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12 Sep 2023
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Linking intrinsic scales of ecological processes to characteristic scales of biodiversity and functioning patterns

The impact of process at different scales on diversity and ecosystem functioning: a huge challenge

Recommended by ORCID_LOGO based on reviews by Shai Pilosof, Gian Marco Palamara and 1 anonymous reviewer

Scale is a big topic in ecology [1]. Environmental variation happens at particular scales. The typical scale at which organisms disperse is species-specific, but, as a first approximation, an ensemble of similar species, for instance, trees, could be considered to share a typical dispersal scale. Finally, characteristic spatial scales of species interactions are, in general, different from the typical scales of dispersal and environmental variation. Therefore, conceptually, we can distinguish these three characteristic spatial scales associated with three different processes: species selection for a given environment (E), dispersal (D), and species interactions (I), respectively.  

From the famous species-area relation to the spatial distribution of biomass and species richness, the different macro-ecological patterns we usually study emerge from an interplay between dispersal and local interactions in a physical environment that constrains species establishment and persistence in every location. To make things even more complicated, local environments are often modified by the species that thrive in them, which establishes feedback loops.  It is usually assumed that local interactions are short-range in comparison with species dispersal, and dispersal scales are typically smaller than the scales at which the environment varies (I < D < E, see [2]), but this should not always be the case. 

The authors of this paper [2] relax this typical assumption and develop a theoretical framework to study how diversity and ecosystem functioning are affected by different relations between the typical scales governing interactions, dispersal, and environmental variation. This is a huge challenge. First, diversity and ecosystem functioning across space and time have been empirically characterized through a wide variety of macro-ecological patterns. Second, accommodating local interactions, dispersal and environmental variation and species environmental preferences to model spatiotemporal dynamics of full ecological communities can be done also in a lot of different ways. One can ask if the particular approach suggested by the authors is the best choice in the sense of producing robust results, this is, results that would be predicted by alternative modeling approaches and mathematical analyses [3]. The recommendation here is to read through and judge by yourself.  

The main unusual assumption underlying the model suggested by the authors is non-local species interactions. They introduce interaction kernels to weigh the strength of the ecological interaction with distance, which gives rise to a system of coupled integro-differential equations. This kernel is the key component that allows for control and varies the scale of ecological interactions. Although this is not new in ecology [4], and certainly has a long tradition in physics ---think about the electric or the gravity field, this approach has been widely overlooked in the development of the set of theoretical frameworks we have been using over and over again in community ecology, such as the Lotka-Volterra equations or, more recently, the metacommunity concept [5].

In Physics, classic fields have been revised to account for the fact that information cannot travel faster than light. In an analogous way, a focal individual cannot feel the presence of distant neighbors instantaneously. Therefore, non-local interactions do not exist in ecological communities. As the authors of this paper point out, they emerge in an effective way as a result of non-random movements, for instance, when individuals go regularly back and forth between environments (see [6], for an application to infectious diseases), or even migrate between regions. And, on top of this type of movement, species also tend to disperse and colonize close (or far) environments. Individual mobility and dispersal are then two types of movements, characterized by different spatial-temporal scales in general. Species dispersal, on the one hand, and individual directed movements underlying species interactions, on the other, are themselves diverse across species, but it is clear that they exist and belong to two distinct categories. 

In spite of the long and rich exchange between the authors' team and the reviewers, it was not finally clear (at least, to me and to one of the reviewers) whether the model for the spatio-temporal dynamics of the ecological community (see Eq (1) in [2]) is only presented as a coupled system of integro-differential equations on a continuous landscape for pedagogical reasons, but then modeled on a discrete regular grid for computational convenience. In the latter case, the system represents a regular network of local communities,  becomes a system of coupled ODEs, and can be numerically integrated through the use of standard algorithms. By contrast,  in the former case, the system is meant to truly represent a community that develops on continuous time and space, as in reaction-diffusion systems. In that case, one should keep in mind that numerical instabilities can arise as an artifact when integrating both local and non-local spatio-temporal systems. Spatial patterns could be then transient or simply result from these instabilities. Therefore, when analyzing spatiotemporal integro-differential equations, special attention should be paid to the use of the right numerical algorithms. The authors share all their code at https://zenodo.org/record/5543191, and all this can be checked out. In any case, the whole discussion between the authors and the reviewers has inherent value in itself, because it touches on several limitations and/or strengths of the author's approach,  and I highly recommend checking it out and reading it through.

