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04 Apr 2023
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Data stochasticity and model parametrisation impact the performance of species distribution models: insights from a simulation study

Species Distribution Models: the delicate balance between signal and noise

Recommended by based on reviews by Alejandra Zarzo Arias and 1 anonymous reviewer

Species Distribution Models (SDMs) are one of the most commonly used tools to predict where species are, where they may be in the future, and, at times, what are the variables driving this prediction. As such, applying an SDM to a dataset is akin to making a bet: that the known occurrence data are informative, that the resolution of predictors is adequate vis-à-vis the scale at which their impact is expressed, and that the model will adequately capture the shape of the relationships between predictors and predicted occurrence.

In this contribution, Lambert & Virgili (2023) perform a comprehensive assessment of different sources of complications to this process, using replicated simulations of two synthetic species. Their experimental process is interesting, in that both the data generation and the data analysis stick very close to what would happen in "real life". The use of synthetic species is particularly relevant to the assessment of SDM robustness, as they enable the design of species for which the shape of the relationship is given: in short, we know what the model should capture, and can evaluate the model performance against a ground truth that lacks uncertainty.

Any simulation study is limited by the assumptions established by the investigators; when it comes to spatial data, the "shape" of the landscape, both in terms of auto-correlation and in where the predictors are available. Lambert & Virgili (2023) nicely circumvent these issues by simulating synthetic species against the empirical distribution of predictors; in other words, the species are synthetic, but the environment for which the prediction is made is real. This is an important step forward when compared to the use of e.g. neutral landscapes (With 1997), which can have statistical properties that are not representative of natural landscapes (see e.g. Halley et al., 2004).

A striking point in the study by Lambert & Virgili (2023) is that they reveal a deep, indeed deeper than expected, stochasticity in SDMs; whether this is true in all models remains an open question, but does not invalidate their recommendation to the community: the interpretation of outcomes is a delicate exercise, especially because measures that inform on the goodness of the model fit do not capture the predictive quality of the model outputs. This preprint is both a call to more caution, and a call to more curiosity about the complex behavior of SDMs, while also providing a sensible template to perform future analyses of the potential issues with predictive models.


References

Halley, J. M., et al. (2004) “Uses and Abuses of Fractal Methodology in Ecology: Fractal Methodology in Ecology.” Ecology Letters, vol. 7, no. 3, pp. 254–71. https://doi.org/10.1111/j.1461-0248.2004.00568.x.

Lambert, Charlotte, and Auriane Virgili (2023). Data Stochasticity and Model Parametrisation Impact the Performance of Species Distribution Models: Insights from a Simulation Study. bioRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2023.01.17.524386

With, Kimberly A. (1997) “The Application of Neutral Landscape Models in Conservation Biology. Aplicacion de Modelos de Paisaje Neutros En La Biologia de La Conservacion.” Conservation Biology, vol. 11, no. 5, pp. 1069–80. https://doi.org/10.1046/j.1523-1739.1997.96210.x.

Data stochasticity and model parametrisation impact the performance of species distribution models: insights from a simulation studyCharlotte Lambert, Auriane Virgili<p>Species distribution models (SDM) are widely used to describe and explain how species relate to their environment, and predict their spatial distributions. As such, they are the cornerstone of most of spatial planning efforts worldwide. SDM can...Biogeography, Habitat selection, Macroecology, Marine ecology, Spatial ecology, Metacommunities & Metapopulations, Species distributions, Statistical ecologyTimothée Poisot2023-01-20 09:43:51 View
13 May 2023
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Symbiotic nutrient cycling enables the long-term survival of Aiptasia in the absence of heterotrophic food sources

Constraining the importance of heterotrophic vs autotrophic feeding in photosymbiotic cnidarians

Recommended by based on reviews by 2 anonymous reviewers

The symbiosis with autotrophic dinoflagellate algae has enabled heterotrophic Cnidaria to thrive in nutrient-poor tropical waters (Muscatine and Porter 1977; Stanley 2006). In particular, mixotrophy, i.e. the ability to acquire nutrients through both autotrophy and heterotrophy, confers a competitive edge in oligotrophic waters, allowing photosymbiotic Cnidaria to outcompete benthic organisms limited to a single diet (e.g., McCook 2001). However, the relative importance of autotrophy vs heterotrophy in sustaining symbiotic cnidarian’s nutrition is still the subject of intense research. In fact, figuring out the cellular mechanisms by which symbiotic Cnidaria acquire a balanced diet for their metabolism and growth is relevant to our understanding of their physiology under varying environmental conditions and in response to anthropogenic perturbations.

