3] Tibblin P, Berggren H, Nordahl O, Larsson P, Forsman A (2016) Causes and consequences of intra-specific variation in vertebral number. Scientific Reports, 6, 1–12. doi: 10.1038/srep26372
[4] Peabody RB, Brodie ED (1975) Effect of temperature, salinity and photoperiod on the number of trunk vertebrae in Ambystoma maculatum. Copeia, 1975, 741–746. doi: 10.2307/1443326
[5] Lindsey CC, Moodie GEE (1967) The effect of incubation temperature on vertebral count in the chicken. Canadian Journal of Zoology, 45, 891–892. doi: 10.1139/z67-099
[6] Galis F, Dooren TJMV, Feuth JD, Metz JAJ, Witkam A, Ruinard S, Steigenga MJ, Wunaendts LCD (2006) Extreme selection in humans against homeotic transformations of cervical vertebrae. Evolution, 60, 2643–2654. doi: 10.1111/j.0014-3820.2006.tb01896.x
[7] Buchholtz EA, Stepien CC (2009) Anatomical transformation in mammals: developmental origin of aberrant cervical anatomy in tree sloths. Evolution and Development, 11, 69–79. doi: 10.1111/j.1525-142X.2008.00303.x
[8] Knight F, Connor C, Venkataramanan R, Asher RJ. (2020). Body temperatures, life history, and skeletal morphology in the nine-banded armadillo (Dasypus novemcinctus). PCI-Ecology. doi: 10.17863/CAM.50971
[9] McNab BK (1980) Energetics and the limits to a temperate distribution in armadillos. Journal of Mammalogy, 61, 606–627. doi: 10.2307/1380307
[10] Asher RJ, Lin KH, Kardjilov N, Hautier L (2011) Variability and constraint in the mammalian vertebral column. Journal of Evolutionary Biology, 24, 1080–1090. doi: 10.1111/j.1420-9101.2011.02240.x

Body temperatures, life history, and skeletal morphology in the nine-banded armadillo (Dasypus novemcinctus)Frank Knight, Cristin Connor, Ramji Venkataramanan, Robert J. Asher<p>The nine banded armadillo (*Dasypus novemcinctus*) is the only xenarthran mammal to have naturally expanded its range into the middle latitudes of the USA. It is not known to hibernate, but has been associated with unusually labile core body te...Behaviour & Ethology, Evolutionary ecology, Life history, Physiology, ZoologyMar Sobral2019-11-22 22:57:31 View
29 Dec 2018
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The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web

From deserts to avocado orchards - understanding realized trophic interactions in communities

