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31 May 2023
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Conservation networks do not match the ecological requirements of amphibians

Amphibians under scrutiny - When human-dominated landscape mosaics are not in full compliance with their ecological requirements

Recommended by ORCID_LOGO based on reviews by Peter Vermeiren and 1 anonymous reviewer

Among vertebrates, amphibians are one of the most diverse groups with more than 7,000 known species. Amphibians occupy various ecosystems, including forests, wetlands, and freshwater habitats. Amphibians are known to be highly sensitive to changes in their environment, particularly to water quality and habitat degradation, so that monitoring abundance of amphibian populations can provide early warning signs of ecosystem disturbances that may also affect other organisms including humans (Bishop et al., 2012). Accordingly, efforts in habitat preservation and sustainable land and water management are necessary to safeguard amphibian populations.

In this context, Matutini et al. (2023) compared ecological requirements of amphibian species with the quality of agricultural landscape mosaics. Doing so, they identified critical gaps in existing conservation tools that include protected areas, green infrastructures, and inventoried sites. Matutini et al. (2023) focused on nine amphibian species in the Pays-de-la-Loire region where the landscape has been fashioned over the years by human activities. Three of the chosen amphibian species are living in a dense hedgerow mosaic landscape, while five others are more generalists.

Matutini et al. (2023) established multi-species habitat suitability maps, together with their levels of confidence, by combining single species maps with a probabilistic stacking method at 500-m resolution. From these maps, habitats were classified in five categories, from not suitable to highly suitable. Then, the circuit theory was used to map the potential connections between each highly suitable patch at the regional scale. Finally, comparing suitability maps with existing conservation tools, Matutini et al. (2023) were able to assess their coverage and efficiency.

Whatever their species status (endangered or not), Matutini et al. (2023) highlighted some discrepancies between the ecological requirements of amphibians in terms of habitat quality and the conservation tools of the landscape mosaic within which they are evolving. More specifically, Matutini et al. (2023) found that protected areas and inventoried sites covered only a small proportion of highly suitable habitats, while green infrastructures covered around 50% of the potential habitat for amphibian species. Such a lack of coverage and efficiency of protected areas brings to light that geographical sites with amphibian conservation challenges are known but not protected. Regarding the landscape fragmentation, Matutini et al. (2023) found that generalist amphibian species have a more homogeneous distribution of suitable habitats at the regional scale. They also identified two bottlenecks between two areas of suitable habitats, a situation that could prove critical to amphibian movements if amphibians were forced to change habitats to global change.

In conclusion, Matutini et al. (2023) bring convincing arguments in support of land-use species-conservation planning based on a better consideration of human-dominated landscape mosaics in full compliance with ecological requirements of the species that inhabit the regions concerned.

References

Bishop, P.J., Angulo, A., Lewis, J.P., Moore, R.D., Rabb, G.B., Moreno, G., 2012. The Amphibian Extinction Crisis - what will it take to put the action into the Amphibian Conservation Action Plan? Sapiens - Surveys and Perspectives Integrating Environment and Society 5, 1–16. http://journals.openedition.org/sapiens/1406

Matutini, F., Baudry, J., Fortin, M.-J., Pain, G., Pithon, J., 2023. Conservation networks do not match ecological requirements of amphibians. bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.07.18.500425

Conservation networks do not match the ecological requirements of amphibiansMatutini Florence, Jacques Baudry, Marie-Josée Fortin, Guillaume Pain, Joséphine Pithon<p style="text-align: justify;">1. Amphibians are among the most threatened taxa as they are highly sensitive to habitat degradation and fragmentation. They are considered as model species to evaluate habitats quality in agricultural landscapes. I...Biodiversity, Biogeography, Human impact, Landscape ecology, Macroecology, Spatial ecology, Metacommunities & Metapopulations, Species distributions, Terrestrial ecologySandrine Charles2022-09-20 14:40:03 View
06 Jan 2021
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Comparing statistical and mechanistic models to identify the drivers of mortality within a rear-edge beech population