In this study's long-term starvation experiment, Radecker & Meibom (2023) investigated the survival of the photosymbiotic sea anemone Aiptasia in the absence of heterotrophic feeding. After one year of heterotrophic starvation, Apitasia anemones remained fully viable but showed an 85 % reduction in biomass. Using 13C-bicarbonate and 15N-ammonium labeling, electron microscopy and NanoSIMS imaging, the authors could clearly show that the contribution of algal-derived nutrients to the host metabolism remained unaffected as a result of increased algal photosynthesis and more efficient carbon translocation. At the same time, the absence of heterotrophic feeding caused severe nitrogen limitation in the starved Apitasia anemones.

Overall, this study provides valuable insights into nutrient exchange within the symbiosis between Cnidaria and dinoflagellate algae at the cellular level and sheds new light on the importance of heterotrophic feeding as a nitrogen acquisition strategy for holobiont growth in oligotrophic waters.

REFERENCES

McCook L (2001) Competition between corals and algal turfs along a gradient of terrestrial influence in the nearshore central Great Barrier Reef. Coral Reefs 19:419–425. https://doi.org/10.1007/s003380000119

Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460. https://doi.org/10.2307/1297526

Radecker N, Meibom A (2023) Symbiotic nutrient cycling enables the long-term survival of Aiptasia in the absence of heterotrophic food sources. bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.12.07.519152

Stanley GD Jr (2006) Photosymbiosis and the evolution of modern coral reefs. Science 312:857–858. https://doi.org/10.1126/science.1123701

Symbiotic nutrient cycling enables the long-term survival of Aiptasia in the absence of heterotrophic food sourcesNils Radecker, Anders Meibom<p style="text-align: justify;">Phototrophic Cnidaria are mixotrophic organisms that can complement their heterotrophic diet with nutrients assimilated by their algal endosymbionts. Metabolic models suggest that the translocation of photosynthates...Eco-evolutionary dynamics, Microbial ecology & microbiology, SymbiosisUlisse Cardini2022-12-12 10:50:55 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
24 Mar 2023
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Rapid literature mapping on the recent use of machine learning for wildlife imagery

Review of machine learning uses for the analysis of images on wildlife

Recommended by based on reviews by Falk Huettmann and 1 anonymous reviewer

In the field of ecology, there is a growing interest in machine (including deep) learning for processing and automatizing repetitive analyses on large amounts of images collected from camera traps, drones and smartphones, among others. These analyses include species or individual recognition and classification, counting or tracking individuals, detecting and classifying behavior. By saving countless times of manual work and tapping into massive amounts of data that keep accumulating with technological advances, machine learning is becoming an essential tool for ecologists. We refer to recent papers for more details on machine learning for ecology and evolution (Besson et al. 2022, Borowiec et al. 2022, Christin et al. 2019, Goodwin et al. 2022, Lamba et al. 2019, Nazir & Kaleem 2021, Perry et al. 2022, Picher & Hartig 2023, Tuia et al. 2022, Wäldchen & Mäder 2018).

