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18 Apr 2024
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Insights on the effect of mega-carcass abundance on the population dynamics of a facultative scavenger predator and its prey

Unveiling the influence of carrion pulses on predator-prey dynamics

Recommended by ORCID_LOGO based on reviews by Eli Strauss and 1 anonymous reviewer

Most, if not all, predators consume carrion in some circumstances (Sebastián-Gonzalez et al. 2023). Consequently, significant fluctuations in carrion availability can impact predator-prey dynamics by altering the ratio of carrion to live prey in the predators' diet (Roth 2003). Changes in carrion availability may lead to reduced predation when carrion is more abundant (hypo-predation) and intensified predation if predator populations surge in response to carrion influxes but subsequently face scarcity (hyper-predation), (Moleón et al. 2014, Mellard et al. 2021). However, this relationship between predation and scavenging is often challenging because of the lack of empirical data.
 
In the study conducted by Sidous et al. (2024), they used a large database on the abundance of spotted hyenas and their prey in Zimbabwe and Multivariate Autoregressive State-Space Models to calculate hyena and prey population densities and trends over a 60-year span. The researchers took advantage of abrupt fluctuations in elephant carcass availability that produced alternating periods of high and low carrion availability related to changing management strategies (i.e., elephant culling and water supply).
 
Interestingly, their analyses reveal a coupling of predator and prey densities over time, but they do not detect an effect of carcass availability on predator and prey dynamics. However, the density of prey and hyena was partially driven by the different temporal periods, suggesting some subtle effects of carrion availability on population trends. While it is acknowledged that other variables likely impact the population dynamics of hyenas and their prey, this is the first attempt to understand the influence of carrion pulses on predator-prey interactions across an extensive temporal scale. I hope this helps to establish a new research line on the effect of large carrion pulses, as this is currently largely understudied, even though the occurrence of carrion pulses, such as mass mortality events, is expected to increase over time (Fey et al. 2015).
 
References
 
Courchamp, F. et al. 2000. Rabbits killing birds: modelling the hyperpredation process. J. Anim. Ecol. 69: 154-164.
https://doi.org/10.1046/j.1365-2656.2000.00383.x

Fey, S. B. et al. 2015. Recent shifts in the occurrence, cause, and magnitude of animal mass mortality events. PNAS 112: 1083-1088.
https://doi.org/10.1073/pnas.1414894112
 
Mellard, J. P. et al. 2021. Effect of scavenging on predation in a food web. Ecol. Evol. 11: 6742- 6765.
https://doi.org/10.1002/ece3.7525

Moleón, M. et al. 2014. Inter-specific interactions linking predation and scavenging in terrestrial vertebrate assemblages. Biol. Rev. Camb. Philos. Soc. 89: 1042-1054.
https://doi.org/10.1111/brv.12097
 
Roth, J. 2003. Variability in marine resources affects arctic fox population dynamics. J. Anim. Ecol. 72: 668-676.
https://doi.org/10.1046/j.1365-2656.2003.00739.x
 
Sebastián-González, E. et al. 2023. The underestimated role of carrion in diet studies. Global Ecol. Biogeogr. 32: 1302-1310.
https://doi.org/10.1111/geb.13707
 
Sidous, M. et al. 2024. Insights on the effect of mega-carcass abundance on 1 the population dynamics of a facultative scavenger predator and its prey. bioRxiv, ver. 2 peer-reviewed and recommended by PCI Ecology.
https://doi.org/10.1101/2023.11.08.566247

Insights on the effect of mega-carcass abundance on the population dynamics of a facultative scavenger predator and its preyMellina Sidous; Sarah Cubaynes; Olivier Gimenez; Nolwenn Drouet-Hoguet; Stephane Dray; Loic Bollache; Daphine Madhlamoto; Nobesuthu Adelaide Ngwenya; Herve Fritz; Marion Valeix<p>The interplay between facultative scavenging and predation has gained interest in the last decade. The prevalence of scavenging induced by the availability of large carcasses may modify predator density or behaviour, potentially affecting prey....Community ecologyEsther Sebastián González Eli Strauss2023-11-14 15:27:16 View
29 Mar 2021
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Temperature predicts the maximum tree-species richness and water and frost shape the residual variation

New light on the baseline importance of temperature for the origin of geographic species richness gradients

Recommended by based on reviews by Rafael Molina-Venegas and 2 anonymous reviewers

Whether environmental conditions –in particular energy and water availability– are sufficient to account for species richness gradients (e.g. Currie 1991), or the effects of other biotic and historical or regional factors need to be considered as well (e.g. Ricklefs 1987), was the subject of debate during the 1990s and 2000s (e.g. Francis & Currie 2003; Hawkins et al. 2003, 2006; Currie et al. 2004; Ricklefs 2004). The metabolic theory of ecology (Brown et al. 2004) provided a solid and well-rooted theoretical support for the preponderance of energy as the main driver for richness variations. As any good piece of theory, it provided testable predictions about the sign and shape (i.e. slope) of the relationship between temperature –a key aspect of ambient energy– and species richness. However, these predictions were not supported by empirical evaluations (e.g. Kreft & Jetz 2007; Algar et al. 2007; Hawkins et al. 2007a), as the effects of a myriad of other environmental gradients, regional factors and evolutionary processes result in a wide variety of richness–temperature responses across different groups and regions (Hawkins et al. 2007b; Hortal et al. 2008). So, in a textbook example of how good theoretical work helps advancing science even if proves to be (partially) wrong, the evaluation of this aspect of the metabolic theory of ecology led to current understanding that, while species richness does respond to current climatic conditions, many other ecological, evolutionary and historical factors do modify such response across scales (see, e.g., Ricklefs 2008; Hawkins 2008; D’Amen et al. 2017). And the kinetic model linking mean annual temperature and species richness (Allen et al. 2002; Brown et al. 2004) was put aside as being, perhaps, another piece of the puzzle of the origin of current diversity gradients.

Segovia (2021) puts together an elegant way of reinvigorating this part of the metabolic theory of ecology. He uses quantile regressions to model just the upper parts of the relationship between species richness and mean annual temperature, rather than modelling its central tendency through the classical linear regression family of methods –as was done in the past. This assumes that the baseline effect of ambient energy does produce the negative linear relationship between richness and temperature predicted by the kinetic model (Allen et al. 2002), but also that this effect only poses an upper limit for species richness, and the effects of other factors may result in lower levels of species co-occurrence, thus producing a triangular rather than linear relationship. The results of Segovia’s simple and elegant analytical design show unequivocally that the predictions of the kinetic model become progressively more explanatory towards the upper quartiles of the relationship between species richness and temperature along over 10,000 tree local inventories throughout the Americas, reaching over 70% of explanatory power for the upper 5% of the relationship (i.e. the 95% quantile). This confirms to a large extent his reformulation of the predictions of the kinetic model. 

