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26 May 2021
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Spatial distribution of local patch extinctions drives recovery dynamics in metacommunities

Unity makes strength: clustered extinctions have stronger, longer-lasting effects on metacommunities dynamics

Recommended by based on reviews by David Murray-Stoker and Frederik De Laender

In this article, Saade et al. (2021) investigate how the rate of local extinctions and their spatial distribution affect recolonization dynamics in metacommunities. They use an elegant combination of microcosm experiments with metacommunities of freshwater ciliates and mathematical modelling mirroring their experimental system. Their main findings are (i) that local patch extinctions increase both local (α-) and inter-patch (β-) diversity in a transient way during the recolonization process, (ii) that these effects depend more on the spatial distribution of extinctions (dispersed or clustered) than on their amount, and (iii) that they may spread regionally.
Microcosm experiments are already quite cool just by themselves and have contributed largely to conceptual advances in community ecology (see Fraser and Keddy 1997, or Jessup et al. 2004 for reviews on this topic), but they are here exploited to a whole further level by the fitting of a metapopulation dynamics model. The model allows both to identify the underlying mechanisms most likely to generate the patterns observed (here, competitive interactions) and to assess the robustness of these patterns when considering larger spatial or temporal scales. This release of experimental limitations allows here for the analysis of quantitative metrics of spatial structure, like the distance to the closest patch, which gives an interesting insight into the functional basis of the effect of the spatial distribution of extinctions.

A major strength of this study is that it highlights the importance of considering the spatial structure explicitly. Recent work on ecological networks has shown repeatedly that network structure affects the propagation of pathogens (Badham and Stocker 2010), invaders (Morel-Journel et al. 2019), or perturbation events (Gilarranz et al. 2017). Here, the spatial structure of the metacommunity is a regular grid of patches, but the distribution of extinction events may be either regularly dispersed (i.e., extinct patches are distributed evenly over the grid and are all surrounded by non-extinct patches only) or clustered (all extinct patches are neighbours). This has a direct effect on the neighbourhood of perturbed patches, and because perturbations have mostly local effects, their recovery dynamics are dominated by the composition of this immediate neighbourhood. In landscapes with dispersed extinctions, the neighbourhood of a perturbed patch is not affected by the amount of extinctions, and neither is its recovery time. In contrast, in landscapes with clustered extinctions, the amount of extinctions affects the depth of the perturbed area, which takes longer to recover when it is larger. Interestingly, the spatial distribution of extinctions here is functionally equivalent to differences in connectivity between perturbed and unperturbed patches, which results in contrasted “rescue recovery” and “mixing recovery” regimes as described by Zelnick et al. (2019).
 
Furthermore, this study focuses on local dynamics of competition and short-term, transient patterns that may have been overlooked by more classical, equilibrium-based approaches of dynamical systems of metacommunities. Indeed, in a metacommunity composed of several competitors, early theoretical work demonstrated that species coexistence is possible at the regional scale only, provided that spatial heterogeneity creates spatial variance in fitness or precludes the superior competitor from accessing certain habitat patches (Skellam 1951, Levins 1969). In the spatially homogeneous experimental system of Saade et al., one of the three ciliate species ends up dominating the community at equilibrium. However, following local, one-time extinction events, the community endures a recolonization process in which differences in dispersal may provide temporary spatial niches for inferior competitors. These transient patterns might prove essential to understand and anticipate the resilience of natural systems that are under increasing pressure, and enduring ever more frequent and intense perturbations (IPBES 2019). Spatial autocorrelation in extinction events was previously identified as a risk for stability and persistence of metacommunities (Ruokolainen 2013, Kahilainen et al. 2018). These new results show that autocorrelated perturbations also have longer-lasting effects, which is likely to increase their overall impact on metacommunity dynamics. As spatial and temporal autocorrelation of temperature and extreme climatic events are expected to increase (Di Cecco and Gouthier 2018), studies that investigate how metacommunities respond to the structure of the distribution of perturbations are more necessary than ever.
 
References


Badham J, Stocker R (2010) The impact of network clustering and assortativity on epidemic behaviour. Theoretical Population Biology, 77, 71–75. https://doi.org/10.1016/j.tpb.2009.11.003
 
Di Cecco GJ, Gouhier TC (2018) Increased spatial and temporal autocorrelation of temperature under climate change. Scientific Reports, 8, 14850. https://doi.org/10.1038/s41598-018-33217-0
 
Fraser LH, Keddy P (1997) The role of experimental microcosms in ecological research. Trends in Ecology & Evolution, 12, 478–481. https://doi.org/10.1016/S0169-5347(97)01220-2
 
Gilarranz LJ, Rayfield B, Liñán-Cembrano G, Bascompte J, Gonzalez A (2017) Effects of network modularity on the spread of perturbation impact in experimental metapopulations. Science, 357, 199–201. https://doi.org/10.1126/science.aal4122
 
IPBES (2019) Summary for policymakers of the global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. S. Díaz, J. Settele, E. S. Brondízio E.S., H. T. Ngo, M. Guèze, J. Agard, A. Arneth, P. Balvanera, K. A. Brauman, S. H. M. Butchart, K. M. A. Chan, L. A. Garibaldi, K. Ichii, J. Liu, S. M. Subramanian, G. F. Midgley, P. Miloslavich, Z. Molnár, D. Obura, A. Pfaff, S. Polasky, A. Purvis, J. Razzaque, B. Reyers, R. Roy Chowdhury, Y. J. Shin, I. J. Visseren-Hamakers, K. J. Willis, and C. N. Zayas (eds.). IPBES secretariat, Bonn, Germany. 56 pages. https://doi.org/10.5281/zenodo.3553579 
 