In their paper, Nakagawa et al. (2023) conducted a systematic review of the literature on machine learning for wildlife imagery. Interestingly, the authors used a method unfamiliar to ecologists but well-established in medicine called rapid review, which has the advantage of being quickly completed compared to a fully comprehensive systematic review while being representative (Lagisz et al., 2022). Through a rigorous examination of more than 200 articles, the authors identified trends and gaps, and provided suggestions for future work. Listing all their findings would be counterproductive (you’d better read the paper), and I will focus on a few results that I have found striking, fully assuming a biased reading of the paper. First, Nakagawa et al. (2023) found that most articles used neural networks to analyze images, in general through collaboration with computer scientists. A challenge here is probably to think of teaching computer vision to the generations of ecologists to come (Cole et al. 2023). Second, the images were dominantly collected from camera traps, with an increase in the use of aerial images from drones/aircrafts that raise specific challenges. Third, the species concerned were mostly mammals and birds, suggesting that future applications should aim to mitigate this taxonomic bias, by including, e.g., invertebrate species. Fourth, most papers were written by authors affiliated with three countries (Australia, China, and the USA) while India and African countries provided lots of images, likely an example of scientific colonialism which should be tackled by e.g., capacity building and the involvement of local collaborators. Last, few studies shared their code and data, which obviously impedes reproducibility. Hopefully, with the journals’ policy of mandatory sharing of codes and data, this trend will be reversed. 

REFERENCES

Besson M, Alison J, Bjerge K, Gorochowski TE, Høye TT, Jucker T, Mann HMR, Clements CF (2022) Towards the fully automated monitoring of ecological communities. Ecology Letters, 25, 2753–2775. https://doi.org/10.1111/ele.14123

Borowiec ML, Dikow RB, Frandsen PB, McKeeken A, Valentini G, White AE (2022) Deep learning as a tool for ecology and evolution. Methods in Ecology and Evolution, 13, 1640–1660. https://doi.org/10.1111/2041-210X.13901

Christin S, Hervet É, Lecomte N (2019) Applications for deep learning in ecology. Methods in Ecology and Evolution, 10, 1632–1644. https://doi.org/10.1111/2041-210X.13256

Cole E, Stathatos S, Lütjens B, Sharma T, Kay J, Parham J, Kellenberger B, Beery S (2023) Teaching Computer Vision for Ecology. https://doi.org/10.48550/arXiv.2301.02211

Goodwin M, Halvorsen KT, Jiao L, Knausgård KM, Martin AH, Moyano M, Oomen RA, Rasmussen JH, Sørdalen TK, Thorbjørnsen SH (2022) Unlocking the potential of deep learning for marine ecology: overview, applications, and outlook†. ICES Journal of Marine Science, 79, 319–336. https://doi.org/10.1093/icesjms/fsab255

Lagisz M, Vasilakopoulou K, Bridge C, Santamouris M, Nakagawa S (2022) Rapid systematic reviews for synthesizing research on built environment. Environmental Development, 43, 100730. https://doi.org/10.1016/j.envdev.2022.100730

Lamba A, Cassey P, Segaran RR, Koh LP (2019) Deep learning for environmental conservation. Current Biology, 29, R977–R982. https://doi.org/10.1016/j.cub.2019.08.016

Nakagawa S, Lagisz M, Francis R, Tam J, Li X, Elphinstone A, Jordan N, O’Brien J, Pitcher B, Sluys MV, Sowmya A, Kingsford R (2023) Rapid literature mapping on the recent use of machine learning for wildlife imagery. EcoEvoRxiv, ver. 4 peer-reviewed and recommended by Peer Community in Ecology.  https://doi.org/10.32942/X2H59D

Nazir S, Kaleem M (2021) Advances in image acquisition and processing technologies transforming animal ecological studies. Ecological Informatics, 61, 101212. https://doi.org/10.1016/j.ecoinf.2021.101212

Perry GLW, Seidl R, Bellvé AM, Rammer W (2022) An Outlook for Deep Learning in Ecosystem Science. Ecosystems, 25, 1700–1718. https://doi.org/10.1007/s10021-022-00789-y

Pichler M, Hartig F Machine learning and deep learning—A review for ecologists. Methods in Ecology and Evolution, n/a. https://doi.org/10.1111/2041-210X.14061

