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07 Oct 2024
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Guidance framework to apply best practices in ecological data analysis: Lessons learned from building Galaxy-Ecology

Best practices for ecological analysis are required to act on concrete challenges

Recommended by ORCID_LOGO based on reviews by Nick Isaac and 1 anonymous reviewer

A core challenge facing ecologists is to work through an ever-increasing amount of data. The accelerating decline in biodiversity worldwide, mounting pressure of anthropogenic impacts, and increasing demand for actionable indicators to guide effective policy means that monitoring will only intensify, and rely on tools that can generate even more information (Gonzalez et al., 2023). How, then, do we handle this new volume and diversity of data?

This is the question Royaux et al. (2024) are tackling with their contribution. By introducing both a conceptual ("How should we think about our work?") and an operational ("Here is a tool to do our work with") framework, they establish a series of best practices for the analysis of ecological data.

It is easy to think about best practices in ecological data analysis in its most proximal form: is it good statistical practice? Is the experimental design correct? These have formed the basis of many recommendations over the years (see e.g. Popovic et al., 2024, for a recent example). But the contribution of Royaux et al. focuses on a different part of the analysis pipeline: the computer science (and software engineering) aspect of it.

As data grows in volume and complexity, the code needed to handle it follows the same trend. It is not a surprise, therefore, to see that the demand for programming skills in ecologists has doubled recently (Feng et al., 2020), prompting calls to make computational literacy a core component of undergraduate education (Farrell & Carrey, 2018). But beyond training, an obvious way to make computational analysis ecological data more reliable and effective is to build better tools. This is precisely what Royaux et al. have achieved.

They illustrate their approach through their experience building Galaxy-Ecology, a computing environment for ecological analysis: by introducing a clear taxonomy of computing concepts (data exploration, pre-processing, analysis, representation), with a hierarchy between them (formatting, data correction, anonymization), they show that we can think about the pipeline going from data to results in a way that is more systematized, and therefore more prone to generalization.

We may buckle at the idea of yet another ontology, or yet another framework, for our work, but I am convinced that the work of Royaux et al. is precisely what our field needs. Because their levels of atomization (their term for the splitting of complex pipelines into small, single-purpose tasks) are easy to understand, and map naturally onto tasks that we already perform, it is likely to see wide adoption. Solving the big, existential challenges of monitoring and managing biodiversity at the global scale requires the adoption of good practices, and a tool like Galaxy-Ecology goes a long way towards this goal.

References

Farrell, K.J., and Carey, C.C. (2018). Power, pitfalls, and potential for integrating computational literacy into undergraduate ecology courses. Ecol. Evol. 8, 7744-7751.
https://doi.org/10.1002/ece3.4363

Feng, X., Qiao, H., and Enquist, B. (2020). Doubling demands in programming skills call for ecoinformatics education. Frontiers in Ecology and the Environment 18, 123-124.
https://doi.org/10.1002/fee.2179
 
Gonzalez, A., Vihervaara, P., Balvanera, P., Bates, A.E., Bayraktarov, E., Bellingham, P.J., Bruder, A., Campbell, J., Catchen, M.D., Cavender-Bares, J., et al. (2023). A global biodiversity observing system to unite monitoring and guide action. Nat. Ecol. Evol., 1-5. 
https://doi.org/10.1038/s41559-023-02171-0
 
Popovic, G., Mason, T.J., Drobniak, S.M., Marques, T.A., Potts, J., Joo, R., Altwegg, R., Burns, C.C.I., McCarthy, M.A., Johnston, A., et al. (2024). Four principles for improved statistical ecology. Methods Ecol. Evol. 15, 266-281.
https://doi.org/10.1111/2041-210X.14270
 
Coline Royaux, Jean-Baptiste Mihoub, Marie Jossé, Dominique Pelletier, Olivier Norvez, Yves Reecht, Anne Fouilloux, Helena Rasche, Saskia Hiltemann, Bérénice Batut, Marc Eléaume, Pauline Seguineau, Guillaume Massé, Alan Amossé, Claire Bissery, Romain Lorrilliere, Alexis Martin, Yves Bas, Thimothée Virgoulay, Valentin Chambon, Elie Arnaud, Elisa Michon, Clara Urfer, Eloïse Trigodet, Marie Delannoy, Gregoire Loïs, Romain Julliard, Björn Grüning, Yvan Le Bras (2024) Guidance framework to apply best practices in ecological data analysis: Lessons learned from building Galaxy-Ecology. EcoEvoRxiv, ver.3 peer-reviewed and recommended by PCI Ecology. 
https://doi.org/10.32942/X2G033