Jessup CM, Kassen R, Forde SE, Kerr B, Buckling A, Rainey PB, Bohannan BJM (2004) Big questions, small worlds: microbial model systems in ecology. Trends in Ecology & Evolution, 19, 189–197. https://doi.org/10.1016/j.tree.2004.01.008
 
Kahilainen A, van Nouhuys S, Schulz T, Saastamoinen M (2018) Metapopulation dynamics in a changing climate: Increasing spatial synchrony in weather conditions drives metapopulation synchrony of a butterfly inhabiting a fragmented landscape. Global Change Biology, 24, 4316–4329. https://doi.org/10.1111/gcb.14280

Levins R (1969) Some Demographic and Genetic Consequences of Environmental Heterogeneity for Biological Control1. Bulletin of the Entomological Society of America, 15, 237–240. https://doi.org/10.1093/besa/15.3.237
 
Morel-Journel T, Assa CR, Mailleret L, Vercken E (2019) Its all about connections: hubs and invasion in habitat networks. Ecology Letters, 22, 313–321. https://doi.org/10.1111/ele.13192

Ruokolainen L (2013) Spatio-Temporal Environmental Correlation and Population Variability in Simple Metacommunities. PLOS ONE, 8, e72325. https://doi.org/10.1371/journal.pone.0072325

Saade C, Kefi S, Gougat-Barbera C, Rosenbaum B, Fronhofer EA (2021) Spatial distribution of local patch extinctions drives recovery dynamics in metacommunities. bioRxiv, 2020.12.03.409524, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2020.12.03.409524
 
Skellam JG (1951) Random Dispersal in Theoretical Populations. Biometrika, 38, 196–218. https://doi.org/10.2307/2332328
 
Zelnik YR, Arnoldi J-F, Loreau M (2019) The three regimes of spatial recovery. Ecology, 100, e02586. https://doi.org/10.1002/ecy.2586

Spatial distribution of local patch extinctions drives recovery dynamics in metacommunitiesCamille Saade, Sonia Kéfi, Claire Gougat-Barbera, Benjamin Rosenbaum, and Emanuel A. Fronhofer<p style="text-align: justify;">Human activities lead more and more to the disturbance of plant and animal communities with local extinctions as a consequence. While these negative effects are clearly visible at a local scale, it is less clear how...Biodiversity, Coexistence, Colonization, Community ecology, Competition, Dispersal & Migration, Experimental ecology, Landscape ecology, Spatial ecology, Metacommunities & MetapopulationsElodie Vercken2020-12-08 15:55:20 View
02 Jun 2021
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Identifying drivers of spatio-temporal variation in survival in four blue tit populations

Blue tits surviving in an ever-changing world

Recommended by ORCID_LOGO based on reviews by Ana Sanz-Aguilar and Vicente García-Navas

How long individuals live has a large influence on a number of biological processes, both for the individuals themselves as well as for the populations they live in. For a given species, survival is often summarized in curves showing the probability to survive from one age to the next. However, these curves often hide a large amount of variation in survival. Variation can occur from chance, or if individuals have different genotypes or phenotypes that can influence how long they might live, or if environmental conditions are not the same across time or space. Such spatiotemporal variations in the conditions that individuals experience can lead to complex patterns of evolution (Kokko et al. 2017) but because of the difficulties to obtain the relevant data they have not been studied much in natural populations.
 
In this manuscript, Bastianelli and colleagues (2021) identify which environmental and population conditions are associated with variation in annual survival of blue tits. The analyses are based on an impressive dataset, tracking a total of almost 5500 adults in four populations studied for at least 19 years. The authors describe two core results. First, average annual survival is lower in deciduous forests compared to evergreen forests. The differences in average annual survival between the forest types link with previously described differences, with individuals having larger clutches (Charmantier et al. 2016) and higher aggression (Dubuc-Messier et al. 2017) in the populations where adult survival is lower. Second, there are huge fluctuations from one year to the next in the percentage of individuals surviving which occur similarly in all populations. Even though survival covaried across the four populations, this variation was not associated with any of the local or global climate indices the authors investigated.
 
Studies like these are fundamental to our understanding of population change. They are important from an applied side as they can reveal the sustainability of populations and inform potential management options. On a basic research side, they reveal how evolution operates in populations. Theoretical studies predict that individuals are often not adapted to average conditions they experience, but either selected to balance the extremes they encounter  or to make the best during harsh conditions when it really matters (Lewontin & Cohen 1969).
 
This study also opens the door to new research, highlighting that demographic studies should pay attention to variation in survival and other life history traits. For blue tits specifically, the study shows that in order to understand the demography of populations we need a better mechanistic understanding of the environmental and physiological pressures influencing whether individuals die or not to make predictions whether and how climate or other ecological effects shape variation in survival.
 
References
 
Bastianelli O, Robert A, Doutrelant C, Franceschi C de, Giovannini P, Charmantier A (2021) Identifying drivers of spatio-temporal variation in survival in four blue tit populations. bioRxiv, 2021.01.28.428563, ver. 4 peer-reviewed and recommended by Peer community in Ecology. https://doi.org/10.1101/2021.01.28.428563

Charmantier A, Doutrelant C, Dubuc-Messier G, Fargevieille A, Szulkin M (2016) Mediterranean blue tits as a case study of local adaptation. Evolutionary Applications, 9, 135–152. https://doi.org/10.1111/eva.12282

Dubuc-Messier G, Réale D, Perret P, Charmantier A (2017) Environmental heterogeneity and population differences in blue tits personality traits. Behavioral Ecology, 28, 448–459. https://doi.org/10.1093/beheco/arw148