Beyond these methodological issues, extensive model explorations for the different parameter combinations are presented. Several results are reported, but, in practice, what is then the main conclusion we could highlight here among all of them?  The authors suggest that "it will be difficult to manage landscapes to preserve biodiversity and ecosystem functioning simultaneously, despite their causative relationship", because, first, "increasing dispersal and interaction scales had opposing
effects" on these two patterns, and, second, unexpectedly, "ecosystems attained the highest biomass in scenarios which also led to the lowest levels of biodiversity". If these results come to be fully robust, this is, they pass all checks by other research teams trying to reproduce them using alternative approaches, we will have to accept that we should preserve biodiversity on its own rights and not because it enhances ecosystem functioning or provides particular beneficial services to humans. 

References

[1] Levin, S. A. 1992. The problem of pattern and scale in ecology. Ecology 73:1943–1967. https://doi.org/10.2307/1941447

[2] Yuval R. Zelnik, Matthieu Barbier, David W. Shanafelt, Michel Loreau, Rachel M. Germain. 2023. Linking intrinsic scales of ecological processes to characteristic scales of biodiversity and functioning patterns. bioRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Ecology.  https://doi.org/10.1101/2021.10.11.463913

[3] Baron, J. W. and Galla, T. 2020. Dispersal-induced instability in complex ecosystems. Nature Communications  11, 6032. https://doi.org/10.1038/s41467-020-19824-4

[4] Cushing, J. M. 1977. Integrodifferential equations and delay models in population dynamics 
 Springer-Verlag, Berlin. https://doi.org/10.1007/978-3-642-93073-7

[5] M. A. Leibold, M. Holyoak, N. Mouquet, P. Amarasekare, J. M. Chase, M. F. Hoopes, R. D. Holt, J. B. Shurin, R. Law, D. Tilman, M. Loreau, A. Gonzalez. 2004. The metacommunity concept: a framework for multi-scale community ecology. Ecology Letters, 7(7): 601-613. https://doi.org/10.1111/j.1461-0248.2004.00608.x

[6] M. Pardo-Araujo, D. García-García, D. Alonso, and F. Bartumeus. 2023. Epidemic thresholds and human mobility. Scientific reports 13 (1), 11409. https://doi.org/10.1038/s41598-023-38395-0

Linking intrinsic scales of ecological processes to characteristic scales of biodiversity and functioning patternsYuval R. Zelnik, Matthieu Barbier, David W. Shanafelt, Michel Loreau, Rachel M. Germain<p style="text-align: justify;">Ecology is a science of scale, which guides our description of both ecological processes and patterns, but we lack a systematic understanding of how process scale and pattern scale are connected. Recent calls for a ...Biodiversity, Community ecology, Dispersal & Migration, Ecosystem functioning, Landscape ecology, Theoretical ecologyDavid Alonso2021-10-13 23:24:45 View
10 Aug 2023
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Coexistence of many species under a random competition-colonization trade-off

Assembly in metacommunities driven by a competition-colonization tradeoff: more species in, more species out

Recommended by based on reviews by Canan Karakoç and 1 anonymous reviewer

The output of a community model depends on how you set its parameters. Thus, analyses of specific parameter settings hardwire the results to specific ecological scenarios. Because more general answers are often of interest, one tradition is to give models a statistical treatment: one summarizes how model parameters vary across species, and then predicts how changing the summary, instead of the individual parameters themselves, would change model output. Arguably the best-known example is the work initiated by May, showing that the properties of a community matrix, encoding effects species have on each other near their equilibrium, determine stability (1,2). More recently, this statistical treatment has also been applied to one of community ecology’s more prickly and slippery subjects: community assembly, which deals with the question “Given some regional species pool, which species will be able to persist together at some local ecosystem?”. Summaries of how species grow and interact in this regional pool predict the fraction of survivors and their relative abundances, the kind of dynamics, and various kinds of stability (3,4). One common characteristic of such statistical treatments is the assumption of disorder: if species do not interact in too structured ways, simple and therefore powerful predictions ensue that often stand up to scrutiny in relatively ordered systems. 
 