Further, the neat study from Segovia (2021) also provides evidence confirming that the well-known spatial non-stationarity in the richness–temperature relationship (see Cassemiro et al. 2007) also applies to its upper-bound segment. Both the explanatory power and the slope of the relationship in the 95% upper quantile vary widely between biomes, reaching values similar to the predictions of the kinetic model only in cold temperate environments ­–precisely where temperature becomes more important than water availability as a constrain to plant life (O’Brien 1998; Hawkins et al. 2003). Part of these variations are indeed related with changes in water deficit and number of frost days along the XXth Century, as shown by the residuals of this paper (Segovia 2021) and a more detailed separate study (Segovia et al. 2020). This pinpoints the importance of the relative balance between water and energy as two of the main climatic factors constraining species diversity gradients, confirming the value of hypotheses that date back to Humboldt’s work (see Hawkins 2001, 2008). There is however a significant amount of unexplained variation in Segovia’s analyses, in particular in the progressive departure of the predictions of the kinetic model as we move towards the tropics, or downwards along the lower quantiles of the richness–temperature relationship. This calls for a deeper exploration of the factors that modify the baseline relationship between richness and energy, opening a new avenue for the macroecological investigation of how different forces and processes shape up geographical diversity gradients beyond the mere energetic constrains imposed by the basal limitations of multicellular life on Earth.

References

Algar, A.C., Kerr, J.T. and Currie, D.J. (2007) A test of Metabolic Theory as the mechanism underlying broad-scale species-richness gradients. Global Ecology and Biogeography, 16, 170-178. doi: https://doi.org/10.1111/j.1466-8238.2006.00275.x

Allen, A.P., Brown, J.H. and Gillooly, J.F. (2002) Global biodiversity, biochemical kinetics, and the energetic-equivalence rule. Science, 297, 1545-1548. doi: https://doi.org/10.1126/science.1072380

Brown, J.H., Gillooly, J.F., Allen, A.P., Savage, V.M. and West, G.B. (2004) Toward a metabolic theory of ecology. Ecology, 85, 1771-1789. doi: https://doi.org/10.1890/03-9000

Cassemiro, F.A.d.S., Barreto, B.d.S., Rangel, T.F.L.V.B. and Diniz-Filho, J.A.F. (2007) Non-stationarity, diversity gradients and the metabolic theory of ecology. Global Ecology and Biogeography, 16, 820-822. doi: https://doi.org/10.1111/j.1466-8238.2007.00332.x

Currie, D.J. (1991) Energy and large-scale patterns of animal- and plant-species richness. The American Naturalist, 137, 27-49. doi: https://doi.org/10.1086/285144

Currie, D.J., Mittelbach, G.G., Cornell, H.V., Field, R., Guegan, J.-F., Hawkins, B.A., Kaufman, D.M., Kerr, J.T., Oberdorff, T., O'Brien, E. and Turner, J.R.G. (2004) Predictions and tests of climate-based hypotheses of broad-scale variation in taxonomic richness. Ecology Letters, 7, 1121-1134. doi: https://doi.org/10.1111/j.1461-0248.2004.00671.x

D'Amen, M., Rahbek, C., Zimmermann, N.E. and Guisan, A. (2017) Spatial predictions at the community level: from current approaches to future frameworks. Biological Reviews, 92, 169-187. doi: https://doi.org/10.1111/brv.12222

Francis, A.P. and Currie, D.J. (2003) A globally consistent richness-climate relationship for Angiosperms. American Naturalist, 161, 523-536. doi: https://doi.org/10.1086/368223

Hawkins, B.A. (2001) Ecology's oldest pattern? Trends in Ecology & Evolution, 16, 470. doi: https://doi.org/10.1016/S0169-5347(01)02197-8 

Hawkins, B.A. (2008) Recent progress toward understanding the global diversity gradient. IBS Newsletter, 6.1, 5-8. https://escholarship.org/uc/item/8sr2k1dd

Hawkins, B.A., Field, R., Cornell, H.V., Currie, D.J., Guégan, J.-F., Kaufman, D.M., Kerr, J.T., Mittelbach, G.G., Oberdorff, T., O'Brien, E., Porter, E.E. and Turner, J.R.G. (2003) Energy, water, and broad-scale geographic patterns of species richness. Ecology, 84, 3105-3117. doi: https://doi.org/10.1890/03-8006

Hawkins, B.A., Diniz-Filho, J.A.F., Jaramillo, C.A. and Soeller, S.A. (2006) Post-Eocene climate change, niche conservatism, and the latitudinal diversity gradient of New World birds. Journal of Biogeography, 33, 770-780. doi: https://doi.org/10.1111/j.1365-2699.2006.01452.x

Hawkins, B.A., Albuquerque, F.S., Araújo, M.B., Beck, J., Bini, L.M., Cabrero-Sañudo, F.J., Castro Parga, I., Diniz-Filho, J.A.F., Ferrer-Castán, D., Field, R., Gómez, J.F., Hortal, J., Kerr, J.T., Kitching, I.J., León-Cortés, J.L., et al. (2007a) A global evaluation of metabolic theory as an explanation for terrestrial species richness gradients. Ecology, 88, 1877-1888. doi:10.1890/06-1444.1. doi: https://doi.org/10.1890/06-1444.1

Hawkins, B.A., Diniz-Filho, J.A.F., Bini, L.M., Araújo, M.B., Field, R., Hortal, J., Kerr, J.T., Rahbek, C., Rodríguez, M.Á. and Sanders, N.J. (2007b) Metabolic theory and diversity gradients: Where do we go from here? Ecology, 88, 1898–1902. doi: https://doi.org/10.1890/06-2141.1

Hortal, J., Rodríguez, J., Nieto-Díaz, M. and Lobo, J.M. (2008) Regional and environmental effects on the species richness of mammal assemblages. Journal of Biogeography, 35, 1202–1214. doi: https://doi.org/10.1111/j.1365-2699.2007.01850.x

Kreft, H. and Jetz, W. (2007) Global patterns and determinants of vascular plant diversity. Proceedings of the National Academy of Sciences USA, 104, 5925-5930. doi: https://doi.org/10.1073/pnas.0608361104

O'Brien, E. (1998) Water-energy dynamics, climate, and prediction of woody plant species richness: an interim general model. Journal of Biogeography, 25, 379-398. doi: https://doi.org/10.1046/j.1365-2699.1998.252166.x

Ricklefs, R.E. (1987) Community diversity: Relative roles of local and regional processes. Science, 235, 167-171. doi: https://doi.org/10.1126/science.235.4785.167

Ricklefs, R.E. (2004) A comprehensive framework for global patterns in biodiversity. Ecology Letters, 7, 1-15. doi: https://doi.org/10.1046/j.1461-0248.2003.00554.x

Ricklefs, R.E. (2008) Disintegration of the ecological community. American Naturalist, 172, 741-750. doi: https://doi.org/10.1086/593002

Segovia, R.A. (2021) Temperature predicts the maximum tree-species richness and water and frost shape the residual variation. bioRxiv, 836338, ver. 4 peer-reviewed and recommended by Peer community in Ecology. doi: https://doi.org/10.1101/836338