Kokko H, Chaturvedi A, Croll D, Fischer MC, Guillaume F, Karrenberg S, Kerr B, Rolshausen G, Stapley J (2017) Can Evolution Supply What Ecology Demands? Trends in Ecology & Evolution, 32, 187–197. https://doi.org/10.1016/j.tree.2016.12.005

Lewontin RC, Cohen D (1969) On Population Growth in a Randomly Varying Environment. Proceedings of the National Academy of Sciences, 62, 1056–1060. https://doi.org/10.1073/pnas.62.4.1056

Identifying drivers of spatio-temporal variation in survival in four blue tit populationsOlivier Bastianelli, Alexandre Robert, Claire Doutrelant, Christophe de Franceschi, Pablo Giovannini, Anne Charmantier<p style="text-align: justify;">In a context of rapid climate change, the influence of large-scale and local climate on population demography is increasingly scrutinized, yet studies are usually focused on one population. Demographic parameters, i...Climate change, Demography, Evolutionary ecology, Life history, Population ecologyDieter Lukas2021-01-29 15:24:23 View
31 May 2022
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Sexual coercion in a natural mandrill population

Rare behaviours can have strong effects: evidence for sexual coercion in mandrills

Recommended by ORCID_LOGO based on reviews by Micaela Szykman Gunther and 1 anonymous reviewer

Sexual coercion can be defined as the use by a male of force, or threat of force, which increases the chances that a female will mate with him at a time when she is likely to be fertile, and/or decrease the chances that she will mate with other males, at some cost to the female (Smuts & Smuts 1993). It has been evidenced in a wide range of species and may play an important role in the evolution of sexual conflict and social systems. However, identifying sexual coercion in natural systems can be particularly challenging. Notably, while male behaviour may have immediate consequences on mating success (“harassment”), the mating benefits may be delayed in time (“intimidation”), and in such cases, evidencing coercion requires detailed temporal data at the individual level. Moreover, in some species male aggressive behaviours may be subtle or rare and hence hardly observed, yet still have important effects on female mating probability and fitness. Therefore, investigating the occurrence and consequences of sexual coercion in such species is particularly relevant but studying it in a statistically robust way is likely to require a considerable amount of time spent observing individuals.

In this paper, Smit et al. (2022) test three clear predictions of the sexual coercion hypothesis in a natural population of Mandrills, where severe male aggression towards females is rare: (1) male aggression is more likely on sexually receptive females than on females in other reproductive states, (2) receptive females are more likely to be injured and (3) male aggression directed towards females is positively related to subsequent probability of copulation between those dyads. They also tested an alternative hypothesis, the “aggressive male phenotype” under which the correlation between male aggression towards females and subsequent mating could be statistically explained by male overall aggressivity. In agreement with the three predictions of the sexual coercion hypothesis, (1) male aggression was on average 5 times more likely, and (2) injuries twice as likely, to be observed on sexually receptive females than on females in other reproductive states and (3) copulation between males and sexually receptive females was twice more likely to be observed when aggression by this male was observed on the female before sexual receptivity. There was no support for the aggressive male hypothesis.

The reviewers and I were highly positive about this study, notably regarding the way it is written and how the predictions are carefully and clearly stated, tested, interpreted, and discussed.

This study is a good illustration of a case where some behaviours may not be common or obvious yet have strong effects and likely important consequences and thus be clearly worth studying. More generally, it shows once more the importance of detailed long-term studies at the individual level for our understanding of the ecology and evolution of wild populations.

It is also a good illustration of the challenges faced, when comparing the likelihood of contrasting hypotheses means we need to alter sample sizes and/or the likelihood to observe at all some behaviours. For example, observing copulation within minutes after aggression (and therefore, showing statistical support for “harassment”) is inevitably less likely than observing copulations on the longer-term (and therefore showing statistical support for “intimidation”, when of course effort is put into recording such behavioural data on the long-term). Such challenges might partly explain some apparently intriguing results. For example, why are swollen females more aggressed by males if only aggression before the swollen period seems associated with more chances of mating? Here, the authors systematically provide effect sizes (and confidence intervals) and often describe the effects in an intuitive biological way (e.g., “Swollen females were, on average, about five times more likely to become injured”). This clearly helps the reader to not merely compare statistical significances but also the biological strengths of the estimated effects and the uncertainty around them. They also clearly acknowledge limits due to sample size when testing the harassment hypothesis, yet they provide precious information on the probability of observing mating (a rare behaviour) directly after aggression (already a rare behaviour!), that is, 3 times out of 38 aggressions observed between a male and a swollen female. Once again, this highlights how important it is to be able to pursue the enormous effort put so far into closely and continuously monitoring this wild population.

Finally, this study raises exciting new questions, notably regarding to what extent females exhibit “counter-strategies” in response to sexual coercion, notably whether there is still scope for female mate choice under such conditions, and what are the fitness consequences of these dynamic conflicting sexual interactions. No doubt these questions will sooner than later be addressed by the authors, and I am looking forward to reading their upcoming work.

References

Smit N, Baniel A, Roura-Torres B, Amblard-Rambert P, Charpentier MJE, Huchard E (2022) Sexual coercion in a natural mandrill population. bioRxiv, 2022.02.07.479393, ver. 5 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.02.07.479393

Smuts BB, Smuts R w. (1993) Male Aggression and Sexual Coercion of Females in Nonhuman Primates and Other Mammals: Evidence and Theoretical Implications. In: Advances in the Study of Behavior (eds Slater PJB, Rosenblatt JS, Snowdon CT, Milinski M), pp. 1–63. Academic Press. https://doi.org/10.1016/S0065-3454(08)60404-0

Sexual coercion in a natural mandrill populationNikolaos Smit, Alice Baniel, Berta Roura-Torres, Paul Amblard-Rambert, Marie J. E. Charpentier, Elise Huchard<p style="text-align: justify;">Increasing evidence indicates that sexual coercion is widespread. While some coercive strategies are conspicuous, such as forced copulation or sexual harassment, less is known about the ecology and evolution of inti...Behaviour & EthologyMatthieu Paquet2022-02-11 09:32:49 View
24 Nov 2023
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Consistent individual positions within roosts in Spix's disc-winged bats

Consistent individual differences in habitat use in a tropical leaf roosting bat

Recommended by based on reviews by Annemarie van der Marel and 2 anonymous reviewers

Consistent individual differences in habitat use are found across species and can play a role in who an individual mates with, their risk of predation, and their ability to compete with others (Stuber et al. 2022). However, the data informing such hypotheses come primarily from temperate regions (Stroud & Thompson 2019, Titley et al. 2017). This calls into question the generalizability of the conclusions from this research until further investigations can be conducted in tropical regions.

