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04 Sep 2024
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InsectChange: Comment

Why we need to clean the Augean stables of ecology – the case of InsectChange

Recommended by ORCID_LOGO based on reviews by Bradley Cardinale and 1 anonymous reviewer

As biodiversity has become a major global concern for a variety of stakeholders, and society in general, assessments of biodiversity trends at all spatial scales have flourished in the past decades. To assess trends, one needs data, and the more precise the data, the more precise the trend. Or, if precision is not perfect, uncertainty in the data must be acknowledged and accounted for. Such considerations have already been raised in ecology, most notably regarding the value of species distribution data to model the current and future distribution of species (Rocchini et al., 2011, Duputié et al., 2014, Tessarolo et al., 2021), leading to serious doubts regarding the value of public databases (Maldonado et al., 2015). And more recently similar issues have been raised regarding databases of species traits (Augustine et al., 2024), emphasizing the importance of good data practice and traceability.

Science is by nature a self-correcting human process, with many steps of the scientific activity prone to errors and misinterpretations. Collation of ecological data, sadly, is proof of this. Spurred by the astonishing results of Hallmann et al. (2017) regarding the decline of insect biomass, and to more precisely answer the question of biodiversity trends in insects and settle an ongoing debate (Cardinale et al., 2018), van Klink et al. (2020, 2021) established the InsectChange database. Several perceptive comments have already been made regarding the possible issues in the methods and interpretations of this study (Desquilbet et al., 2020, Jähnig et al., 2021, Duchenne et al., 2022). However, the biggest issue might have been finally unearthed by Gaume & Desquilbet (2024): with poorly curated data, the InsectChange database is unlikely to support most of the initial claims regarding insect biodiversity trends.

The compilation of errors and inconsistencies present in InsectChange and evinced by Gaume & Desquilbet (2024) is stunning to say the least, with a mix of field and experimental data combined without regard for experimental manipulation of environmental factors, non-standardised transformations of abundances, the use of non-insect taxa to compute insect trends, and inadequate geographical localizations of samplings. I strongly advise all colleagues interested in the study of biodiversity from global databases to consider the points raised by the authors, as it is quite likely that other databases might suffer from the same ailments as well. Reading this paper is also educating and humbling in its own way, since the publication of the original papers based on InsectChange seems to have proceeded without red flags from reviewers or editors. The need for publishing fast results that will make the next buzz, thus obeying the natural selection of bad science (Smaldino and McElreath, 2016), might be the systemic culprit. However, this might also be the opportunity ecology needs to consider the reviewing and curation of data as a crucial step of science quality assessment. To make final assessments, let us proceed with less haste.

References

Augustine, S. P., Bailey-Marren, I., Charton, K. T., Kiel, N. G. & Peyton, M. S. (2024) Improper data practices erode the quality of global ecological databases and impede the progress of ecological research. Global Change Biology, 30, e17116. https://doi.org/10.1111/gcb.17116

Cardinale, B. J., Gonzalez, A., Allington, G. R. H. & Loreau, M. (2018) Is local biodiversity declining or not? A summary of the debate over analysis of species richness time trends. Biological Conservation, 219, 175-183. https://doi.org/10.1016/j.biocon.2017.12.021

Desquilbet, M., Gaume, L., Grippa, M., Céréghino, R., Humbert, J.-F., Bonmatin, J.-M., Cornillon, P.-A., Maes, D., Van Dyck, H. & Goulson, D. (2020) Comment on “Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances”. Science, 370, eabd8947. https://doi.org/10.1126/science.abd8947

Duchenne, F., Porcher, E., Mihoub, J.-B., Loïs, G. & Fontaine, C. (2022) Controversy over the decline of arthropods: a matter of temporal baseline? Peer Community Journal, 2. https://doi.org/10.24072/pcjournal.131

Duputié, A., Zimmermann, N. E. & Chuine, I. (2014) Where are the wild things? Why we need better data on species distribution. Global Ecology and Biogeography, 23, 457-467. https://doi.org/10.1111/geb.12118

Gaume, L. & Desquilbet, M. (2024) InsectChange: Comment. biorXiv, ver.4 peer-reviewed and recommended by PCI Ecology https://doi.org/10.1101/2023.06.17.545310

Hallmann, C. A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., Schwan, H., Stenmans, W., Müller, A., Sumser, H., Hörren, T., Goulson, D. & de Kroon, H. (2017) More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLOS ONE, 12, e0185809. https://doi.org/10.1371/journal.pone.0185809

Jähnig, S. C., Baranov, V., Altermatt, F., Cranston, P., Friedrichs-Manthey, M., Geist, J., He, F., Heino, J., Hering, D., Hölker, F., Jourdan, J., Kalinkat, G., Kiesel, J., Leese, F., Maasri, A., Monaghan, M. T., Schäfer, R. B., Tockner, K., Tonkin, J. D. & Domisch, S. (2021) Revisiting global trends in freshwater insect biodiversity. WIREs Water, 8, e1506. https://doi.org/10.1002/wat2.1506

Maldonado, C., Molina, C. I., Zizka, A., Persson, C., Taylor, C. M., Albán, J., Chilquillo, E., Rønsted, N. & Antonelli, A. (2015) Estimating species diversity and distribution in the era of Big Data: to what extent can we trust public databases? Global Ecology and Biogeography, 24, 973-984. https://doi.org/10.1111/geb.12326

Rocchini, D., Hortal, J., Lengyel, S., Lobo, J. M., Jiménez-Valverde, A., Ricotta, C., Bacaro, G. & Chiarucci, A. (2011) Accounting for uncertainty when mapping species distributions: The need for maps of ignorance. Progress in Physical Geography, 35, 211-226. https://doi.org/10.1177/0309133311399491

Smaldino, P. E. & McElreath, R. (2016) The natural selection of bad science. Royal Society Open Science, 3. https://doi.org/10.1098/rsos.160384

Tessarolo, G., Ladle, R. J., Lobo, J. M., Rangel, T. F. & Hortal, J. (2021) Using maps of biogeographical ignorance to reveal the uncertainty in distributional data hidden in species distribution models. Ecography, 44, 1743-1755. https://doi.org/10.1111/ecog.05793

van Klink, R., Bowler, D. E., Comay, O., Driessen, M. M., Ernest, S. K. M., Gentile, A., Gilbert, F., Gongalsky, K. B., Owen, J., Pe'er, G., Pe'er, I., Resh, V. H., Rochlin, I., Schuch, S., Swengel, A. B., Swengel, S. R., Valone, T. J., Vermeulen, R., Wepprich, T., Wiedmann, J. L. & Chase, J. M. (2021) InsectChange: a global database of temporal changes in insect and arachnid assemblages. Ecology, 102, e03354. https://doi.org/10.1002/ecy.3354

van Klink, R., Bowler, D. E., Gongalsky, K. B., Swengel, A. B., Gentile, A. & Chase, J. M. (2020) Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances. Science, 368, 417-420. https://doi.org/10.1126/science.aax9931