Segovia, R.A., Pennington, R.T., Baker, T.R., Coelho de Souza, F., Neves, D.M., Davis, C.C., Armesto, J.J., Olivera-Filho, A.T. and Dexter, K.G. (2020) Freezing and water availability structure the evolutionary diversity of trees across the Americas. Science Advances, 6, eaaz5373. doi: https://doi.org/10.1126/sciadv.aaz5373

Temperature predicts the maximum tree-species richness and water and frost shape the residual variationRicardo A. Segovia<p>The kinetic hypothesis of biodiversity proposes that temperature is the main driver of variation in species richness, given its exponential effect on biological activity and, potentially, on rates of diversification. However, limited support fo...Biodiversity, Biogeography, Botany, Macroecology, Species distributionsJoaquín Hortal2019-11-10 20:56:40 View
08 Jan 2020
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Studies of NH4+ and NO3- uptake ability of subalpine plants and resource-use strategy identified by their functional traits

Nitrate or not nitrate. That is the question

Recommended by based on reviews by Vincent Maire and 1 anonymous reviewer

The article by Legay et al. [1] addresses two main issues: the links between belowground and aboveground plant traits and the links between plant strategies (as defined by these traits) and the capacity to absorb nitrate and ammonium. I recommend this work because these are important and current issues. The literature on plant traits is extremely rich and the existence of a leaf economic spectrum linked to a gradient between conservative and acquisitive plants is now extremely well established [2-3]. Many teams are now working on belowground traits and possible links with the aboveground gradients [4-5]. It seems indeed that there is a root economic spectrum but this spectrum is apparently less pronounced than the leaf economic spectrum. The existence of links between the two spectrums are still controversial and are likely not universal as suggested by discrepant results and after all a plant could have a conservative strategy aboveground and an acquisitive strategy belowground (or vice-versa) because, indeed, constraints are different belowground and aboveground (for example because in given ecosystem/vegetation type light may be abundant but not water or mineral nutrients). The various results obtained also suggest that we do not full understand the diversity of belowground strategies, what is at stake with these strategies, and the links with root characteristics.
Each time I give a conference on the work we are carrying out on African grasses that likely absorb ammonium preferentially because they inhibit nitrification [6-7], somebody asks me a question about the fact that plant essentially absorb nitrate because ammonium is toxic and nitrate more available in the soil. The present article confirms that this is not the case and that, though there are currently some teams working on the subject, we do not really know for the moment whether plants absorb nitrate or ammonium, in which proportion, how plastic this proportion is within individuals and within species. This subject seems to me crucial because it is linked to (1) the capacity of ecosystems to conserve nitrogen [8], because nitrate, much more than ammonium, goes out of ecosystems through leaching and denitrification, (2) to carbon cycling and plant energy budget because absorbing nitrate requires spending mucho more energy than absorbing ammonium because nitrate must be reduced before being incorporated in plant biomass, which is very energy costly. These two issues are naturally very relevant to develop efficient cropping systems in terms of carbon and nitrogen.
Interestingly, the present article, comparing three grass species in different sites, suggests that there is no trade-off between the absorption of nitrate and ammonium: more acquisitive individuals tend to absorb more ammonium and nitrate. This is contrary to hypotheses we made to predict the outcome of competition between plants absorbing nitrate and ammonium in different proportions [9] but should be tested in the future comparing many different types of plants. The results also suggest that more conservative plants absorb relatively more ammonium, which makes sense because this allows them to spare the energy necessary to reduce nitrate. This leads to the question of the effect of these strategies on nitrogen retention within the ecosystem. If nitrification is high (low), absorbing ammonium is not efficient and likely leads to high (low) nitrogen losses. This should be tested in the future. Moreover, the authors have measured the absorption of nitrate and ammonium through measurements at the root scale on cut roots. This should be complemented by measurements at the whole plant scale.

References

[1] Legay, N., Grassein, F., Arnoldi, C., Segura, R., Laîné, P., Lavorel, S. and Clément, J.-C. (2020). Studies of NH4+ and NO3- uptake ability of subalpine plants and resource-use strategy identified by their functional traits. bioRxiv, 372235, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/372235
[2] Shipley, B., Lechowicz, M.J., Wright, I. & Reich, P.B. (2006) Fundamental trade-offs generating the worldwide leaf economics spectrum. Ecology, 87, 535-541. doi: 10.1890/05-1051
[3] Reich, P.B. (2014) The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto. J. Ecol., 102, 275-301. doi: 10.1111/1365-2745.12211
[4] Maire, V., Gross, N., Pontes, L.D.S., Picon-Cochard, C. & Soussana, J.F. (2009) Trade-off between root nitrogen acquisition and shoot nitrogen utilization across 13 co-occurring pasture grass species. Func. Ecol., 23, 668-679. doi: 10.1111/j.1365-2435.2009.01557.x
[5] Roumet, C., Birouste, M., Picon-Cochard, C., Ghestem, M., Osman, N., Vrignon-Brenas, S., Cao, K.F. & Stokes, A. (2016) Root structure-function relationships in 74 species: evidence of a root economics spectrum related to carbon economy. New. Phytol., 210, 815-826. doi: 10.1111/nph.13828
[6] Lata, J.-C., Degrange, V., Raynaud, X., Maron, P.-A., Lensi, R. & Abbadie, L. (2004) Grass populations control nitrification in savanna soils. Funct. Ecol., 18, 605-611. doi: 10.1111/j.0269-8463.2004.00880.x
[7] Srikanthasamy, T., Leloup, J., N’Dri, A.B., Barot, S., Gervaix, J., Koné, A.W., Koffi, K.F., Le Roux, X., Raynaud, X. & Lata, J.-C. (2018) Contrasting effects of grasses and trees on microbial N-cycling in an African humid savanna. Soil Biol. Biochem., 117, 153-163. doi: 10.1016/j.soilbio.2017.11.016
[8] Boudsocq, S., Lata, J.C., Mathieu, J., Abbadie, L. & Barot, S. (2009) Modelling approach to analyze the effects of nitrification inhibition on primary production. Func. Ecol., 23, 220-230. doi: 10.1111/j.1365-2435.2008.01476.x
[9] Boudsocq, S., Niboyet, A., Lata, J.-C., Raynaud, X., Loeuille, N., Mathieu, J., Blouin, M., Abbadie, L. & Barot, S. (2012) Plant preference for ammonium versus nitrate: a neglected determinant of ecosystem functioning? Am. Nat., 180, 60-69. doi: 10.1086/665997

Studies of NH4+ and NO3- uptake ability of subalpine plants and resource-use strategy identified by their functional traitsLegay Nicolas, Grassein Fabrice, Arnoldi Cindy, Segura Raphaël, Laîné Philippe, Lavorel Sandra, Clément Jean-Christophe<p>The leaf economics spectrum (LES) is based on a suite of leaf traits related to plant functioning and ranges from resource-conservative to resource-acquisitive strategies. However, the relationships with root traits, and the associated belowgro...Community ecology, Physiology, Terrestrial ecologySébastien Barot2018-07-19 14:22:28 View
06 Mar 2020
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The persistence in time of distributional patterns in marine megafauna impacts zonal conservation strategies