Giacomini and colleagues (2023) tackled this task in an investigation of consistent individual differences in habitat use in the Central American tropics. They explored whether Spix’s disc-winged bats form positional hierarchies in roosts, which is an excellent start to learning more about the social behavior of this species - a species that is difficult to directly observe. They found that individual bats use their roosting habitat in predictable ways by positioning themselves consistently either in the bottom, middle, or top of the roost leaf. Individuals chose the same positions across time and across different roost sites. They also found that age and sex play a role in which sections individuals are positioned in.

Their research shows that consistent individual differences in habitat use are present in a tropical system, and sets the stage for further investigations into social behavior in this species, particularly whether there is a dominance hierarchy among individuals and whether some positions in the roost are more protective and sought after than others.

References

Giacomini G, Chaves-Ramirez S, Hernandez-Pinson A, Barrantes JP, Chaverri G. (2023). Consistent individual positions within roosts in Spix's disc-winged bats. bioRxiv, https://doi.org/10.1101/2022.11.04.515223 

Stroud, J. T., & Thompson, M. E. (2019). Looking to the past to understand the future of tropical conservation: The importance of collecting basic data. Biotropica, 51(3), 293-299. https://doi.org/10.1111/btp.12665

Stuber, E. F., Carlson, B. S., & Jesmer, B. R. (2022). Spatial personalities: a meta-analysis of consistent individual differences in spatial behavior. Behavioral Ecology, 33(3), 477-486. https://doi.org/10.1093/beheco/arab147 

Titley, M. A., Snaddon, J. L., & Turner, E. C. (2017). Scientific research on animal biodiversity is systematically biased towards vertebrates and temperate regions. PloS one, 12(12), e0189577. https://doi.org/10.1371/journal.pone.0189577

Consistent individual positions within roosts in Spix's disc-winged batsGiada Giacomini, Silvia Chaves-Ramirez, Andres Hernandez-Pinson, Jose Pablo Barrantes, Gloriana Chaverri<p style="text-align: justify;">Individuals within both moving and stationary groups arrange themselves in a predictable manner; for example, some individuals are consistently found at the front of the group or in the periphery and others in the c...Behaviour & Ethology, Social structure, ZoologyCorina Logan2022-11-05 17:39:35 View
07 Jun 2023
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High intraspecific growth variability despite strong evolutionary heritage in a neotropical forest

Environmental and functional determinants of tree performance in a neotropical forest: the imprint of evolutionary legacy on growth strategies

Recommended by ORCID_LOGO based on reviews by David Murray-Stoker, Camille Girard and Jelena Pantel

The hyperdiverse tropical forests have long fascinated ecologists because the fact that so many species persist at a low density at a local scale remains hard to explain. Both niche-based and neutral hypotheses have been tested, primarily based on analyzing the taxonomic composition of tropical forest plots (Janzen 1970; Hubbell 2001). Studies of the functional and phylogenetic structure of tropical tree communities have further aimed to better assess the importance of niche-based processes. For instance, Baraloto et al. (2012) found that co-occurring species were functionally and phylogenetically more similar in a neotropical forest, suggesting a role of environmental filtering. Likewise, Schmitt et al. (2021) found the influence of environmental filtering on the functional composition of an Indian rainforest. Yet these studies evidenced non-random trait-environment association based on the composition of assemblages only (in terms of occurrences and abundances). A major challenge remains to further address whether and how tree performance varies among species and individuals in tropical forests.

Functional traits are related to components of individual fitness (Violle et al. 2007). Recently, more and more emphasis has been put on examining the relationship between functional trait values and demographic parameters (Salguero-Gómez et al. 2018), in order to better understand how functional trait values determine species population dynamics and abundances in assemblages. Fortunel et al. (2018) found an influence of functional traits on species growth variation related to topography, and less clearly to neighborhood density (crowding). Poorter et al. (2018) observed 44% of trait variation within species in a neotropical forest. Although individual trait values would be expected to be better predictors of performance than average values measured at the species level, Poorter et al still found a poor relationship.

Schmitt et al. (2023) examined how abiotic conditions and biotic interactions (considering neighborhood density) influenced the variation of individual potential tree growth, in a tropical forest plot located in French Guiana. They also considered the link between species-averaged values of growth potential and functional traits. Schmitt et al. (2023) found substantial variation in growth potential within species, that functional traits explained 40% of the variation of species-averaged growth and, noticeably, that the taxonomic structure (used as random effect in their model) explained a third of the variation in individual growth.

Although functional traits of roots, wood and leaves could predict a significant part of species growth potential, much variability of tree growth occurred within species. Intraspecific trait variation can thus be huge in response to changing abiotic and biotic contexts across individuals. The information on phylogenetic relationships can still provide a proxy of the integrated phenotypic variation that is under selection across the phylogeny, and determine a variation in growth strategies among individuals. The similarity of the phylogenetic structure suggests a joint selection of these growth strategies and related functional traits during events of convergent evolution. Baraloto et al. (2012) already noted that phylogenetic distance can be a proxy of niche overlap in tropical tree communities. Here, Schmitt et al. further demonstrate that evolutionary heritage is significantly related to individual growth variation, and plead for better acknowledging this role in future studies.