InsectChange: CommentLaurence Gaume, Marion Desquilbet<p>The InsectChange database (van Klink et al. 2021) underlying the meta-analysis by van Klink et al. (2020a) compiles worldwide time series of the abundance and biomass of invertebrates reported as insects and arachnids, as well as ecological dat...Biodiversity, Climate change, Freshwater ecology, Landscape ecology, Meta-analyses, Species distributions, Terrestrial ecology, ZoologyFrancois Massol2024-01-04 18:57:01 View
19 Feb 2020
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Soil variation response is mediated by growth trajectories rather than functional traits in a widespread pioneer Neotropical tree

Growth trajectories, better than organ-level functional traits, reveal intraspecific response to environmental variation

Recommended by ORCID_LOGO based on reviews by Georges Kunstler and François Munoz

Functional traits are “morpho-physio-phenological traits which impact fitness indirectly via their effects on growth, reproduction and survival” [1]. Most functional traits are defined at organ level, e.g. for leaves, roots and stems, and reflect key aspects of resource acquisition and resource use by organisms for their development and reproduction [2]. More rarely, some functional traits can be related to spatial development, such as vegetative height and lateral spread in plants.
Organ-level traits are especially popular because they can be measured in a standard way and easily compared over many plants. But these traits can broadly vary during the life of an organism. For instance, Roggy et al. [3] found that Leaf Mass Area can vary from 30 to 140 g.m^(-2) between seedling and adult stages for the canopy tree Dicorynia guianensis in French Guiana. Fortunel et al. [4] have also showed that developmental stages much contribute to functional trait variation within several Micropholis tree species in lowland Amazonia.
The way plants grow and invest resources into organs is variable during life and allows defining specific developmental sequences and architectural models [5,6]. There is clear ontogenic variation in leaf number, leaf properties and ramification patterns. Ontogenic variations reflect changing adaptation of an individual over its life, depending on the changing environmental conditions.
In this regard, measuring a single functional trait at organ level in adult trees should miss the variation of resource acquisition and use strategies over time. Thus we should built a more integrative approach of ecological development, also called “eco-devo” approach [7].
Although the ecological significance of ontogeny and developmental strategies is now well known, the extent to which it contributes to explain species survival and coexistence in communities is still broadly ignored in functional ecology. Levionnois et al. [8] investigated intraspecific variation of functional traits and growth trajectories in a typical, early-successional tree species in French Guiana, Amazonia. This species, Cecropia obtusa, is generalist regarding soil type and can be found on both white sand and ferralitic soil. The study examines whether there in intraspecific variation in functional traits and growth trajectories of C. obtusa in response to the contrasted soil types.
The tree communities observed on the two types of soils include species with distinctive functional trait values, that is, there are changes in species composition related to different species strategies along the classical wood and leaf economic spectra. The populations of C. obtusa found on the two soils showed some difference in functional traits, but it did not concern traits related to the main economic spectra. Conversely, the populations showed different growth strategies, in terms of spatial and temporal development.
The major lessons we can learn from the study are:
(i) Functional traits measured at organ level cannot reflect well how long-lived plants collect and invest resources during their life. The results show the potential of considering architectural and developmental traits together with organ-level functional traits, to better acknowledge the variation in ecological strategies over plant life, and thus to better understand community assembly processes.
(ii) What makes functional changes between communities differs when considering interspecific and intraspecific variation. Species turnover should encompass different corteges of soil specialists. These specialists are sorted along economic spectra, as shown in tropical rainforests and globally [2]. Conversely, a generalist species such as C. obtusa does occur on contrasted soil, which entails that it can accommodate the contrasted ecological conditions. However, the phenotypic adjustment is not related to how leaves and wood ensure photosynthesis, water and nutrient acquisition, but regards the way the resources are allocated to growth and reproduction over time.
The results of the study stress the need to better integrate growth strategies and ontogeny in the research agenda of functional ecology. We can anticipate that organ-level functional traits and growth trajectories will be more often considered together in ecological studies. The integration should help better understand the temporal niche of organisms, and how organisms can coexist in space and time with other organisms during their life. Recently, Klimešová et al. [9] have proposed standardized protocols for collecting plant modularity traits. Such effort to propose easy-to-measure traits representing plant development and ontogeny, with clear functional roles, should foster the awaited development of an “eco-devo” approach.

References

[1] Violle, C., Navas, M. L., Vile, D., Kazakou, E., Fortunel, C., Hummel, I., & Garnier, E. (2007). Let the concept of trait be functional!. Oikos, 116(5), 882-892. doi: 10.1111/j.0030-1299.2007.15559.x
[2] Díaz, S. et al. (2016). The global spectrum of plant form and function. Nature, 529(7585), 167-171. doi: 10.1038/nature16489
[3] Roggy, J. C., Nicolini, E., Imbert, P., Caraglio, Y., Bosc, A., & Heuret, P. (2005). Links between tree structure and functional leaf traits in the tropical forest tree Dicorynia guianensis Amshoff (Caesalpiniaceae). Annals of forest science, 62(6), 553-564. doi: 10.1051/forest:2005048
[4] Fortunel, C., Stahl, C., Heuret, P., Nicolini, E. & Baraloto, C. (2020). Disentangling the effects of environment and ontogeny on tree functional dimensions for congeneric species in tropical forests. New Phytologist. doi: 10.1111/nph.16393
[5] Barthélémy, D., & Caraglio, Y. (2007). Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Annals of botany, 99(3), 375-407. doi: 10.1093/aob/mcl260
[6] Hallé, F., & Oldeman, R. A. (1975). An essay on the architecture and dynamics of growth of tropical trees. Kuala Lumpur: Penerbit Universiti Malaya.
[7] Sultan, S. E. (2007). Development in context: the timely emergence of eco-devo. Trends in Ecology & Evolution, 22(11), 575-582. doi: 10.1016/j.tree.2007.06.014
[8] Levionnois, S., Tysklind, N., Nicolini, E., Ferry, B., Troispoux, V., Le Moguedec, G., Morel, H., Stahl, C., Coste, S., Caron, H. & Heuret, P. (2020). Soil variation response is mediated by growth trajectories rather than functional traits in a widespread pioneer Neotropical tree. bioRxiv, 351197, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/351197
[9] Klimešová, J. et al. (2019). Handbook of standardized protocols for collecting plant modularity traits. Perspectives in Plant Ecology, Evolution and Systematics, 40, 125485. doi: 10.1016/j.ppees.2019.125485

Soil variation response is mediated by growth trajectories rather than functional traits in a widespread pioneer Neotropical treeSébastien Levionnois, Niklas Tysklind, Eric Nicolini, Bruno Ferry, Valérie Troispoux, Gilles Le Moguedec, Hélène Morel, Clément Stahl, Sabrina Coste, Henri Caron, Patrick Heuret<p style="text-align: justify;">1- Trait-environment relationships have been described at the community level across tree species. However, whether interspecific trait-environment relationships are consistent at the intraspecific level is yet unkn...Botany, Eco-evolutionary dynamics, Habitat selection, Ontogeny, Tropical ecologyFrançois Munoz2018-06-21 17:13:17 View
22 Nov 2021
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Beating your neighbor to the berry patch

When more competitors means less harvested resource

Recommended by ORCID_LOGO based on reviews by Francois Massol, Jeremy Van Cleve and 1 anonymous reviewer

In this paper, Alan R. Rogers (2021) examines the dynamics of foraging strategies for a resource that gains value over time (e.g., ripening fruits), while there is a fixed cost of attempting to forage the resource, and once the resource is harvested nothing is left for other harvesters. For this model, not any pure foraging strategy is evolutionary stable. A mixed equilibrium exists, i.e., with a mixture of foraging strategies within the population, which is still evolutionarily unstable. Nonetheless, Alan R. Rogers shows that for a large number of competitors and/or high harvesting cost, the mixture of strategies remains close to the mixed equilibrium when simulating the dynamics. Surprisingly, in a large population individuals will less often attempt to forage the resource and will instead “go fishing”. The paper also exposes an experiment of the game with students, which resulted in a strategy distribution somehow close to the theoretical mixture of strategies.

