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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
20 Feb 2024
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Functional trade-offs: exploring the temporal response of field margin plant communities to climate change and agricultural practices

Unravelling plant diversity in agricultural field margins in France: plant species better adapted to climate change need other agricultures to persist

Recommended by ORCID_LOGO based on reviews by Ignasi Bartomeus, Clelia Sirami and Diego Gurvich

Agricultural field margin plants, often referred to as “spontaneous” species, are key for the stabilization of several social-ecological processes related to crop production such as pollination or pest control (Tamburini et al. 2020). Because of its beneficial function, increasing the diversity of field margin flora becomes as important as crop diversity in process-based agricultures such as agroecology. Contrary, supply-dependent intensive agricultures produce monocultures and homogenized environments that might benefit their productivity, which generally includes the control or elimination of the field margin flora (Emmerson et al. 2016, Aligner 2018). Considering that different agricultural practices are produced by (and produce) different territories (Moore 2020) and that they are also been shaped by current climate change, we urgently need to understand how agricultural intensification constrains the potential of territories to develop agriculture more resilient to such change (Altieri et al., 2015). Thus, studies unraveling how agricultural practices' effects on agricultural field margin flora interact with those of climate change is of main importance, as plant strategies better adapted to such social-ecological processes may differ.        
 
In this vein, the study of Poinas et al. (2024) can be considered a key contribution. It exemplifies how agricultural intensification practiced in the context of climate change can constrain the potential of agricultural field margin flora to cope with climatic variations. The authors found that the incidence of plant strategies better adapted to climate change (conservative/stress-tolerant and Mediterranean species) increased with higher temperatures and lower soil moisture, and with lower intensity of margin management. In contrast, the incidence of ruderal species decreased with climate change. Thus, increasing or even maintaining current levels of agricultural intensification may affect the potential of French agriculture to move to sustainable process-based agricultures because of the reduction of plant diversity, particularly of vegetation better adapted to climate change. 
 
By using an impressive dataset spanning 9 years and 555 agricultural margins in continental France, Poinas et al. (2024) investigated temporal changes in climatic variables (temperature and soil moisture), agricultural practices (herbicide and fertilizers quantity, the frequency of margin mowing or grinding), plant taxonomical and functional diversity, plant strategies (Grime 1977, 1988) and relationships between these temporal changes. Temporal changes in plant strategies were associated with those observed in climatic variables and agricultural practices. Even such associations seem to be mediated by spatial changes, as described in the supplementary material and in their most recent article (Poinas et al. 2023), changes in climatic variables registered in a decade shaped plant strategies and therefore the diversity and functional potential of agricultural field margins. These results are clearly synthesized in Figures 6 and 7 of the present contribution.
 
As shown by Poinas et al. (2024), in the context of climate change, decreasing agricultural intensification will produce more diverse agricultural field margins by promoting the persistence of plant species better adapted to higher temperatures and lower soil moisture. Thus, adopting other agricultural practices (e.g., agroforestry, agroecology) will produce territories with a higher potential to move to sustainable processes-based agricultures that may better cope with climate change by harboring higher biocultural diversity (Altieri et al. 2015).

References

Alignier, A., 2018. Two decades of change in a field margin vegetation metacommunity as a result of field margin structure and management practice changes. Agric., Ecosyst. & Environ., 251, 1–10. https://doi.org/10.1016/j.agee.2017.09.013 

Altieri, M.A., Nicholls, C.I., Henao, A., Lana, M.A., 2015. Agroecology and the design of climate change-resilient farming systems. Agron. Sustain. Dev. 35, 869–890. https://doi.org/10.1007/s13593-015-0285-2

Emmerson, M., Morales, M. B., Oñate, J. J., Batary, P., Berendse, F., Liira, J., Aavik, T., Guerrero, I., Bommarco, R., Eggers, S., Pärt, T., Tscharntke, T., Weisser, W., Clement, L. & Bengtsson, J. (2016). How agricultural intensification affects biodiversity and ecosystem services. In Adv. Ecol. Res. 55, 43-97. https://doi.org/10.1016/bs.aecr.2016.08.005

Grime, J. P., 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. The American Naturalist, 111(982), 1169–1194. https://doi.org/10.1086/283244

Grime, J. P., 1988. The C-S-R model of primary plant strategies—Origins, implications and tests. In L. D. Gottlieb & S. K. Jain, Plant Evolutionary Biology (pp. 371–393). Springer Netherlands. https://doi.org/10.1007/978-94-009-1207-6_14

Moore, J., 2020. El capitalismo en la trama de la vida (Capitalism in The Web of Life). Traficantes de sueños, Madrid, Spain. 