The importance of spatio-temporal dynamics on MPA's design

Recommended by based on reviews by Ana S. L. Rodrigues and 1 anonymous reviewer

Marine protected areas (MPA) have arisen as the main approach for conservation of marine species. Fishes, marine mammals and birds can be conservation targets that justify the implementation of these areas. However, MPAs undergo many of the problems faced by their terrestrial equivalent. One of the major concerns is that these conservation areas are spatially constrained, by logistic reasons, and many times these constraints caused that key areas for the species (reproductive sites, refugees, migration) fall outside the limits, making conservation efforts even more difficult. Lambert et al. [1] evaluate at what point the Bay of Biscay MPA contains key ecological areas for several emblematic species. The evaluation incorporated a spatio-temporal dimension. To evaluate these ideas, authors evaluate two population descriptors: aggregation and persistence of several species of cetaceans and seabirds.
The authors determined that despite the MPA contains key areas for some species, for many others the key areas fall outside the MPA (aggregation sites) or observed aggregation sites are poorly persistent in time. They found that aggregation and persistence behave as two uncorrelated descriptors of the spatio-temporal distribution of populations. Variability of both characteristics was species-specific, but in all cases the message is clear: both features must be taken into account to evaluate the effectiveness of MPAs. Both conclusions pointed out to the difficulties that a strategy based on MPAs could face when the target are those species with low aggregation or those where key sites show low persistence in time.
Conceptually, the manuscript and its conclusions are very interesting, specially its recommendation of including temporal variability of species abundances and aggregation in the design of MPAs. However, despite the clear biological importance of persistence and aggregation of the conservation targets for the design of a MPA, its implementation will still be an extremely complex task. A first constraint is that important areas for one species could not be relevant for others, making the design of the MPA difficult because the more target species we include the larger the area needed for the MPA. As a consequence, the management of the MPA turns difficult and expensive as the area increases. These increased costs could be a key point for accepting/rejecting the implementation of these MPAs for governments. Also larger areas could imply highest level of conflict with local communities or stakeholders. In many the inclusion inside MPAs of areas with traditional social or economic use will be a major source of conflict with the people.
Despite these difficulties, the results of Lambert et al. [1] give us a key message for improving MPA’s design. The best strategy for including their conclusions in the effective implementation of these areas will be the next target in conservation research.

References

[1] Lambert, C., Dorémus, G. and V. Ridoux (2020) The persistence in time of distributional patterns in marine megafauna impacts zonal conservation strategies. bioRxiv, 790634, ver. 3 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/790634

The persistence in time of distributional patterns in marine megafauna impacts zonal conservation strategiesCharlotte Lambert, Ghislain Dorémus, Vincent Ridoux<p>The main type of zonal conservation approaches corresponds to Marine Protected Areas (MPAs), which are spatially defined and generally static entities aiming at the protection of some target populations by the implementation of a management pla...Conservation biology, Habitat selection, Species distributionsSergio Estay2019-10-03 08:47:17 View
29 Dec 2018
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The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web

From deserts to avocado orchards - understanding realized trophic interactions in communities

Recommended by based on reviews by Owen Petchey and 2 anonymous reviewers

The late eminent ecologist Gary Polis once stated that “most catalogued food-webs are oversimplified caricatures of actual communities” and are “grossly incomplete representations of communities in terms of both diversity and trophic connections.” Not content with that damning indictment, he went further by railing that “theorists are trying to explain phenomena that do not exist” [1]. The latter critique might have been push back for Robert May´s ground-breaking but ultimately flawed research on the relationship between food-web complexity and stability [2]. Polis was a brilliant ecologist, and his thinking was clearly influenced by his experiences researching desert food webs. Those food webs possess an uncommon combination of properties, such as frequent omnivory, cannibalism, and looping; high linkage density (L/S); and a nearly complete absence of apex consumers, since few species completely lack predators or parasites [3]. During my PhD studies, I was lucky enough to visit Joshua Tree National Park on the way to a conference in New England, and I could immediately see the problems posed by desert ecosystems. At the time, I was ruminating on the “harsh-benign” hypothesis [4], which predicts that the relative importance of abiotic and biotic forces should vary with changes in local environmental conditions (from harsh to benign). Specifically, in more “harsh” environments, abiotic factors should determine community composition whilst weakening the influence of biotic interactions. However, in the harsh desert environment I saw first-hand evidence that species interactions were not diminished; if anything, they were strengthened. Teddy-bear chollas possessed murderously sharp defenses to protect precious water, creosote bushes engaged in belowground “chemical warfare” (allelopathy) to deter potential competitors, and rampant cannibalism amongst scorpions drove temporal and spatial ontogenetic niche partitioning. Life in the desert was hard, but you couldn´t expect your competition to go easy on you.
If that experience colored my thinking about nature’s reaction to a capricious environment, then the seminal work by Robert Paine on the marine rocky shore helped further cement the importance of biotic interactions. The insights provided by Paine [5] brings us closer to the research reported in the preprint “The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web” [6], given that the authors in that study hold the environment constant and test the interactions between different permutations of a simple community. Paine [5] was able to elegantly demonstrate using the chief protagonist Pisaster ochraceus (a predatory echinoderm also known as the purple sea star) that a keystone consumer could exert strong top-down control that radically reshaped the interactions amongst other community members. What was special about this study was that the presence of Pisaster promoted species diversity by altering competition for space by sedentary species, providing a rare example of an ecological network experiment combining trophic and non-trophic interactions. Whilst there are increasing efforts to describe these interactions (e.g., competition and facilitation) in multiplex networks [7], the authors of “The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web” [6] have avoided strictly competitive interactions for the sake of simplicity. They do focus on two trophic forms of competition, namely intraguild predation and apparent competition. These two interaction motifs, along with prey switching are relevant to my own research on the influence of cross-ecosystem prey subsidies to receiving food webs [8]. In particular, the apparent competition motif may be particularly important in the context of emergent adult aquatic insects as prey subsidies to terrestrial consumers. This was demonstrated by Henschel et al. [9] where the abundances of emergent adult aquatic midges in riparian fields adjacent to a large river helped stimulate higher abundances of spiders and lower abundances of herbivorous leafhoppers, leading to a trophic cascade. The aquatic insects had a bottom-up effect on spiders and this subsidy facilitated a top-down effect that cascaded from spiders to leafhoppers to plants. The apparent competition motif becomes relevant because the aquatic midges exerted a negative indirect effect on leafhoppers mediated through their common arachnid predators.
In the preprint “The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web” [6], the authors have described different permutations of a simple mite community present in avocado orchards (Persea americana). This community comprises of two predators (Euseius stipulatus and Neoseiulus californicus), one herbivore as shared prey (Oligonychus perseae), and pollen of Carpobrotus edulis as alternative food resource, with the potential for the intraguild predation and apparent competition interaction motifs to be expressed. The authors determined that these motifs should be realized based off pairwise feeding trials. It is common for food-web researchers to depict potential food webs, which contain all species sampled and all potential trophic links based on laboratory feeding trials (as demonstrated here) or from observational data and literature reviews [10]. In reality, not all these potential feeding links are realized because species may partition space and time, thus driving alternative food-web architectures. In “The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web” [6], the authors are able to show that placing species in combinations that should yield more complex interaction motifs based off pairwise feeding trials fails to deliver – the predators revert to their preferred prey resulting in modular and simple trophic chains to be expressed. Whilst these realized interaction motifs may be stable, there might also be a tradeoff with function by yielding less top-down control than desirable when considering the potential for ecosystem services such as pest management. These are valuable insights, although it should be noted that here the fundamental niche is described in a strictly Eltonian sense as a trophic role [11]. Adding additional niche dimensions (sensu [12]), such as a thermal gradient could alter the observed interactions, although it might be possible to explain these contingencies through metabolic and optimal foraging theory combined with species traits. Nonetheless, the results of these experiments further demonstrate the need for ecologists to cross-validate theory with empirical approaches to develop more realistic and predictive food-web models, lest they invoke the wrath of Gary Polis´ ghost by “trying to explain phenomena that do not exist”.