The economist John F. Nash Jr. (1950) gained the Nobel Prize of economy in 1994 for his game theoretical contributions. He gave his name to the “Nash equilibrium”, which represents a set of individual strategies that is reached whenever all the players have nothing to gain by changing their strategy while the strategies of others are unchanged. Alan R. Rogers shows that the mixed equilibrium in the foraging game is such a Nash equilibrium. Yet it is evolutionarily unstable insofar as a distribution close to the equilibrium can invade.

The insights of the study are twofold. First, it sheds light on the significance of Nash equilibrium in an ecological context of foraging strategies. Second, it shows that an evolutionarily unstable state can rule the composition of the ecological system. Therefore, the contribution made by the paper should be most significant to better understand the dynamics of competitive communities and their eco-evolutionary trajectories. 

References

Nash JF (1950) Equilibrium points in n-person games. Proceedings of the National Academy of Sciences, 36, 48–49. https://doi.org/10.1073/pnas.36.1.48

Rogers AR (2021) Beating your Neighbor to the Berry Patch. bioRxiv, 2020.11.12.380311, ver. 8 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2020.11.12.380311

 

Beating your neighbor to the berry patchAlan R. Rogers<p style="text-align: justify;">Foragers often compete for resources that ripen (or otherwise improve) gradually. What strategy is optimal in this situation? It turns out that there is no optimal strategy. There is no evolutionarily stable strateg...Behaviour & Ethology, Evolutionary ecology, ForagingFrançois Munoz Erol Akçay, Jorge Peña, Sébastien Lion, François Rousset, Ulf Dieckmann , Troy Day , Corina Tarnita , Florence Debarre , Daniel Friedman , Vlastimil Krivan , Ulf Dieckmann 2020-12-10 18:38:49 View
01 Mar 2022
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Dissimilarity of species interaction networks: quantifying the effect of turnover and rewiring

How to evaluate and interpret the contribution of species turnover and interaction rewiring when comparing ecological networks?

Recommended by ORCID_LOGO based on reviews by Ignasi Bartomeus and 1 anonymous reviewer

A network includes a set of vertices or nodes (e.g., species in an interaction network), and a set of edges or links (e.g., interactions between species). Whether and how networks vary in space and/or time are questions often addressed in ecological research. 

Two ecological networks can differ in several extents: in that species are different in the two networks and establish new interactions (species turnover), or in that species that are present in both networks establish different interactions in the two networks (rewiring). The ecological meaning of changes in network structure is quite different according to whether species turnover or interaction rewiring plays a greater role. Therefore, much attention has been devoted in recent years on quantifying and interpreting the relative changes in network structure due to species turnover and/or rewiring.

Poisot et al. (2012) proposed to partition the global variation in structure between networks, \( \beta_{WN} \) (WN = Whole Network) into two terms: \( \beta_{OS} \) (OS = Only Shared species) and \( \beta_{ST} \) (ST = Species Turnover), such as \( \beta_{WN} = \beta_{OS} + \beta_{ST} \).

The calculation lays on enumerating the interactions between species that are common or not to two networks, as illustrated on Figure 1 for a simple case. Specifically, Poisot et al. (2012) proposed to use a Sorensen type measure of network dissimilarity, i.e., \( \beta_{WN} = \frac{a+b+c}{(2a+b+c)/2} -1=\frac{b+c}{2a+b+c} \) , where \( a \) is the number of interactions shared between the networks, while \( b \) and \( c \) are interaction numbers unique to one and the other network, respectively. \( \beta_{OS} \) is calculated based on the same formula, but only for the subnetworks including the species common to the two networks, in the form \( \beta_{OS} = \frac{b_{OS}+c_{OS}}{2a_{OS}+b_{OS}+c_{OS}} \) (e.g., Fig. 1). \( \beta_{ST} \) is deduced by subtracting \( \beta_{OS} \) from \( \beta_{WN} \) and represents in essence a "dissimilarity in interaction structure introduced by dissimilarity in species composition" (Poisot et al. 2012).

Figure 1. Ecological networks exemplified in Fründ (2021) and discussed in Poisot (2022). a is the number of shared links (continuous lines in right figures), while b+c is the number of edges unique to one or the other network (dashed lines in right figures).

Alternatively, Fründ (2021) proposed to define \( \beta_{OS} = \frac{b_{OS}+c_{OS}}{2a+b+c} \) and \( \beta_{ST} = \frac{b_{ST}+c_{ST}}{2a+b+c} \), where \( b_{ST}=b-b_{OS} \)  and \( c_{ST}=c-c_{OS} \) , so that the components \( \beta_{OS} \) and \( \beta_{ST} \) have the same denominator. In this way, Fründ (2021) partitioned the count of unique \( b+c=b_{OS}+b_{ST}+c_{ST} \) interactions, so that \( \beta_{OS} \) and \( \beta_{ST} \) sums to \( \frac{b_{OS}+c_{OS}+b_{ST}+c_{ST}}{2a+b+c} = \frac{b+c}{2a+b+c} = \beta_{WN} \). Fründ (2021) advocated that this partition allows a more sensible comparison of \( \beta_{OS} \) and \( \beta_{ST} \), in terms of the number of links that contribute to each component.

For instance, let us consider the networks 1 and 2 in Figure 1 (left panel) such as \( a_{OS}=2 \) (continuous lines in right panel), \( b_{ST} + c_{ST} = 1 \) and \( b_{OS} + c_{OS} = 1 \) (dashed lines in right panel), and thereby \( a = 2 \), \( b+c=2 \), \( \beta_{WN} = 1/3 \). Fründ (2021) measured \( \beta_{OS}=\beta_{ST}=1/6 \) and argued that it is appropriate insofar as it reflects that the number of unique links in the OS and ST components contributing to network dissimilarity (dashed lines) are actually equal. Conversely, the formula of Poisot et al. (2012) yields \( \beta_{OS}=1/5 \), hence \( \beta_{ST} = \frac{1}{3}-\frac{1}{5}=\frac{2}{15}<\beta_{OS} \). Fründ (2021) thus argued that the method of Poisot tends to underestimate the contribution of species turnover.