Poinas, I., Fried, G., Henckel, L., & Meynard, C. N., 2023. Agricultural drivers of field margin plant communities are scale-dependent. Bas. App. Ecol. 72, 55-63. https://doi.org/10.1016/j.baae.2023.08.003

Poinas, I., Meynard, C. N., Fried, G., 2024. Functional trade-offs: exploring the temporal response of field margin plant communities to climate change and agricultural practices, bioRxiv, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2023.03.03.530956

Tamburini, G., Bommarco, R., Wanger, T.C., Kremen, C., Van Der Heijden, M.G., Liebman, M., Hallin, S., 2020. Agricultural diversification promotes multiple ecosystem services without compromising yield. Sci. Adv. 6, eaba1715. https://doi.org/10.1126/sciadv.aba1715

Functional trade-offs: exploring the temporal response of field margin plant communities to climate change and agricultural practicesIsis Poinas, Christine N Meynard, Guillaume Fried<p style="text-align: justify;">Over the past decades, agricultural intensification and climate change have led to vegetation shifts. However, functional trade-offs linking traits responding to climate and farming practices are rarely analyzed, es...Agroecology, Biodiversity, Botany, Climate change, Community ecologyJulia Astegiano2023-03-04 15:40:35 View
21 Oct 2020
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Why scaling up uncertain predictions to higher levels of organisation will underestimate change

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

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

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

References

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

Why scaling up uncertain predictions to higher levels of organisation will underestimate changeJames Orr, Jeremy Piggott, Andrew Jackson, Jean-François Arnoldi<p>Uncertainty is an irreducible part of predictive science, causing us to over- or underestimate the magnitude of change that a system of interest will face. In a reductionist approach, we may use predictions at the level of individual system com...Community ecology, Ecosystem functioning, Theoretical ecologyElisa ThebaultAnonymous2020-06-02 15:41:12 View
01 Apr 2019
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The inherent multidimensionality of temporal variability: How common and rare species shape stability patterns

Diversity-Stability and the Structure of Perturbations

Recommended by ORCID_LOGO and based on reviews by Frederic Barraquand and 1 anonymous reviewer

In his 1972 paper “Will a Large Complex System Be Stable?” [1], May challenges the idea that large communities are more stable than small ones. This was the beginning of a fundamental debate that still structures an entire research area in ecology: the diversity-stability debate [2]. The most salient strength of May’s work was to use a mathematical argument to refute an idea based on the observations that simple communities are less stable than large ones. Using the formalism of dynamical systems and a major results on the distribution of the eigen values for random matrices, May demonstrated that the addition of random interactions destabilizes ecological communities and thus, rich communities with a higher number of interactions should be less stable. But May also noted that his mathematical argument holds true only if ecological interactions are randomly distributed and thus concluded that this must not be true! This is how the contradiction between mathematics and empirical observations led to new developments in the study of ecological networks.
Since 1972, the theoretical corpus of ecology has advanced, building on the formalism of dynamical systems, ecologists have revealed that ecological interactions are indeed not randomly distributed [3,4], but general rules are still missing and we are far from understanding what determine the exact network topology of a given community. One promising avenue is to understand the relationship between different facets of the concept of stability [5,6]. Indeed, the classical approach to determine whether a system is stable is qualitative: if a system returns to its equilibrium when it is slightly moved away from it, then the system is considered stable. But there are several other aspects that are worth scrutinizing. For instance, when a system returns to its equilibrium, one can characterize the corresponding transient dynamics [7,8], that is asking fundamental questions such as: what is the trajectory of return? How long does it take to return to the equilibrium? Another fundamental question is whether the system remains qualitatively stable when the distributions of interactions strengths change? From a biological standpoint, all of these questions matter as all these aspects of stability may partially explain the actual structure of ecological networks, and hence, frameworks that integrate several facets of stability are much needed.
The study by Arnoldi et al. [9] is a significant step towards such a framework. The strength of their formalism is threefold. First, instead of considering separately the system and its perturbations, they considering the fluctuations of a perturbed ecological systems and thus, perturbations are parts of the ecological system. Second, they use of a broad definition of perturbation that encompasses the types of perturbations (whether the individual respond synchronously or not), their intensity and their direction (how the perturbations are correlated across species). Third, they quantify the instability of the system using variability which integrates the consequences of perturbations over the whole set of species of a community: such a measure is comparable across communities and accounts for the trivial effect of the perturbations on the system dynamics.
Using this framework, the authors show that interactions within a stable community leads to a general relationship between variability and the abundance of individually perturbed species: if individuals of species respond in synchrony to a perturbation, then the more abundant the species perturbed the higher the variability of the system, but the relationship is reverse when individual respond asynchronously. A direct implications of these results for the classical debate is that the diversity-stability relationship is negative for the former type of perturbations (as in May’s seminal paper) but positive for the latter type. Hence, the rigorous work of Arnoldi and colleagues sheds a new light upon the classical debate: the nature of the perturbation regime prevailing within a community affects the slope of the diversity-stability relationships and given the vast diversity of ecological communities, this may very well be one of the reasons why the debate still endures.
From a historical perspective, it is interesting that ecologists have gone from looking at random webs to structured webs and now, in a sense, Arnoldi et al. are unpacking the role of differentially structured perturbations. The work they achieved will doubtlessly be followed by further theoretical investigations. One natural research avenue is to revisit the role of the topology of ecological networks with this framework: how the distribution of interactions and their strength affect the general relationship they unravel? Finally, this study demonstrate that the impact of the abundance of a species on the variability of the system depends on the nature of the perturbation regime and so the distribution of species abundances within a community should be determined by the prevailing perturbation regime which is a prediction that remains to be tested.