References

[1] Polis, G. A. (1991). Complex trophic interactions in deserts: an empirical critique of food-web theory. The American Naturalist, 138(1), 123-155. doi: 10.1086/285208
[2] May, R. M. (1973). Stability and complexity in model ecosystems. Princeton University Press, Princeton, NJ, USA
[3] Dunne, J. A. (2006). The network structure of food webs. In Pascual, M., & Dunne, J. A. (eds) Ecological Networks: Linking Structure to Dynamics in Food Webs. Oxford University Press, New York, USA, 27-86
[4] Menge, B. A., & Sutherland, J. P. (1976). Species diversity gradients: synthesis of the roles of predation, competition, and temporal heterogeneity. The American Naturalist, 110(973), 351-369. doi: 10.1086/283073
[5] Paine, R. T. (1966). Food web complexity and species diversity. The American Naturalist, 100(910), 65-75. doi: 10.1086/282400
[6] Torres-Campos, I., Magalhães, S., Moya-Laraño, J., & Montserrat, M. (2018). The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web. bioRxiv, 324178, ver. 5 peer-reviewed and recommended by PCI Ecol. doi: 10.1101/324178
[7] Kéfi, S., Berlow, E. L., Wieters, E. A., Joppa, L. N., Wood, S. A., Brose, U., & Navarrete, S. A. (2015). Network structure beyond food webs: mapping non‐trophic and trophic interactions on Chilean rocky shores. Ecology, 96(1), 291-303. doi: 10.1890/13-1424.1
[8] Burdon, F. J., & Harding, J. S. (2008). The linkage between riparian predators and aquatic insects across a stream‐resource spectrum. Freshwater Biology, 53(2), 330-346. doi: 10.1111/j.1365-2427.2007.01897.x
[9] Henschel, J. R., Mahsberg, D., & Stumpf, H. (2001). Allochthonous aquatic insects increase predation and decrease herbivory in river shore food webs. Oikos, 93(3), 429-438. doi: 10.1034/j.1600-0706.2001.930308.x
[10] Brose, U., Pavao-Zuckerman, M., Eklöf, A., Bengtsson, J., Berg, M. P., Cousins, S. H., Mulder, C., Verhoef, H. A., & Wolters, V. (2005). Spatial aspects of food webs. In de Ruiter, P., Wolters, V., Moore, J. C., & Melville-Smith, K. (eds) Dynamic Food Webs. vol 3. Academic Press, Burlington, 463-469
[11] Elton, C. (1927). Animal Ecology. Sidgwick and Jackson, London, UK
[12] Hutchinson, G. E. (1957). Concluding Remarks. Cold Spring Harbor Symposia on Quantitative Biology, 22, 415-427. doi: 10.1101/sqb.1957.022.01.039

The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food webInmaculada Torres-Campos, Sara Magalhães, Jordi Moya-Laraño, Marta Montserrat<p>The mathematical theory describing small assemblages of interacting species (community modules or motifs) has proved to be essential in understanding the emergent properties of ecological communities. These models use differential equations to ...Community ecology, Experimental ecologyFrancis John Burdon2018-05-16 19:34:10 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
17 May 2023
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Distinct impacts of food restriction and warming on life history traits affect population fitness in vertebrate ectotherms

Effect of food conditions on the Temperature-Size Rule

Recommended by based on reviews by Wolf Blanckenhorn and Wilco Verberk

Temperature-size rule (TSR) is a phenomenon of plastic changes in body size in response to temperature, originally observed in more than 80% of ectothermic organisms representing various groups (Atkinson 1994). In particular, ectotherms were observed to grow faster and reach smaller size at higher temperature and grow slower and achieve larger size at lower temperature. This response has fired the imagination of researchers since its invention, due to its counterintuitive pattern from an evolutionary perspective (Berrigan and Charnov 1994). The main question to be resolved is: why do organisms grow fast and achieve smaller sizes under more favourable conditions (= relatively higher temperature), while they grow longer and achieve larger sizes under less favourable conditions (relatively lower temperature), if larger size means higher fitness, while longer development may be risky? 

This evolutionary conundrum still awaits an ultimate explanation (Angilletta Jr et al. 2004; Angilletta and Dunham 2003; Verberk et al. 2021). Although theoretical modelling has shown that such a growth pattern can be achieved as a response to temperature alone, with a specific combination of energetic parameters and external mortality (Kozłowski et al. 2004), it has been suggested that other temperature-dependent environmental variables may be the actual drivers of this pattern. One of the most frequently invoked variable is the relative oxygen availability in the environment (e.g., Atkinson et al. 2006; Audzijonyte et al. 2019; Verberk et al. 2021; Woods 1999), which decreases with temperature increase. Importantly, this effect is more pronounced in aquatic systems (Forster et al. 2012). However, other temperature-dependent parameters are also being examined in the context of their possible effect on TSR induction and strength.

Food availability is among the interfering factors in this regard. In aquatic systems, nutritional conditions are generally better at higher temperature, while a range of relatively mild thermal conditions is considered. However, there are no conclusive results so far on how nutritional conditions affect the plastic body size response to acute temperature changes. A study by Bazin et al. (2023) examined this particular issue, the effects of food and temperature on TSR, in medaka fish. An important value of the study was to relate the patterns found to fitness. This is a rare and highly desirable approach since evolutionary significance of any results cannot be reliably interpreted unless shown as expressed in light of fitness. 

