Although monitoring the prevalence of pathogens in wildlife is crucial, there are logistical constraints that make this difficult, costly, and unpractical. This problem is often compounded when attempting to measure the temporal dynamics of prevalence. To improve the detection rate, a commonly used technique is pooling samples, where multiple individuals are analyzed at once. Yet, this introduces further potential biases: low-prevalence samples are effectively diluted through pooling, creating a false negative risk; negative samples are masked by the inclusion of positive samples, possibly artificially inflating the estimate of prevalence (and masking the inter-sample variability).

In their contribution, Borremans et al. (2024) come up with a modelling technique to provide accurate predictions of prevalence dynamics using a mix of pooled and individual samples. Because this model represents the pooling of individual samples as a complete mixing process, it can accurately estimate the prevalence dynamics from pooled samples only.

It is particularly noteworthy that the model provides an estimation of the false negative rate of the test. When there are false negatives (or more accurately, when the true rate at which false negatives happens), the value of the effect coefficients for individual-level covariates are likely to be off, potentially by a substantial amount. But besides more accurate coefficient estimation, the actual false negative rate is important information about the overall performance of the infection test.

The model described in this article also allows for a numerical calculation of the probability density function of infection. It is worth spending some time on how this is achieved, as I found the approach relying on combinatorics to be particularly interesting. When pooling, both the number of individuals that are mixed is known, and so is the measurement made on the pooled samples. The question is to figure out the number of individuals that because they are infectious, contribute to this score. The approach used by the authors is to draw (with replacement) possible positive and negative test outcomes assuming a number of positive individuals, and from this to estimate a pathogen concentration in the positive samples. This pathogen concentration can be transformed into its test outcome, and this value taken over all possible combinations is a conditional estimate of the test outcome, knowing the number of pooled individuals, and estimating the number of positive ones.

This approach is where the use of individual samples informs the model: by providing additional corrections for the relative volume of sample each individual provides, and by informing the transformation of test values into virus concentrations.

The authors make a strong case that their model can provide robust estimates of prevalence even in the presence of common field epidemiology pitfalls, and notably incomplete individual-level information. More importantly, because the model can work from pooled samples only, it gives additional value to samples that would otherwise have been discarded because they did not allow for prevalence estimates.

References

Benny Borremans, Caylee A. Falvo, Daniel E. Crowley, Andrew Hoegh, James O. Lloyd-Smith, Alison J. Peel, Olivier Restif, Manuel Ruiz-Aravena, Raina K. Plowright (2024) Reconstructing prevalence dynamics of wildlife pathogens from pooled and individual samples. bioRxiv, ver.3 peer-reviewed and recommended by PCI Ecology https://doi.org/10.1101/2023.11.02.565200

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

Guiding and monitoring the efficiency of conservation efforts needs robust scientific background information, of which one key element is estimating wildlife abundance and its spatial and temporal variation. As raw counts are by nature incomplete counts of a population, correcting for detectability is required (Clobert, 1995; Turlure et al., 2018). This can be done with Capture-Mark-Recapture protocols (Iijima, 2020). Techniques for marking individuals are diverse, e.g. writing on butterfly wings, banding birds, or using natural specific patterns in the individual’s body such as leopard fur or whale tail. Advancement in technology opens new opportunities for developing marking techniques, including strategies to limit mark identification errors (Burchill & Pavlic, 2019), and for using active marks that can transmit data remotely or be read automatically.

The details of such methodological developments frequently remain unpublished, the method being briefly described in studies that use it. For a few years, there has been however a renewed interest in proper publishing of methods for ecology and evolution. This study by Folk & Mennerat (2023) fits in this context, offering a nice example of detailed description and testing of a method to mark salmon ectoparasites using RFID tags. Such tags are extremely small, yet easy to use, even with automatic recording procedure. The study provides a very good basis protocol that should help researchers working for small species, in particular invertebrates. The study is complemented by a video illustrating the placement of the tag so the reader who would like to replicate the procedure can get a very precise idea of it.

References

Burchill, A. T., & Pavlic, T. P. (2019). Dude, where’s my mark? Creating robust animal identification schemes informed by communication theory. Animal Behaviour, 154, 203–208. https://doi.org/10.1016/j.anbehav.2019.05.013

Clobert, J. (1995). Capture-recapture and evolutionary ecology: A difficult wedding ? Journal of Applied Statistics, 22(5–6), 989–1008.