References

[1] May, Robert M (1972). Will a Large Complex System Be Stable? Nature 238, 413–414. doi: 10.1038/238413a0
[2] McCann, Kevin Shear (2000). The Diversity–Stability Debate. Nature 405, 228–233. doi: 10.1038/35012234
[3] Rooney, Neil, Kevin McCann, Gabriel Gellner, and John C. Moore (2006). Structural Asymmetry and the Stability of Diverse Food Webs. Nature 442, 265–269. doi: 10.1038/nature04887
[4] Jacquet, Claire, Charlotte Moritz, Lyne Morissette, Pierre Legagneux, François Massol, Philippe Archambault, and Dominique Gravel (2016). No Complexity–Stability Relationship in Empirical Ecosystems. Nature Communications 7, 12573. doi: 10.1038/ncomms12573
[5] Donohue, Ian, Helmut Hillebrand, José M. Montoya, Owen L. Petchey, Stuart L. Pimm, Mike S. Fowler, Kevin Healy, et al. (2016). Navigating the Complexity of Ecological Stability. Ecology Letters 19, 1172–1185. doi: 10.1111/ele.12648
[6] Arnoldi, Jean-François, and Bart Haegeman (2016). Unifying Dynamical and Structural Stability of Equilibria. Proceedings of the Royal Society A: Mathematical, Physical and Engineering Science 472, 20150874. doi: 10.1098/rspa.2015.0874
[7] Caswell, Hal, and Michael G. Neubert (2005). Reactivity and Transient Dynamics of Discrete-Time Ecological Systems. Journal of Difference Equations and Applications 11, 295–310. doi: 10.1080/10236190412331335382
[8] Arnoldi, J-F., M. Loreau, and B. Haegeman (2016). Resilience, Reactivity and Variability: A Mathematical Comparison of Ecological Stability Measures. Journal of Theoretical Biology 389, 47–59. doi: 10.1016/j.jtbi.2015.10.012
[9] Arnoldi, Jean-Francois, Michel Loreau, and Bart Haegeman. (2019). The Inherent Multidimensionality of Temporal Variability: How Common and Rare Species Shape Stability Patterns.” BioRxiv, 431296, ver. 3 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/431296

The inherent multidimensionality of temporal variability: How common and rare species shape stability patternsJean-François Arnoldi, Michel Loreau, Bart Haegeman<p>Empirical knowledge of ecosystem stability and diversity-stability relationships is mostly based on the analysis of temporal variability of population and ecosystem properties. Variability, however, often depends on external factors that act as...Biodiversity, Coexistence, Community ecology, Competition, Interaction networks, Theoretical ecologyKevin Cazelles2018-10-02 14:01:03 View
29 Jun 2024
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Reassessment of French breeding bird population sizes using citizen science and accounting for species detectability

Reassessment of French breeding bird population sizes: from citizen science observations to nationwide estimates

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

Estimating populations size of widespread, common species in a relatively large and heterogeneous country like France is difficult for several reasons, from having a sample covering well the diverse ecological gradients to accounting for detectability, the fact that absence of a species may represent a false negative, the species being present but not detected. Bird communities have been the focus of a very large number of studies, with some countries like the UK having long traditions of monitoring both common and rare species. Nabias et al. use a large, structured citizen science project to provide new estimates of common bird species, accounting for detectability and using different habitat and climate covariates to extrapolate abundance to non-sampled areas. About 2/3 of the species had estimates higher than what would have been expected using a previous attempt at estimating population size based in part on expert knowledge and projected using estimates of trends to the period covered by the citizen science sampling. Some species showed large differences between the two estimates, which could be in part explained by accounting for detectability.

This paper uses what is called model-based inference (as opposed to design-based inference, that uses the design to make inferences about the whole population; Buckland et al. 2000), both in terms of detectability and habitat suitability. The estimates obtained depend on how well the model components approximate the underlying processes, which in a complex dataset like this one is not easy to assess. But it clearly shows that detectability may have substantial implications for the population size estimates. This is of course not new but has rarely been done at this scale and using a large sample obtained on many species. Interesting further work could focus on testing the robustness of the model-based approach by for example sampling new plots and compare the expected values to the observed values. Such a sampling could be stratified to maximize the discrimination between expected low and high abundances, at least for species where the estimates might be considered as uncertain, or for which estimating population sizes is deemed important.