Tuia D, Kellenberger B, Beery S, Costelloe BR, Zuffi S, Risse B, Mathis A, Mathis MW, van Langevelde F, Burghardt T, Kays R, Klinck H, Wikelski M, Couzin ID, van Horn G, Crofoot MC, Stewart CV, Berger-Wolf T (2022) Perspectives in machine learning for wildlife conservation. Nature Communications, 13, 792. https://doi.org/10.1038/s41467-022-27980-y

Wäldchen J, Mäder P (2018) Machine learning for image-based species identification. Methods in Ecology and Evolution, 9, 2216–2225. https://doi.org/10.1111/2041-210X.13075

Rapid literature mapping on the recent use of machine learning for wildlife imageryShinichi Nakagawa, Malgorzata Lagisz, Roxane Francis, Jessica Tam, Xun Li, Andrew Elphinstone, Neil R. Jordan, Justine K. O’Brien, Benjamin J. Pitcher, Monique Van Sluys, Arcot Sowmya, Richard T. Kingsford<p>1. Machine (especially deep) learning algorithms are changing the way wildlife imagery is processed. They dramatically speed up the time to detect, count, classify animals and their behaviours. Yet, we currently have a very few systematic liter...Behaviour & Ethology, Conservation biologyOlivier GimenezAnonymous2022-10-31 22:05:46 View
27 Jan 2023
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Spatial heterogeneity of interaction strength has contrasting effects on synchrony and stability in trophic metacommunities

How does spatial heterogeneity affect stability of trophic metacommunities?

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

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

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

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

References

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

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

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

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

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

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

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

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

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

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

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

Spatial heterogeneity of interaction strength has contrasting effects on synchrony and stability in trophic metacommunitiesPierre Quévreux, Bart Haegeman and Michel Loreau<p>&nbsp;Spatial heterogeneity is a fundamental feature of ecosystems, and ecologists have identified it as a factor promoting the stability of population dynamics. In particular, differences in interaction strengths and resource supply between pa...Dispersal & Migration, Food webs, Interaction networks, Spatial ecology, Metacommunities & Metapopulations, Theoretical ecologyWerner Ulrich2022-10-26 13:38:34 View
28 Dec 2022
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Deleterious effects of thermal and water stresses on life history and physiology: a case study on woodlouse

An experimental approach for understanding how terrestrial isopods respond to environmental stressors

Recommended by based on reviews by Aaron Yilmaz and Michael Morris

​​In this article, the authors discuss the results of their study investigating the effects of heat stress and moisture stress on a terrestrial isopod Armadilldium vulgare, the common woodlouse [1]. Specifically, the authors have assessed how increased temperature or decreased moisture affects life history traits (such as growth, survival, and reproduction) as well as physiological traits (immune cell parameters and \( beta \)-galactosidase activity). This article quantitatively evaluates the effects of the two stressors on woodlouse. Terrestrial isopods like woodlouse are sensitive to thermal and moisture stress [2; 3] and are therefore good models to test hypotheses in global change biology and for monitoring ecosystem health.

​An important feature of this study is the combination of experimental, laboratory, and analytical techniques. Experiments were conducted under controlled conditions in the laboratory by modulating temperature and moisture, life history and physiological traits were measured/analyzed and then tested using models. Both stressors had negative impacts on survival and reproduction of woodlouse, and result in premature ageing. Although thermal stress did not affect survival, it slowed woodlouse growth. Moisture stress did not have a detectable effect on woodlouse growth but decreased survival and reproductive success. An important insight from this study is that effects of heat and moisture stressors on woodlouse are not necessarily linear, and experimental approaches can be used to better elucidate the mechanisms and understand how these organisms respond to environmental stress.