Guidance framework to apply best practices in ecological data analysis: Lessons learned from building Galaxy-EcologyColine Royaux, Jean-Baptiste Mihoub, Marie Jossé, Dominique Pelletier, Olivier Norvez, Yves Reecht, Anne Fouilloux, Helena Rasche, Saskia Hiltemann, Bérénice Batut, Marc Eléaume, Pauline Seguineau, Guillaume Massé, Alan Amossé, Claire Bissery, Rom...<p>Numerous conceptual frameworks exist for best practices in research data and analysis (e.g. Open Science and FAIR principles). In practice, there is a need for further progress to improve transparency, reproducibility, and confidence in ecology...Statistical ecologyTimothée Poisot2024-04-12 10:13:59 View
29 Aug 2024
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Flexible reproductive seasonality in Africa-dwelling papionins is associated with low environmental productivity and high climatic unpredictability

Reproductive flexibility shapes primate survival in a changing climate driven by environmental unpredictability

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

As seasonal cycles become increasingly disrupted, our understanding of the ecology and evolution of reproductive seasonality in tropical vertebrates remains limited (Bronson 2009). To predict how changes in seasonality might impact these animals, it is crucial to identify which elements of their varied reproductive patterns are connected to the equally varied patterns of rainfall seasonality (within-year fluctuations) or the significant climatic unpredictability (year-to-year variations) characteristic of the intertropical region. 

Dezeure et al. (2024) provide a comprehensive examination of reproductive seasonality in papionin monkeys across diverse African environments. By investigating the ecological and evolutionary determinants of reproductive timing, the authors offer novel insights into how climatic factors, particularly environmental unpredictability, shape reproductive strategies in these primates. This study stands out not only for its methodological rigour but also for its contribution to our understanding of how primates adapt their reproductive behaviours to varying environmental pressures. The findings have broad implications, particularly in the context of ongoing climate change, which is expected to increase environmental unpredictability globally. The innovative approach of this paper lies in its multifaceted examination of reproductive seasonality, which integrates data from 21 wild populations of 11 papionin species. The study employs a robust statistical framework, incorporating Bayesian phylogenetic generalised linear mixed models to control for phylogenetic relatedness among species. This methodological choice is crucial because it allows the authors to disentangle the effects of environmental variables from evolutionary history, providing a more accurate picture of how current ecological factors influence reproductive strategies.

The study’s focus on environmental unpredictability as a determinant of reproductive seasonality is particularly noteworthy. While previous research has established the importance of environmental seasonality (Janson and Verdolin 2005), this paper breaks new ground by showing that the magnitude of year-to-year variation in rainfall – rather than just the seasonal distribution of rainfall – plays a critical role in determining the intensity of reproductive seasonality. This finding is supported by the significant negative correlation between reproductive seasonality and environmental unpredictability, which the authors demonstrate across multiple populations and species. The results of this study are important for several reasons. First, they challenge the traditional view that reproductive seasonality is primarily driven by within-year environmental fluctuations. By showing that inter-annual variability in rainfall is a stronger predictor of reproductive timing than intra-annual variability, the authors suggest that primates, like papionins, have evolved flexible reproductive strategies to cope with the unpredictable availability of resources. This flexibility is likely an adaptive response to the highly variable environments that many African primates inhabit, where food availability can vary dramatically not just within a year but from year to year. Second, the study highlights the role of reproductive flexibility in the evolutionary success of papionins. The authors provide compelling evidence that species within the Papio genus, for example, exhibit significant variability in reproductive timing both within and between populations. This variability suggests that these species possess a remarkable ability to adjust their reproductive strategies in response to local environmental conditions, which may have contributed to their widespread distribution across diverse habitats in Africa. This finding aligns with the work of Brockman and Schaik (2005), who argued that reproductive flexibility is a key factor in the success of primates in unpredictable environments.

The study also contributes to our understanding of the evolutionary transition from seasonal to non-seasonal breeding in primates. The authors propose that the loss of strict reproductive seasonality in some papionin species may represent an adaptive shift toward greater reproductive flexibility. This shift could be driven by the need to maximise reproductive success in environments where the timing of resource peaks is difficult to predict. The authors’ findings support this hypothesis, as they show that populations living in more unpredictable environments tend to have lower reproductive seasonality. The broader implications of this study (Dezeure et al. 2024) extend beyond the specific case of papionin monkeys. The findings have relevance for the study of reproductive strategies in other long-lived, tropical mammals that face similar environmental challenges. As climate change is expected to increase the frequency and intensity of environmental unpredictability, understanding how species have historically adapted to such conditions can provide valuable insights into their potential resilience or vulnerability to future changes.