The authors compared the body size of fish kept at 20°C and 30°C under conditions of food abundance or food restriction. The results showed that the TSR (smaller body size at 30°C compared to 20°C) was observed in both food treatments, but the effect was delayed during fish development under food restriction. Regarding the relevance to fitness, increased temperature resulted in more eggs laid but higher mortality, while food restriction increased survival but decreased the number of eggs laid in both thermal treatments. Overall, food restriction seemed to have a more severe effect on development at 20°C than at 30°C, contrary to the authors’ expectations. 

I found this result particularly interesting. One possible interpretation, also suggested by the authors, is that the relative oxygen availability, which was not controlled for in this study, could have affected this pattern. According to theoretical predictions confirmed in quite many empirical studies so far, oxygen restriction is more severe at higher temperatures. Perhaps for these particular two thermal treatments and in the case of the particular species studied, this restriction was more severe for organismal performance than the food restriction. This result is an example that all three variables, temperature, food and oxygen, should be taken into account in future studies if the interrelationship between them is to be understood in the context of TSR. It also shows that the reasons for growing smaller in warm may be different from those for growing larger in cold, as suggested, directly or indirectly, in some previous studies (Hessen et al. 2010; Leiva et al. 2019). 

Since medaka fish represent predatory vertebrates, the results of the study contribute to the issue of global warming effect on food webs, as the authors rightly point out. This is an important issue because the general decrease in the size or organisms in the aquatic environment with global warming is a fact (e.g., Daufresne et al. 2009), while the question of how this might affect entire communities is not trivial to resolve (Ohlberger 2013). 

REFERENCES

Angilletta Jr, M. J., T. D. Steury & M. W. Sears, 2004. Temperature, growth rate, and body size in ectotherms: fitting pieces of a life–history puzzle. Integrative and Comparative Biology 44:498-509. https://doi.org/10.1093/icb/44.6.498

Angilletta, M. J. & A. E. Dunham, 2003. The temperature-size rule in ectotherms: Simple evolutionary explanations may not be general. American Naturalist 162(3):332-342. https://doi.org/10.1086/377187

Atkinson, D., 1994. Temperature and organism size – a biological law for ectotherms. Advances in Ecological Research 25:1-58. https://doi.org/10.1016/S0065-2504(08)60212-3

Atkinson, D., S. A. Morley & R. N. Hughes, 2006. From cells to colonies: at what levels of body organization does the 'temperature-size rule' apply? Evolution & Development 8(2):202-214 https://doi.org/10.1111/j.1525-142X.2006.00090.x

Audzijonyte, A., D. R. Barneche, A. R. Baudron, J. Belmaker, T. D. Clark, C. T. Marshall, J. R. Morrongiello & I. van Rijn, 2019. Is oxygen limitation in warming waters a valid mechanism to explain decreased body sizes in aquatic ectotherms? Global Ecology and Biogeography 28(2):64-77 https://doi.org/10.1111/geb.12847

Bazin, S., Hemmer-Brepson, C., Logez, M., Sentis, A. & Daufresne, M. 2023. Distinct impacts of food restriction and warming on life history traits affect population fitness in vertebrate ectotherms. HAL, ver.3  peer-reviewed and recommended by PCI Ecology. https://hal.inrae.fr/hal-03738584v3

Berrigan, D. & E. L. Charnov, 1994. Reaction norms for age and size at maturity in response to temperature – a puzzle for life historians. Oikos 70:474-478. https://doi.org/10.2307/3545787

Daufresne, M., K. Lengfellner & U. Sommer, 2009. Global warming benefits the small in aquatic ecosystems. Proceedings of the National Academy of Sciences USA 106(31):12788-93 https://doi.org/10.1073/pnas.0902080106

Forster, J., A. G. Hirst & D. Atkinson, 2012. Warming-induced reductions in body size are greater in aquatic than terrestrial species. Proceedings of the National Academy of Sciences of the United States of America 109(47):19310-19314. https://doi.org/10.1073/pnas.1210460109

Hessen, D. O., P. D. Jeyasingh, M. Neiman & L. J. Weider, 2010. Genome streamlining and the elemental costs of growth. Trends in Ecology & Evolution 25(2):75-80. https://doi.org/10.1016/j.tree.2009.08.004

Kozłowski, J., M. Czarnoleski & M. Dańko, 2004. Can optimal resource allocation models explain why ectotherms grow larger in cold? Integrative and Comparative Biology 44(6):480-493. https://doi.org/10.1093/icb/44.6.480

Leiva, F. P., P. Calosi & W. C. E. P. Verberk, 2019. Scaling of thermal tolerance with body mass and genome size in ectotherms: a comparison between water- and air-breathers. Philosophical Transactions of the Royal Society B 374:20190035. https://doi.org/10.1098/rstb.2019.0035

Ohlberger, J., 2013. Climate warming and ectotherm body szie - from individual physiology to community ecology. Functional Ecology 27:991-1001. https://doi.org/10.1111/1365-2435.12098

Verberk, W. C. E. P., D. Atkinson, K. N. Hoefnagel, A. G. Hirst, C. R. Horne & H. Siepel, 2021. Shrinking body sizes in response to warming: explanations for the temperature-size rule with special emphasis on the role of oxygen. Biological Reviews 96:247-268. https://doi.org/10.1111/brv.12653

Woods, H. A., 1999. Egg-mass size and cell size: effects of temperature on oxygen distribution. American Zoologist 39:244-252. https://doi.org/10.1093/icb/39.2.244

Distinct impacts of food restriction and warming on life history traits affect population fitness in vertebrate ectothermsSimon Bazin, Claire Hemmer-Brepson, Maxime Logez, Arnaud Sentis, Martin Daufresne<p>The reduction of body size with warming has been proposed as the third universal response to global warming, besides geographical and phenological shifts. Observed body size shifts in ectotherms are mostly attributed to the temperature size rul...Climate change, Experimental ecology, Freshwater ecology, Phenotypic plasticity, Population ecologyAleksandra Walczyńska2022-07-27 09:28:29 View
07 Aug 2023
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Heather pollen is not necessarily a healthy diet for bumble bees

The importance of understanding bee nutrition

Recommended by ORCID_LOGO based on reviews by Cristina Botías and 1 anonymous reviewer

​​Contrasting with the great alarm on bee declines, it is astonishing how little basic biology we know about bees, including on abundant and widespread species that are becoming model species. Plant-pollinator relationships are one of the cornerstones of bee ecology, and researchers are increasingly documenting bees' diets. However, we rarely know which effects feeding on different flowers has on bees' health. This paper (Tourbez et al. 2023) uses an elegant experimental setting to test the effect of heather pollen on bumblebees' (Bombus terrestris) reproductive success. This is a timely question as heather is frequently used by bumblebees, and its nectar has been reported to reduce parasite infections. In fact, it has been suggested that bumblebees can medicate themselves when infected (Richardson et al. 2014), and the pollen of some Asteraceae has been shown to help them fight parasites (Gekière​ et al. 2022). The starting hypothesis is that heather pollen contains flavonoids that might have a similar effect. Unfortunately, Tourbez​ and collaborators do not support this hypothesis, showing a negative effect of heather pollen, in particular its flavonoids, in bumblebees offspring, and an increase in parasite loads when fed on flavonoids. This is important because it challenges the idea that many pollen and nectar chemical compounds might have a medicinal use, and force us to critically analyze the effect of chemical compounds in each particular case. The results open several questions, such as why bumblebees collect heather pollen, or in which concentrations or pollen mixes it is deleterious. A limitation of the study is that it uses micro-colonies, and extrapolating this to real-world conditions is always complex. Understanding bee declines require a holistic approach starting with bee physiology and scaling up to multispecies population dynamics.  