While the role of fitness differences in tropical tree community dynamics remained to be assessed, the present study provides new evidence that individual growth does vary depending on evolutionary relationships, which can reflect the roles of selection and adaptation on growth strategies. Therefore, investigating both the influence of functional traits and phylogenetic relationships on individual performance remains a promising avenue of research, for functional and community ecology in general.

REFERENCES

Baraloto, Christopher, Olivier J. Hardy, C. E. Timothy Paine, Kyle G. Dexter, Corinne Cruaud, Luke T. Dunning, Mailyn-Adriana Gonzalez, et al. 2012. « Using functional traits and phylogenetic trees to examine the assembly of tropical tree communities ». Journal of Ecology, 100: 690‑701.
https://doi.org/10.1111/j.1365-2745.2012.01966.x
 
Fortunel Claire, Lasky Jesse R., Uriarte María, Valencia Renato, Wright S.Joseph, Garwood Nancy C., et Kraft Nathan J. B. 2018. « Topography and neighborhood crowding can interact to shape species growth and distribution in a diverse Amazonian forest ». Ecology, 99(10): 2272-2283. https://doi.org/10.1002/ecy.2441
 
Hubbell, S. P. 2001. The Unified Neutral Theory of Biodiversity and Biogeography. 1 vol. Princeton and Oxford: Princeton University Press. https://www.jstor.org/stable/j.ctt7rj8w
 
Janzen, Daniel H. 1970. « Herbivores and the number of tree species in tropical forests ». American Naturalist, 104(940): 501-528. https://doi.org/10.1086/282687
 
Poorter, Lourens, Carolina V. Castilho, Juliana Schietti, Rafael S. Oliveira, et Flávia R. C. Costa. 2018. « Can traits predict individual growth performance? A test in a hyperdiverse tropical forest ». New Phytologist, 219 (1): 109‑21. https://doi.org/10.1111/nph.15206
 
Salguero-Gómez, Roberto, Cyrille Violle, Olivier Gimenez, et Dylan Childs. 2018. « Delivering the promises of trait-based approaches to the needs of demographic approaches, and vice versa ». Functional Ecology, 32 (6): 1424‑35. https://doi.org/10.1111/1365-2435.13148
 
Schmitt, Sylvain, Valérie Raevel, Maxime Réjou‐Méchain, Narayanan Ayyappan, Natesan Balachandran, Narayanan Barathan, Gopalakrishnan Rajashekar, et François Munoz. 2021. « Canopy and understory tree guilds respond differently to the environment in an Indian rainforest ». Journal of Vegetation Science, e13075. https://doi.org/10.1111/jvs.13075
 
Sylvain Schmitt, Bruno Hérault, et Géraldine Derroire. 2023. « High intraspecific growth variability despite strong evolutionary heritage in a neotropical forest ». bioRxiv, 2022.07.27.501745, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.07.27.501745
 
Violle, C., M. L. Navas, D. Vile, E. Kazakou, C. Fortunel, I. Hummel, et E. Garnier. 2007. « Let the concept of trait be functional! » Oikos, 116(5), 882-892. https://doi.org/10.1111/j.0030-1299.2007.15559.x

High intraspecific growth variability despite strong evolutionary heritage in a neotropical forestSylvain Schmitt, Bruno Hérault, Géraldine Derroire<p style="text-align: justify;">Individual tree growth is a key determinant of species performance and a driver of forest dynamics and composition. Previous studies on tree growth unravelled the variation in species growth as a function of demogra...Community ecology, Demography, Population ecologyFrançois Munoz Jelena Pantel, David Murray-Stoker2022-08-01 14:29:04 View
31 Aug 2023
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Assessing species interactions using integrated predator-prey models

Addressing the daunting challenge of estimating species interactions from count data

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

Trophic interactions are at the heart of community ecology. Herbivores consume plants, predators consume herbivores, and pathogens and parasites infect, and sometimes kill, individuals of all species in a food web. Given the ubiquity of trophic interactions, it is no surprise that ecologists and evolutionary biologists strive to accurately characterize them. 

The outcome of an interaction between individuals of different species depends upon numerous factors such as the age, sex, and even phenotype of the individuals involved and the environment in which they are in. Despite this complexity, biologists often simplify an interaction down to a single number, an interaction coefficient that describes the average outcome of interactions between members of the populations of the species. Models of interacting species tend to be very simple, and interaction coefficients are often estimated from time series of population sizes of interacting species. Although biologists have long known that this approach is often approximate and sometimes unsatisfactory, work on estimating interaction strengths in more complex scenarios, and using ecological data beyond estimates of abundance, is still in its infancy. 

In their paper, Matthieu Paquet and Frederic Barraquand (2023)​ develop a demographic model of a predator and its prey. They then simulate demographic datasets that are typical of those collected by ecologists and use integrated population modelling to explore whether they can accurately retrieve the values interaction coefficients included in their model. They show that they can with good precision and accuracy. The work takes an important step in showing that accurate interaction coefficients can be estimated from the types of individual-based data that field biologists routinely collect, and it paves for future work in this area.

As if often the case with exciting papers such as this, the work opens up a number of other avenues for future research. What happens as we move from demographic models of two species interacting such as those used by Paquet and Barraquand​ to more realistic scenarios including multiple species? How robust is the approach to incorrectly specified process or observation models, core components of integrated population modelling that require detailed knowledge of the system under study? 