​This article is timely given the increasing attention on biological monitoring and ecosystem health.​

References:

[1] Depeux C, Branger A, Moulignier T, Moreau J, Lemaître J-F, Dechaume-Moncharmont F-X, Laverre T, Pauhlac H, Gaillard J-M, Beltran-Bech S (2022) Deleterious effects of thermal and water stresses on life history and physiology: a case study on woodlouse. bioRxiv, 2022.09.26.509512., ver. 3 peer-reviewd and recommended by PCI Ecology. https://doi.org/10.1101/2022.09.26.509512

[2] ​Warburg MR, Linsenmair KE, Bercovitz K (1984) The effect of climate on the distribution and abundance of isopods. In: Sutton SL, Holdich DM, editors. The Biology of Terrestrial Isopods. Oxford: Clarendon Press. pp. 339–367.​

[3] Hassall M, Helden A, Goldson A, Grant A (2005) Ecotypic differentiation and phenotypic plasticity in reproductive traits of Armadillidium vulgare (Isopoda: Oniscidea). Oecologia 143: 51–60.​ https://doi.org/10.1007/s00442-004-1772-3

Deleterious effects of thermal and water stresses on life history and physiology: a case study on woodlouseCharlotte Depeux, Angele Branger, Theo Moulignier, Jérôme Moreau, Jean-Francois Lemaitre, Francois-Xavier Dechaume-Moncharmont, Tiffany Laverre, Hélène Paulhac, Jean-Michel Gaillard, Sophie Beltran-Bech<p>We tested independently the influences of increasing temperature and decreasing moisture on life history and physiological traits in the arthropod <em>Armadillidium vulgare</em>. Both increasing temperature and decreasing moisture led individua...Biodiversity, Evolutionary ecology, Experimental ecology, Life history, Physiology, Terrestrial ecology, ZoologyAniruddha Belsare2022-09-28 13:13:47 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
24 May 2023
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Evolutionary determinants of reproductive seasonality: a theoretical approach

When does seasonal reproduction evolve?

Recommended by based on reviews by Francois-Xavier Dechaume-Moncharmont, Nigel Yoccoz and 1 anonymous reviewer

Have you ever wondered why some species breed seasonally while others do not? You might think it is all down to lattitude and the harshness of winters but it turns out it is quite a bit more complicated than that. A consequence of this is that climate change may result in the evolution of the degree of seasonal reproduction, with some species perhaps becoming less seasonal and others more so even in the same habitat. 

Burtschell et al. (2023) investigated how various factors influence seasonal breeding by building an individual-based model of a baboon population from which they calculated the degree of seasonality for the fittest reproductive strategy. They then altered key aspects of their model to examine how these changes impacted the degree of seasonality in the reproductive strategy. What they found is fascinating. 

The degree of seasonality in reproductive strategy is expected to increase with increased seasonality in the environment, decreased food availability, increased energy expenditure, and how predictable resource availability is. Interestingly, neither female cycle length nor extrinsic infant mortality influenced the degree of seasonality in reproduction.

What this means in reality for seasonal species is more challenging to understand. Some environments appear to be becoming more seasonal yet less predictable, and some species appear to be altering their daily energy budgets in response to changing climate in quite complex ways. As with pretty much everything in biology, Burtschell et al.'s work reveals much nuance and complexity, and that predicting how species might alter their reproductive timing is fraught with challenges.

The paper is very well written. With a simpler model it may have proven possible to achieve analytical solutions, but this is a very minor gripe. The reviewers were positive about the paper, and I have little doubt it will be well-cited. 

REFERENCES

Burtschell L, Dezeure J, Huchard E, Godelle B (2023) Evolutionary determinants of reproductive seasonality: a theoretical approach. bioRxiv, 2022.08.22.504761, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.08.22.504761

Evolutionary determinants of reproductive seasonality: a theoretical approachLugdiwine Burtschell, Jules Dezeure, Elise Huchard, Bernard Godelle<p style="text-align: justify;">Reproductive seasonality is a major adaptation to seasonal cycles and varies substantially among organisms. This variation, which was long thought to reflect a simple latitudinal gradient, remains poorly understood ...Evolutionary ecology, Life history, Theoretical ecologyTim Coulson Nigel Yoccoz2022-08-23 21:37:28 View
24 Jan 2023
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Four decades of phenology in an alpine amphibian: trends, stasis, and climatic drivers