References

Gekière, A., Semay, I., Gérard, M., Michez, D., Gerbaux, P., & Vanderplanck, M. 2022. Poison or Potion: Effects of Sunflower Phenolamides on Bumble Bees and Their Gut Parasite. Biology, 11(4), 545.​ https://doi.org/10.3390/biology11040545

Richardson, L.L., Adler, L.S., Leonard, A.S., Andicoechea, J., Regan, K.H., Anthony, W.E., Manson, J.S., &​ Irwin, R.E. 2015. Secondary metabolites in floral nectar reduce parasite infections in bumblebees. Proceedings of the Royal Society of London B: Biological Sciences 282 (1803), 20142471. https://doi.org/10.1098/rspb.2014.2471

Tourbez, C., Semay, I., Michel, A., Michez, D., Gerbaux, P., Gekière A. & Vanderplanck, M. 2023. Heather pollen is not necessarily a healthy diet for bumble bees. Zenodo, ver 3, reviewed and recommended by PCI Ecology. https://doi.org/10.5281/zenodo.8192036​​

Heather pollen is not necessarily a healthy diet for bumble bees Clément Tourbez, Irène Semay, Apolline Michel, Denis Michez, Pascal Gerbaux, Antoine Gekière, Maryse Vanderplanck<p>There is evidence that specialised metabolites of flowering plants occur in both vegetative parts and floral resources (i.e., pollen and nectar), exposing pollinators to their biological activities. While such metabolites may be toxic to bees, ...Botany, Chemical ecology, Host-parasite interactions, Pollination, ZoologyIgnasi Bartomeus2023-04-10 21:22:34 View
10 Jan 2024
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Beyond variance: simple random distributions are not a good proxy for intraspecific variability in systems with environmental structure

Two paradigms for intraspecific variability

Recommended by ORCID_LOGO based on reviews by Simon Blanchet and Bart Haegeman

Community ecology usually concerns itself with understanding the causes and consequences of diversity at a given taxonomic resolution, most classically at the species level. Yet there is no doubt that diversity exists at all scales, and phenotypic variability within a taxon can be comparable to differences between taxa, as observed from bacteria to fish and trees. The question that motivates an active and growing body of work (e.g. Raffard et al 2019) is not so much whether intraspecific variability matters, but what we get wrong by ignoring it and how to incorporate it into our understanding of communities. There is no established way to think about diversity at multiple nested taxonomic levels, and it is tempting to summarize intraspecific variability simply by measuring species mean and variance in any trait and metric.

In this study, Girard-Tercieux et al (2023a) propose that, to understand its impact on community-level outcomes and in particular on species coexistence, we should carefully distinguish between two ways of thinking about intraspecific variability:

-"unstructured" variation, where every individual's features are like an independent random draw from a species-specific distribution, for instance, due to genetic lottery and developmental accidents

-"structured" variation that is due to each individual encountering a different but enduring microenvironment.

The latter type of variability may still appear complex and random-like when the environment is high-dimensional (i.e. multifaceted, with many different factors contributing to each individual's performance and development). Thus, it is not necessarily "structured" in the sense of being easily understood -- we may need to measure more aspects of the environment than is practical if we want to fully predict these variations.

What distinguishes this "structured" variability is that it is, in a loose sense, inheritable: individuals from the same species that grow in the same microenvironment will have the same performance, in a repeatable fashion. Thus, if each species is best at exploiting at least a fraction of environmental conditions, it is likely to avoid extinction by competition, except in the unlucky case of no propagule reaching any of the favorable sites.
By contrast, drawing each individual's preferences and performance randomly at each generation (from its own species distribution, but independently from other and past individuals) leads to stochastic dynamics, so-called ecological drift, that easily induce a large number of species extinctions.

The core intuition, that the complex spatial structure and high-dimensional nature of the environment plays a key explanatory role in species coexistence, is a running thread through several of the authors' work (e.g. Clark et al 2010), clearly inspired by their focus on tropical forests. This study, by tackling the question of intraspecific determinants of interspecific outcomes, makes a compelling addition to this line of investigation, coming as a theoretical companion to a more data-oriented study (Girard-Tercieux et al 2023b). But I believe it raises a question that is even broader in scope.

This kind of intraspecific variability, due to different individuals growing in different microenvironments, is perhaps most relevant for trees and other sessile organisms, but the distinction made here between "unstructured" and "structured" variability can likely be extended to many other ecological settings.

In my understanding, what matters most in "structured" variability is not so much it stemming from a fixed environment, but rather it being maintained across generations, rather than possibly lost by drift. This difference between variability in the form of "frozen" randomness and in the form of stochastic drift over time is highly relevant in other theoretical fields (e.g. in physics, where it is the difference between a disordered solid and a liquid), and thus, I expect that it is a meaningful distinction to make throughout community ecology.

References

James S. Clark, David Bell, Chengjin Chu, Benoit Courbaud, Michael Dietze, Michelle Hersh, Janneke HilleRisLambers et al. (2010) "High‐dimensional coexistence based on individual variation: a synthesis of evidence." Ecological Monographs 80, no. 4 : 569-608. https://doi.org/10.1890/09-1541.1

Camille Girard-Tercieux, Ghislain Vieilledent, Adam Clark, James S. Clark, Benoît Courbaud, Claire Fortunel, Georges Kunstler, Raphaël Pélissier, Nadja Rüger, Isabelle Maréchaux (2023a) "Beyond variance: simple random distributions are not a good proxy for intraspecific variability in systems with environmental structure." bioRxiv, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.08.06.503032

Camille Girard‐Tercieux, Isabelle Maréchaux, Adam T. Clark, James S. Clark, Benoît Courbaud, Claire Fortunel, Joannès Guillemot et al. (2023b) "Rethinking the nature of intraspecific variability and its consequences on species coexistence." Ecology and Evolution 13, no. 3 : e9860. https://doi.org/10.1002/ece3.9860

Allan Raffard, Frédéric Santoul, Julien Cucherousset, and Simon Blanchet. (2019) "The community and ecosystem consequences of intraspecific diversity: A meta‐analysis." Biological Reviews 94, no. 2: 648-661. https://doi.org/10.1111/brv.12472