Recommended by based on reviews by Owen Petchey and 2 anonymous reviewers

The late eminent ecologist Gary Polis once stated that “most catalogued food-webs are oversimplified caricatures of actual communities” and are “grossly incomplete representations of communities in terms of both diversity and trophic connections.” Not content with that damning indictment, he went further by railing that “theorists are trying to explain phenomena that do not exist” [1]. The latter critique might have been push back for Robert May´s ground-breaking but ultimately flawed research on the relationship between food-web complexity and stability [2]. Polis was a brilliant ecologist, and his thinking was clearly influenced by his experiences researching desert food webs. Those food webs possess an uncommon combination of properties, such as frequent omnivory, cannibalism, and looping; high linkage density (L/S); and a nearly complete absence of apex consumers, since few species completely lack predators or parasites [3]. During my PhD studies, I was lucky enough to visit Joshua Tree National Park on the way to a conference in New England, and I could immediately see the problems posed by desert ecosystems. At the time, I was ruminating on the “harsh-benign” hypothesis [4], which predicts that the relative importance of abiotic and biotic forces should vary with changes in local environmental conditions (from harsh to benign). Specifically, in more “harsh” environments, abiotic factors should determine community composition whilst weakening the influence of biotic interactions. However, in the harsh desert environment I saw first-hand evidence that species interactions were not diminished; if anything, they were strengthened. Teddy-bear chollas possessed murderously sharp defenses to protect precious water, creosote bushes engaged in belowground “chemical warfare” (allelopathy) to deter potential competitors, and rampant cannibalism amongst scorpions drove temporal and spatial ontogenetic niche partitioning. Life in the desert was hard, but you couldn´t expect your competition to go easy on you.
If that experience colored my thinking about nature’s reaction to a capricious environment, then the seminal work by Robert Paine on the marine rocky shore helped further cement the importance of biotic interactions. The insights provided by Paine [5] brings us closer to the research reported in the preprint “The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web” [6], given that the authors in that study hold the environment constant and test the interactions between different permutations of a simple community. Paine [5] was able to elegantly demonstrate using the chief protagonist Pisaster ochraceus (a predatory echinoderm also known as the purple sea star) that a keystone consumer could exert strong top-down control that radically reshaped the interactions amongst other community members. What was special about this study was that the presence of Pisaster promoted species diversity by altering competition for space by sedentary species, providing a rare example of an ecological network experiment combining trophic and non-trophic interactions. Whilst there are increasing efforts to describe these interactions (e.g., competition and facilitation) in multiplex networks [7], the authors of “The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web” [6] have avoided strictly competitive interactions for the sake of simplicity. They do focus on two trophic forms of competition, namely intraguild predation and apparent competition. These two interaction motifs, along with prey switching are relevant to my own research on the influence of cross-ecosystem prey subsidies to receiving food webs [8]. In particular, the apparent competition motif may be particularly important in the context of emergent adult aquatic insects as prey subsidies to terrestrial consumers. This was demonstrated by Henschel et al. [9] where the abundances of emergent adult aquatic midges in riparian fields adjacent to a large river helped stimulate higher abundances of spiders and lower abundances of herbivorous leafhoppers, leading to a trophic cascade. The aquatic insects had a bottom-up effect on spiders and this subsidy facilitated a top-down effect that cascaded from spiders to leafhoppers to plants. The apparent competition motif becomes relevant because the aquatic midges exerted a negative indirect effect on leafhoppers mediated through their common arachnid predators.
In the preprint “The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web” [6], the authors have described different permutations of a simple mite community present in avocado orchards (Persea americana). This community comprises of two predators (Euseius stipulatus and Neoseiulus californicus), one herbivore as shared prey (Oligonychus perseae), and pollen of Carpobrotus edulis as alternative food resource, with the potential for the intraguild predation and apparent competition interaction motifs to be expressed. The authors determined that these motifs should be realized based off pairwise feeding trials. It is common for food-web researchers to depict potential food webs, which contain all species sampled and all potential trophic links based on laboratory feeding trials (as demonstrated here) or from observational data and literature reviews [10]. In reality, not all these potential feeding links are realized because species may partition space and time, thus driving alternative food-web architectures. In “The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web” [6], the authors are able to show that placing species in combinations that should yield more complex interaction motifs based off pairwise feeding trials fails to deliver – the predators revert to their preferred prey resulting in modular and simple trophic chains to be expressed. Whilst these realized interaction motifs may be stable, there might also be a tradeoff with function by yielding less top-down control than desirable when considering the potential for ecosystem services such as pest management. These are valuable insights, although it should be noted that here the fundamental niche is described in a strictly Eltonian sense as a trophic role [11]. Adding additional niche dimensions (sensu [12]), such as a thermal gradient could alter the observed interactions, although it might be possible to explain these contingencies through metabolic and optimal foraging theory combined with species traits. Nonetheless, the results of these experiments further demonstrate the need for ecologists to cross-validate theory with empirical approaches to develop more realistic and predictive food-web models, lest they invoke the wrath of Gary Polis´ ghost by “trying to explain phenomena that do not exist”.