References

Buckland, S. T., Goudie, I. B. J., & Borchers, D. L. (2000). Wildlife Population Assessment: Past Developments and Future Directions. Biometrics, 56(1), 1-12. https://doi.org/10.1111/j.0006-341X.2000.00001.x

 Nabias, J., Barbaro, L., Fontaine, B., Dupuy, J., Couzi, L., et al. (2024) Reassessment of French breeding bird population sizes using citizen science and accounting for species detectability. HAL, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://hal.science/hal-04478371

Reassessment of French breeding bird population sizes using citizen science and accounting for species detectabilityJean Nabias, Luc Barbaro, Benoit Fontaine, Jérémy Dupuy, Laurent Couzi, Clément Vallé, Romain Lorrillière<p style="text-align: justify;">Higher efficiency in large-scale and long-term biodiversity monitoring can be obtained through the use of Essential Biodiversity Variables, among which species population sizes provide key data for conservation prog...Biogeography, Macroecology, Spatial ecology, Metacommunities & Metapopulations, Species distributions, Statistical ecologyNigel Yoccoz2024-02-26 18:10:27 View
18 Dec 2019
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Validating morphological condition indices and their relationship with reproductive success in great-tailed grackles

Are condition indices positively related to each other and to fitness?: a test with grackles

Recommended by based on reviews by Javier Seoane and Isabel López-Rull

Reproductive succes, as a surrogate of individual fitness, depends both on extrinsic and intrinsic factors [1]. Among the intrinsic factors, resource level or health are considered important potential drivers of fitness but exceedingly difficult to measure directly. Thus, a host of proxies have been suggested, known as condition indices [2]. The question arises whether all condition indices consistently measure the same "inner state" of individuals and whether all of them similarly correlate to individual fitness. In this preregistration, Berens and colleagues aim to answer this question for two common condition indices, fat score and scaled mass index (Fig. 1), using great-tailed grackles as a model system. Although this question is not new, it has not been satisfactorily solved and both reviewers found merit in the attempt to clarify this matter.

Figure 1. Hypothesized relationships between two condition indices and reproductive success. Single arrow heads indicate causal relationships; double arrow heads indicate only correlation. In a best case scenario, all relationships should be positive and linear.
A problem in adressing this question with grackles is limited population, ergo sample, size and limited possibilites of recapture individuals. Some relationships can be missed due to low statistical power. Unfortunately, existing tools for power analysis fall behind complex designs and the one planned for this study. Thus, any potentially non significant relationship has to be taken cautiously. Nevertheless, even if grackles will not provide a definitive answer (they never meant to do it), this preregistration can inspire broader explorations of matches and mismatches across condition indices and species, as well as uncover non-linear relationships with reproductive success.

References

[1] Roff, D. A. (2001). Life history evolution. Oxford University Press, Oxford.
[2] Labocha, M. K.; Hayes, J. P. (2012). Morphometric indices of body condition in birds: a review. Journal of Ornithology 153: 1–22. doi: 10.1007/s10336-011-0706-1

Validating morphological condition indices and their relationship with reproductive success in great-tailed gracklesJennifer M. Berens, Corina J. Logan, Melissa Folsom, Luisa Bergeron, Kelsey B. McCuneMorphological variation among individuals has the potential to influence multiple life history characteristics such as dispersal, migration, reproductive fitness, and survival (Wilder, Raubenheimer, and Simpson (2016)). Theoretically, individuals ...Behaviour & Ethology, Conservation biology, Demography, Morphometrics, Preregistrations, ZoologyMarcos Mendez2019-08-05 20:05:56 View
30 Jan 2020
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Diapause is not selected as a bet-hedging strategy in insects: a meta-analysis of reaction norm shapes

When to diapause or not to diapause? Winter predictability is not the answer

Recommended by based on reviews by Kévin Tougeron, Md Habibur Rahman Salman and 1 anonymous reviewer

Winter is a harsh season for many organisms that have to cope with food shortage and potentially lethal temperatures. Many species have evolved avoidance strategies. Among them, diapause is a resistance stage many insects use to overwinter. For an insect, it is critical to avoid lethal winter temperatures and thus to initiate diapause before winter comes, while making the most of autumn suitable climatic conditions [1,2]. Several cues can be used to appreciate that winter is coming, including day length and temperature [3]. But climate changes, temperatures rise and become more variable from year to year, which imposes strong pressure upon insect phenology [4]. How can insects adapt to changes in the mean and variance of winter onset?
In this paper, Jens Joschinski and Dries Bonte [5] address this question by using a well conducted meta-analysis of 458 diapause reaction norms obtained from 60 primary studies. They first ask first if insect mean diapause timing is tuned to match winter onset. They further ask if insects adapt to climatic unpredictability through a bet-hedging strategy by playing it safe and avoid risk (conservative bet-hedging) or on the contrary by avoiding to put all their eggs in one basket and spread the risk among their offspring (diversified bet-hedging). From published papers, the authors extracted data on mean diapause timing and information on latitude from which they retrieved day length inducing diapause, the date of winter onset and the day length at winter onset.
They found a positive correlation between latitude and the day length inducing diapause. On the contrary they found positive but (very) weak correlation between the date of winter onset and the date of diapause, thus indicating that diapause timing is not as optimally adapted to local environments as expected, particularly at high latitudes. They only found weak correlations between climate unpredictability and variability in diapause timing, and no correlation between climate unpredictability and deviation from optimal diapause timing. Together, these findings go against the hypothesis that insects use diversified or conservative bet-hedging strategies to cope with uncertainty in climatic conditions.
This is what makes the study thought provoking: the results do not match the theory well. Not because of a lack of data or a narrow scope, but because diapause is a complex trait that is determined by a large array of physiological and ecological factors [3]. Determining what are these factors is of particular interest in the face of the current climate change. This study shows what does not determine the timing of insect diapause. Researchers now know where to look at to improve our understanding of this key aspect of insect adaptation to climatic conditions.