To clarify and avoid misinterpretation of the calculation of \( \beta_{OS} \) and \( \beta_{ST} \) in Poisot et al. (2012), Poisot (2022) provides a new, in-depth mathematical analysis of the decomposition of \( \beta_{WN} \). Poisot et al. (2012) quantify in \( \beta_{OS} \) the actual contribution of rewiring in network structure for the subweb of common species. Poisot (2022) thus argues that \( \beta_{OS} \) relates only to the probability of rewiring in the subweb, while the definition of \( \beta_{OS} \) by Fründ (2021) is relative to the count of interactions in the global network (considered in denominator), and is thereby dependent on both rewiring probability and species turnover. Poisot (2022) further clarifies the interpretation of \( \beta_{ST} \). \( \beta_{ST} \) is obtained by subtracting \( \beta_{OS} \) from \( \beta_{WN} \) and thus represents the influence of species turnover in terms of the relative architectures of the global networks and of the subwebs of shared species. Coming back to the example of Fig.1., the Poisot et al. (2012) formula posits that \( \frac{\beta_{ST}}{\beta_{WN}}=\frac{2/15}{1/3}=2/5 \), meaning that species turnover contributes two-fifths of change in network structure, while rewiring in the subweb of common species contributed three fifths.  Conversely, the approach of Fründ (2021) does not compare the architectures of global networks and of the subwebs of shared species, but considers the relative contribution of unique links to network dissimilarity in terms of species turnover and rewiring. 

Poisot (2022) concludes that the partition proposed in Fründ (2021) does not allow unambiguous ecological interpretation of rewiring. He provides guidelines for proper interpretation of the decomposition proposed in Poisot et al. (2012).

References

Fründ J (2021) Dissimilarity of species interaction networks: how to partition rewiring and species turnover components. Ecosphere, 12, e03653. https://doi.org/10.1002/ecs2.3653

Poisot T, Canard E, Mouillot D, Mouquet N, Gravel D (2012) The dissimilarity of species interaction networks. Ecology Letters, 15, 1353–1361. https://doi.org/10.1111/ele.12002

Poisot T (2022) Dissimilarity of species interaction networks: quantifying the effect of turnover and rewiring. EcoEvoRxiv Preprints, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.32942/osf.io/gxhu2

Dissimilarity of species interaction networks: quantifying the effect of turnover and rewiringTimothée Poisot<p style="text-align: justify;">Despite having established its usefulness in the last ten years, the decomposition of ecological networks in components allowing to measure their β-diversity retains some methodological ambiguities. Notably, how to ...Biodiversity, Interaction networks, Theoretical ecologyFrançois Munoz2021-07-31 00:18:41 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
18 Sep 2024
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Predicting species distributions in the open ocean with convolutional neural networks

The potential of Convolutional Neural Networks for modeling species distributions

Recommended by ORCID_LOGO based on reviews by Jean-Olivier Irisson, Sakina-Dorothee Ayata and 1 anonymous reviewer

Morand et al. (2024) designed convolutional neural networks to predict the occurrences of 38 marine animals worldwide. The environmental predictors were sea surface temperature, chlorophyll concentration, salinity and fifteen others. The time of some of the predictors was chosen to be as close as possible to the time of the observed occurrence.

This approach has previously only been applied to the analysis of the distribution of terrestrial plant species (Botella et al. 2018, Deneu et al. 2021), so the application here to very different marine ecosystems and organisms is a novelty worth highlighting and discussing.

A very interesting feature of PCI Ecology is that reviews are provided with the final manuscript and the present recommendation text.

In the case of the Morand et al. article, the reviewers provided very detailed and insightful comments that deserve to be published and read alongside the article.

The reviewers' comments question the ecological significance and implications of choosing fine temporal and spatial scales in CNN distribution modelling in order to obtain species distribution modelling (SDM).

The main question debated during the review process was whether the CNN modeling approach used here can be defined as a kind of niche modeling.

The fact is that most of the organisms studied here are mobile, and the authors have taken into account precise environmental information at dates close to those of species appearance (for example, "Temperature and chlorophyll values were also included 15 and 5 days before the occurrences"). In doing so, they took into account the fine spatial and temporal scales of species occurrences and environmental conditions, which can be influenced by both environmental preferences and the movement behaviors of individuals. The question then arises: does this approach really represent the ecological niches of the marine organisms selected? Given that most selected organisms may have specific seasonal movement dynamics, the CNN model also learns the individual movement behaviors of organisms over seasons and years. The ecological niche is a broader concept that takes into account all the environmental conditions that enable species to persist over the course of their lives and over generations. This differs from the case of sessile land plants, which must respond to the environmental context only at the points of appearance.

This is not a shortcoming of the methodology proposed here but rather an interesting conceptual issue to be considered and discussed. Modelling the occurrence of individuals at a given time and position can characterize not only the species' niche but also the dynamics of organisms' temporal movements. As a result, the model predicts the position of individuals at a given time, while the niche should also represent the role of environmental conditions faced by individuals at other times in their lives.
A relevant perspective would then be to analyze whether and how the neural network can help disentangle the ranges of environmental conditions defining the niche from those influencing the movement dynamics of individuals.

Another interesting point is that the CNN model is used here as a multi-species classifier, meaning that it provides the ranked probability that a given observation corresponds to one of the 38 species considered in the study, depending on the environmental conditions at the location and time of the observation. In other words, the model provides the relative chance of choosing each of the 38 species at a given time and place. Imagine that you are only studying two species that have exactly the same niche, a standard SDM approach should provide a high probability of occurrence close to 1 in localities where environmental conditions are very and equally suited to both species, while the CNN classifier would provide a value close to 0.5 for both species, meaning that we have an equal chance of choosing one or the other. Consequently, the fact that the probability given by the classifier is higher for a species at a given point than at another point does not (necessarily) mean that the first point presents better environmental conditions for that species but rather that we are more likely to choose it over one of the other species at this point than at another. In fact, the classification task also reflects whether the other 37 species are more or less likely to be found at each point. The classifier, therefore, does not provide the relative probability of occurrence of a species in space but rather a relative chance of finding it instead of one of the other 37 species at each point of space and time.

It is important that an ecologist designing a multi-species classifier for species distribution modelling is well aware of this point and does not interpret the variation of probabilities for a species in space as an indication of more or less suitable habitat for that specific species. On the other hand, predicting the relative probabilities of finding species to a given point at a given time gives an indication of the dynamics of their local co-occurrence. In this respect, the CNN approach is closer to a joint species distribution model (jSDM). As Ovaskainen et al. (2017) mention, "By simultaneously drawing on the information from multiple species, these (jSDM) models allow one to seek community-level patterns in how species respond to their environment". Let's return to the two species example we used above. The fact that the probabilities are 0.5 for both species actually suggests that both species can coexist at the same abundance at this location. In this respect, the CNN multi-species classifier offers promising prospects for the prediction of assemblages and habitats thanks to the relative importance of the most characteristic/dominant species from a species pool. The species pool comprises all classified species and must be sufficiently representative of the ecological diversity of species niches in the area.