Alpine ecology and their dynamics under climate change

Recommended by based on reviews by Nigel Yoccoz and 1 anonymous reviewer

​​Research about the effects of climate change on ecological communities has been abundant in the last decades. In particular, studies about the effects of climate change on mountain ecosystems have been key for understanding and communicating the consequences of this global phenomenon. Alpine regions show higher increases in warming in comparison to low-altitude ecosystems and this trend is likely to continue. This warming has caused reduced snowfall and/or changes in the duration of snow cover. For example, Notarnicola (2020) reported that 78% of the world’s mountain areas have experienced a snow cover decline since 2000. In the same vein, snow cover has decreased by 10% compared with snow coverage in the late 1960s (Walther et al., 2002) and snow cover duration has decreased at a rate of 5 days/decade (Choi et al., 2010). These changes have impacted the dynamics of high-altitude plant and animal populations. Some impacts are changes in the hibernation of animals, the length of the growing season for plants and the soil microbial composition (Chávez et al. 2021).

Lenzi et al. (2023), give us an excellent study using long-term data on alpine amphibian populations. Authors show how climate change has impacted the reproductive phenology of Bufo bufo, especially the breeding season starts 30 days earlier than ~40 years ago. This earlier breeding is associated with the increasing temperatures and reduced snow cover in these alpine ecosystems. However, these changes did not occur in a linear trend but a marked acceleration was observed until mid-1990s with a later stabilization. Authors associated these nonlinear changes with complex interactions between the global trend of seasonal temperatures and site-specific conditions. 

Beyond the earlier breeding season, changes in phenology can have important impacts on the long-term viability of alpine populations. Complex interactions could involve positive and negative effects like harder environmental conditions for propagules, faster development of juveniles, or changes in predation pressure. This study opens new research opportunities and questions like the urgent assessment of the global impact of climate change on animal fitness. This study provides key information for the conservation of these populations.

References

Chávez RO, Briceño VF, Lastra JA, Harris-Pascal D, Estay SA (2021) Snow Cover and Snow Persistence Changes in the Mocho-Choshuenco Volcano (Southern Chile) Derived From 35 Years of Landsat Satellite Images. Frontiers in Ecology and Evolution, 9. https://doi.org/10.3389/fevo.2021.643850

Choi G, Robinson DA, Kang S (2010) Changing Northern Hemisphere Snow Seasons. Journal of Climate, 23, 5305–5310. https://doi.org/10.1175/2010JCLI3644.1

Lenzi O, Grossenbacher K, Zumbach S, Lüscher B, Althaus S, Schmocker D, Recher H, Thoma M, Ozgul A, Schmidt BR (2022) Four decades of phenology in an alpine amphibian: trends, stasis, and climatic drivers.bioRxiv, 2022.08.16.503739, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.08.16.503739

Notarnicola C (2020) Hotspots of snow cover changes in global mountain regions over 2000–2018. Remote Sensing of Environment, 243, 111781. https://doi.org/10.1016/j.rse.2020.111781

Four decades of phenology in an alpine amphibian: trends, stasis, and climatic driversOmar Lenzi, Kurt Grossenbacher, Silvia Zumbach, Beatrice Luescher, Sarah Althaus, Daniela Schmocker, Helmut Recher, Marco Thoma, Arpat Ozgul, Benedikt R. Schmidt<p style="text-align: justify;">Strong phenological shifts in response to changes in climatic conditions have been reported for many species, including amphibians, which are expected to breed earlier. Phenological shifts in breeding are observed i...Climate change, Population ecology, ZoologySergio EstayAnonymous, Nigel Yoccoz2022-08-18 08:25:21 View
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Using repeatability of performance within and across contexts to validate measures of behavioral flexibility

Do reversal learning methods measure behavioral flexibility?

Recommended by based on reviews by Maxime Dahirel and Aparajitha Ramesh

Assessing the reliability of the methods we use in actually measuring the intended trait should be one of our first priorities when designing a study – especially when the trait in question is not directly observable and is measured through a proxy. 