References

[1] Dyck, H. V., Bonte, D., Puls, R., Gotthard, K., and Maes, D. (2015). The lost generation hypothesis: could climate change drive ectotherms into a developmental trap? Oikos, 124(1), 54–61. doi: 10.1111/oik.02066
[2] Gallinat, A. S., Primack, R. B., and Wagner, D. L. (2015). Autumn, the neglected season in climate change research. Trends in Ecology & Evolution, 30(3), 169–176. doi: 10.1016/j.tree.2015.01.004
[3] Tougeron, K. (2019). Diapause research in insects: historical review and recent work perspectives. Entomologia Experimentalis et Applicata, 167(1), 27–36. doi: 10.1111/eea.12753
[4] Bale, J. S., and Hayward, S. a. L. (2010). Insect overwintering in a changing climate. Journal of Experimental Biology, 213(6), 980–994. doi: 10.1242/jeb.037911
[5] Joschinski, J., and Bonte, D. (2020). Diapause is not selected as a bet-hedging strategy in insects: a meta-analysis of reaction norm shapes. BioRxiv, 752881, ver. 3 recommended and peer-reviewed by PCI Ecology. doi: 10.1101/752881

Diapause is not selected as a bet-hedging strategy in insects: a meta-analysis of reaction norm shapesJens Joschinski and Dries BonteMany organisms escape from lethal climatological conditions by entering a resistant resting stage called diapause, and it is essential that this strategy remains optimally timed with seasonal change. Climate change therefore exerts selection press...Maternal effects, Meta-analyses, Phenotypic plasticity, Terrestrial ecologyBastien Castagneyrol2019-09-20 11:47:47 View
03 Feb 2023
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The role of climate change and niche shifts in divergent range dynamics of a sister-species pair

Drivers of range expansion in a pair of sister grackle species

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

The spatial distribution of a species is driven by both biotic and abiotic factors that may change over time (Soberón & Nakamura, 2009; Paquette & Hargreaves, 2021).  Therefore, species ranges are dynamic, especially in humanized landscapes where changes occur at high speeds (Sirén & Morelli, 2020). The distribution of many species is being reduced because of human impacts; however, some species are expanding their distributions, even over their niche (Lustenhouwer & Parker, 2022). One of the factors that may lead to a geographic niche expansion is behavioral flexibility (Mikhalevich et al., 2017), but the mechanisms determining range expansion through behavioral changes are not fully understood. 

The PCI Ecology study by Summers et al. (2023) uses a very large database on the current and historic distribution of two species of grackles that have shown different trends in their distribution. The great-tailed grackle has largely expanded its range over the 20th century, while the range of the boat-tailed grackle has remained very similar. They take advantage of this differential response in the distribution of the two species and run several analyses to test whether it was a change in habitat availability, in the realized niche, in habitat connectivity or in in the other traits or conditions that previously limited the species range, what is driving the observed distribution of the species. The study finds a change in the niche of great-tailed grackle, consistent with the high behavioral flexibility of the species.

The two reviewers and I have seen a lot of value in this study because 1) it addresses a very timely question, especially in the current changing world; 2) it is a first step to better understanding if behavioral attributes may affect species’ ability to change their niche; 3) it contrasts the results using several complementary statistical analyses, reinforcing their conclusions; 4) it is based on the preregistration Logan et al (2021), and any deviations from it are carefully explained and justified in the text and 5) the limitations of the study have been carefully discussed. It remains to know if the boat-tailed grackle has more limited behavioral flexibility than the great-tailed grackle, further confirming the results of this study.
 
References

Logan CJ, McCune KB, Chen N, Lukas D (2021) Implementing a rapid geographic range expansion - the role of behavior and habitat changes. http://corinalogan.com/Preregistrations/gxpopbehaviorhabitat.html

Lustenhouwer N, Parker IM (2022) Beyond tracking climate: Niche shifts during native range expansion and their implications for novel invasions. Journal of Biogeography, 49, 1481–1493. https://doi.org/10.1111/jbi.14395

Mikhalevich I, Powell R, Logan C (2017) Is behavioural flexibility evidence of cognitive complexity? How evolution can inform comparative cognition. Interface Focus, 7, 20160121. https://doi.org/10.1098/rsfs.2016.0121

Paquette A, Hargreaves AL (2021) Biotic interactions are more often important at species’ warm versus cool range edges. Ecology Letters, 24, 2427–2438. https://doi.org/10.1111/ele.13864

Sirén APK, Morelli TL (2020) Interactive range-limit theory (iRLT): An extension for predicting range shifts. Journal of Animal Ecology, 89, 940–954. https://doi.org/10.1111/1365-2656.13150

Soberón J, Nakamura M (2009) Niches and distributional areas: Concepts, methods, and assumptions. Proceedings of the National Academy of Sciences, 106, 19644–19650. https://doi.org/10.1073/pnas.0901637106

Summers JT, Lukas D, Logan CJ, Chen N (2022) The role of climate change and niche shifts in divergent range dynamics of a sister-species pair. EcoEvoRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.32942/osf.io/879pe

