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

Individuals can respond to environmental changes that they undergo directly (within-generation plasticity) but also through transgenerational plasticity, providing lasting effects that are transmitted to the next generations (Donelson et al. 2012; Munday et al. 2013; Kuijper & Hoyle 2015; Auge et al. 2017, Tariel et al. 2020). These parental effects can affect offspring via various mechanisms, notably via maternal transmission of hormones to the eggs or growing embryos (Mousseau & Fox 1998). While the effects of environmental quality may simply carry-over to the next generation (e.g., females in stressful environments give birth to offspring in poorer condition), parental effects may also be a mechanism that adjusts offspring phenotype in response to environmental variation and predictability, and thereby match offspring's phenotype to future environmental conditions (Gluckman et al. 2005; Marshall & Uller 2007; Dey et al. 2016; Yin et al. 2019), for example by preparing their offspring to an expected stressful environment.

When females experience stress during gestation or egg formation, elevations in glucocorticoids (GC) are expected to affect offspring phenotype in many ways, from the offspring's own GC levels, to their growth and survival (Sheriff et al. 2017). This is a well established idea, but how strong is the evidence for this? A meta-analysis on birds found no clear effect of corticosterone manipulation on offspring traits (38 studies on 9 bird species for corticosterone manipulation; Podmokła et al. 2018). Another meta-analysis including 14 vertebrate species found no clear effect of prenatal stress on offspring GC (Thayer et al. 2018). Finally, a meta-analysis on wild vertebrates (23 species) found no clear effect of GC-mediated maternal effects on offspring traits (MacLeod et al. 2021). As often when facing such inconclusive results, context dependence has been suggested as one potential reason for such inconsistencies, for exemple sex specific effects (Groothuis et al. 2019, 2020). However, sex specific measures on offspring are scarce (Podmokła et al. 2018). Moreover, the literature available is still limited to a few, mostly “model” species.

With their study, Amin et al. (2024) show the way to improve our understanding on GC transmission from mother to offspring and its effects in several aspects. First they used innovative non-invasive methods (which could broaden the range of species available to study) by quantifying cortisol metabolites from faecal samples collected from pregnant females, as proxy for maternal GC level, and relating it to GC levels from hairs of their neonate offspring. Second they used a free ranging large mammal (taxa from which literature is missing): the fallow deer (Dama dama). Third, they provide sex specific measures of GC levels. And finally but importantly, they are exemplary in their transparency regarding 1) the exploratory nature of their study, 2) their statistical thinking and procedure, and 3) the study limitations (e.g., low sample size and high within individual variation of measurements). I hope this study will motivate more research (on the fallow deer, and on other species) to broaden and strengthen our understanding of sex specific effects of maternal stress and CG levels on offspring phenotype and fitness.

References

Amin, B., Fishman, R., Quinn, M., Matas, D., Palme, R., Koren, L., & Ciuti, S. (2024). Sex differences in the relationship between maternal and foetal glucocorticoids in a free-ranging large mammal. bioRxiv, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2023.05.04.538920 

Auge, G.A., Leverett, L.D., Edwards, B.R. & Donohue, K. (2017). Adjusting phenotypes via within-and across-generational plasticity. New Phytologist, 216, 343–349. https://doi.org/10.1111/nph.14495

Dey, S., Proulx, S.R. & Teotonio, H. (2016). Adaptation to temporally fluctuating environments by the evolution of maternal effects. PLoS biology, 14, e1002388. https://doi.org/10.1371/journal.pbio.1002388

Donelson, J.M., Munday, P.L., McCormick, M.I. & Pitcher, C.R. (2012). Rapid transgenerational acclimation of a tropical reef fish to climate change. Nature Climate Change, 2, 30. https://doi.org/10.1038/nclimate1323

Gluckman, P.D., Hanson, M.A. & Spencer, H.G. (2005). Predictive adaptive responses and human evolution. Trends in ecology & evolution, 20, 527–533. https://doi.org/10.1016/j.tree.2005.08.001

Groothuis, Ton GG, Bin-Yan Hsu, Neeraj Kumar, and Barbara Tschirren. "Revisiting mechanisms and functions of prenatal hormone-mediated maternal effects using avian species as a model." Philosophical Transactions of the Royal Society B 374, no. 1770 (2019): 20180115. https://doi.org/10.1098/rstb.2018.0115

Groothuis, Ton GG, Neeraj Kumar, and Bin-Yan Hsu. "Explaining discrepancies in the study of maternal effects: the role of context and embryo." Current Opinion in Behavioral Sciences 36 (2020): 185-192. https://doi.org/10.1016/j.cobeha.2020.10.006 

Kuijper, B. & Hoyle, R.B. (2015). When to rely on maternal effects and when on phenotypic plasticity? Evolution, 69, 950–968. https://doi.org/10.1111/evo.12635   

MacLeod, Kirsty J., Geoffrey M. While, and Tobias Uller. "Viviparous mothers impose stronger glucocorticoid‐mediated maternal stress effects on their offspring than oviparous mothers." Ecology and Evolution 11, no. 23 (2021): 17238-17259.