Many primate species are already facing significant threats from habitat loss, hunting, and climate change. By identifying the environmental factors that influence reproductive success, Dezeure et al. (2024) study can help inform conservation strategies aimed at protecting the most vulnerable populations. For example, conservation efforts could focus on maintaining or restoring habitat features that promote reproductive flexibility, such as access to a variety of food resources that peak at different times of the year (Chapman et al.).

References

Brockman D, Schaik C (2005) Seasonality in Primates: Studies of Living and Extinct Human and Non-Human Primates. Cambridge University Press. https://doi.org/10.1017/CBO9780511542343

Bronson FH (2009) Climate change and seasonal reproduction in mammals. Philos Trans R Soc B Biol Sci 364:3331–3340. https://doi.org/10.1098/rstb.2009.0140

Chapman CA, Gogarten JF, Golooba M, et al Fifty+ years of primate research illustrates complex drivers of abundance and increasing primate numbers. Am J Primatol n/a:e23577. https://doi.org/10.1002/ajp.23577

Jules Dezeure, Julie Dagorrette, Lugdiwine Burtschell, Shahrina Chowdhury, Dieter Lukas, Larissa Swedell, Elise Huchard (2024) Flexible reproductive seasonality in Africa-dwelling papionins is associated with low environmental productivity and high climatic unpredictability. bioRxiv, ver.2 peer-reviewed and recommended by PCI Ecology https://doi.org/10.1101/2024.05.01.591991

Janson C, Verdolin J (2005) Seasonality of primate births in relation to climate. In: Schaik CP van, Brockman DK (eds) Seasonality in Primates: Studies of Living and Extinct Human and Non-Human Primates. Cambridge University Press, Cambridge, pp 307–350 https://doi.org/10.1017/CBO9780511542343.012

Flexible reproductive seasonality in Africa-dwelling papionins is associated with low environmental productivity and high climatic unpredictabilityJules Dezeure, Julie Dagorrette, Lugdiwine Burtschell, Shahrina Chowdhury, Dieter Lukas, Larissa Swedell, Elise Huchard<p style="text-align: justify;">At a time when seasonal cycles are increasingly disrupted, the ecology and evolution of reproductive seasonality in tropical vertebrates remains poorly understood. In order to predict how changes in seasonality migh...Behaviour & Ethology, Evolutionary ecology, ZoologyCédric Sueur2024-05-04 18:57:25 View
16 Nov 2020
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Intraspecific diversity loss in a predator species alters prey community structure and ecosystem functions

Hidden diversity: how genetic richness affects species diversity and ecosystem processes in freshwater ponds