The complexity of predicting mortality in trees

Recommended by based on reviews by Lisa Hülsmann and 2 anonymous reviewers

One of the main issues of forest ecosystems is rising tree mortality as a result of extreme weather events (Franklin et al., 1987). Eventually, tree mortality reduces forest biomass (Allen et al., 2010), although its effect on forest ecosystem fluxes seems not lasting too long (Anderegg et al., 2016). This controversy about the negative consequences of tree mortality is joined to the debate about the drivers triggering and the mechanisms accelerating tree decline. For instance, there is still room for discussion about carbon starvation or hydraulic failure determining the decay processes (Sevanto et al., 2014) or about the importance of mortality sources (Reichstein et al., 2013). Therefore, understanding and predicting tree mortality has become one of the challenges for forest ecologists in the last decade, doubling the rate of articles published on the topic (*). Although predicting the responses of ecosystems to environmental change based on the traits of species may seem a simplistic conception of ecosystem functioning (Sutherland et al., 2013), identifying those traits that are involved in the proneness of a tree to die would help to predict how forests will respond to climate threatens.
Modelling tree mortality is complex, involving multiple factors acting simultaneously at different scales, from tree genetics to ecosystem dynamics and from microsite conditions to global climatic events. Therefore, taking into account different approaches to reduce uncertainty of the predictions is needed (Bugmann et al., 2019). Petit-Cailleux et al. (2020) uses statistical and process-based models to detect the main mortality drivers of a drought- and frost-prone beech population. Particularly, they assessed the intra-individual characteristics of the population, that may play a decisive role explaining the differences in tree vulnerability to extreme weather events. Comparing the results of both analytical approaches, they find out several key factors, such as defoliation, leaf phenology and tree size, that were consistent between them. Even more, the process-based model showed the physiological mechanisms that may explain the individual vulnerability, for instance higher loss of hydraulic conductance may increase the mortality risk of trees with early budburst phenology and large stem diameter. The authors also successfully model annual mortality rate with a linear relationship including only three parameters: loss of conductance, biomass of reserves and late frost days.
This valuable study is a good example of the complexity in understanding and predicting tree mortality. The authors carried out the ambitious commitment of studying the inter-annual variation in mortality with 14-year dataset. However, it might be not enough time to control for the dependence of temporal data to soundly model mortality rate. The authors also acknowledge that the use of two approaches increases the knowledge from different perspectives, but at the same time comparing their results is difficult because the parameters used are not identical. Particularly, process-based models tend to consider the same microclimatic conditions for every tree in the population, and may produce inconsistences with statistical models. Alternatively, individual-based modelling might overcome some of the incompatibilities between the approaches (Zhu et al., 2019).

(*) Number (and percentage) of articles found in Web of Sciences after searching (December the 10th, 2020) “tree mortality”: from 163 (0.006%) in 2010 to 412 (0.013%) in 2020.

References

Allen et al. (2010). A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest ecology and management, 259(4), 660-684. doi: https://doi.org/10.1016/j.foreco.2009.09.001
Anderegg et al. (2016). When a tree dies in the forest: scaling climate-driven tree mortality to ecosystem water and carbon fluxes. Ecosystems, 19(6), 1133-1147. doi: https://doi.org/10.1007/s10021-016-9982-1
Bugmann et al. (2019). Tree mortality submodels drive simulated long‐term forest dynamics: assessing 15 models from the stand to global scale. Ecosphere, 10(2), e02616. doi: https://doi.org/10.1002/ecs2.2616
Franklin, J. F., Shugart, H. H. and Harmon, M. E. (1987) Death as an ecological process: the causes, consequences, and variability of tree mortality. BioScience, 37, 550–556. doi: https://doi.org/10.2307/1310665
Petit-Cailleux, C., Davi, H., Lefèvre, F., Garrigue, J., Magdalou, J.-A., Hurson, C., Magnanou, E. and Oddou-Muratorio, S. (2020) Comparing statistical and mechanistic models to identify the drivers of mortality within a rear-edge beech population. bioRxiv, 645747, ver 7 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/645747
Reichstein et al. (2013). Climate extremes and the carbon cycle. Nature, 500(7462), 287-295. doi: https://doi.org/10.1038/nature12350
Sevanto, S., Mcdowell, N. G., Dickman, L. T., Pangle, R., and Pockman, W. T. (2014). How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant, cell & environment, 37(1), 153-161. doi: https://doi.org/10.1111/pce.12141
Sutherland et al. (2013). Identification of 100 fundamental ecological questions. Journal of ecology, 101(1), 58-67. doi: https://doi.org/10.1111/1365-2745.12025
Zhu, Y., Liu, Z., and Jin, G. (2019). Evaluating individual-based tree mortality modeling with temporal observation data collected from a large forest plot. Forest Ecology and Management, 450, 117496. doi: https://doi.org/10.1016/j.foreco.2019.117496

Comparing statistical and mechanistic models to identify the drivers of mortality within a rear-edge beech populationCathleen Petit-Cailleux, Hendrik Davi, François Lefevre, Christophe Hurson, Joseph Garrigue, Jean-André Magdalou, Elodie Magnanou and Sylvie Oddou-Muratorio<p>Since several studies have been reporting an increase in the decline of forests, a major issue in ecology is to better understand and predict tree mortality. The interactions between the different factors and the physiological processes giving ...Climate change, Physiology, Population ecologyLucía DeSoto2019-05-24 11:37:38 View
27 May 2019
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Community size affects the signals of ecological drift and selection on biodiversity