Finally, CNN-based species distribution modelling is a powerful and promising tool for studying the distributions of multi-species assemblages as a function of local environmental features but also of the spatial heterogeneity of each feature around the observation point in space and time (Deneu et al. 2021). It allows acknowledging the complex effects of environmental predictors and the roles of their spatial and temporal heterogeneity through the convolution operations performed in the neural network. As more and more computationally intensive tools become available, and as more and more environmental data becomes available at finer and finer temporal and spatial scales, the CNN approach is likely to be increasingly used to study biodiversity patterns across spatial and temporal scales.

References

Botella, C., Joly, A., Bonnet, P., Monestiez, P., and Munoz, F. (2018). Species distribution modeling based on the automated identification of citizen observations. Applications in Plant Sciences, 6(2), e1029. https://doi.org/10.1002/aps3.1029

Deneu, B., Servajean, M., Bonnet, P., Botella, C., Munoz, F., and Joly, A. (2021). Convolutional neural networks improve species distribution modelling by capturing the spatial structure of the environment. PLoS Computational Biology, 17(4), e1008856. https://doi.org/10.1371/journal.pcbi.1008856

Morand, G., Joly, A., Rouyer, T., Lorieul, T., and Barde, J. (2024) Predicting species distributions in the open ocean with convolutional neural networks. bioRxiv, ver.3 peer-reviewed and recommended by PCI Ecology https://doi.org/10.1101/2023.08.11.551418

Ovaskainen, O., Tikhonov, G., Norberg, A., Guillaume Blanchet, F., Duan, L., Dunson, D., ... and Abrego, N. (2017). How to make more out of community data? A conceptual framework and its implementation as models and software. Ecology letters, 20(5), 561-576. https://doi.org/10.1111/ele.12757

Predicting species distributions in the open ocean with convolutional neural networksGaétan Morand, Alexis Joly, Tristan Rouyer, Titouan Lorieul, Julien Barde<p>As biodiversity plummets due to anthropogenic disturbances, the conservation of oceanic species is made harder by limited knowledge of their distributions and migrations. Indeed, tracking species distributions in the open ocean is particularly ...Marine ecology, Species distributionsFrançois Munoz Jean-Olivier Irisson2023-08-13 07:25:28 View
13 May 2024
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Getting More by Asking for Less: Linking Species Interactions to Species Co-Distributions in Metacommunities

Beyond pairwise species interactions: coarser inference of their joined effects is more relevant

Recommended by ORCID_LOGO based on reviews by Frederik De Laender, Hao Ran Lai and Malyon Bimler

Barbier et al. (2024) investigated the dynamics of species abundances depending on their ecological niche (abiotic component) and on (numerous) competitive interactions. In line with previous evidence and expectations (Barbier et al. 2018), the authors show that it is possible to robustly infer the mean and variance of interaction coefficients from species co-distributions, while it is not possible to infer the individual coefficient values.

The authors devised a simulation framework representing multispecies dynamics in an heterogeneous environmental context (2D grid landscape). They used a Lotka-Volterra framework involving pairwise interaction coefficients and species-specific carrying capacities. These capacities depend on how well the species niche matches the local environmental conditions, through a Gaussian function of the distance of the species niche centers to the local environmental values.

They considered two contrasted scenarios denoted as « Environmental tracking » and « Dispersal limited ». In the latter case, species are initially seeded over the environmental grid and cannot disperse to other cells, while in the former case they can disperse and possibly be more performant in other cells.

The direct effects of species on one another are encoded in an interaction matrix A, and the authors further considered net interactions depending on the inverse of the matrix of direct interactions (Zelnik et al., 2024). The net effects are context-dependent, i.e., it involves the environment-dependent biotic capacities, even through the interaction terms can be defined between species as independent from local environment.

The results presented here underline that the outcome of many individual competitive interactions can only be understood in terms of macroscopic properties. In essence, the results here echoe the mean field theories that investigate the dynamics of average ecological properties instead of the microscopic components (e.g., McKane et al. 2000). In a philosophical perspective, community ecology has long struggled with analyzing and inferring local determinants of species coexistence from species co-occurrence patterns, so that it was claimed that no universal laws can be derived in the discipline (Lawton 1999). Using different and complementary methods and perspectives, recent research has also shown that species assembly parameter values cannot be unambiguously inferred from species co-occurrences only, even in simple designs where an equilibrium can be reached (Poggiato et al. 2021). Although the roles of high-order competitive interactions and intransivity can lead to species coexistence, the simple view of a single loop of competitive interactions is easily challenged when further interactions and complexity is added (Gallien et al. 2024). But should we put so much emphasis on inferring individual interaction coefficients? In a quest to understand the emerging properties of elementary processes, ecological theory could go forward with a more macroscopic analysis and understanding of species coexistence in many communities.

The authors referred several times to an interesting paper from Schaffer (1981), entitled « Ecological abstraction: the consequences of reduced dimensionality in ecological models ». It proposes that estimating individual species competition coefficients is not possible, but that competition can be assessed at the coarser level of organisation, i.e., between ecological guilds. This idea implies that the dimensionality of the competition equations should be greatly reduced to become tractable in practice. Taking together this claim with the results of the present Barbier et al. (2024) paper, it becomes clearer that the nature of competitive interactions can be addressed through « abstracted » quantities, as those of guilds or the moments of the individual competition coefficients (here the average and the standard deviation).

Therefore the scope of Barbier et al. (2024) framework goes beyond statistical issues in parameter inference, but question the way we must think and represent the numerous competitive interactions in a simplified and robust way.

References

Barbier, Matthieu, Jean-François Arnoldi, Guy Bunin, et Michel Loreau. 2018. « Generic assembly patterns in complex ecological communities ». Proceedings of the National Academy of Sciences 115 (9): 2156‑61. https://doi.org/10.1073/pnas.1710352115
 
Barbier, Matthieu, Guy Bunin, et Mathew A Leibold. 2024. « Getting More by Asking for Less: Linking Species Interactions to Species Co-Distributions in Metacommunities ». bioRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2023.06.04.543606
 
Gallien, Laure, Maude  Charlie Cavaliere, Marie  Charlotte Grange, François Munoz, et Tamara Münkemüller. 2024. « Intransitive stability collapses under the influence of dominant competitors ». The American Naturalist. https://doi.org/10.1086/730297
 
Lawton, J. H. 1999. « Are There General Laws in Ecology? » Oikos 84 (février):177‑92. https://doi.org/10.2307/3546712
 
McKane, Alan, David Alonso, et Ricard V Solé. 2000. « Mean-field stochastic theory for species-rich assembled communities ». Physical Review E 62 (6): 8466. https://doi.org/10.1103/PhysRevE.62.8466
 
Poggiato, Giovanni, Tamara Münkemüller, Daria Bystrova, Julyan Arbel, James S. Clark, et Wilfried Thuiller. 2021. « On the Interpretations of Joint Modeling in Community Ecology ». Trends in Ecology & Evolution. https://doi.org/10.1016/j.tree.2021.01.002
 
Schaffer, William M. 1981. « Ecological abstraction: the consequences of reduced dimensionality in ecological models ». Ecological monographs 51 (4): 383‑401. https://doi.org/10.2307/2937321
 
Zelnik, Yuval R., Nuria Galiana, Matthieu Barbier, Michel Loreau, Eric Galbraith, et Jean-François Arnoldi. 2024. « How collectively integrated are ecological communities? » Ecology Letters 27 (1): e14358. https://doi.org/10.1111/ele.14358

Getting More by Asking for Less: Linking Species Interactions to Species Co-Distributions in MetacommunitiesMatthieu Barbier, Guy Bunin, Mathew A. Leibold<p>AbstractOne of the more difficult challenges in community ecology is inferring species interactions on the basis of patterns in the spatial distribution of organisms. At its core, the problem is that distributional patterns reflect the ‘realize...Biogeography, Community ecology, Competition, Spatial ecology, Metacommunities & Metapopulations, Species distributions, Statistical ecology, Theoretical ecologyFrançois Munoz2023-10-21 14:14:16 View
02 Oct 2018
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How optimal foragers should respond to habitat changes? On the consequences of habitat conversion.