Recommended by based on reviews by Andrew Barnes and Jes Hines

Biodiversity loss can have important consequences for ecosystem functions, as exemplified by a large body of literature spanning at least three decades [1–3]. While connections between species diversity and ecosystem functions are now well-defined and understood, the importance of diversity within species is more elusive. Despite a surge in theoretical work on how intraspecific diversity can affect coexistence in simple community types [4,5], not much is known about how intraspecific diversity drives ecosystem processes in more complex community types. One particular challenge is that intraspecific diversity can be expressed as observable variation of functional traits, or instead subsist as genetic variation of which the consequences for ecosystem processes are harder to grasp.
Raffard et al. [6] examined how intraspecific biodiversity loss in a consumer fish changes species diversity at lower trophic levels and ecosystem processes in pond mesocosms. An interesting feature of this experiment is that it crosses functional and genetic intraspecific diversity. To do so, Raffard and colleagues measured and genotyped European minnow (P. phoxinus) individuals sampled from streams across southern France. Combining these collected specimens into experimental ponds allowed them to control functional (population variance of body size) and genetic intraspecific richness (number of genotypes).
Effects on minnow biomass production were mostly small; biomass was significantly reduced only when lowering both functional and genetic richness. However, the consequences for lower trophic levels (zooplankton and macroinvertebrates) were more pronounced and – importantly – not intuitive. For instance, the macroinvertebrate community was less species-diverse at higher minnow functional richness. If minnows with different body sizes would be the main regulator factors [7] explaining macroinvertebrate interactions, one would expect a more diverse set of minnow body sizes (i.e. higher functional minnow richness) to permit higher instead of lower macroinvertebrate richness. At the same time, the macroinvertebrate community was more species-diverse at higher minnow genotype richness, which could indicate unobserved minnow traits determining macroinvertebrate diversity more than the usual suspects (functional consumer richness). Such unobserved traits could be behavioral traits, allowing for resource partitioning among fish.
The consequences of functional minnow diversity loss on zooplankton diversity were negative, as expected in case body size differences among fish would facilitate coexistence of their zooplankton prey, as explained above. However, this was only the case when genetic diversity was high, suggesting nonstraightforward interactive effects of observed and non-observed traits on prey diversity.
The effects of functional and genetic minnow diversity loss on invertebrate (macroinvertebrates and zooplankton) abundance were more consistent than for invertebrate diversity. This suggests again nonstraightforward relationships in this experimental ecosystem, but now between invertebrate diversity and abundance. When using abundance as a proxy for an ecosystem process (which the authors did not), this result illustrates that biodiversity loss in multitrophic communities can have consequences that are challenging to interpret, let alone predict [8,9]. Path analyses showed how the observed changes of invertebrate diversity and abundance co-determined decomposition, a key ecosystem function. These path analyses had highest explanatory power show when including both kinds of intraspecific diversity.
Taken together, the results by Raffard and colleagues suggest that genetic consumer richness can drive species diversity of connected trophic levels and ecosystem processes with similar magnitude as functional diversity. Indeed, the effects of genetic consumer richness were shown to be so strong as to compensate or exacerbate the loss of observed functional richness. The exact mechanisms explaining these effects remain to be identified, however. The possibility that fish grazing by fish with different (observed or not observed) traits regulates coexistence among invertebrate prey, for instance, would depend on how strong fish consumption feeds back on prey growth during a 30-week experiment. As the authors indicate, detailed studies on resource partitioning among consumers (e.g. using stable isotope labelling) can shed light on these matters. Doing so may address a more fundamental question, which is if the mechanisms linking intraspecific diversity to function are different from those linking interspecific diversity to function, and at what time scales.

References

[1] Tilman D, Downing JA (1994) Biodiversity and stability in grasslands. Nature, 367, 363–365. https://doi.org/10.1038/367363a0
[2] Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S (2012) Biodiversity loss and its impact on humanity. Nature, 486, 59–67. https://doi.org/10.1038/nature11148
[3] De Laender F, Rohr JR, Ashauer R, Baird DJ, Berger U, Eisenhauer N, Grimm V, Hommen U, Maltby L, Meliàn CJ, Pomati F, Roessink I, Radchuk V, Brink PJV den (2016) Reintroducing Environmental Change Drivers in Biodiversity–Ecosystem Functioning Research. Trends in Ecology & Evolution, 31, 905–915. https://doi.org/10.1016/j.tree.2016.09.007
[4] Hart SP, Schreiber SJ, Levine JM (2016) How variation between individuals affects species coexistence. Ecology Letters, 19, 825–838. https://doi.org/10.1111/ele.12618
[5] Barabás G, D’Andrea R (2016) The effect of intraspecific variation and heritability on community pattern and robustness. Ecology Letters, 19, 977–986. https://doi.org/10.1111/ele.12636
[6] Raffard A, Cucherousset J, Montoya JM, Richard M, Acoca-Pidolle S, Poésy C, Garreau A, Santoul F, Blanchet S (2020) Intraspecific diversity loss in a predator species alters prey community structure and ecosystem functions. bioRxiv, 2020.06.10.144337, ver. 3 peer-reviewed and recommended by PCI Ecology. https://doi.org/10.1101/2020.06.10.144337
[7] Pásztor L, Botta-Dukát Z, Magyar G, Czárán T, Meszéna G. Theory-Based Ecology: A Darwinian approach. Oxford University Press. https://doi.org/10.1093/acprof:oso/9780199577859.001.0001
[8] Binzer A, Guill C, Rall BC, Brose U (2016) Interactive effects of warming, eutrophication and size structure: impacts on biodiversity and food-web structure. Global Change Biology, 22, 220–227. https://doi.org/10.1111/gcb.13086
[9] Schwarz B, Barnes AD, Thakur MP, Brose U, Ciobanu M, Reich PB, Rich RL, Rosenbaum B, Stefanski A, Eisenhauer N (2017) Warming alters energetic structure and function but not resilience of soil food webs. Nature Climate Change, 7, 895–900. https://doi.org/10.1038/s41558-017-0002-z