Toward an empirical synthesis on the niche versus stochastic debate

Recommended by based on reviews by Kevin Cazelles and Romain Bertrand

As far back as Clements [1] and Gleason [2], the historical schism between deterministic and stochastic perspectives has divided ecologists. Deterministic theories tend to emphasize niche-based processes such as environmental filtering and species interactions as the main drivers of species distribution in nature, while stochastic theories mainly focus on chance colonization, random extinctions and ecological drift [3]. Although the old days when ecologists were fighting fiercely over null models and their adequacy to capture niche-based processes is over [4], the ghost of that debate between deterministic and stochastic perspectives came back to haunt ecologists in the form of the ‘environment versus space’ debate with the development of metacommunity theory [5]. While interest in that question led to meaningful syntheses of metacommunity dynamics in natural systems [6], it also illustrated how context-dependant the answer was [7]. One of the next frontiers in metacommunity ecology is to identify the underlying drivers of this observed context-dependency in the relative importance of ecological processus [7, 8].
Reflecting on seminal work by Robert MacArthur emphasizing different processes at different spatial scales [9, 10] (the so-called ‘MacArthur paradox’), Chase and Myers proposed in 2011 that a key in solving the deterministic versus stochastic debate was probably to turn our attention to how the relative importance of local processes changes across spatial scales [3]. Scale-dependance is a well-acknowledged challenge in ecology, hampering empirical syntheses and comparisons between studies [11-14]. Embracing the scale-dependance of ecological processes would not only lead to stronger syntheses and consolidation of current knowledge, it could also help resolve many current debates or apparent contradictions [11, 15, 16].
The timely study by Siqueira et al. [17] fits well within this historical context by exploring the relative importance of ecological drift and selection across a gradient of community size (number of individuals in a given community). More specifically, they tested the hypothesis that small communities are more dissimilar among each other because of ecological drift compared to large communities, which are mainly structured by niche selection [17]. That smaller populations or communities should be more affected by drift is a mathematical given [18], but the main questions are i) for a given community size how important is ecological drift relative to other processes, and ii) how small does a community have to be before random assembly dominates? The authors answer these questions using an extensive stream dataset with a community size gradient sampled from 200 streams in two climatic regions (Brazil and Finland). Combining linear models with recent null model approaches to measure deviations from random expectations [19], they show that, as expected based on theory and recent experimental work, smaller communities tend to have higher β-diversity, and that those β-diversity patterns could not be distinguished from random assembly processes [17]. Spatial turnover among larger communities is mainly driven by niche-based processes related to species sorting or dispersal dynamics [17]. Given the current environmental context, with many anthropogenic perturbations leading to reduced community size, it is legitimate to wonder, as the authors do, whether we are moving toward a more stochastic and thus less predictable world with obvious implications for the conservation of biodiversity [17].
The real strength of the study by Siqueira et al. [17], in my opinion, is in the inclusion of stream data from boreal and tropical regions. Interestingly and most importantly, the largest communities in the tropical streams are as large as the smallest communities in the boreal streams. This is where the study should really have us reflect on the notions of context-dependency in observed patterns because the negative relationship between community size and β-diversity was only observed in the tropical streams, but not in the boreal streams [17]. This interesting nonlinearity in the response means that a study that would have investigated the drift versus niche-based question only in Finland would have found very different results from the same study in Brazil. Only by integrating such a large scale gradient of community sizes together could the authors show the actual shape of the relationship, which is the first step toward building a comprehensive synthesis on a debate that has challenged ecologists for almost a century.

References

[1] Clements, F. E. (1936). Nature and structure of the climax. Journal of ecology, 24(1), 252-284. doi: 10.2307/2256278
[2] Gleason, H. A. (1917). The structure and development of the plant association. Bulletin of the Torrey Botanical Club, 44(10), 463-481. doi: 10.2307/2479596
[3] Chase, J. M., and Myers, J. A. (2011). Disentangling the importance of ecological niches from stochastic processes across scales. Philosophical transactions of the Royal Society B: Biological sciences, 366(1576), 2351-2363. doi: 10.1098/rstb.2011.0063
[4] Diamond, J. M., and Gilpin, M. E. (1982). Examination of the “null” model of Connor and Simberloff for species co-occurrences on islands. Oecologia, 52(1), 64-74. doi: 10.1007/BF00349013
[5] Leibold M. A., et al. (2004). The metacommunity concept: a framework for multi‐scale community ecology. Ecology letters, 7(7), 601-613. doi: 10.1111/j.1461-0248.2004.00608.x
[6] Cottenie, K. (2005). Integrating environmental and spatial processes in ecological community dynamics. Ecology letters, 8(11), 1175-1182. doi: 10.1111/j.1461-0248.2005.00820.x
[7] Leibold, M. A. and Chase, J. M. (2018). Metacommunity Ecology. Monographs in Population Biology, vol. 59. Princeton University Press. [8] Vellend, M. (2010). Conceptual synthesis in community ecology. The Quarterly review of biology, 85(2), 183-206. doi: 10.1086/652373
[9] MacArthur, R. H., and Wilson, E. O. (1963). An equilibrium theory of insular zoogeography. Evolution, 17(4), 373-387. doi: 10.1111/j.1558-5646.1963.tb03295.x
[10] MacArthur, R. H., and Levins, R. (1967). The limiting similarity, convergence, and divergence of coexisting species. The American Naturalist, 101(921), 377-385. doi: 10.1086/282505
[11] Viana, D. S., and Chase, J. M. (2019). Spatial scale modulates the inference of metacommunity assembly processes. Ecology, 100(2), e02576. doi: 10.1002/ecy.2576
[12] Chave, J. (2013). The problem of pattern and scale in ecology: what have we learned in 20 years?. Ecology letters, 16, 4-16. doi: 10.1111/ele.12048
[13] Patrick, C. J., and Yuan, L. L. (2019). The challenges that spatial context present for synthesizing community ecology across scales. Oikos, 128(3), 297-308. doi: 10.1111/oik.05802
[14] Chase, J. M., and Knight, T. M. (2013). Scale‐dependent effect sizes of ecological drivers on biodiversity: why standardised sampling is not enough. Ecology letters, 16, 17-26. doi: 10.1111/ele.12112
[15] Horváth, Z., Ptacnik, R., Vad, C. F., and Chase, J. M. (2019). Habitat loss over six decades accelerates regional and local biodiversity loss via changing landscape connectance. Ecology letters, 22(6), 1019-1027. doi: 10.1111/ele.13260
[16] Chase, J. M, Gooriah, L., May, F., Ryberg, W. A, Schuler, M. S, Craven, D., and Knight, T. M. (2019). A framework for disentangling ecological mechanisms underlying the island species–area relationship. Frontiers of Biogeography, 11(1). doi: 10.21425/F5FBG40844.
[17] Siqueira T., Saito V. S., Bini L. M., Melo A. S., Petsch D. K. , Landeiro V. L., Tolonen K. T., Jyrkänkallio-Mikkola J., Soininen J. and Heino J. (2019). Community size affects the signals of ecological drift and niche selection on biodiversity. bioRxiv 515098, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/515098
[18] Hastings A., Gross L. J. eds. (2012). Encyclopedia of theoretical ecology (University of California Press, Berkeley).
[19] Chase, J. M., Kraft, N. J., Smith, K. G., Vellend, M., and Inouye, B. D. (2011). Using null models to disentangle variation in community dissimilarity from variation in α‐diversity. Ecosphere, 2(2), 1-11. doi: 10.1890/ES10-00117.1