Marshall, D.J. & Uller, T. (2007). When is a maternal effect adaptive? Oikos, 116, 1957–1963. https://doi.org/10.1111/j.2007.0030-1299.16203.x       

Mousseau, T.A. & Fox, C.W. (1998). Maternal effects as adaptations. Oxford University Press.

Munday, P.L., Warner, R.R., Monro, K., Pandolfi, J.M. & Marshall, D.J. (2013). Predicting evolutionary responses to climate change in the sea. Ecology Letters, 16, 1488–1500. https://doi.org/10.1111/ele.12185

Podmokła, Edyta, Szymon M. Drobniak, and Joanna Rutkowska. "Chicken or egg? Outcomes of experimental manipulations of maternally transmitted hormones depend on administration method–a meta‐analysis." Biological Reviews 93, no. 3 (2018): 1499-1517. https://doi.org/10.1111/brv.12406 

Sheriff, M. J., Bell, A., Boonstra, R., Dantzer, B., Lavergne, S. G., McGhee, K. E., MacLeod, K. J., Winandy, L., Zimmer, C., & Love, O. P. (2017). Integrating ecological and evolutionary context in the study of maternal stress. Integrative and Comparative Biology, 57(3), 437–449. https://doi.org/10.1093/icb/icx105

Tariel, Juliette, Sandrine Plénet, and Émilien Luquet. "Transgenerational plasticity in the context of predator-prey interactions." Frontiers in Ecology and Evolution 8 (2020): 548660. https://doi.org/10.3389/fevo.2020.548660 

Thayer, Zaneta M., Meredith A. Wilson, Andrew W. Kim, and Adrian V. Jaeggi. "Impact of prenatal stress on offspring glucocorticoid levels: A phylogenetic meta-analysis across 14 vertebrate species." Scientific Reports 8, no. 1 (2018): 4942. https://doi.org/10.1038/s41598-018-23169-w 

Yin, J., Zhou, M., Lin, Z., Li, Q.Q. & Zhang, Y.-Y. (2019). Transgenerational effects benefit offspring across diverse environments: a meta-analysis in plants and animals. Ecology letters, 22, 1976–1986. https://doi.org/10.1111/ele.13373

Reduce the impact the intensification of human activities has on the environmental is the challenge the humanity faces today, a major challenge that could be compared to climbing Everest without an oxygen supply. Indeed, over-population, pollution, burning fossil fuels, and deforestation are all evils which have had hugely detrimental effects on the environment such as climate change, soil erosion, poor air quality, and scarcity of drinking water to name but a few. In response to the ever-growing consumer demand, agriculture has intensified massively along with a drastic increase in the use of chemicals to ensure an adequate food supply while controlling crop pests. In this context, to address the disastrous effects of the intensive usage of pesticides on both human health and biodiversity, organic farming (OF) revealed as a miracle remedy with multiple benefits. Delattre et al. (2023) present a powerful modelling approach to decipher the crossed effects of the landscape structure and the OF expansion scenario on the pest abundance, both in organic and conventional (CF) crop fields. To this end, the authors ingeniously combined a grid-based landscape model with a spatially explicit predator-pest model. Based on an extensive in silico simulation process, they explore a diversity of landscape structures differing in their amount of semi-natural habitats (SHN) and in their fragmentation, to finally propose a ranking of various expansion scenarios according to the pest control methods in organic farming as well as to the pest and predators’ dissemination capacities. In total, 9 landscape structures (3 proportions of SHN x 3 fragmentation levels) were crossed with 3 expansion scenarios (RD = a random distribution of OF and CF in the grid; IP = isolated CF are converted; GP = CF within aggregates are converted), 4 pest management practices, 3 initial densities and 36 biological parameter combinations driving the predator’ and pest’s population dynamics. This exhaustive exploration of possible combinations of landscape and farming practices highlighted the main drivers of the various OF expansion scenarios, such as increased spillover of predators in isolated OF/CF fields, increased pest management efficiency in large patches of CF and the importance of the distance between OF and CF. In the end, this study brings to light the crucial role that landscape planning plays when OF practices have limited efficiency on pests. It also provides convincing arguments to the fact that converting to organic isolated CF as a priority seems to be the most promising scenario to limit pest densities in CF crops while improving predator to pest ratios (considered as a proxy of conservation biological control) in OF ones without increasing pest densities. Once further completed with model calibration validation based on observed life history traits data for both predators and pests, this work should be very helpful in sustaining policy makers to convince farmers of engaging in organic farming.

REFERENCES

Delattre T, Memah M-M, Franck P, Valsesia P, Lavigne C (2023) Best organic farming deployment scenarios for pest control: a modeling approach. bioRxiv, 2022.05.31.494006, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.05.31.494006

Michael Raatz (2023) provides here a relevant exploration of higher-order interactions, i.e. interactions involving more than two related species (Terry et al. 2019), in the case of food web and competition interactions. More precisely, he shows by modeling that essential resources may significantly mediate focal species' persistence. Simultaneously, the provision of essential resources may strongly affect the resulting community structure, by driving to extinction first the predator and then, depending on the higher-order interaction, potentially also the associated competitor. 