Intraspecific diversity loss in a predator species alters prey community structure and ecosystem functionsAllan Raffard, Julien Cucherousset, José M. Montoya, Murielle Richard, Samson Acoca-Pidolle, Camille Poésy, Alexandre Garreau, Frédéric Santoul & Simon Blanchet.<p>Loss in intraspecific diversity can alter ecosystem functions, but the underlying mechanisms are still elusive, and intraspecific biodiversity-ecosystem function relationships (iBEF) have been restrained to primary producers. Here, we manipulat...Community ecology, Ecosystem functioning, Experimental ecology, Food webs, Freshwater ecologyFrederik De Laender Andrew Barnes2020-06-15 09:04:53 View
21 Oct 2020
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Why scaling up uncertain predictions to higher levels of organisation will underestimate change

Uncertain predictions of species responses to perturbations lead to underestimate changes at ecosystem level in diverse systems

Recommended by based on reviews by Carlos Melian and 1 anonymous reviewer

Different sources of uncertainty are known to affect our ability to predict ecological dynamics (Petchey et al. 2015). However, the consequences of uncertainty on prediction biases have been less investigated, especially when predictions are scaled up to higher levels of organisation as is commonly done in ecology for instance. The study of Orr et al. (2020) addresses this issue. It shows that, in complex systems, the uncertainty of unbiased predictions at a lower level of organisation (e.g. species level) leads to a bias towards underestimation of change at higher level of organisation (e.g. ecosystem level). This bias is strengthened by larger uncertainty and by higher dimensionality of the system.
This general result has large implications for many fields of science, from economics to energy supply or demography. In ecology, as discussed in this study, these results imply that the uncertainty of predictions of species’ change increases the probability of underestimation of changes of diversity and stability at community and ecosystem levels, especially when species richness is high. The uncertainty of predictions of species’ change also increases the probability of underestimation of change when multiple ecosystem functions are considered at once, or when the combined effect of multiple stressors is considered.
The consequences of species diversity on ecosystem functions and stability have received considerable attention during the last decades (e.g. Cardinale et al. 2012, Kéfi et al. 2019). However, since the bias towards underestimation of change increases with species diversity, future studies will need to investigate how the general statistical effect outlined by Orr et al. might affect our understanding of the well-known relationships between species diversity and ecosystem functioning and stability in response to perturbations.

References

Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S (2012) Biodiversity loss and its impact on humanity. Nature, 486, 59–67. https://doi.org/10.1038/nature11148
Kéfi S, Domínguez‐García V, Donohue I, Fontaine C, Thébault E, Dakos V (2019) Advancing our understanding of ecological stability. Ecology Letters, 22, 1349–1356. https://doi.org/10.1111/ele.13340
Orr JA, Piggott JJ, Jackson A, Arnoldi J-F (2020) Why scaling up uncertain predictions to higher levels of organisation will underestimate change. bioRxiv, 2020.05.26.117200. https://doi.org/10.1101/2020.05.26.117200
Petchey OL, Pontarp M, Massie TM, Kéfi S, Ozgul A, Weilenmann M, Palamara GM, Altermatt F, Matthews B, Levine JM, Childs DZ, McGill BJ, Schaepman ME, Schmid B, Spaak P, Beckerman AP, Pennekamp F, Pearse IS (2015) The ecological forecast horizon, and examples of its uses and determinants. Ecology Letters, 18, 597–611. https://doi.org/10.1111/ele.12443

Why scaling up uncertain predictions to higher levels of organisation will underestimate changeJames Orr, Jeremy Piggott, Andrew Jackson, Jean-François Arnoldi<p>Uncertainty is an irreducible part of predictive science, causing us to over- or underestimate the magnitude of change that a system of interest will face. In a reductionist approach, we may use predictions at the level of individual system com...Community ecology, Ecosystem functioning, Theoretical ecologyElisa ThebaultAnonymous2020-06-02 15:41:12 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
16 Jun 2023
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Colonisation debt: when invasion history impacts current range expansion

Combining stochastic models and experiments to understand dispersal in heterogeneous environments

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

Dispersal is a key element of the natural dynamics of meta-communities, and plays a central role in the success of populations colonizing new landscapes. Understanding how demographic processes may affect the speed at which alien species spread through environmentally-heterogeneous habitat fragments is therefore of key importance to manage biological invasions. This requires studying together the complex interplay of dispersal and population processes, two inextricably related phenomena that can produce many possible outcomes. Stochastic models offer an opportunity to describe this kind of process in a meaningful way, but to ensure that they are realistic (sensu Levins 1966) it is also necessary to combine model simulations with empirical data (Snäll et al. 2007).