This is the case for cognitive traits, which are often quantified through measures of behavioral performance. Behavioral flexibility is of particular interest in the context of great environmental changes that a lot of populations have to experiment. This type of behavioral performance is often measured through reversal learning experiments (Bond 2007). In these experiments, individuals first learn a preference, for example for an object of a certain type of form or color, associated with a reward such as food. The characteristics of the rewarded object then change, and the individuals hence have to learn these new characteristics (to get the reward). The time needed by the individual to make this change in preference has been considered a measure of behavioral flexibility.

Although reversal learning experiments have been widely used, their construct validity to assess behavioral flexibility has not been thoroughly tested. This was the aim of McCune and collaborators' (2023) study, through the test of the repeatability of individual performance within and across contexts of reversal learning, in the great-tailed grackle.

This manuscript presents a post-study of the preregistered study* (Logan et al. 2019) that was peer-reviewed and received an In Principle Recommendation for PCI Ecology (Coulon 2019; the initial preregistration was split into 3 post-studies).
Using 34 great-tailed grackles wild-caught in Tempe, Arizona (USA), the authors tested in aviaries 2 hypotheses:

  • First, that the behavioral flexibility measured by reversal learning is repeatable within individuals across sessions of the same experiment;
  • Second, that there is repeatability of the measured behavioral flexibility (within individuals) across different types of reversal learning experiments (context).

The first hypothesis was tested by measuring the repeatability of the time needed by individuals to switch color preference in a color reversal learning task (colored tubes), over serial sessions of this task. The second one was tested by measuring the time needed by individuals to switch solutions, within 3 different contexts: (1) colored tubes, (2) plastic and (3) wooden multi-access boxes involving several ways to access food.

Despite limited sample sizes, the results of these experiments suggest that there is both temporal and contextual repeatability of behavioral flexibility performance of great-tailed grackles, as measured by reversal learning experiments.

Those results are a first indication of the construct validity of reversal learning experiments to assess behavioral flexibility. As highlighted by McCune and collaborators, it is now necessary to assess the discriminant validity of these experiments, i.e. checking that a different performance is obtained with tasks (experiments) that are supposed to measure different cognitive abilities.
 
* A pre-registered study is a study in which context, aims, hypotheses and methodologies have been written down as an empirical paper, peer-reviewed and pre-accepted before research is undertaken. Pre-registrations are intended to reduce publication bias and reporting bias.
 
REFERENCES
 
Bond, A. B., Kamil, A. C., & Balda, R. P. (2007). Serial reversal learning and the evolution of behavioral
flexibility in three species of north american corvids (Gymnorhinus cyanocephalus, Nucifraga columbiana,
Aphelocoma californica). Journal of Comparative Psychology, 121 (4), 372. https://doi.org/10.1037/0735-7036.121.4.372

Coulon, A. (2019) Can context changes improve behavioral flexibility? Towards a better understanding of species adaptability to environmental changes. Peer Community in Ecology, 100019. https://doi.org/10.24072/pci.ecology.100019

Logan, CJ, Lukas D, Bergeron L, Folsom M, & McCune, K. (2019).  Is behavioral flexibility related to foraging and social behavior in a rapidly expanding species? In Principle Acceptance by PCI Ecology of the Version on 6 Aug 2019. http://corinalogan.com/Preregistrations/g_flexmanip.html

McCune KB, Blaisdell AP, Johnson-Ulrich Z, Lukas D, MacPherson M, Seitz BM, Sevchik A, Logan CJ (2023) Using repeatability of performance within and across contexts to validate measures of behavioral flexibility. EcoEvoRxiv, ver. 5 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.32942/X2R59K

Using repeatability of performance within and across contexts to validate measures of behavioral flexibilityMcCune KB, Blaisdell AP, Johnson-Ulrich Z, Lukas D, MacPherson M, Seitz BM, Sevchik A, Logan CJ<p style="text-align: justify;">Research into animal cognitive abilities is increasing quickly and often uses methods where behavioral performance on a task is assumed to represent variation in the underlying cognitive trait. However, because thes...Behaviour & Ethology, Evolutionary ecology, Preregistrations, ZoologyAurélie Coulon2022-08-15 20:56:42 View