Community size affects the signals of ecological drift and selection on biodiversityTadeu Siqueira, Victor S. Saito, Luis M. Bini, Adriano S. Melo, Danielle K. Petsch, Victor L. Landeiro, Kimmo T. Tolonen, Jenny Jyrkänkallio-Mikkola, Janne Soininen, Jani Heino<p>Ecological drift can override the effects of deterministic niche selection on small populations and drive the assembly of small communities. We tested the hypothesis that smaller local communities are more dissimilar among each other because of...Biodiversity, Coexistence, Community ecology, Competition, Conservation biology, Dispersal & Migration, Freshwater ecology, Spatial ecology, Metacommunities & MetapopulationsEric Harvey2019-01-09 19:06:21 View
11 Mar 2022
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Comment on “Information arms race explains plant-herbivore chemical communication in ecological communities”

Does information theory inform chemical arms race communication?

Recommended by based on reviews by Claudio Ramirez and 2 anonymous reviewers

One of the long-standing questions in evolutionary ecology is on the mechanisms involved in arms race coevolution. One way to address this question is to understand the conditions under which one species evolves traits in response to the presence of a second species and so on. However, specialized pairwise interactions are by far less common in nature than interactions involving a higher number of interacting species (Bascompte, Jordano 2013). While interactions between large sets of species are the norm rather than the exception in mutualistic (pollination, seed dispersal), and antagonist (herbivory, parasitism) relationships, few is known on the way species identify, process, and respond to information provided by other interacting species under field conditions (Schaefer, Ruxton 2011). 

Zu et al. (2020) addressed this general question by developing an interesting information theory-based approach that hypothesized conditional entropy in chemical communication plays a role as proxy of fitness in plant-herbivore communities. More specifically, plant fitness was assumed to be related to the efficiency to code signals by plant species, and herbivore fitness to the capacity to decode plant signals. In this way, from the plant perspective, the elaboration of plant signals that elude decoding by herbivores is expected to be favored, as herbivores are expected to attack plants with simple chemical signals. The empirical observation upon which the model was tested was the redundancy in volatile organic compounds (VOC) found across plant species in a plant-herbivore community. Interestingly, Zu et al.’s model predicted successfully that VOC redundancy in the plant community associates with increased conditional entropy, which conveys herbivore confusion and plant protection against herbivory. In this way, plant species that evolve VOCs already present in the community might be benefitted, ultimately leading to the patterns of VOC redundancy commonly observed in nature.