Beyond variance: simple random distributions are not a good proxy for intraspecific variability in systems with environmental structureCamille Girard-Tercieux, Ghislain Vieilledent, Adam Clark, James S. Clark, Benoit Courbaud, Claire Fortunel, Georges Kunstler, Raphaël Pélissier, Nadja Rüger, Isabelle Maréchaux<p>The role of intraspecific variability (IV) in shaping community dynamics and species coexistence has been intensively discussed over the past decade and modelling studies have played an important role in that respect. However, these studies oft...Biodiversity, Coexistence, Community ecology, Competition, Theoretical ecologyMatthieu Barbier2022-08-07 12:51:30 View
19 Aug 2020
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Three points of consideration before testing the effect of patch connectivity on local species richness: patch delineation, scaling and variability of metrics

Good practice guidelines for testing species-isolation relationships in patch-matrix systems

Recommended by based on reviews by 3 anonymous reviewers

Conservation biology is strongly rooted in the theory of island biogeography (TIB). In island systems where the ocean constitutes the inhospitable matrix, TIB predicts that species richness increases with island size as extinction rates decrease with island area (the species-area relationship, SAR), and species richness increases with connectivity as colonisation rates decrease with island isolation (the species-isolation relationship, SIR)[1]. In conservation biology, patches of habitat (habitat islands) are often regarded as analogous to islands within an unsuitable matrix [2], and SAR and SIR concepts have received much attention as habitat loss and habitat fragmentation are increasingly threatening biodiversity [3,4].
The existence of SAR in patch-matrix systems has been confirmed in several studies, while the relative importance of SIR remains debated [2,5] and empirical evidence is mixed. For example, Thiele et al. [6] showed that connectivity effects are trait specific and more important to explain species richness of short-distant dispersers and of specialist species for which the matrix is less permeable. Some authors have also cautioned that the relative support for or against the existence of SIR may depend on methodological decisions related to connectivity metrics, patch classification, scaling decisions and sample size [7].
In this preprint, Laroche and colleagues [8] argue that methodological limits should be fully understood before questioning the validity of SIR in patch-matrix systems. In consequence, they used a virtual ecologist approach [9] to qualify different methodological aspects and derive good practice guidelines related to patch delineation, patch connectivity indices, and scaling of indices with species dispersal distance.
Laroche et al. [8] simulated spatially-explicit neutral meta-communities with up to 100 species in artificial fractal (patch-matrix) landscapes. Each habitat cell could hold up to 100 individuals. In each time step, some individuals died and were replaced by an individual from the regional species pool depending on relative local and regional abundance as well as dispersal distance to the nearest source habitat cell. Different scenarios were run with varying degrees of spatial autocorrelation in the fractal landscape (determining the clumpiness of habitat cells), the proportion of suitable habitat, and the species dispersal distances (with all species showing the same dispersal distance). Laroche and colleagues then sampled species richness in the simulated meta-communities, computed different local connectivity indices for the simulated landscapes (Buffer index with different radii, dIICflux index and dF index, and, finally, related species richness to connectivity.
The complex simulations allowed Laroche and colleagues [8] to test how methodological choices and landscape features may affect SIR. Overall, they found that patch delineation is crucial and should be fine enough to exclude potential within-patch dispersal limitations, and the scaling of the connectivity indices (in simplified words, the window of analyses) should be tailored to the dispersal distance of the species group. Of course, tuning the scaling parameters will be more complicated when dispersal distances vary across species but overall these results corroborate empirical findings that SIR effects are trait specific [6]. Additionally, the results by Laroche and colleagues [8] indicated that indices based on Euclidian rather than topological distance are more performant and that evidence of SIR is more likely if Buffer indices are highly variable between sampled patches.
Although the study is very technical due to the complex simulation approach and the different methods tested, I hope it will not only help guiding methodological choices but also inspire ecologists to further test or even revisit SIR (and SAR) hypotheses for different systems. Also, Laroche and colleagues propose many interesting avenues that could still be explored in this context, for example determining the optimal grid resolution for the patch delineation in empirical studies.

References

[1] MacArthur, R.H. and Wilson, E.O. (1967) The theory of island biogeography. Princeton University Press, Princeton.
[2] Fahrig, L. (2013) Rethinking patch size and isolation effects: the habitat amount hypothesis. Journal of Biogeography, 40(9), 1649-1663. doi: 10.1111/jbi.12130
[3] Hanski, I., Zurita, G.A., Bellocq, M.I. and Rybicki J (2013) Species–fragmented area relationship. Proceedings of the National Academy of Sciences U.S.A., 110(31), 12715-12720. doi: 10.1073/pnas.1311491110
[4] Giladi, I., May, F., Ristow, M., Jeltsch, F. and Ziv, Y. (2014) Scale‐dependent species–area and species–isolation relationships: a review and a test study from a fragmented semi‐arid agro‐ecosystem. Journal of Biogeography, 41(6), 1055-1069. doi: 10.1111/jbi.12299
[5] Hodgson, J.A., Moilanen, A., Wintle, B.A. and Thomas, C.D. (2011) Habitat area, quality and connectivity: striking the balance for efficient conservation. Journal of Applied Ecology, 48(1), 148-152. doi: 10.1111/j.1365-2664.2010.01919.x
[6] Thiele, J., Kellner, S., Buchholz, S., and Schirmel, J. (2018) Connectivity or area: what drives plant species richness in habitat corridors? Landscape Ecology, 33, 173-181. doi: 10.1007/s10980-017-0606-8
[7] Vieira, M.V., Almeida-Gomes, M., Delciellos, A.C., Cerqueira, R. and Crouzeilles, R. (2018) Fair tests of the habitat amount hypothesis require appropriate metrics of patch isolation: An example with small mammals in the Brazilian Atlantic Forest. Biological Conservation, 226, 264-270. doi: 10.1016/j.biocon.2018.08.008
[8] Laroche, F., Balbi, M., Grébert, T., Jabot, F. and Archaux, F. (2020) Three points of consideration before testing the effect of patch connectivity on local species richness: patch delineation, scaling and variability of metrics. bioRxiv, 640995, ver. 5 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/640995
[9] Zurell, D., Berger, U., Cabral, J.S., Jeltsch, F., Meynard, C.N., Münkemüller, T., Nehrbass, N., Pagel, J., Reineking, B., Schröder, B. and Grimm, V. (2010) The virtual ecologist approach: simulating data and observers. Oikos, 119(4), 622-635. doi: 10.1111/j.1600-0706.2009.18284.x

Three points of consideration before testing the effect of patch connectivity on local species richness: patch delineation, scaling and variability of metricsF. Laroche, M. Balbi, T. Grébert, F. Jabot & F. Archaux<p>The Theory of Island Biogeography (TIB) promoted the idea that species richness within sites depends on site connectivity, i.e. its connection with surrounding potential sources of immigrants. TIB has been extended to a wide array of fragmented...Biodiversity, Community ecology, Dispersal & Migration, Landscape ecology, Spatial ecology, Metacommunities & MetapopulationsDamaris Zurell2019-05-20 16:03:47 View