The role of climate change and niche shifts in divergent range dynamics of a sister-species pairJeremy Summers, Dieter Lukas, Corina J. Logan, Nancy Chen<p>---This is a POST-STUDY manuscript for the PREREGISTRATION, which received in principle acceptance in 2020 from Dr. Sebastián González (reviewed by Caroline Nieberding, Tim Parker, and Pizza Ka Yee Chow; <a href="https://doi.org/10.24072/pci.ec...Behaviour & Ethology, Biogeography, Dispersal & Migration, Human impact, Landscape ecology, Preregistrations, Species distributionsEsther Sebastián González2022-05-26 20:07:33 View
21 Nov 2023
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Pathogen community composition and co-infection patterns in a wild community of rodents

Reservoirs of pestilence: what pathogen and rodent community analyses can tell us about transmission risk

Recommended by ORCID_LOGO based on reviews by Adrian Diaz, Romain Pigeault and 1 anonymous reviewer

Rodents are well known as one of the main animal groups responsible for human-transmitted pathogens. As such, it seems logical to try and survey what kinds of pathogenic microbes might be harboured by wild rodents, in order to establish some baseline surveillance and prevent future zoonotic outbreaks (Bernstein et al., 2022). This is exactly what Abbate et al. (2023) endeavoured and their findings are intimidating. Based on quite a large sampling effort, they collected more than 700 rodents of seven species around two villages in northeastern France. They looked for molecular markers indicative of viral and bacterial infections and proceeded to analyze their pathogen communities using multivariate techniques.

Variation in the prevalence of the different pathogens was found among host species, with e.g. signs of CPXV more prevalent in Cricetidae while some Mycoplasma strains were more prevalent in Muridae. Co-circulation of pathogens was found in all species, with some evidencing signs of up to 12 different pathogen taxa. The diversity of co-circulating pathogens was markedly different between host species and higher in adult hosts, but not affected by sex. The dataset also evinced some slight differences between habitats, with meadows harbouring a little more diversity of rodent pathogens than forests. Less intuitively, some pathogen associations seemed quite repeatable, such as the positive association of Bartonella spp. with CPXV in the montane water vole. The study allowed the authors to test several associations already described in the literature, including associations between different hemotropic Mycoplasma species.

I strongly invite colleagues interested in zoonoses, emerging pandemics and more generally One Health to read the paper of Abbate et al. (2023) and try to replicate them across the world. To prevent the next sanitary crises, monitoring rodents, and more generally vertebrates, population demographics is a necessary and enlightening step (Johnson et al., 2020), but insufficient. Following the lead of colleagues working on rodent ectoparasites (Krasnov et al., 2014), we need more surveys like the one described by Abbate et al. (2023) to understand the importance of the dilution effect in the prevalence and transmission of microbial pathogens (Andreazzi et al., 2023) and the formation of epidemics. We also need other similar studies to assess the potential of different rodent species to carry pathogens more or less capable of infecting other mammalian species (Morand et al., 2015), in other places in the world.

References

Abbate, J. L., Galan, M., Razzauti, M., Sironen, T., Voutilainen, L., Henttonen, H., Gasqui, P., Cosson, J.-F. & Charbonnel, N. (2023) Pathogen community composition and co-infection patterns in a wild community of rodents. BioRxiv, ver.4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2020.02.09.940494 

Andreazzi, C. S., Martinez-Vaquero, L. A., Winck, G. R., Cardoso, T. S., Teixeira, B. R., Xavier, S. C. C., Gentile, R., Jansen, A. M. & D'Andrea, P. S. (2023) Vegetation cover and biodiversity reduce parasite infection in wild hosts across ecological levels and scales. Ecography, 2023, e06579.
https://doi.org/10.1111/ecog.06579
 
Bernstein, A. S., Ando, A. W., Loch-Temzelides, T., Vale, M. M., Li, B. V., Li, H., Busch, J., Chapman, C. A., Kinnaird, M., Nowak, K., Castro, M. C., Zambrana-Torrelio, C., Ahumada, J. A., Xiao, L., Roehrdanz, P., Kaufman, L., Hannah, L., Daszak, P., Pimm, S. L. & Dobson, A. P. (2022) The costs and benefits of primary prevention of zoonotic pandemics. Science Advances, 8, eabl4183.
https://doi.org/10.1126/sciadv.abl4183
 
Johnson, C. K., Hitchens, P. L., Pandit, P. S., Rushmore, J., Evans, T. S., Young, C. C. W. & Doyle, M. M. (2020) Global shifts in mammalian population trends reveal key predictors of virus spillover risk. Proceedings of the Royal Society B: Biological Sciences, 287, 20192736.
https://doi.org/10.1098/rspb.2019.2736
 
Krasnov, B. R., Pilosof, S., Stanko, M., Morand, S., Korallo-Vinarskaya, N. P., Vinarski, M. V. & Poulin, R. (2014) Co-occurrence and phylogenetic distance in communities of mammalian ectoparasites: limiting similarity versus environmental filtering. Oikos, 123, 63-70.
https://doi.org/10.1111/j.1600-0706.2013.00646.x
 