Bass & Kessler performed a series of interesting observations on Zu et al. (2020), that can be organized along three lines of reasoning. First, from an evolutionary perspective, Bass & Kessler note the important point that accepting that conditional information entropy, estimated from the contribution of every plant species to volatile redundancy implies that average plant fitness seems to depend on community-level properties (i.e., what the other species in the community are doing) rather than on population-level characteristics (I.e., what the individuals belonging a population are doing). While the level at which selection acts upon is a longstanding debate (e.g., Goodnight, 1990; Williams, 1992), the model seems to contradict one of the basic tenets of Darwinian evolution. The extent to which this important observation invalidates the contribution of Zu et al. (2020) is open to scrutiny. However, one can indulge the evolutionary criticism by arguing that every theoretical model performs a number of assumptions to preserve the simplicity of analyses. Furthermore, even accepting the criticism, the overall information-based framework is valuable as it provides a fresh perspective to the way coding and decoding chemical information in plant-herbivore interactions may result in arm race coevolution. The question to be assessed by members of the scientific community is how strong the evolutionary assumptions are to be acceptable. A second line of reasoning involves consideration of additional routes of chemical information transfer. If chemical volatiles are involved in another ecological function unrelated to arm race (as they are) such as toxicity, crypsis, aposematism, etc., the conditional information indices considered as proxy to plant and herbivore fitness may be only secondarily related to arms race. This is an interesting observation, which suggests that VOC production may have more than one ecological function, as it often happens in “pleiotropic” traits (Strauss, Irwin 2004). This is an exciting avenue for future research. Finally, a third category of comments involves the relationship between conditional information entropy and plant and herbivore fitness. Bass & Kessler developed a Bayesian treatment of the community-level information developed by Zu et al. (2020) that permitted to estimate fitness on a species rather than community level. Their results revealed that community conditional entropies fail to align with species-level indices, suggesting that conclusions of Strauss & Irwin (2004) are not commensurate with fitness at the species level, where the analysis seems to be pertinent. In general, I strongly recommend Bass & Kessler’s contribution as it provides a series of observations and new perspectives to Zu et al. (2020). Rather than restricting their manuscript to blind criticisms, Bass & Kessler provides new interesting perspectives, which is always welcome as it improves the value and scope of the original work.

References

Bascompte J, Jordano P (2013) Mutualistic Networks. Princeton University Press. https://doi.org/10.23943/princeton/9780691131269.001.0001

Bass E, Kessler A (2022) Comment on “Information arms race explains plant-herbivore chemical communication in ecological communities.” EcoEvoRxiv, ver. 8 peer-reviewed and recommended by Peer Community in Ecology.  https://doi.org/10.32942/osf.io/xsbtm

Goodnight CJ (1990) Experimental Studies of Community Evolution I: The Response to Selection at the Community Level. Evolution, 44, 1614–1624. https://doi.org/10.1111/j.1558-5646.1990.tb03850.x

Schaefer HM, Ruxton GD (2011) Plant-Animal Communication. Oxford University Press, Oxford. https://doi.org/10.1093/acprof:osobl/9780199563609.001.0001

Strauss SY, Irwin RE (2004) Ecological and Evolutionary Consequences of Multispecies Plant-Animal Interactions. Annual Review of Ecology, Evolution, and Systematics, 35, 435–466. https://doi.org/10.1146/annurev.ecolsys.35.112202.130215

Williams GC (1992) Natural Selection: Domains, Levels, and Challenges. Oxford University Press, Oxford, New York.

Zu P, Boege K, del-Val E, Schuman MC, Stevenson PC, Zaldivar-Riverón A, Saavedra S (2020) Information arms race explains plant-herbivore chemical communication in ecological communities. Science, 368, 1377–1381. https://doi.org/10.1126/science.aba2965

Comment on “Information arms race explains plant-herbivore chemical communication in ecological communities”Ethan Bass, André Kessler<p style="text-align: justify;">Zu et al (Science, 19 Jun 2020, p. 1377) propose that an ‘information arms-race’ between plants and herbivores explains plant-herbivore communication at the community level. However, the analysis presented here show...Chemical ecology, Community ecology, Eco-evolutionary dynamics, Evolutionary ecology, Herbivory, Interaction networks, Theoretical ecologyRodrigo Medel2021-10-02 06:06:07 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 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
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
25 May 2021
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Clumpy coexistence in phytoplankton: The role of functional similarity in community assembly

Environmental heterogeneity drives phytoplankton community assembly patterns in a tropical riverine system

Recommended by ORCID_LOGO and ORCID_LOGO based on reviews by Eric Goberville and Dominique Lamy

What predisposes two individuals to form and maintain a relationship is a fundamental question. Using facial recognition to see whether couples' faces change over time to become more and more similar, psychology researchers have concluded that couples tend to be formed from the start between people whose faces are more similar than average [1]. As the saying goes, birds of a feather flock together.

And what about in nature? Are these rules of assembly valid for communities of different species?

In his seminal contribution, Robert MacArthur (1984) wrote ‘To do science is to search for repeated patterns’ [2]. Identifying the mechanisms that govern the arrangement of life is a hot research topic in the field of ecology for decades, and an absolutely essential prerequisite to answer the outstanding question of what shape ecological patterns in multi-species communities such as species-area relationships, relative species abundances, or spatial and temporal turnover of community composition; amid others [3]. To explain ecological patterns in nature, some rely on the concept that every species - through evolutionary processes and the acquisition of a unique set of traits that allow a species to be adapted to its abiotic and biotic environment - occupies a unique niche: Species coexistence comes as the result of niche differentiation [4,5]. Such a view has been challenged by the recognition of the key role of neutral processes [6], however, in which demographic stochasticity contributes to shape multi-species communities and to explain why congener species coexist much more frequently than expected by chance [7,8]. While the niche-based and neutral theories appear seemingly opposed at first sight [9], the dichotomy may be more philosophical than empirical [4,5]. Many examples have come to support that both concepts are not incompatible as they together influence the structure, diversity and functioning of communities [10], and are simply extreme cases of a continuum [11]. From this perspective, extrinsic factors, i.e., environmental heterogeneity, may influence the location of a given community along the niche-neutrality continuum. 