Integrated population models have become a powerful and widely used tool in single-species population ecology. It is high time the techniques are extended to community ecology, and this work takes an important step in showing that this should and can be done. I would hope the paper is widely read and cited.

References

Paquet, M., & Barraquand, F. (2023). Assessing species interactions using integrated predator-prey models. EcoEvoRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.32942/X2RC7W

Assessing species interactions using integrated predator-prey modelsMatthieu Paquet, Frederic Barraquand<p style="text-align: justify;">Inferring the strength of species interactions from demographic data is a challenging task. The Integrated Population Modelling (IPM) approach, bringing together population counts, capture-recapture, and individual-...Community ecology, Demography, Food webs, Population ecology, Statistical ecologyTim Coulson Ilhan Özgen-Xian2023-01-05 17:02:22 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.
 
References

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. https://doi.org/10.1890/04-1903

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. https://doi.org/10.1111/j.1461-0248.2011.01736.x

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. https://doi.org/10.1007/s10584-021-03077-1

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. https://doi.org/10.1101/2021.08.17.456665

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. https://doi.org/10.1016/j.gecco.2015.11.002

Verner D (2013) Tunisia in a Changing Climate : Assessment and Actions for Increased Resilience and Development. World Bank, Washington, DC. https://doi.org/10.1596/978-0-8213-9857-9  

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
29 May 2023
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Using integrated multispecies occupancy models to map co-occurrence between bottlenose dolphins and fisheries in the Gulf of Lion, French Mediterranean Sea

Mapping co-occurence of human activities and wildlife from multiple data sources

Recommended by based on reviews by Mason Fidino and 1 anonymous reviewer

Two fields of research have grown considerably over the past twenty years: the investigation of human-wildlife conflicts (e.g. see Treves & Santiago-Ávila 2020), and multispecies occupancy modelling (Devarajan et al. 2020). In their recent study, Lauret et al. (2023) combined both in an elegant methodological framework, applied to the study of the co-occurrence of fishing activities and bottlenose dolphins in the French Mediterranean.

A common issue with human-wildlife conflicts (and, in particular, fishery by-catch) is that data is often only available from those conflicts or interactions, limiting the validity of the predictions (Kuiper et al. 2022). Lauret et al. use independent data sources informing the occurrence of fishing vessels and dolphins, combined in a Bayesian multispecies occupancy model where vessels are "the other species". I particularly enjoyed that approach, as integration of human activities in ecological models can be extremely complex, but can also translate in phenomena that can be captured as one would of individuals of a species, as long as the assumptions are made clearly. Here, the model is made more interesting by accounting for environmental factors (seabed depth) borrowing an approach from Generalized Additive Models in the Bayesian framework. While not pretending to provide (yet) practical recommendations to help conserve bottlenose dolphins (and other wildlife conflicts), this study and the associated code are a promising step in that direction.

REFERENCES

Devarajan, K., Morelli, T.L. & Tenan, S. (2020), Multi-species occupancy models: review, roadmap, and recommendations. Ecography, 43: 1612-1624. https://doi.org/10.1111/ecog.04957

Kuiper, T., Loveridge, A.J. and Macdonald, D.W. (2022), Robust mapping of human–wildlife conflict: controlling for livestock distribution in carnivore depredation models. Anim. Conserv., 25: 195-207. https://doi.org/10.1111/acv.12730

Lauret V, Labach H, David L, Authier M, & Gimenez O (2023) Using integrated multispecies occupancy models to map co-occurrence between bottlenose dolphins and fisheries in the Gulf of Lion, French Mediterranean Sea. Ecoevoarxiv, ver. 2 peer-reviewed and recommended by PCI Ecology. https://doi.org/10.32942/osf.io/npd6u

Treves, A. & Santiago-Ávila, F.J. (2020). Myths and assumptions about human-wildlife conflict and coexistence. Conserv. Biol. 34, 811–818.  https://doi.org/10.1111/cobi.13472

Using integrated multispecies occupancy models to map co-occurrence between bottlenose dolphins and fisheries in the Gulf of Lion, French Mediterranean SeaValentin Lauret, Hélène Labach, Léa David, Matthieu Authier, Olivier Gimenez<p style="text-align: justify;">In the Mediterranean Sea, interactions between marine species and human activities are prevalent. The coastal distribution of bottlenose dolphins (<em>Tursiops truncatus</em>) and the predation pressure they put on ...Marine ecology, Population ecology, Species distributionsPaul Caplat2022-10-21 11:13:36 View
28 Apr 2023
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Most diverse, most neglected: weevils (Coleoptera: Curculionoidea) are ubiquitous specialized brood-site pollinators of tropical flora

Pollination-herbivory by weevils claiming for recognition: the Cinderella among pollinators

Recommended by based on reviews by Susan Kirmse, Carlos Eduardo Nunes and 2 anonymous reviewers

Since Charles Darwin times, and probably earlier, naturalists have been eager to report the rarest pollinators being discovered, and this still happens even in recent times; e.g., increased evidence of lizards, cockroaches, crickets or earwigs as pollinators (Suetsugu 2018, Komamura et al. 2021, de Oliveira-Nogueira et al. 2023), shifts to invasive animals as pollinators, including passerine birds and rats (Pattemore & Wilcove 2012), new amazing cases of mimicry in pollination, such as “bleeding” flowers that mimic wounded insects (Heiduk et al., 2023) or even the possibility that a tree frog is reported for the first time as a pollinator (de Oliveira-Nogueira et al. 2023). This is in part due to a natural curiosity of humans about rarity, which pervades into scientific insight (Gaston 1994). Among pollinators, the apparent rarity of some interaction types is sometimes a symptom of a lack of enough inquiry. This seems to be the case of weevil pollination, given that these insects are widely recognized as herbivores, particularly those that use plant parts to nurse their breed and never were thought they could act also as mutualists, pollinating the species they infest. This is known as a case of brood site pollination mutualism (BSPM), which also involves an antagonistic counterpart (herbivory) to which plants should face. This is the focus of the manuscript (Haran et al. 2023) we are recommending here. There is wide treatment of this kind of pollination in textbooks, albeit focused on yucca-yucca moth and fig-fig wasp interactions due to their extreme specialization (Pellmyr 2003, Kjellberg et al. 2005), and more recently accompanied by Caryophyllaceae-moth relationship (Kephart et al. 2006). 