Today, all ecologists should be aware of the potential effects of high-order interactions on species' (and likely on ecosystem's) fate (Golubski et al. 2016, Grilli et al. 2017). Yet, we should soon be prepared to include any high-order interaction into any interaction network (i.e. not only between species, but also between species and abiotic components, and between biotic, anthropogenic and abiotic components too). For this purpose, we will need innovative approaches such as hypergraphs (Golubski et al. 2016) and discrete-event models (Gaucherel and Pommereau 2019, Thomas et al. 2022) able to manage highly complex interactions, with numerous interacting components and variables. Such a rigorous study is a necessary and preliminary step in taking into account such a higher complexity. 

References

Gaucherel, C. and F. Pommereau. 2019. Using discrete systems to exhaustively characterize the dynamics of an integrated ecosystem. Methods in Ecology and Evolution 00:1–13. https://doi.org/10.1111/2041-210X.13242

Golubski, A. J., E. E. Westlund, J. Vandermeer, and M. Pascual. 2016. Ecological Networks over the Edge: Hypergraph Trait-Mediated Indirect Interaction (TMII) Structure trends in Ecology & Evolution 31:344-354. https://doi.org/10.1016/j.tree.2016.02.006

Grilli, J., G. Barabas, M. J. Michalska-Smith, and S. Allesina. 2017. Higher-order interactions stabilize dynamics in competitive network models. Nature 548:210-213. https://doi.org/10.1038/nature23273

Raatz, M. 2023. Provision of essential resources as a persistence strategy in food webs. bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2023.01.27.525839

Terry, J. C. D., R. J. Morris, and M. B. Bonsall. 2019. Interaction modifications lead to greater robustness than pairwise non-trophic effects in food webs. Journal of Animal Ecology 88:1732-1742. https://doi.org/10.1111/1365-2656.13057

Thomas, C., M. Cosme, C. Gaucherel, and F. Pommereau. 2022. Model-checking ecological state-transition graphs. PLoS Computational Biology 18:e1009657. https://doi.org/10.1371/journal.pcbi.1009657

Mimicry between species has long attracted the attention of scientists. Over a century ago, Bates first proposed that palatable species should gain a benefit by resembling unpalatable species (Bates 1862). Not long after, Müller suggested that there could also be a mutual advantage for two unpalatable species to mimic one another to reduce predator error (Müller 1879). These forms of mimicry, Batesian and Müllerian, are now widely studied, providing broad insights into behaviour, ecology and evolution.

Numerous taxa, including both invertebrates and vertebrates, show examples of Batesian or Müllerian mimicry. Bees and wasps provide a particularly interesting case due to the differences in defence between females and males of the same species. While both males and females may display warning colours, only females can sting and inject venom to cause pain and allow escape from predators. Therefore, males are palatable mimics and can resemble females of their own species or females of another species (dual sex-limited mimicry). This asymmetry in defence could have impacts on both population structure and community assembly, yet research into mimicry largely focuses on systems without sex differences.

Here, Boutin and colleagues (2023) use a differential equations model to explore the effect of mimicry on population structure and community assembly for sex-limited defended species. Specifically, they address three questions, 1) how do female noxiousness and sex-ratio influence the extinction risk of a single species?; 2) what is the effect of mimicry on species co-existence? and 3) how does dual sex-limited mimicry influence species co-existence? Their results reveal contexts in which populations with undefended males can persist, the benefit of Müllerian mimicry for species coexistence and that dual sex-limited mimicry can have a destabilising impact on species coexistence.

The results not only contribute to our understanding of how mimicry is maintained in natural systems but also demonstrate how changes in relative abundance or population structure of one species could impact another species. Further insight into the population and community dynamics of insects is particularly important given the current population declines (Goulson 2019; Seibold et al 2019).

References

Bates, H. W. 1862. Contributions to the insect fauna of the Amazon Valley, Lepidoptera: Heliconidae. Trans. Linn. Soc. Lond. 23:495- 566. https://doi.org/10.1111/j.1096-3642.1860.tb00146.x

Boutin, M., Costa, M., Fontaine, C., Perrard, A., Llaurens, V. 2022 Influence of sex-limited mimicry on extinction risk in Aculeata: a theoretical approach. bioRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.10.21.513153

Goulson, D. 2019. The insect apocalypse, and why it matters. Curr. Biol. 29: R967-R971. https://doi.org/10.1016/j.cub.2019.06.069

Müller, F. 1879. Ituna and Thyridia; a remarkable case of mimicry in butterflies. Trans. Roy. Entom. Roc. 1879:20-29.

Seibold, S., Gossner, M. M., Simons, N. K., Blüthgen, N., Müller, J., Ambarlı, D., ... & Weisser, W. W. 2019. Arthropod decline in grasslands and forests is associated with landscape-level drivers. Nature, 574: 671-674. https://doi.org/10.1038/s41586-019-1684-3