The walk of species in nature is therefore neither random nor ecologically predestined. In microbial assemblages, the co-existence of these two antagonistic mechanisms has been shown both theoretically and empirically. It has been shown that a combination of stabilising (niche) and equalising (neutral) mechanisms was responsible for the existence of groups of coexistent species (clumps) in a phytoplankton rich community [12]. Analysing interannual changes (2003-2009) in the weekly abundance of diatoms and dinoflagellates located in a temperate coastal ecosystem of the Western English Channel, Mutshinda et al. [13] found a mixture of biomass dynamics consistent with the neutrality-niche continuum hypothesis. While niche processes explained the dynamic of phytoplankton functional groups (i.e., diatoms vs. dinoflagellates) in terms of biomass, neutral processes mainly dominated - 50 to 75% of the time - the dynamics at the species level within functional groups [13]. From one endpoint to another, defining the location of a community along the continuum is all matter of scale [4,11].

In their study, testing predictions made by an emergent neutrality model, Graco-Roza et al. [14] provide empirical evidence that neutral and niche processes joined together to shape and drive planktonic communities in a riverine ecosystem. Body size - the 'master trait' - is used here as a discriminant ecological dimension along the niche axis. From their analysis, they not only show that the specific abundance is organised in clumps and gaps along the niche axis, but also reveal that different clumps exist along the river course. They identify two main clumps in body size - with species belonging to three different morphologically-based functional groups - and characterise that among-species differences in biovolume are driven by functional redundancy at the clump level; species functional distinctiveness being related to the relative biovolume of species. By grouping their variables according to seasons (cold-dry vs. warm-wet) or river elevation profile (upper, medium and lower course), they hereby highlight how environmental heterogeneity contributes to shape species assemblages and their dynamics and conclude that emergent neutrality models are a powerful approach to explain species coexistence; and therefore ecological patterns.

References

[1] Tea-makorn PP, Kosinski M (2020) Spouses’ faces are similar but do not become more similar with time. Scientific Reports, 10, 17001. https://doi.org/10.1038/s41598-020-73971-8.

[2] MacArthur RH (1984) Geographical Ecology: Patterns in the Distribution of Species. Princeton University Press.

[3] Vellend M (2020) The Theory of Ecological Communities (MPB-57). Princeton University Press.

[4] Wennekes PL, Rosindell J, Etienne RS (2012) The Neutral—Niche Debate: A Philosophical Perspective. Acta Biotheoretica, 60, 257–271. https://doi.org/10.1007/s10441-012-9144-6.

[5] Gravel D, Guichard F, Hochberg ME (2011) Species coexistence in a variable world. Ecology Letters, 14, 828–839. https://doi.org/10.1111/j.1461-0248.2011.01643.x.

[6] Hubbell SP (2001) The Unified Neutral Theory of Biodiversity and Biogeography (MPB-32). Princeton University Press.

[7] Leibold MA, McPeek MA (2006) Coexistence of the Niche and Neutral Perspectives in Community Ecology. Ecology, 87, 1399–1410. https://doi.org/10.1890/0012-9658(2006)87[1399:COTNAN]2.0.CO;2.

[8] Pielou EC (1977) The Latitudinal Spans of Seaweed Species and Their Patterns of Overlap. Journal of Biogeography, 4, 299–311. https://doi.org/10.2307/3038189.

[9] Holt RD (2006) Emergent neutrality. Trends in Ecology & Evolution, 21, 531–533. https://doi.org/10.1016/j.tree.2006.08.003

[10] Scheffer M, Nes EH van (2006) Self-organized similarity, the evolutionary emergence of groups of similar species. Proceedings of the National Academy of Sciences, 103, 6230–6235. https://doi.org/10.1073/pnas.0508024103.

[11] Gravel D, Canham CD, Beaudet M, Messier C (2006) Reconciling niche and neutrality: the continuum hypothesis. Ecology Letters, 9, 399–409. https://doi.org/10.1111/j.1461-0248.2006.00884.x.

[12] Vergnon R, Dulvy NK, Freckleton RP (2009) Niches versus neutrality: uncovering the drivers of diversity in a species-rich community. Ecology Letters, 12, 1079–1090. https://doi.org/10.1111/j.1461-0248.2009.01364.x.

[13] Mutshinda CM, Finkel ZV, Widdicombe CE, Irwin AJ (2016) Ecological equivalence of species within phytoplankton functional groups. Functional Ecology, 30, 1714–1722. https://doi.org/10.1111/1365-2435.12641.