[1] Polis, G. A. (1991). Complex trophic interactions in deserts: an empirical critique of food-web theory. The American Naturalist, 138(1), 123-155. doi: 10.1086/285208
[2] May, R. M. (1973). Stability and complexity in model ecosystems. Princeton University Press, Princeton, NJ, USA
[3] Dunne, J. A. (2006). The network structure of food webs. In Pascual, M., & Dunne, J. A. (eds) Ecological Networks: Linking Structure to Dynamics in Food Webs. Oxford University Press, New York, USA, 27-86
[4] Menge, B. A., & Sutherland, J. P. (1976). Species diversity gradients: synthesis of the roles of predation, competition, and temporal heterogeneity. The American Naturalist, 110(973), 351-369. doi: 10.1086/283073
[5] Paine, R. T. (1966). Food web complexity and species diversity. The American Naturalist, 100(910), 65-75. doi: 10.1086/282400
[6] Torres-Campos, I., Magalhães, S., Moya-Laraño, J., & Montserrat, M. (2018). The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web. bioRxiv, 324178, ver. 5 peer-reviewed and recommended by PCI Ecol. doi: 10.1101/324178
[7] Kéfi, S., Berlow, E. L., Wieters, E. A., Joppa, L. N., Wood, S. A., Brose, U., & Navarrete, S. A. (2015). Network structure beyond food webs: mapping non‐trophic and trophic interactions on Chilean rocky shores. Ecology, 96(1), 291-303. doi: 10.1890/13-1424.1
[8] Burdon, F. J., & Harding, J. S. (2008). The linkage between riparian predators and aquatic insects across a stream‐resource spectrum. Freshwater Biology, 53(2), 330-346. doi: 10.1111/j.1365-2427.2007.01897.x
[9] Henschel, J. R., Mahsberg, D., & Stumpf, H. (2001). Allochthonous aquatic insects increase predation and decrease herbivory in river shore food webs. Oikos, 93(3), 429-438. doi: 10.1034/j.1600-0706.2001.930308.x
[10] Brose, U., Pavao-Zuckerman, M., Eklöf, A., Bengtsson, J., Berg, M. P., Cousins, S. H., Mulder, C., Verhoef, H. A., & Wolters, V. (2005). Spatial aspects of food webs. In de Ruiter, P., Wolters, V., Moore, J. C., & Melville-Smith, K. (eds) Dynamic Food Webs. vol 3. Academic Press, Burlington, 463-469
[11] Elton, C. (1927). Animal Ecology. Sidgwick and Jackson, London, UK
[12] Hutchinson, G. E. (1957). Concluding Remarks. Cold Spring Harbor Symposia on Quantitative Biology, 22, 415-427. doi: 10.1101/sqb.1957.022.01.039

The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food webInmaculada Torres-Campos, Sara Magalhães, Jordi Moya-Laraño, Marta Montserrat<p>The mathematical theory describing small assemblages of interacting species (community modules or motifs) has proved to be essential in understanding the emergent properties of ecological communities. These models use differential equations to ...Community ecology, Experimental ecologyFrancis John Burdon2018-05-16 19:34:10 View
28 Mar 2019
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Direct and transgenerational effects of an experimental heat wave on early life stages in a freshwater snail

Escargots cooked just right: telling apart the direct and indirect effects of heat waves in freashwater snails

Recommended by based on reviews by Amanda Lynn Caskenette, Kévin Tougeron and arnaud sentis