Folk, A., & Mennerat, A. (2023). Methods for tagging an ectoparasite, the salmon louse Lepeophtheirus salmonis (p. 2023.08.31.555695). bioRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2023.08.31.555695

Iijima, H. (2020). A Review of Wildlife Abundance Estimation Models: Comparison of Models for Correct Application. Mammal Study, 45(3), 177–188. https://doi.org/10.3106/ms2019-0082

Turlure, C., Pe’er, G., Baguette, M., & Schtickzelle, N. (2018). A simplified mark–release–recapture protocol to improve the cost effectiveness of repeated population size quantification. Methods in Ecology and Evolution, 9(3), 645–656. https://doi.org/10.1111/2041-210X.12900

How would a plant trait evolve if it is involved in interacting with both a pollinator and an herbivore species? The answer by Yacine and Loeuille is straightforward: it is not trivial, but it can explain many situations found in natural populations.

Yacine and Loeuille applied the well-known Adaptive Dynamics framework to a system with three interacting protagonists: a herbivore, a pollinator, and a plant. The evolution of a plant trait is followed under the assumption that it regulates the frequency of interaction with the two other species. As one can imagine, that is where problems begin: interacting more with pollinators seems good, but what if at the same time it implies interacting more with herbivores? And that's not a silly idea, as there are many cases where herbivores and pollinators share the same cues to detect plants, such as colors or chemical compounds.

They found that depending on the trade-off between the two types of interactions and their density-dependent effects on plant fitness, the possible joint ecological and evolutionary outcomes are numerous. When herbivory prevails, evolution can make the ménage-à-trois ecologically unstable, as one or even two species can go extinct, leaving the plant alone. Evolution can also make the coexistence of the three species more stable when pollination services prevail, or lead to the appearance of a second plant species through branching diversification of the plant trait when herbivory and pollination are balanced.

Yacine and Loeuille did not only limit themselves to saying "it is possible," but they also did much work evaluating when each evolutionary outcome would occur. They numerically explored in great detail the adaptive landscape of the plant trait for a large range of parameter values. They showed that the global picture is overall robust to parameter variations, strengthening the plausibility that the evolution of a trait involved in antagonistic interactions can explain many of the correlations between plant and animal traits or phylogenies found in nature.

Are we really there yet? Of course not, as some assumptions of the model certainly limit its scope. Are there really cases where plants' traits evolve much faster than herbivores' and pollinators' traits? Certainly not, but the model is so general that it can apply to any analogous system where one species is caught between a mutualistic and a predator species, including potential species that evolve much faster than the two others. And even though this limitation might cast doubt on the generality of the model's predictions, studying a system where a species' trait and a preference trait coevolve is possible, as other models have already been studied (see Fritsch et al. 2021 for a review in the case of evolution in food webs). We can bet this is the next step taken by Yacine and Loeuille in a similar framework with the same fundamental model, promising fascinating results, especially regarding the evolution of complex communities when species can accumulate after evolutionary branchings.

Relaxing another assumption seems more challenging as it would certainly need to change the model itself: interacting species generally do not play fixed roles, as being mutualistic or antagonistic might generally be density-dependent (Holland and DeAngelis 2010). How would the exchange of resources between three interacting species evolve? It is an open question.

References

Fritsch, C., Billiard, S., & Champagnat, N. (2021). Identifying conversion efficiency as a key mechanism underlying food webs adaptive evolution: a step forward, or backward? Oikos, 130(6), 904-930.
https://doi.org/10.1111/oik.07421
 
Holland, J. N., & DeAngelis, D. L. (2010). A consumer-resource approach to the density‐dependent population dynamics of mutualism. Ecology, 91(5), 1286-1295.
https://doi.org/10.1890/09-1163.1

Yacine, Y., & Loeuille, N. (2024) Attracting pollinators vs escaping herbivores: eco-evolutionary dynamics of plants confronted with an ecological trade-off. bioRxiv 2021.12.02.470900; doi: https://doi.org/10.1101/2021.12.02.470900

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