Optimal foraging in a changing world: old questions, new perspectives

Recommended by ORCID_LOGO based on reviews by Frederick Adler, Andrew Higginson and 1 anonymous reviewer

Marginal value theorem (MVT) is an archetypal model discussed in every behavioural ecology textbook. Its popularity is largely explained but the fact that it is possible to solve it graphically (at least in its simplest form) with the minimal amount of equations, which is a sensible strategy for an introductory course in behavioural ecology [1]. Apart from this heuristic value, one may be tempted to disregard it as a naive toy model. After a burst of interest in the 70's and the 80's, the once vivid literature about optimal foraging theory (OFT) has lost its momentum [2]. Yet, OFT and MVT have remained an active field of research in the parasitoidologists community, mostly because the sampling strategy of a parasitoid in patches of hosts and its resulting fitness gain are straightforward to evaluate, which eases both experimental and theoretical investigations [3].
This preprint [4] is in line with the long-established literature on OFT. It follows two theoretical articles [5,6] in which Vincent Calcagno and co-authors assessed the effect of changes in the environmental conditions on optimal foraging strategy. This time, they did not modify the shape of the gain function (describing the diminishing return of the cumulative intake as a function of the residency time in a patch) but the relative frequencies of good and bad patches. At first sight, that sounds like a minor modification of their earlier models. Actually, even the authors initially were fooled by the similarities before spotting the pitfalls. Here, they genuinely point out the erroneous verbal prediction in their previous paper in which some non-trivial effects of the change in patch frequencies have been overlooked. The present study indeed provides a striking example of ecological fallacy, and more specifically of Simpson's paradox which occurs when the aggregation of subgroups modifies the apparent pattern at the scale of the entire population [7,8]. In the case of MVT under constraints of habitat conversion, the increase of the residency times in both bad and good patches can result in a decrease of the average residency time at the level of the population. This apparently counter-intuitive property can be observed, for instance, when the proportion of bad quality patches strongly increases, which increases the probability that the individual forages on theses quickly exploited patches, and thus decreases its average residency time on the long run.
The authors thus put the model on the drawing board again. Proper assessment of the effect of change in the frequency of patch quality is more mathematically challenging than when one considers only changes in the shape of the gain function. The expected gain must be evaluated at the scale of the entire habitat instead of single patch. Overall, this study, which is based on a rigorous formalism, stands out as a warning against too rapid interpretations of theoretical outputs. It is not straightforward to generalize the predictions of previous models without careful evaluating their underlying hypotheses. The devil is in the details: some slight, seemingly minor, adjustments of the assumptions may have some major consequences.
The authors discussed the general conditions leading to changes in residency times or movement rates. Yet, it is worth pointing out again that it would be a mistake to blindly consider these theoretical results as forecasts for the foragers' behaviour in natura. OFT models has for a long time been criticized for sweeping under the carpet the key questions of the evolutionary dynamics and the maintenance of the optimal strategy in a population [9,10]. The distribution of available options is susceptible to change rapidly due to modifications of the environmental conditions or, even more simply, the presence of competitors which continuously remove the best options from the pool of available options [11]. The key point here is that the constant monitoring of available options implies cognitive (neural tissue is one of the most metabolically expensive tissues) and ecological costs: assessment and adjustment to the environmental conditions requires time, energy, and occasional mistakes (cost of naiveté, [12]). While rarely considered in optimal analyses, these costs should severely constraint the evolution of the subtle decision rules. Under rapidly fluctuating conditions, it could be more profitable to maintain a sub-optimal strategy (but performing reasonably well on the long run) than paying the far from negligible costs implied by the pursuit of optimal strategies [13,14]. For instance, in the analysis presented in this preprint, it is striking how close the fitness gains of the plastic and the non-plastic forager are, particularly if one remembers that the last-mentioned cognitive and ecological costs have been neglected in these calculations.
Yet, even if one can arguably question its descriptive value, such models are worth more than a cursory glance. They still have normative value insofar that they provide upper bounds for the response to modifications of the environmental conditions. Such insights are precious to design future experiments on the question. Being able to compare experimentally measured behaviours with the extremes of the null model (stubborn non-plastic forager) and the optimal strategy (only achievable by an omniscient daemon) informs about the cognitive bias or ecological costs experienced by real life foragers. I thus consider that this model, and more generally most OFT models, are still a valuable framework which deserves further examination.

References

[1] Fawcett, T. W. & Higginson, A. D. 2012 Heavy use of equations impedes communication among biologists. Proc. Natl. Acad. Sci. 109, 11735–11739. doi: 10.1073/pnas.1205259109
[2] Owens, I. P. F. 2006 Where is behavioural ecology going? Trends Ecol. Evol. 21, 356–361. doi: 10.1016/j.tree.2006.03.014
[3] Louâpre, P., Fauvergue, X., van Baaren, J. & Martel, V. 2015 The male mate search: an optimal foraging issue? Curr. Opin. Insect Sci. 9, 91–95. doi: 10.1016/j.cois.2015.02.012
[4] Calcagno, V., Hamelin, F., Mailleret, L., & Grognard, F. (2018). How optimal foragers should respond to habitat changes? On the consequences of habitat conversion. bioRxiv, 273557, ver. 4 peer-reviewed and recommended by PCI Ecol. doi: 10.1101/273557
[5] Calcagno, V., Grognard, F., Hamelin, F. M., Wajnberg, É. & Mailleret, L. 2014 The functional response predicts the effect of resource distribution on the optimal movement rate of consumers. Ecol. Lett. 17, 1570–1579. doi: 10.1111/ele.12379
[6] Calcagno, V., Mailleret, L., Wajnberg, É. & Grognard, F. 2013 How optimal foragers should respond to habitat changes: a reanalysis of the Marginal Value Theorem. J. Math. Biol. 69, 1237–1265. doi: 10.1007/s00285-013-0734-y
[7] Galipaud, M., Bollache, L., Wattier, R., Dechaume-Moncharmont, F.-X. & Lagrue, C. 2015 Overestimation of the strength of size-assortative pairing in taxa with cryptic diversity: a case of Simpson's paradox. Anim. Behav. 102, 217–221. doi: 10.1016/j.anbehav.2015.01.032
[8] Kievit, R. A., Frankenhuis, W. E., Waldorp, L. J. & Borsboom, D. 2013 Simpson's paradox in psychological science: a practical guide. Front. Psychol. 4, 513. doi: 10.3389/fpsyg.2013.00513
[9] Bolduc, J.-S. & Cézilly, F. 2012 Optimality modelling in the real world. Biol. Philos. 27, 851–869. doi: 10.1007/s10539-012-9333-3
[10] Pierce, G. J. & Ollason, J. G. 1987 Eight reasons why optimal foraging theory is a complete waste of time. Oikos 49, 111–118. doi: 10.2307/3565560
[11] Dechaume-Moncharmont, F.-X., Brom, T. & Cézilly, F. 2016 Opportunity costs resulting from scramble competition within the choosy sex severely impair mate choosiness. Anim. Behav. 114, 249–260. doi: 10.1016/j.anbehav.2016.02.019
[12] Snell-Rood, E. C. 2013 An overview of the evolutionary causes and consequences of behavioural plasticity. Anim. Behav. 85, 1004–1011. doi: 10.1016/j.anbehav.2012.12.031
[13] Fawcett, T. W., Fallenstein, B., Higginson, A. D., Houston, A. I., Mallpress, D. E. W., Trimmer, P. C. & McNamara, J. M. 2014 The evolution of decision rules in complex environments. Trends Cogn. Sci. 18, 153–161. doi: 10.1016/j.tics.2013.12.012
[14] Marshall, J. A. R., Trimmer, P. C., Houston, A. I. & McNamara, J. M. 2013 On evolutionary explanations of cognitive biases. Trends Ecol. Evol. 28, 469-473. doi: 10.1016/j.tree.2013.05.013