[14] Graco-Roza C, Segura AM, Kruk C, Domingos P, Soininen J, Marinho MM (2021) Clumpy coexistence in phytoplankton: The role of functional similarity in community assembly. bioRxiv, 869966, ver. 6 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/869966

 

Clumpy coexistence in phytoplankton: The role of functional similarity in community assemblyCaio Graco-Roza, Angel M. Segura, Carla Kruk, Patricia Domingos, Janne Soininen, Marcelo M. Marinho<p style="text-align: justify;">Emergent neutrality (EN) suggests that species must be sufficiently similar or sufficiently different in their niches to avoid interspecific competition. Such a scenario results in a transient pattern with clumps an...Coexistence, Community ecology, Theoretical ecologyCédric Hubas2020-01-23 16:11:32 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
28 Mar 2024
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Changes in length-at-first return of a sea trout (Salmo trutta) population in northern France

Why are trout getting smaller?

Recommended by based on reviews by Jan Kozlowski and 1 anonymous reviewer

Decline in body size over time have been widely observed in fish (but see Solokas et al. 2023), and the ecological consequences of this pattern can be severe (e.g., Audzijonyte et al. 2013, Oke et al. 2020). Therefore, studying the interrelationships between life history traits to understand the causal mechanisms of this pattern is timely and valuable. 

This phenomenon was the subject of a study by Josset et al. (2024), in which the authors analysed data from 39 years of trout trapping in the Bresle River in France. The authors focused mainly on the length of trout on their first return from the sea.   

The most important results of the study were the decrease in fish length-at-first return and the change in the age structure of first-returning trout towards younger (and earlier) returning fish. It seems then that the smaller size of trout is caused by a shorter time spent in the sea rather than a change in a growth pattern, as length-at-age remained relatively constant, at least for those returning earlier. Fish returning after two years spent in the sea had a relatively smaller length-at-age. The authors suggest this may be due to local changes in conditions during fish's stay in the sea, although there is limited environmental data to confirm the causal effect. Another question is why there are fewer of these older fish. The authors point to possible increased mortality from disease and/or overfishing.

These results may suggest that the situation may be getting worse, as another study finding was that “the more growth seasons an individual spent at sea, the greater was its length-at-first return.” The consequences may be the loss of the oldest and largest individuals, whose disproportionately high reproductive contribution to the population is only now understood (Barneche et al. 2018, Marshall and White 2019). 

References

Audzijonyte, A. et al. 2013. Ecological consequences of body size decline in harvested fish species: positive feedback loops in trophic interactions amplify human impact. Biol Lett 9, 20121103. https://doi.org/10.1098/rsbl.2012.1103

Barneche, D. R. et al. 2018. Fish reproductive-energy output increases disproportionately with body size. Science Vol 360, 642-645. https://doi.org/10.1126/science.aao6868

Josset, Q. et al. 2024. Changes in length-at-first return of a sea trout (Salmo trutta) population in northern France. biorXiv, 2023.11.21.568009, ver 4, Peer-reviewed and recommended by PCI Ecology. https://doi.org/10.1101/2023.11.21.568009

Marshall, D. J. and White, C. R. 2019. Have we outgrown the existing models of growth? Trends in Ecology & Evolution, 34, 102-111. https://doi.org/10.1016/j.tree.2018.10.005

Oke, K. B. et al. 2020. Recent declines in salmon body size impact ecosystems and fisheries. Nature Communications, 11, 4155. https://doi.org/10.1038/s41467-020-17726-z

Solokas, M. A. et al. 2023. Shrinking body size and climate warming: many freshwater salmonids do not follow the rule. Global Change Biology, 29, 2478-2492. https://doi.org/10.1111/gcb.16626

Changes in length-at-first return of a sea trout (*Salmo trutta*) population in northern FranceQuentin Josset, Laurent Beaulaton, Atso Romakkaniemi, Marie Nevoux<p style="text-align: justify;">The resilience of sea trout populations is increasingly concerning, with evidence of major demographic changes in some populations. Based on trapping data and related scale collection, we analysed long-term changes ...Biodiversity, Evolutionary ecology, Freshwater ecology, Life history, Marine ecologyAleksandra Walczyńska2023-11-23 14:36:39 View
03 Apr 2020
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Body temperatures, life history, and skeletal morphology in the nine-banded armadillo (Dasypus novemcinctus)

Is vertebral count in mammals influenced by developmental temperature? A study with Dasypus novemcinctus

Recommended by based on reviews by Darin Croft and ?