Here we find a detailed review that shows that the most diverse BSPM, in terms of number of plant and pollinator species involved, is that of weevils in the tropics. The mechanism of BSPM does not involve a unique morphological syndrome, as it is mostly functional and thus highly dependent on insect biology (Fenster & al. 2004), whereas the flower phenotypes are highly divergent among species. Probably, the inconspicuous nature of the interaction, and the overwhelming role of weevils as seed predators, even as pests, are among the causes of the neglection of weevils as pollinators, as it could be in part the case of ants as pollinators (de Vega et al. 2014). The paper by Haran et al (2023) comes to break this point.

Thus, the rarity of weevil pollination in former reports is not a consequence of an anecdotical nature of this interaction, even for the BSPM, according to the number of cases the authors are reporting, both in terms of plant and pollinator species involved. This review has a classical narrative format which involves a long text describing the natural history behind the cases. It is timely and fills the gap for this important pollination interaction for biodiversity and also for economic implications for fruit production of some crops. Former reviews have addressed related topics on BSPM but focused on other pollinators, such as those mentioned above. Besides, the review put much effort into the animal side of the interaction, which is not common in the pollination literature. Admittedly, the authors focus on the detailed description of some paradigmatic cases, and thereafter suggest that these can be more frequently reported in the future, based on varied evidence from morphology, natural history, ecology, and distribution of alleged partners. This procedure was common during the development of anthecology, an almost missing term for floral ecology (Baker 1983), relying on accumulative evidence based on detailed observations and experiments on flowers and pollinators. Currently, a quantitative approach based on the tools of macroecological/macroevolutionary analyses is more frequent in reviews. However, this approach requires a high amount of information on the natural history of the partnership, which allows for sound hypothesis testing. By accumulating this information, this approach allows the authors to pose specific questions and hypotheses which can be tested, particularly on the efficiency of the systems and their specialization degree for both the plants and the weevils, apparently higher for the latter. This will guarantee that this paper will be frequently cited by floral ecologists and evolutionary biologists and be included among the plethora of floral syndromes already described, currently based on more explicit functional grounds (Fenster et al. 2004). In part, this is one of the reasons why the sections focused on future prospects is so large in the review. 

I foresee that this mutualistic/antagonistic relationship will provide excellent study cases for the relative weight of these contrary interactions among the same partners and its relationship with pollination specialization-generalization and patterns of diversification in the plants and/or the weevils. As new studies are coming, it is possible that BSPM by weevils appears more common in non-tropical biogeographical regions. In fact, other BSPM are not so uncommon in other regions (Prieto-Benítez et al. 2017). In the future, it would be desirable an appropriate testing of the actual effect of phylogenetic niche conservatism, using well known and appropriately selected BSPM cases and robust phylogenies of both partners in the mutualism. Phylogenetic niche conservatism is a central assumption by the authors to report as many cases as possible in their review, and for that they used taxonomic relatedness. As sequence data and derived phylogenies for large numbers of vascular plant species are becoming more frequent (Jin & Quian 2022), I would recommend the authors to perform a comparative analysis using this phylogenetic information. At least, they have included information on phylogenetic relatedness of weevils involved in BSPM which allow some inferences on the multiple origins of this interaction. This is a good start to explore the drivers of these multiple origins through the lens of comparative biology.

References

Baker HG (1983) An Outline of the History of Anthecology, or Pollination Biology. In: L Real (ed). Pollination Biology. Academic Press.

de-Oliveira-Nogueira CH, Souza UF, Machado TM, Figueiredo-de-Andrade CA, Mónico AT, Sazima I, Sazima M, Toledo LF (2023). Between fruits, flowers and nectar: The extraordinary diet of the frog Xenohyla truncate. Food Webs 35: e00281. https://doi.org/10.1016/j.fooweb.2023.e00281

Fenster CB W, Armbruster S, Wilson P, Dudash MR, Thomson JD (2004). Pollination syndromes and floral specialization. Annu. Rev. Ecol. Evol. Syst. 35: 375–403. https://doi.org/10.1146/annurev.ecolsys.34.011802.132347

Gaston KJ (1994). What is rarity? In KJ Gaston (ed): Rarity. Population and Community Biology Series, vol 13. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-0701-3_1

Haran J, Kergoat GJ, Bruno, de Medeiros AS (2023) Most diverse, most neglected: weevils (Coleoptera: Curculionoidea) are ubiquitous specialized brood-site pollinators of tropical flora. hal. 03780127, version 2 peer-reviewed and recommended by Peer Community in Ecology. https://hal.inrae.fr/hal-03780127

Heiduk A, Brake I, Shuttleworth A, Johnson SD (2023) ‘Bleeding’ flowers of Ceropegia gerrardii (Apocynaceae-Asclepiadoideae) mimic wounded insects to attract kleptoparasitic fly pollinators. New Phytologist. https://doi.org/10.1111/nph.18888

Jin, Y., & Qian, H. (2022). V. PhyloMaker2: An updated and enlarged R package that can generate very large phylogenies for vascular plants. Plant Diversity, 44(4), 335-339. https://doi.org/10.1016/j.pld.2022.05.005

Kjellberg F, Jousselin E, Hossaert-Mckey M, Rasplus JY (2005). Biology, ecology, and evolution of fig-pollinating wasps (Chalcidoidea, Agaonidae). In: A. Raman et al (eds) Biology, ecology and evolution of gall-inducing arthropods 2, 539-572. Science Publishers, Enfield.