How optimal foragers should respond to habitat changes? On the consequences of habitat conversion.Vincent Calcagno, Frederic Hamelin, Ludovic Mailleret, Frederic GrognardThe Marginal Value Theorem (MVT) provides a framework to predict how habitat modifications related to the distribution of resources over patches should impact the realized fitness of individuals and their optimal rate of movement (or patch residen...Behaviour & Ethology, Dispersal & Migration, Foraging, Landscape ecology, Spatial ecology, Metacommunities & Metapopulations, Theoretical ecologyFrancois-Xavier Dechaume-Moncharmont2018-03-05 10:42:11 View
01 Feb 2020
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Evidence of tool use in a seabird?

Touchy matter: the delicate balance between Morgan’s canon and open-minded description of advanced cognitive skills in the animal

Recommended by ORCID_LOGO based on reviews by Valérie Dufour and Alex Taylor

In a recent paper published in PNAS, Fayet et al. [1] reported scarce field observations of two Atlantic puffins (four years apart) apparently scratching their bodies using sticks, which was interpreted by the authors as evidence of tool use in this species. In a short response, Benjamin Farrar [2] raises serious concerns about this interpretation and proposes simpler, more parsimonious, mechanisms explaining the observed behaviour: a textbook case of Morgan's canon.
In virtually all introductory lectures on animal behaviour, students are advised to exercise caution when interpreting empirical data and weighting alternative explanations. We are sometimes prisoner of our assumptions: our desire of beliefs in advanced cognitive skills in non-human species make us more receptive to facts confirming our preconceptions than to simpler, less exciting, interpretations (a phenomenon known as "confirmation bias" in psychology). We must resist the temptation to accept appealing explanations without enough critical thinking. Our students are thus taught to apply the Lloyd Morgan's canon, a variant of one of the most important heuristics in Science, the principle of parsimony or Occam's razor, rephrased by Morgan [3, page 53] in the context of animal behaviour: "In no case may we interpret an action as the outcome of a higher psychical faculty, if it can be interpreted as the outcome of the exercise of one that stands lower in the psychological scale". In absence of evidence to the contrary, one should postulate the simplest cognitive skill consistent with the observed behaviour. While sometimes criticized from an epistemological point of view [4-6], it remains an essential and largely accepted framework of animal cognition. It has repeatedly proved to be a useful guide in the minefield of comparative psychology. Classical ethology questions related to the existence of, for instance, meta-cognition [7], intentionality or problem solving [8] have been convincingly investigated using this principle.
Yet, there is a downside to this conservative approach. Blind reference to Morgan's canon may narrow our theoretical thinking about animal cognition [7,9]. It could be counter-productive to systematically deny advanced cognitive skills in animals. On the contrary, keeping our mind open to unplanned observations, unexpected discoveries, or serendipity [10], and being prepared to accept new hypotheses, sometimes fairly remote from the dominant paradigm, may be a fruitful research strategy. To quote Darwin's famous letter to Alfred Wallace: "I am a firm believer, that without speculation there is no good and original observation" [11]. Brief notes in specialized scientific journals, or even in grey literature (by enthusiast amateur ornithologists, ichthyologists, or entomologists), constitutes a rich array of anecdotal observations. For instance, Sol et al. [12] convincingly compared the innovation propensity across bird species by screening ornithology literature using keywords like 'never reported', 'not seen before', 'first report', 'unusual' or 'novel'. Even if "the plural of anecdote is not data" as the saying goes, such descriptions of novel behaviours, even single-subject observations, are indisputably precious: taxonomic ubiquity of a behaviour is a powerful argument in favour of evolutionary convergence. Of course, a race to the bottom, amplified by the inevitable media hypes around scientific articles questioning human exceptionalism, is another possible scientific trap for behavioural biologists in search of skills characteristic of so-called advanced species, but never described so far in supposedly cognitively simpler organisms. As stated by Franz de Waal [9]: "I have nothing against anecdotes, especially if they have been caught on camera or come from reputable observers who know their animals; but I do view them as a starting point of research, never an end point".
In the case of the two video observations of puffins apparently using sticks as scratching tool, it must be considered as a mere anecdote unless scientists systematically investigate this behaviour. In his constructive criticism of Fayet et al.'s paper, Benjamin Farrar [2] proposes interesting directions of research and testable predictions. A correlation between the background rate of stick picking and the rate of stick preening would indicate that this behaviour was more likely explained by fluke than genuine innovation in this species.