Morand, S., Bordes, F., Chen, H.-W., Claude, J., Cosson, J.-F., Galan, M., Czirjak, G. Á., Greenwood, A. D., Latinne, A., Michaux, J. & Ribas, A. (2015) Global parasite and Rattus rodent invasions: The consequences for rodent-borne diseases. Integrative Zoology, 10, 409-423.
https://doi.org/10.1111/1749-4877.12143

Pathogen community composition and co-infection patterns in a wild community of rodentsJessica Lee Abbate, Maxime Galan, Maria Razzauti, Tarja Sironen, Liina Voutilainen, Heikki Henttonen, Patrick Gasqui, Jean-François Cosson, Nathalie Charbonnel<p style="text-align: justify;">Rodents are major reservoirs of pathogens that can cause disease in humans and livestock. It is therefore important to know what pathogens naturally circulate in rodent populations, and to understand the factors tha...Biodiversity, Coexistence, Community ecology, Eco-immunology & Immunity, Epidemiology, Host-parasite interactions, Population ecology, Species distributionsFrancois Massol2020-02-11 12:42:28 View
28 Apr 2023
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Most diverse, most neglected: weevils (Coleoptera: Curculionoidea) are ubiquitous specialized brood-site pollinators of tropical flora

Pollination-herbivory by weevils claiming for recognition: the Cinderella among pollinators

Recommended by based on reviews by Susan Kirmse, Carlos Eduardo Nunes and 2 anonymous reviewers

Since Charles Darwin times, and probably earlier, naturalists have been eager to report the rarest pollinators being discovered, and this still happens even in recent times; e.g., increased evidence of lizards, cockroaches, crickets or earwigs as pollinators (Suetsugu 2018, Komamura et al. 2021, de Oliveira-Nogueira et al. 2023), shifts to invasive animals as pollinators, including passerine birds and rats (Pattemore & Wilcove 2012), new amazing cases of mimicry in pollination, such as “bleeding” flowers that mimic wounded insects (Heiduk et al., 2023) or even the possibility that a tree frog is reported for the first time as a pollinator (de Oliveira-Nogueira et al. 2023). This is in part due to a natural curiosity of humans about rarity, which pervades into scientific insight (Gaston 1994). Among pollinators, the apparent rarity of some interaction types is sometimes a symptom of a lack of enough inquiry. This seems to be the case of weevil pollination, given that these insects are widely recognized as herbivores, particularly those that use plant parts to nurse their breed and never were thought they could act also as mutualists, pollinating the species they infest. This is known as a case of brood site pollination mutualism (BSPM), which also involves an antagonistic counterpart (herbivory) to which plants should face. This is the focus of the manuscript (Haran et al. 2023) we are recommending here. There is wide treatment of this kind of pollination in textbooks, albeit focused on yucca-yucca moth and fig-fig wasp interactions due to their extreme specialization (Pellmyr 2003, Kjellberg et al. 2005), and more recently accompanied by Caryophyllaceae-moth relationship (Kephart et al. 2006). 

Here we find a detailed review that shows that the most diverse BSPM, in terms of number of plant and pollinator species involved, is that of weevils in the tropics. The mechanism of BSPM does not involve a unique morphological syndrome, as it is mostly functional and thus highly dependent on insect biology (Fenster & al. 2004), whereas the flower phenotypes are highly divergent among species. Probably, the inconspicuous nature of the interaction, and the overwhelming role of weevils as seed predators, even as pests, are among the causes of the neglection of weevils as pollinators, as it could be in part the case of ants as pollinators (de Vega et al. 2014). The paper by Haran et al (2023) comes to break this point.

Thus, the rarity of weevil pollination in former reports is not a consequence of an anecdotical nature of this interaction, even for the BSPM, according to the number of cases the authors are reporting, both in terms of plant and pollinator species involved. This review has a classical narrative format which involves a long text describing the natural history behind the cases. It is timely and fills the gap for this important pollination interaction for biodiversity and also for economic implications for fruit production of some crops. Former reviews have addressed related topics on BSPM but focused on other pollinators, such as those mentioned above. Besides, the review put much effort into the animal side of the interaction, which is not common in the pollination literature. Admittedly, the authors focus on the detailed description of some paradigmatic cases, and thereafter suggest that these can be more frequently reported in the future, based on varied evidence from morphology, natural history, ecology, and distribution of alleged partners. This procedure was common during the development of anthecology, an almost missing term for floral ecology (Baker 1983), relying on accumulative evidence based on detailed observations and experiments on flowers and pollinators. Currently, a quantitative approach based on the tools of macroecological/macroevolutionary analyses is more frequent in reviews. However, this approach requires a high amount of information on the natural history of the partnership, which allows for sound hypothesis testing. By accumulating this information, this approach allows the authors to pose specific questions and hypotheses which can be tested, particularly on the efficiency of the systems and their specialization degree for both the plants and the weevils, apparently higher for the latter. This will guarantee that this paper will be frequently cited by floral ecologists and evolutionary biologists and be included among the plethora of floral syndromes already described, currently based on more explicit functional grounds (Fenster et al. 2004). In part, this is one of the reasons why the sections focused on future prospects is so large in the review. 