In their recent preprint, Miller, Clenet, et al. (5) subscribe to this tradition and consider tractable assembly scenarios (6) to study the outcome of assembly in a metacommunity. They recover a result of remarkable simplicity: roughly half of the species pool makes it into the final assemblage. Their vehicle is Tilman’s classic metacommunity model (7), where colonization rates are traded off with competitive ability. More precisely, in this model, one ranks species according to their colonization rate and attributes a greater competitive strength to lower-ranked species, which makes competition strictly hierarchical and thus departs from the disorder usually imposed by statistical approaches. The authors then leverage the simplicity of the species interaction network implied by this recursive setting to analytically probe how many species survive assembly. This turns out to be a fixed fraction that is distributed according to a Binomial with a mean of 0.5. While these results should not be extrapolated beyond the system at hand (4), they are important for two reasons. First, they imply that, within the framework of metacommunities driven by competition-colonization tradeoffs, richer species pools will produce richer communities: there is no upper bound on species richness, other than the one set by the raw material available for assembly. Second, this conclusion does not rely on simulation or equation solving and is, therefore, a hopeful sign of the palatability of the problem, if formalized in the right way. Their paper then shows that varying some of the settings does not change the main conclusion: changing how colonization rates distribute across species, and therefore the nature of the tradeoff, or the order with which species invade seems not to disrupt the big picture. Only when invaders are created “de novo” during assembly, a scenario akin to “de novo” mutation, a smaller fraction of species will survive assembly. 
 
As always, logical extensions of this study involve complicating the model and then looking if the results stay on par. The manuscript cites switching to other kinds of competition-colonization tradeoffs, and the addition of spatial heterogeneity as two potential avenues for further research. While certainly of merit, alternative albeit more bumpy roads would encompass models with radically different behavior. Most notably, one wonders how priority effects would play out. The current analysis shows that different invasion orders always lead to the same final composition, and therefore the same final species richness, confirming earlier results from models with similar structures (6). In models with priority effects, different invasion orders will surely lead to different compositions at the end. However, if one only cares about how many (and not which) species survive, it is unsure how much priority effects will qualitatively affect assembly. Because priority effects are varied in their topological manifestation (8), an important first step will be to evaluate which kinds of priority effects are compliant with formal analysis. 
 
References
 
1. May, R. M. (1972). Will a Large Complex System be Stable? Nature 238, 413–414. https://doi.org/10.1038/238413a0

2. Allesina, S. & Tang, S. (2015). The stability–complexity relationship at age 40: a random matrix perspective. Population Ecology, 57, 63–75. https://doi.org/10.1007/s10144-014-0471-0

3. Bunin, G. (2016). Interaction patterns and diversity in assembled ecological communities. Preprint at http://arxiv.org/abs/1607.04734.

4. Barbier, M., Arnoldi, J.-F., Bunin, G. & Loreau, M. (2018). Generic assembly patterns in complex ecological communities. Proceeding of the National Academy of Sciences, 115, 2156–2161. https://doi.org/10.1073/pnas.1710352115

5. Miller, Z. R., Clenet, M., Libera, K. D., Massol, F. & Allesina, S. (2023). Coexistence of many species under a random competition-colonization trade-off. bioRxiv 2023.03.23.533867, ver 3 peer-reviewed and recommended by PCI Ecology. https://doi.org/10.1101/2023.03.23.533867

6. Serván, C. A. & Allesina, S. (2021). Tractable models of ecological assembly. Ecology Letters, 24, 1029–1037. https://doi.org/10.1111/ele.13702

7. Tilman, D. (1994). Competition and Biodiversity in Spatially Structured Habitats. Ecology, 75, 2–16. https://doi.org/10.2307/1939377

8. Song, C., Fukami, T. & Saavedra, S. (2021). Untangling the complexity of priority effects in multispecies communities. Ecolygy Letters, 24, 2301–2313. https://doi.org/10.1111/ele.13870

Coexistence of many species under a random competition-colonization trade-offZachary R. Miller, Maxime Clenet, Katja Della Libera, François Massol, Stefano Allesina<p>The competition-colonization trade-off is a well-studied coexistence mechanism for metacommunities. In this setting, it is believed that coexistence of all species requires their traits to satisfy restrictive conditions limiting their similarit...Biodiversity, Coexistence, Colonization, Community ecology, Competition, Population ecology, Spatial ecology, Metacommunities & Metapopulations, Theoretical ecologyFrederik De Laender2023-03-30 20:42:48 View