Mammals show a very low level of variation in vertebral count, both among and within species, in comparison to other vertebrates [1]. Jordan’s rule for fishes states that the vertebral number among species increases with latitude, due to ambient temperatures during development [2]. Temperature has also been shown to influence vertebral count within species in fish [3], amphibians [4], and birds [5]. However, in mammals the count appears to be constrained, on the one hand, by a possible relationship between the development of the skeleton and the proliferations of cell lines with associated costs (neural malformations, cancer etc., [6]), and on the other by the cervical origin of the diaphragm [7].
Knight et al. [8] investigate the effect of intrauterine temperature variation on skeletal morphology during development, and focus on a particular mammal, Dasypus novemcinctus, or nine-banded armadillo. Armadillos (Xenarthra) and are characterized by relatively low body temperatures and low basal rates of metabolism. Dasypus novemcinctus is the only xenarthran mammal to have naturally expanded its range into the middle latitudes of the U.S., and one of the few mammals that invaded North America from South America. It is one of few placentals that withstand considerable decrease of body temperature without torpor. It presents a resting body temperature that is low and variable for a placental mammal of its size [9] and is the only vertebrate that gives birth to monozygotic quadruplets. Among 42 monotreme, marsupial and placental genera, Dasypus novemcinctus shows the highest variation of thoracolumbar vertebral count [10].
The particularities of Dasypus novemcinctus regarding vertebral count variation and ability to withstand variable temperature qualify it as a target organism for study of the relationship between skeleton morphology and temperature in mammals.
Knight et al. [8] explored variability in vertebral count within Dasypus novemcinctus to understand whether temperature during development determines skeleton morphology. To this end they experimented with 22 armadillos (19 with data) and litters from 12 pregnant females, in two environments, for three years — an impressive effort and experimental setup. Moreover, they used a wide variety of advanced experimental and analytical techniques. For example, they implanted intra-abdominal, long-term temperature recorders, which recorded data every 6 to 120 minutes for up to several months. They analysed body temperature periodicity by approximation of the recordings with Fourier series, and they CT-scanned fetuses.
All 19 individuals (from which data could be gathered) exhibited substantial daily variation in body temperature. Several intriguing results emerged such as the counter-intuitive finding that the mammals’ body temperature fluctuates more indoors than outdoors. Furthermore, three females (out of 12) were found to have offspring with atypical skeletons, and two of these mothers presented an extremely low internal temperature early in pregnancy. Additionally, genetically identical quadruplets differed skeletally among themselves within two litters.
Results are not yet definitive about the relationship of temperature during development and vertebral count in Dasypus novemcinctus. However, Knight et al. [8] demonstrated that nine-banded armadillos survive with high daily internal temperature fluctuations and successfully bring to term offspring which vary in skeletal morphology among and within genetically identical litters despite major temperature extremes.

References

[1] Hautier L, Weisbecker V, Sánchez-Villagra MR, Goswami A, Asher RJ (2010) Skeletal development in sloths and the evolution of mammalian vertebral patterning. Proceedings of the National Academy of Sciences, 107, 18903–18908. doi: 10.1073/pnas.1010335107
[2] Jordan, D.S. (1892) Relations of temperature to vertebrae among fishes. Proceedings of the United States National Museum, 1891, 107-120. doi: 10.5479/si.00963801.14-845.107
[3] Tibblin P, Berggren H, Nordahl O, Larsson P, Forsman A (2016) Causes and consequences of intra-specific variation in vertebral number. Scientific Reports, 6, 1–12. doi: 10.1038/srep26372
[4] Peabody RB, Brodie ED (1975) Effect of temperature, salinity and photoperiod on the number of trunk vertebrae in Ambystoma maculatum. Copeia, 1975, 741–746. doi: 10.2307/1443326
[5] Lindsey CC, Moodie GEE (1967) The effect of incubation temperature on vertebral count in the chicken. Canadian Journal of Zoology, 45, 891–892. doi: 10.1139/z67-099
[6] Galis F, Dooren TJMV, Feuth JD, Metz JAJ, Witkam A, Ruinard S, Steigenga MJ, Wunaendts LCD (2006) Extreme selection in humans against homeotic transformations of cervical vertebrae. Evolution, 60, 2643–2654. doi: 10.1111/j.0014-3820.2006.tb01896.x
[7] Buchholtz EA, Stepien CC (2009) Anatomical transformation in mammals: developmental origin of aberrant cervical anatomy in tree sloths. Evolution and Development, 11, 69–79. doi: 10.1111/j.1525-142X.2008.00303.x
[8] Knight F, Connor C, Venkataramanan R, Asher RJ. (2020). Body temperatures, life history, and skeletal morphology in the nine-banded armadillo (Dasypus novemcinctus). PCI-Ecology. doi: 10.17863/CAM.50971
[9] McNab BK (1980) Energetics and the limits to a temperate distribution in armadillos. Journal of Mammalogy, 61, 606–627. doi: 10.2307/1380307
[10] Asher RJ, Lin KH, Kardjilov N, Hautier L (2011) Variability and constraint in the mammalian vertebral column. Journal of Evolutionary Biology, 24, 1080–1090. doi: 10.1111/j.1420-9101.2011.02240.x

Body temperatures, life history, and skeletal morphology in the nine-banded armadillo (Dasypus novemcinctus)Frank Knight, Cristin Connor, Ramji Venkataramanan, Robert J. Asher<p>The nine banded armadillo (*Dasypus novemcinctus*) is the only xenarthran mammal to have naturally expanded its range into the middle latitudes of the USA. It is not known to hibernate, but has been associated with unusually labile core body te...Behaviour & Ethology, Evolutionary ecology, Life history, Physiology, ZoologyMar Sobral2019-11-22 22:57:31 View