Morel-Journel et al. (2023) put together stochastic models and experimental data to study how population density may affect the speed at which alien species spread through a heterogeneous landscape. They do it by focusing on what they call ‘colonisation debt’, which is merely the impact that population density at the invasion front may have on the speed at which the species colonizes patches of different carrying capacities. They investigate this issue through two largely independent approaches. First, a stochastic model of dispersal throughout the patches of a linear, 1-dimensional landscape, which accounts for different degrees of density-dependent growth. And second, a microcosm experiment of a parasitoid wasp colonizing patches with different numbers of host eggs. In both cases, they compare the velocity of colonization of patches with lower or higher carrying capacity than the previous one (i.e. what they call upward or downward gradients).

Their results show that density-dependent processes influence the speed at which new fragments are colonized is significantly reduced by positive density dependence. When either population growth or dispersal rate depend on density, colonisation debt limits the speed of invasion, which turns out to be dependent on the strength and direction of the gradient between the conditions of the invasion front, and the newly colonized patches. Although this result may be quite important to understand the meta-population dynamics of dispersing species, it is important to note that in their study the environmental differences between patches do not take into account eventual shifts in the scenopoetic conditions (i.e. the values of the environmental parameters to which species niches’ respond to; Hutchinson 1978, see also Soberón 2007). Rather, differences arise from variations in the carrying capacity of the patches that are consecutively invaded, both in the in silico and microcosm experiments. That is, they account for potential differences in the size or quality of the invaded fragments, but not on the costs of colonizing fragments with different environmental conditions, which may also determine invasion speed through niche-driven processes. This aspect can be of particular importance in biological invasions or under climate change-driven range shifts, when adaptation to new environments is often required (Sakai et al. 2001; Whitney & Gabler 2008; Hill et al. 2011).

The expansion of geographical distribution ranges is the result of complex eco-evolutionary processes where meta-community dynamics and niche shifts interact in a novel physical space and/or environment (see, e.g., Mestre et al. 2020). Here, the invasibility of native communities is determined by niche variations and how similar are the traits of alien and native species (Hui et al. 2023). Within this context, density-dependent processes will build upon and heterogeneous matrix of native communities and environments (Tischendorf et al. 2005), to eventually determine invasion success. What the results of Morel-Journel et al. (2023) show is that, when the invader shows density dependence, the invasion process can be slowed down by variations in the carrying capacity of patches along the dispersal front. This can be particularly useful to manage biological invasions; ongoing invasions can be at least partially controlled by manipulating the size or quality of the patches that are most adequate to the invader, controlling host populations to reduce carrying capacity. But further, landscape manipulation of such kind could be used in a preventive way, to account in advance for the effects of the introduction of alien species for agricultural exploitation or biological control, thereby providing an additional safeguard to practices such as the introduction of parasitoids to control plagues. These practical aspects are certainly worth exploring further, together with a more explicit account of the influence of the abiotic conditions and the characteristics of the invaded communities on the success and speed of biological invasions.

REFERENCES

Hill, J.K., Griffiths, H.M. & Thomas, C.D. (2011) Climate change and evolutionary adaptations at species' range margins. Annual Review of Entomology, 56, 143-159. https://doi.org/10.1146/annurev-ento-120709-144746

Hui, C., Pyšek, P. & Richardson, D.M. (2023) Disentangling the relationships among abundance, invasiveness and invasibility in trait space. npj Biodiversity, 2, 13. https://doi.org/10.1038/s44185-023-00019-1

Hutchinson, G.E. (1978) An introduction to population biology. Yale University Press, New Haven, CT.

Levins, R. (1966) The strategy of model building in population biology. American Scientist, 54, 421-431. 

Mestre, A., Poulin, R. & Hortal, J. (2020) A niche perspective on the range expansion of symbionts. Biological Reviews, 95, 491-516. https://doi.org/10.1111/brv.12574

Morel-Journel, T., Haond, M., Duan, L., Mailleret, L. & Vercken, E. (2023) Colonisation debt: when invasion history impacts current range expansion. bioRxiv, 2022.11.13.516255, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.11.13.516255

Snäll, T., B. O'Hara, R. & Arjas, E. (2007) A mathematical and statistical framework for modelling dispersal. Oikos, 116, 1037-1050. https://doi.org/10.1111/j.0030-1299.2007.15604.x