Amongst the many challenges and forms of environmental change that organisms face in our era of global change, climate change is perhaps one of the most straightforward and amenable to investigation. First, measurements of day-to-day temperatures are relatively feasible and accessible, and predictions regarding the expected trends in Earth surface temperature are probably some of the most reliable we have. It appears quite clear, in particular, that beyond the overall increase in average temperature, the heat waves locally experienced by organisms in their natural habitats are bound to become more frequent, more intense, and more long-lasting [1]. Second, it is well appreciated that temperature is a major environmental factor with strong impacts on different facets of organismal development and life-history [2-4]. These impacts have reasonably clear mechanistic underpinnings, with definite connections to biochemistry, physiology, and considerations on energetics. Third, since variation in temperature is a challenge already experienced by natural populations across their current and historical ranges, it is not a completely alien form of environmental change. Therefore, we already learnt quite a lot about it in several species, and so did the species, as they may be expected to have evolved dedicated adaptive mechanisms to respond to elevated temperatures. Last, but not least, temperature is quite amenable to being manipulated as an experimental factor.
For all these reasons, experimental studies of the consequences of increased temperature hit some of a sweetspot and are a source of very nice research, in many different organisms. The work by Leicht and Seppala [5] complements a sequence of earlier studies by this group, using the freshwater snail Lymnaea stagnalis as their model system [6-7].
In the present study, the authors investigate how a heat wave (a period of abnormally elevated temperature, here 25°C versus a normal 15°C) may have indirect effects on the next generation, through maternal effects. They question whether such indirect effects exist, and if they exist, how they compare, in terms of effect size, with the (more straightforward) direct effects observed in individuals that directly experience a heat wave. Transgenerational effects are well-known to occur following periods of physiological stress, and might thus have non negligible contributions to the overall effect of warming.
In this freshwater snail, heat has very strong direct effects: mortality increases at high temperature, but survivors grow much bigger, with a greater propensity to lay eggs and a (spectacular) three-fold increase in the number of eggs laid [6]. Considering that, it is easy to consider that transgenerational effects should be small game. And indeed, the present study also observes the big and obvious direct effects of elevated temperature: higher mortality, but greater propensity to oviposit. However, it was also found that the eggs were smaller if from mothers exposed to high temperature, with a correspondingly smaller size of hatchlings. This suggests that a heat wave causes the snails to lay more eggs, but smaller ones, reminiscent of a size-number trade-off. Unfortunately, clutch size could not be measured in this experiment, so this cannot be investigated any further. For this trait, the indirect effect may indeed be regarded as small game : eggs and hatchlings were about 15 % smaller, an effect size pretty small compared to the mammoth direct positive effect of temperature on shell length (see Figure 4 ; and also [6]). The same is true for developmental time (Figure 3).
However, for some traits the story was different. In particular, it was found that the (smaller) eggs produced from heated mothers were more likely to hatch by almost 10% (Figure 2). Here the indirect effect not only goes against the direct effect (hatching rate is lower at high temperature), but it also has similar effect size. As a consequence, taking into account both the indirect and direct effects, hatching success is essentially the same at 15°C and 25°C (Figure 2). Survival also had comparable effect sizes for direct and indirect effects. Indeed, survival was reduced by about 20% regardless of whom endured the heat stress (the focal individual or her mother; Figure 4). Interestingly, the direct and indirect effects were not quite cumulative: if a mother experienced a heat wave, heating up the offspring did not do much more damage, as though the offspring were ‘adapted’ to the warmer conditions (but keep in mind that, surprisingly, the authors’ stats did not find a significant interaction; Table 2).
At the end of the day, even though at first heat seems a relatively simple and understandable component of environmental change, this study shows how varied its effects can be effects on different components of individual fitness. The overall impact most likely is a mix of direct and indirect effects, of shifts along allocation trade-offs, and of maladaptive and adaptive responses, whose overall ecological significance is not so easy to grasp. That said, this study shows that direct and indirect (maternal) effects can sometimes go against one another and have similar intensities. Indirect effects should therefore not be overlooked in this kind of studies. It also gives a hint of what an interesting challenge it is to understand the adaptive or maladaptive nature of organism responses to elevated temperatures, and to evaluate their ultimate fitness consequences.