References

[1] Fayet, A. L., Hansen, E. S., and Biro, D. (2020). Evidence of tool use in a seabird. Proceedings of the National Academy of Sciences, 117(3), 1277–1279. doi: 10.1073/pnas.1918060117
[2] Farrar, B. G. (2020). Evidence of tool use in a seabird? PsyArXiv, 463hk, ver. 5 recommended and peer-reviewed by Peer Community In Ecology. doi: 10.31234/osf.io/463hk
[3] Morgan, C. L. (1894). An introduction to comparative psychology. London, UK: Walter Scott, Ltd. Retrieved from https://archive.org/details/introductiontoco00morg/page/53/mode/2up
[4] Meketa, I. (2014). A critique of the principle of cognitive simplicity in comparative cognition. Biology and Philosophy, 29(5), 731–745. doi: 10.1007/s10539-014-9429-z
[5] Fitzpatrick, S. (2017). Against Morgan's Canon. In K. Andrews and J. Beck (Eds.), The Routledge handbook of philosophy of animal minds (pp. 437–447). London, UK: Routledge, Taylor and Francis Group. doi: 10.4324/9781315742250.ch42
[6] Starzak, T. (2017). Interpretations without justification: a general argument against Morgan's Canon. Synthese, 194(5), 1681–1701. doi: 10.1007/s11229-016-1013-4
[7] Arbilly, M., and Lotem, A. (2017). Constructive anthropomorphism: a functional evolutionary approach to the study of human-like cognitive mechanisms in animals. Proceedings of the Royal Society B: Biological Sciences, 284(1865), 20171616. doi: 10.1098/rspb.2017.1616
[8] Taylor, A. H., Knaebe, B., and Gray, R. D. (2012). An end to insight? New Caledonian crows can spontaneously solve problems without planning their actions. Proceedings of the Royal Society B: Biological Sciences, 279(1749), 4977–4981. doi: 10.1098/rspb.2012.1998
[9] de Waal, F. (2016). Are we smart enough to know how smart animals are? New-York, USA: W. W. Norton and Company.
[10] Scheffer, M. (2014). The forgotten half of scientific thinking. Proceedings of the National Academy of Sciences, 111(17), 6119–6119. doi: 10.1073/pnas.1404649111
[11] Darwin, C. R. (1857). Letter to A. R. Wallace, 22 December 1857. Retrieved 30 January 2020, from https://www.darwinproject.ac.uk/letter/DCP-LETT-2192.xml
[12] Sol, D., Lefebvre, L., and Rodríguez-Teijeiro, J. D. (2005). Brain size, innovative propensity and migratory behaviour in temperate Palaearctic birds. Proceedings of the Royal Society B: Biological Sciences, 272(1571), 1433–1441. doi: 10.1098/rspb.2005.3099

Evidence of tool use in a seabird?Benjamin G. FarrarFayet, Hansen and Biro (1) provide two observations of Atlantic puffins, *Fratercula arctica*, performing self-directed actions while holding a stick in their beaks. The authors interpret this as evidence of tool use as they suggest that the stick...Behaviour & EthologyFrancois-Xavier Dechaume-Moncharmont2020-01-22 11:55:27 View
28 Sep 2020
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The dynamics of spawning acts by a semelparous fish and its associated energetic costs

Extreme weight loss: when accelerometer could reveal reproductive investment in a semelparous fish species

Recommended by ORCID_LOGO based on reviews by Aidan Jonathan Mark Hewison, Loïc Teulier and 1 anonymous reviewer

Continuous observation of animal behaviour could be quite a challenge in the field, and the situation becomes even more complicated with aquatic species mostly active at night. In such cases, biologging techniques are real game changers in ecology, behavioural ecology or eco-physiology. An accelerating number of methodological applications of these tools in natural condition are thus published each year [1]. Biologging is not limited to movement ecology. For instance, fine grain information about energy expenditure can be inferred from body acceleration [2], and accelerometers has already proven useful in monitoring reproductive costs in some fish species [3,4]. The first part of the study by Tentelier et al. [5] is in line with this growing literature. It describes measurements of energy expenditure during reproduction in a fish species, Allis shad (Alosa Alosa), based on tail beat frequency and occurrence of spawning acts. The study has been convincingly conducted, and the results are important for fish biologists. But this is not the whole story: the authors added to this otherwise classical study a very original and insightful analysis which deserves closer interest.
Tentelier et al. propose to use static accelerometer to monitor change in body roundness through the reproductive season. These semelparous fish first mature and built up reserves in the Atlantic Ocean and migrate into fresh water to reproduce. Contrary to iteroparous species, female shads do not have to strategically preserve energy for future reproduction. The females die few days after spawning having exhausted their energetic reserves: they typically lose almost half of their body mass during the spawning season. The beautiful idea in this study was to track down information about this dramatic slimming in the accelerometer data. Indeed, the accelerometer was attached on the side of the fish (close to the dorsal fin). A change in its angle with the vertical plane could be correlated with the change in roundness, the angle declining with the female thinning. Accelerometers have already been used to record body posture [6] but, in the present study, the novelty was to monitor the change in body shape.
Unfortunately, the data by Tentelier et al. are inconclusive so far. Broadly speaking, the accelerometer angle recorded declined through the spawning season, indicating an average slimming of the females, but there was no correlation between the change in angle and the mass loss at the individual level. This was partly due to the fact that the dorsal position of the accelerometer was not optimized to measures egg laying whose effects are mostly observable on ventral side.
Yet, this nice idea deserves more scrutiny. The method seems to be sensitive enough to detect inflation of swim bladder, the gas-filled organ helping the fish to control their position in the water column, as the accelerometer angle increased when the fish stayed close to the water surface. Additional works and proper calibration are certainly needed to validate the use of accelerometer angle as a proxy for body roundness. The actual data were not strong enough to justify a standalone publication on the subject, but it would have been shame to lose traces of such analysis and keep it in the file drawer. This is why I strongly support its report as a side question in a broader study. Science progresses not only with neat conclusive studies but also when unexpected (apparently anecdotal) observations stimulate new researches.

References

[1] Börger L, Bijleveld AI, Fayet AL, Machovsky‐Capuska GE, Patrick SC, Street GM and Vander Wal E. (2020) Biologging special feature. J. Anim. Ecol. 89, 6–15. 10.1111/1365-2656.13163
[2] Wilson RP et al. (2020) Estimates for energy expenditure in free‐living animals using acceleration proxies: A reappraisal. J. Anim. Ecol. 89, 161–172. 10.1111/1365-2656.13040
[3] Tsuda Y, Kawabe R, Tanaka H, Mitsunaga Y, Hiraishi T, Yamamoto K and Nashimoto K. (2006) Monitoring the spawning behaviour of chum salmon with an acceleration data logger. Ecol. Freshw. Fish 15, 264–274. 10.1111/j.1600-0633.2006.00147.x
[4] Sakaji H, Hamada K, Naito Y. 2018 Identifying spawning events of greater amberjack using accelerometers. Mar. Biol. Res. 14, 637–641. 10.1080/17451000.2018.1492140
[5] Tentelier C, Bouchard C, Bernardin A, Tauzin A, Aymes J-C, Lange F, Récapet C, Rives J (2020) The dynamics of spawning acts by a semelparous fish and its associated energetic costs. bioRxiv, 436295. doi: 10.1101/436295 ver. 7 peer-reviewed and recommended by PCI Ecology. 10.1101/436295
[6] Brown DD, Kays R, Wikelski M, Wilson R, Klimley AP. 2013 Observing the unwatchable through acceleration logging of animal behavior. Anim. Biotelemetry 1, 20. 10.1186/2050-3385-1-20

The dynamics of spawning acts by a semelparous fish and its associated energetic costsCédric Tentelier, Colin Bouchard, Anaïs Bernardin, Amandine Tauzin, Jean-Christophe Aymes, Frédéric Lange, Charlotte Recapet, Jacques Rives<p>1. During the reproductive season, animals have to manage both their energetic budget and gamete stock. In particular, for semelparous capital breeders with determinate fecundity and no parental care other than gametic investment, the depletion...Behaviour & Ethology, Freshwater ecology, Life historyFrancois-Xavier Dechaume-Moncharmont2020-06-04 15:18:56 View