Sakai, A.K., Allendorf, F.W., Holt, J.S., Lodge, D.M., Molofsky, J., With, K.A., Baughman, S., Cabin, R.J., Cohen, J.E., Ellstrand, N.C., McCauley, D.E., O'Neil, P., Parker, I.M., Thompson, J.N. & Weller, S.G. (2001) The population biology of invasive species. Annual Review of Ecology and Systematics, 32, 305-332. https://doi.org/10.1146/annurev.ecolsys.32.081501.114037

Soberón, J. (2007) Grinnellian and Eltonian niches and geographic distributions of species. Ecology Letters, 10, 1115-1123. https://doi.org/10.1111/j.1461-0248.2007.01107.x

Tischendorf, L., Grez, A., Zaviezo, T. & Fahrig, L. (2005) Mechanisms affecting population density in fragmented habitat. Ecology and Society, 10, 7. https://doi.org/10.5751/ES-01265-100107

Whitney, K.D. & Gabler, C.A. (2008) Rapid evolution in introduced species, 'invasive traits' and recipient communities: challenges for predicting invasive potential. Diversity and Distributions, 14, 569-580. https://doi.org/10.1111/j.1472-4642.2008.00473.x

Colonisation debt: when invasion history impacts current range expansionThibaut Morel-Journel, Marjorie Haond, Lana Duan, Ludovic Mailleret, Elodie Vercken<p>Demographic processes that occur at the local level, such as positive density dependence in growth or dispersal, are known to shape population range expansion, notably by linking carrying capacity to invasion speed. As a result of these process...Biological invasions, Colonization, Dispersal & Migration, Experimental ecology, Landscape ecology, Population ecology, Spatial ecology, Metacommunities & Metapopulations, Theoretical ecologyJoaquín HortalAnonymous, Anonymous2022-11-16 15:52:08 View
27 Nov 2023
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Modeling Tick Populations: An Ecological Test Case for Gradient Boosted Trees

Gradient Boosted Trees can deliver more than accurate ecological predictions

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

Tick-borne diseases are an important burden on public health all over the globe, making accurate forecasts of tick population a key ingredient in a successful public health strategy. Over long time scales, tick populations can undergo complex dynamics, as they are sensitive to many non-linear effects due to the complex relationships between ticks and the relevant (numerical) features of their environment.

But luckily, capturing complex non-linear responses is a task that machine learning thrives on. In this contribution, Manley et al. (2023) explore the use of Gradient Boosted Trees to predict the distribution (presence/absence) and abundance of ticks across New York state.

This is an interesting modelling challenge in and of itself, as it looks at the same ecological question as an instance of a classification problem (presence/absence) or of a regression problem (abundance). In using the same family of algorithm for both, Manley et al. (2023) provide an interesting showcase of the versatility of these techniques. But their article goes one step further, by setting up a multi-class categorical model that estimates jointly the presence and abundance of a population. I found this part of the article particularly elegant, as it provides an intermediate modelling strategy, in between having two disconnected models for distribution and abundance, and having nested models where abundance is only predicted for the present class (see e.g. Boulangeat et al., 2012, for a great description of the later).

One thing that Manley et al. (2023) should be commended for is their focus on opening up the black box of machine learning techniques. I have never believed that ML models are more inherently opaque than other families of models, but the focus in this article on explainable machine learning shows how these models might, in fact, bring us closer to a phenomenological understanding of the mechanisms underpinning our observations.

There is also an interesting discussion in this article, on the rate of false negatives in the different models that are being benchmarked. Although model selection often comes down to optimizing the overall quality of the confusion matrix (for distribution models, anyway), depending on the type of information we seek to extract from the model, not all types of errors are created equal. If the purpose of the model is to guide actions to control vectors of human pathogens, a false negative (predicting that the vector is absent at a site where it is actually present) is a potentially more damaging outcome, as it can lead to the vector population (and therefore, potentially, transmission) increasing unchecked.