[1] Meehl, G. A., & Tebaldi, C. (2004). More intense, more frequent, and longer lasting heat waves in the 21st century. Science (New York, N.Y.), 305(5686), 994–997. doi: 10.1126/science.1098704
[2] Adamo, S. A., & Lovett, M. M. E. (2011). Some like it hot: the effects of climate change on reproduction, immune function and disease resistance in the cricket Gryllus texensis. The Journal of Experimental Biology, 214(Pt 12), 1997–2004. doi: 10.1242/jeb.056531
[3] Deutsch, C. A., Tewksbury, J. J., Tigchelaar, M., Battisti, D. S., Merrill, S. C., Huey, R. B., & Naylor, R. L. (2018). Increase in crop losses to insect pests in a warming climate. Science (New York, N.Y.), 361(6405), 916–919. doi: 10.1126/science.aat3466
[4] Sentis, A., Hemptinne, J.-L., & Brodeur, J. (2013). Effects of simulated heat waves on an experimental plant–herbivore–predator food chain. Global Change Biology, 19(3), 833–842. doi: 10.1111/gcb.12094
[5] Leicht, K., & Seppälä, O. (2019). Direct and transgenerational effects of an experimental heat wave on early life stages in a freshwater snail. BioRxiv, 449777, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/449777
[6] Leicht, K., Seppälä, K., & Seppälä, O. (2017). Potential for adaptation to climate change: family-level variation in fitness-related traits and their responses to heat waves in a snail population. BMC Evolutionary Biology, 17(1), 140. doi: 10.1186/s12862-017-0988-x
[7] Leicht, K., Jokela, J., & Seppälä, O. (2013). An experimental heat wave changes immune defense and life history traits in a freshwater snail. Ecology and Evolution, 3(15), 4861–4871. doi: 10.1002/ece3.874

Direct and transgenerational effects of an experimental heat wave on early life stages in a freshwater snailKatja Leicht, Otto Seppälä<p>Global climate change imposes a serious threat to natural populations of many species. Estimates of the effects of climate change‐mediated environmental stresses are, however, often based only on their direct effects on organisms, and neglect t...Climate changevincent calcagno2018-10-22 22:19:22 View
06 May 2022
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Effects of climate warming on the pine processionary moth at the southern edge of its range: a retrospective analysis on egg survival in Tunisia

Even the current climate change winners could end up being losers

Recommended by based on reviews by Matt Hill, Philippe Louapre, José Hodar and Corentin Iltis

Climate change is accelerating (IPCC 2022), and so applies ever stronger selective pressures on biodiversity (Segan et al. 2016). Possible responses include range shifts or adaptations to new climatic conditions (Bellard et al. 2012), but there is still much uncertainty about the extent of most species' adaptive capacities and the impact of extreme climatic events.
The pine processionary is a major pest of pine trees in the Mediterranean area. It is notably one of the few species for which a clear link between recent climate change and its northward expansion has been established (Battisti et al. 2005), and as such is often considered as globally benefitting from climate change. However, recent results show a retraction of its range at the southern limit (Bourougaaoui et al. 2021), exposed to high warming (+1.4°C in Tunisia since 1901 as opposed to +1.12°C on average in the Northern hemisphere) and extreme summer temperature events (Verner et al. 2013). Thus, it is possible that the species' adaptive abilities are being challenged at the southern limit of its native range by the magnitude of observed climate change.
In this work, Bourougaaoui et al. (2022) investigate how climate change over the last 30 years has impacted the reproductive success of the pine processionary moth in Tunisia. A major methodological interest of this study is that they used data both from historical collections and from recent samplings, which raised a challenge for running a longitudinal analysis as sampling locations differed between the two periods. By applying a grouping method to local climatic data, the authors were able to define several large climatic clusters within the country, and analyze long-term data from different sites within the same clusters. They find that both fecundity and hatching rate decreased over the period, while at the same time both the average temperature increased and climate variability increased. One of the main conclusions is that recurrent episodes of extreme heat during summer might have a larger impact than the long-term increase of average temperature, which strongly echoes how the intensification of weather extremes is currently proving one of the most important dimensions of climate change.
However, a most interesting hypothesis also arises from the analysis of the differences between climatic clusters: preexisting adaptations to heat, for instance, phenological shifts that allow the most sensitive stages to develop earlier in the season before the extreme heat events are most likely to occur, might actually reduce impacts in the historically warmest areas. Thus the greatest climate vulnerability might not always stand where one expects it.

Battisti A, Stastny M, Netherer S, Robinet C, Schopf A, Roques A, Larsson S (2005) Expansion of Geographic Range in the Pine Processionary Moth Caused by Increased Winter Temperatures. Ecological Applications, 15, 2084–2096.

Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F (2012) Impacts of climate change on the future of biodiversity. Ecology Letters, 15, 365–377.

Bourougaaoui A, Ben Jamâa ML, Robinet C (2021) Has North Africa turned too warm for a Mediterranean forest pest because of climate change? Climatic Change, 165, 46.

Bourougaaoui A, Robinet C, Jamaa MLB, Laparie M (2022) Effects of climate warming on the pine processionary moth at the southern edge of its range: a retrospective analysis on egg survival in Tunisia. bioRxiv, 2021.08.17.456665, ver. 5 peer-reviewed and recommended by Peer Community in Ecology.

IPCC. 2022. Climate Change 2022: Impacts, Adaptation, and Vulnerability. Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change [H.-O. Pörtner, D.C. Roberts, M. Tignor, E.S. Poloczanska, K. Mintenbeck, A. Alegría, M. Craig, S. Langsdorf, S. Löschke, V. Möller, A. Okem, B. Rama (eds.)]. Cambridge University Press. In Press.

Segan DB, Murray KA, Watson JEM (2016) A global assessment of current and future biodiversity vulnerability to habitat loss–climate change interactions. Global Ecology and Conservation, 5, 12–21.

Verner D (2013) Tunisia in a Changing Climate : Assessment and Actions for Increased Resilience and Development. World Bank, Washington, DC.  

Effects of climate warming on the pine processionary moth at the southern edge of its range: a retrospective analysis on egg survival in TunisiaAsma Bourougaaoui, Christelle Robinet, Mohamed Lahbib Ben Jamâa, Mathieu Laparie<p style="text-align: justify;">In recent years, ectotherm species have largely been impacted by extreme climate events, essentially heatwaves. In Tunisia, the pine processionary moth (PPM), <em>Thaumetopoea pityocampa</em>, is a highly damaging p...Climate change, Dispersal & Migration, Life history, Phenotypic plasticity, Species distributions, Terrestrial ecology, Thermal ecology, ZoologyElodie Vercken2021-08-19 11:03:13 View
06 Jan 2021
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Comparing statistical and mechanistic models to identify the drivers of mortality within a rear-edge beech population

The complexity of predicting mortality in trees

Recommended by based on reviews by Lisa Hülsmann and 2 anonymous reviewers

One of the main issues of forest ecosystems is rising tree mortality as a result of extreme weather events (Franklin et al., 1987). Eventually, tree mortality reduces forest biomass (Allen et al., 2010), although its effect on forest ecosystem fluxes seems not lasting too long (Anderegg et al., 2016). This controversy about the negative consequences of tree mortality is joined to the debate about the drivers triggering and the mechanisms accelerating tree decline. For instance, there is still room for discussion about carbon starvation or hydraulic failure determining the decay processes (Sevanto et al., 2014) or about the importance of mortality sources (Reichstein et al., 2013). Therefore, understanding and predicting tree mortality has become one of the challenges for forest ecologists in the last decade, doubling the rate of articles published on the topic (*). Although predicting the responses of ecosystems to environmental change based on the traits of species may seem a simplistic conception of ecosystem functioning (Sutherland et al., 2013), identifying those traits that are involved in the proneness of a tree to die would help to predict how forests will respond to climate threatens.
Modelling tree mortality is complex, involving multiple factors acting simultaneously at different scales, from tree genetics to ecosystem dynamics and from microsite conditions to global climatic events. Therefore, taking into account different approaches to reduce uncertainty of the predictions is needed (Bugmann et al., 2019). Petit-Cailleux et al. (2020) uses statistical and process-based models to detect the main mortality drivers of a drought- and frost-prone beech population. Particularly, they assessed the intra-individual characteristics of the population, that may play a decisive role explaining the differences in tree vulnerability to extreme weather events. Comparing the results of both analytical approaches, they find out several key factors, such as defoliation, leaf phenology and tree size, that were consistent between them. Even more, the process-based model showed the physiological mechanisms that may explain the individual vulnerability, for instance higher loss of hydraulic conductance may increase the mortality risk of trees with early budburst phenology and large stem diameter. The authors also successfully model annual mortality rate with a linear relationship including only three parameters: loss of conductance, biomass of reserves and late frost days.
This valuable study is a good example of the complexity in understanding and predicting tree mortality. The authors carried out the ambitious commitment of studying the inter-annual variation in mortality with 14-year dataset. However, it might be not enough time to control for the dependence of temporal data to soundly model mortality rate. The authors also acknowledge that the use of two approaches increases the knowledge from different perspectives, but at the same time comparing their results is difficult because the parameters used are not identical. Particularly, process-based models tend to consider the same microclimatic conditions for every tree in the population, and may produce inconsistences with statistical models. Alternatively, individual-based modelling might overcome some of the incompatibilities between the approaches (Zhu et al., 2019).