Komamura R, Koyama K, Yamauchi T, Konno Y, Gu L (2021). Pollination contribution differs among insects visiting Cardiocrinum cordatum flowers. Forests 12: 452. https://doi.org/10.3390/f12040452

Pattemore DE, Wilcove DS (2012) Invasive rats and recent colonist birds partially compensate for the loss of endemic New Zealand pollinators. Proc. R. Soc. B 279: 1597–1605. https://doi.org/10.1098/rspb.2011.2036

Pellmyr O (2003) Yuccas, yucca moths, and coevolution: a review. Ann. Missouri Bot. Gard. 90: 35-55. https://doi.org/10.2307/3298524

Prieto-Benítez S, Yela JL, Giménez-Benavides L (2017) Ten years of progress in the study of Hadena-Caryophyllaceae nursery pollination. A review in light of new Mediterranean data. Flora, 232, 63-72. https://doi.org/10.1016/j.flora.2017.02.004

Suetsugu K (2019) Social wasps, crickets and cockroaches contribute to pollination of the holoparasitic plant Mitrastemon yamamotoi (Mitrastemonaceae) in southern Japan. Plant Biology 21 176–182. https://doi.org/10.1111/plb.12889

Most diverse, most neglected: weevils (Coleoptera: Curculionoidea) are ubiquitous specialized brood-site pollinators of tropical floraJulien Haran, Gael J. Kergoat, Bruno A. S. de Medeiros<p style="text-align: justify;">In tropical environments, and especially tropical rainforests, a major part of pollination services is provided by diverse insect lineages. Unbeknownst to most, beetles, and more specifically hyperdiverse weevils (C...Biodiversity, Evolutionary ecology, Pollination, Tropical ecologyJuan Arroyo2022-09-28 11:54:37 View
12 Apr 2023
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Feeding and growth variations affect δ13C and δ15N budgets during ontogeny in a lepidopteran larva

Refining our understanding how nutritional conditions affect 13C and 15N isotopic fractionation during ontogeny in a herbivorous insect

Recommended by based on reviews by Anton Potapov and 1 anonymous reviewer

Using stable isotope fractionation to disentangle and understand the trophic positions of animals within the food webs they are embedded within has a long tradition in ecology (Post, 2002; Scheu, 2002). Recent years have seen increasing application of the method with several recent reviews summarizing past advancements in this field (e.g. Potapov et al., 2019; Quinby et al., 2020).

In their new manuscript, Charberet and colleagues (2023) set out to refine our understanding of the processes that lead to nitrogen and carbon stable isotope fractionation by investigating how herbivorous insect larvae (specifically, the noctuid moth Spodoptera littoralis) respond to varying nutritional conditions (from starving to ad libitum feeding) in terms of stable isotopes enrichment. Though the underlying mechanisms have been experimentally investigated before in terrestrial invertebrates (e.g. in wolf spiders; Oelbermann & Scheu, 2002), the elegantly designed and adequately replicated experiments by Charberet and colleagues add new insights into this topic. Particularly, the authors provide support for the hypotheses that (A) 15N is disproportionately accumulated under fast growth rates (i.e. when fed ad libitum) and that (B) 13C is accumulated under low growth rates and starvation due to depletion of 13C-poor fat tissues. Applying this knowledge to field samples where feeding conditions are usually not known in detail is not straightforward, but the new findings could still help better interpretation of field data under specific conditions that make starvation for herbivores much more likely (e.g. droughts).

Overall this study provides important methodological advancements for a better understanding of plant-herbivore interactions in a changing world.

REFERENCES 

Charberet, S., Maria, A., Siaussat, D., Gounand, I., & Mathieu, J. (2023). Feeding and growth variations affect δ13C and δ15N budgets during ontogeny in a lepidopteran larva. bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.11.09.515573

Oelbermann, K., & Scheu, S. (2002). Stable Isotope Enrichment (δ 15N and δ 13C) in a Generalist Predator (Pardosa lugubris, Araneae: Lycosidae): Effects of Prey Quality. Oecologia, 130(3), 337–344. https://doi.org/10.1007/s004420100813

Post, D. M. (2002). Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology, 83(3), 703–718. https://doi.org/10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2

Potapov, A. M., Tiunov, A. V., & Scheu, S. (2019). Uncovering trophic positions and food resources of soil animals using bulk natural stable isotope composition. Biological Reviews, 94(1), 37–59. https://doi.org/10.1111/brv.12434

Quinby, B. M., Creighton, J. C., & Flaherty, E. A. (2020). Stable isotope ecology in insects: A review. Ecological Entomology, 45(6), 1231–1246. https://doi.org/10.1111/een.12934

Scheu, S. (2002). The soil food web: Structure and perspectives. European Journal of Soil Biology, 38(1), 11–20. https://doi.org/10.1016/S1164-5563(01)01117-7

Feeding and growth variations affect δ13C and δ15N budgets during ontogeny in a lepidopteran larvaSamuel M. Charberet, Annick Maria, David Siaussat, Isabelle Gounand, Jérôme Mathieu<p style="text-align: justify;">Isotopes are widely used in ecology to study food webs and physiology. The fractionation observed between trophic levels in nitrogen and carbon isotopes, explained by isotopic biochemical selectivity, is subject to ...Experimental ecology, Food webs, PhysiologyGregor Kalinkat2022-11-16 15:23:31 View