References

Boulangeat I, Gravel D, Thuiller W. Accounting for dispersal and biotic interactions to disentangle the drivers of species distributions and their abundances: The role of dispersal and biotic interactions in explaining species distributions and abundances. Ecol Lett. 2012;15: 584-593.
https://doi.org/10.1111/j.1461-0248.2012.01772.x

Manley W, Tran T, Prusinski M, Brisson D. (2023) Modeling tick populations: An ecological test case for gradient boosted trees. bioRxiv, 2023.03.13.532443, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2023.03.13.532443

Modeling Tick Populations: An Ecological Test Case for Gradient Boosted TreesWilliam Manley, Tam Tran, Melissa Prusinski, Dustin Brisson<p style="text-align: justify;">General linear models have been the foundational statistical framework used to discover the ecological processes that explain the distribution and abundance of natural populations. Analyses of the rapidly expanding ...Parasitology, Species distributions, Statistical ecologyTimothée PoisotAnonymous, Anonymous2023-03-23 23:41:17 View
06 Oct 2020
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Implementing a rapid geographic range expansion - the role of behavior and habitat changes

The role of behavior and habitat availability on species geographic expansion

Recommended by ORCID_LOGO based on reviews by Caroline Marie Jeanne Yvonne Nieberding, Pizza Ka Yee Chow, Tim Parker and 1 anonymous reviewer

Understanding the relative importance of species-specific traits and environmental factors in modulating species distributions is an intriguing question in ecology [1]. Both behavioral flexibility (i.e., the ability to change the behavior in changing circumstances) and habitat availability are known to influence the ability of a species to expand its geographic range [2,3]. However, the role of each factor is context and species dependent and more information is needed to understand how these two factors interact. In this pre-registration, Logan et al. [4] explain how they will use Great-tailed grackles (Quiscalus mexicanus), a species with a flexible behavior and a rapid geographic range expansion, to evaluate the relative role of habitat and behavior as drivers of the species’ expansion [4]. The authors present very clear hypotheses, predicted results and also include alternative predictions. The rationales for all the hypotheses are clearly stated, and the methodology (data and analyses plans) are described with detail. The large amount of information already collected by the authors for the studied species during previous projects warrants the success of this study. It is also remarkable that the authors will make all their data available in a public repository, and that the pre-registration in already stored in GitHub, supporting open access and reproducible science. I agree with the three reviewers of this pre-registration about its value and I think its quality has largely improved during the review process. Thus, I am happy to recommend it and I am looking forward to seeing the results.

References

[1] Gaston KJ. 2003. The structure and dynamics of geographic ranges. Oxford series in Ecology and Evolution. Oxford University Press, New York.

[2] Sol D, Lefebvre L. 2000. Behavioural flexibility predicts invasion success in birds introduced to new zealand. Oikos. 90(3): 599–605. https://doi.org/10.1034/j.1600-0706.2000.900317.x

[3] Hanski I, Gilpin M. 1991. Metapopulation dynamics: Brief history and conceptual domain. Biological journal of the Linnean Society. 42(1-2): 3–16. https://doi.org/10.1111/j.1095-8312.1991.tb00548.x

[4] Logan CJ, McCune KB, Chen N, Lukas D. 2020. Implementing a rapid geographic range expansion - the role of behavior and habitat changes (http://corinalogan.com/Preregistrations/gxpopbehaviorhabitat.html) In principle acceptance by PCI Ecology of the version on 16 Dec 2021 https://github.com/corinalogan/grackles/blob/0fb956040a34986902a384a1d8355de65010effd/Files/Preregistrations/gxpopbehaviorhabitat.Rmd.

Implementing a rapid geographic range expansion - the role of behavior and habitat changesLogan CJ, McCune KB, Chen N, Lukas D<p>It is generally thought that behavioral flexibility, the ability to change behavior when circumstances change, plays an important role in the ability of a species to rapidly expand their geographic range (e.g., Lefebvre et al. (1997), Griffin a...Behaviour & Ethology, Biological invasions, Dispersal & Migration, Foraging, Habitat selection, Human impact, Phenotypic plasticity, Preregistrations, ZoologyEsther Sebastián GonzálezAnonymous, Caroline Marie Jeanne Yvonne Nieberding, Tim Parker2020-05-14 11:18:57 View
01 Mar 2024
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Cities as parasitic amplifiers? Malaria prevalence and diversity in great tits along an urbanization gradient

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

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

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

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

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

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

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

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

Cities as parasitic amplifiers? Malaria prevalence and diversity in great tits along an urbanization gradientAude E. Caizergues, Benjamin Robira, Charles Perrier, Melanie Jeanneau, Arnaud Berthomieu, Samuel Perret, Sylvain Gandon, Anne Charmantier<p style="text-align: justify;">Urbanization is a worldwide phenomenon that modifies the environment. By affecting the reservoirs of pathogens and the body and immune conditions of hosts, urbanization alters the epidemiological dynamics and divers...Epidemiology, Host-parasite interactions, Human impactAdrian DiazAnonymous, Gauthier Dobigny, Ana Paula Mansilla2023-09-11 20:24:44 View
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