(*) Number (and percentage) of articles found in Web of Sciences after searching (December the 10th, 2020) “tree mortality”: from 163 (0.006%) in 2010 to 412 (0.013%) in 2020.


Allen et al. (2010). A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest ecology and management, 259(4), 660-684. doi:
Anderegg et al. (2016). When a tree dies in the forest: scaling climate-driven tree mortality to ecosystem water and carbon fluxes. Ecosystems, 19(6), 1133-1147. doi:
Bugmann et al. (2019). Tree mortality submodels drive simulated long‐term forest dynamics: assessing 15 models from the stand to global scale. Ecosphere, 10(2), e02616. doi:
Franklin, J. F., Shugart, H. H. and Harmon, M. E. (1987) Death as an ecological process: the causes, consequences, and variability of tree mortality. BioScience, 37, 550–556. doi:
Petit-Cailleux, C., Davi, H., Lefèvre, F., Garrigue, J., Magdalou, J.-A., Hurson, C., Magnanou, E. and Oddou-Muratorio, S. (2020) Comparing statistical and mechanistic models to identify the drivers of mortality within a rear-edge beech population. bioRxiv, 645747, ver 7 peer-reviewed and recommended by Peer Community in Ecology.
Reichstein et al. (2013). Climate extremes and the carbon cycle. Nature, 500(7462), 287-295. doi:
Sevanto, S., Mcdowell, N. G., Dickman, L. T., Pangle, R., and Pockman, W. T. (2014). How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant, cell & environment, 37(1), 153-161. doi:
Sutherland et al. (2013). Identification of 100 fundamental ecological questions. Journal of ecology, 101(1), 58-67. doi:
Zhu, Y., Liu, Z., and Jin, G. (2019). Evaluating individual-based tree mortality modeling with temporal observation data collected from a large forest plot. Forest Ecology and Management, 450, 117496. doi:

Comparing statistical and mechanistic models to identify the drivers of mortality within a rear-edge beech populationCathleen Petit-Cailleux, Hendrik Davi, François Lefevre, Christophe Hurson, Joseph Garrigue, Jean-André Magdalou, Elodie Magnanou and Sylvie Oddou-Muratorio<p>Since several studies have been reporting an increase in the decline of forests, a major issue in ecology is to better understand and predict tree mortality. The interactions between the different factors and the physiological processes giving ...Climate change, Physiology, Population ecologyLucía DeSoto2019-05-24 11:37:38 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.


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.

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.

Kays R., Crofoot M. C., Jetz W. & Wikelski M. 2015. Terrestrial animal tracking as an eye on life and planet. Science, 348 (6240).

Marchetti K: & Price T. 1989. Differences in the foraging of juvenile and adult birds: the importance of developmental constraints. Biological Reviews, 64: 51-70.

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.

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

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.

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.

Whitford M & Klimley A. P. An overview of behavioral, physiological, and environmental sensors used in animal biotelemetry and biologging studies. Animal Biotelemetry, 7: 26.

Wooller R.D., Bradley J. S. & Croxall J. P. 1992. Long-term population studies of seabirds. Trends in Ecology and Evolution, 7: 111-114.

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