I foresee that this mutualistic/antagonistic relationship will provide excellent study cases for the relative weight of these contrary interactions among the same partners and its relationship with pollination specialization-generalization and patterns of diversification in the plants and/or the weevils. As new studies are coming, it is possible that BSPM by weevils appears more common in non-tropical biogeographical regions. In fact, other BSPM are not so uncommon in other regions (Prieto-Benítez et al. 2017). In the future, it would be desirable an appropriate testing of the actual effect of phylogenetic niche conservatism, using well known and appropriately selected BSPM cases and robust phylogenies of both partners in the mutualism. Phylogenetic niche conservatism is a central assumption by the authors to report as many cases as possible in their review, and for that they used taxonomic relatedness. As sequence data and derived phylogenies for large numbers of vascular plant species are becoming more frequent (Jin & Quian 2022), I would recommend the authors to perform a comparative analysis using this phylogenetic information. At least, they have included information on phylogenetic relatedness of weevils involved in BSPM which allow some inferences on the multiple origins of this interaction. This is a good start to explore the drivers of these multiple origins through the lens of comparative biology.

References

Baker HG (1983) An Outline of the History of Anthecology, or Pollination Biology. In: L Real (ed). Pollination Biology. Academic Press.

de-Oliveira-Nogueira CH, Souza UF, Machado TM, Figueiredo-de-Andrade CA, Mónico AT, Sazima I, Sazima M, Toledo LF (2023). Between fruits, flowers and nectar: The extraordinary diet of the frog Xenohyla truncate. Food Webs 35: e00281. https://doi.org/10.1016/j.fooweb.2023.e00281

Fenster CB W, Armbruster S, Wilson P, Dudash MR, Thomson JD (2004). Pollination syndromes and floral specialization. Annu. Rev. Ecol. Evol. Syst. 35: 375–403. https://doi.org/10.1146/annurev.ecolsys.34.011802.132347

Gaston KJ (1994). What is rarity? In KJ Gaston (ed): Rarity. Population and Community Biology Series, vol 13. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-0701-3_1

Haran J, Kergoat GJ, Bruno, de Medeiros AS (2023) Most diverse, most neglected: weevils (Coleoptera: Curculionoidea) are ubiquitous specialized brood-site pollinators of tropical flora. hal. 03780127, version 2 peer-reviewed and recommended by Peer Community in Ecology. https://hal.inrae.fr/hal-03780127

Heiduk A, Brake I, Shuttleworth A, Johnson SD (2023) ‘Bleeding’ flowers of Ceropegia gerrardii (Apocynaceae-Asclepiadoideae) mimic wounded insects to attract kleptoparasitic fly pollinators. New Phytologist. https://doi.org/10.1111/nph.18888

Jin, Y., & Qian, H. (2022). V. PhyloMaker2: An updated and enlarged R package that can generate very large phylogenies for vascular plants. Plant Diversity, 44(4), 335-339. https://doi.org/10.1016/j.pld.2022.05.005

Kjellberg F, Jousselin E, Hossaert-Mckey M, Rasplus JY (2005). Biology, ecology, and evolution of fig-pollinating wasps (Chalcidoidea, Agaonidae). In: A. Raman et al (eds) Biology, ecology and evolution of gall-inducing arthropods 2, 539-572. Science Publishers, Enfield.

Komamura R, Koyama K, Yamauchi T, Konno Y, Gu L (2021). Pollination contribution differs among insects visiting Cardiocrinum cordatum flowers. Forests 12: 452. https://doi.org/10.3390/f12040452

Pattemore DE, Wilcove DS (2012) Invasive rats and recent colonist birds partially compensate for the loss of endemic New Zealand pollinators. Proc. R. Soc. B 279: 1597–1605. https://doi.org/10.1098/rspb.2011.2036

Pellmyr O (2003) Yuccas, yucca moths, and coevolution: a review. Ann. Missouri Bot. Gard. 90: 35-55. https://doi.org/10.2307/3298524

Prieto-Benítez S, Yela JL, Giménez-Benavides L (2017) Ten years of progress in the study of Hadena-Caryophyllaceae nursery pollination. A review in light of new Mediterranean data. Flora, 232, 63-72. https://doi.org/10.1016/j.flora.2017.02.004

Suetsugu K (2019) Social wasps, crickets and cockroaches contribute to pollination of the holoparasitic plant Mitrastemon yamamotoi (Mitrastemonaceae) in southern Japan. Plant Biology 21 176–182. https://doi.org/10.1111/plb.12889

Most diverse, most neglected: weevils (Coleoptera: Curculionoidea) are ubiquitous specialized brood-site pollinators of tropical floraJulien Haran, Gael J. Kergoat, Bruno A. S. de Medeiros<p style="text-align: justify;">In tropical environments, and especially tropical rainforests, a major part of pollination services is provided by diverse insect lineages. Unbeknownst to most, beetles, and more specifically hyperdiverse weevils (C...Biodiversity, Evolutionary ecology, Pollination, Tropical ecologyJuan Arroyo2022-09-28 11:54:37 View