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12 Aug 2021
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A study on the role of social information sharing leading to range expansion in songbirds with large vocal repertoires: Enhancing our understanding of the Great-Tailed Grackle (Quiscalus mexicanus) alarm call

Does the active vocabulary in Great-tailed Grackles supports their range expansion? New study will find out

Recommended by Jan Oliver Engler based on reviews by Guillermo Fandos and 2 anonymous reviewers

Alarm calls are an important acoustic signal that can decide the life or death of an individual. Many birds are able to vary their alarm calls to provide more accurate information on e.g. urgency or even the type of a threatening predator. According to the acoustic adaptation hypothesis, the habitat plays an important role too in how acoustic patterns get transmitted. This is of particular interest for range-expanding species that will face new environmental conditions along the leading edge. One could hypothesize that the alarm call repertoire of a species could increase in newly founded ranges to incorporate new habitats and threats individuals might face. Hence selection for a larger active vocabulary might be beneficial for new colonizers. Using the Great-Tailed Grackle (Quiscalus mexicanus) as a model species, Samantha Bowser from Arizona State University and Maggie MacPherson from Louisiana State University want to find out exactly that. 

The Great-Tailed Grackle is an appropriate species given its high vocal diversity. Also, the species consists of different subspecies that show range expansions along the northern range edge yet to a varying degree. Using vocal experiments and field recordings the researchers have a high potential to understand more about the acoustic adaptation hypothesis within a range dynamic process. 

Over the course of this assessment, the authors incorporated the comments made by two reviewers into a strong revision of their research plans. With that being said, the few additional comments made by one of the initial reviewers round up the current stage this interesting research project is in. 

To this end, I can only fully recommend the revised research plan and am much looking forward to the outcomes from the author’s experiments, modeling, and field data. With the suggestions being made at such an early stage I firmly believe that the final outcome will be highly interesting not only to an ornithological readership but to every ecologist and biogeographer interested in drivers of range dynamic processes.

References

Bowser, S., MacPherson, M. (2021). A study on the role of social information sharing leading to range expansion in songbirds with large vocal repertoires: Enhancing our understanding of the Great-Tailed Grackle (Quiscalus mexicanus) alarm call. In principle recommendation by PCI Ecology. https://doi.org/10.17605/OSF.IO/2UFJ5. Version 3

A study on the role of social information sharing leading to range expansion in songbirds with large vocal repertoires: Enhancing our understanding of the Great-Tailed Grackle (Quiscalus mexicanus) alarm call Samantha Bowser, Maggie MacPherson<p>The acoustic adaptation hypothesis posits that animal sounds are influenced by the habitat properties that shape acoustic constraints (Ey and Fischer 2009, Morton 2015, Sueur and Farina 2015).Alarm calls are expected to signal important habitat...Biogeography, Biological invasions, Coexistence, Dispersal & Migration, Habitat selection, Landscape ecologyJan Oliver Engler Darius Stiels, Anonymous2020-12-01 18:11:02 View
14 May 2019
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Field assessment of precocious maturation in salmon parr using ultrasound imaging

OB-GYN for salmon parrs

Recommended by ORCID_LOGO based on reviews by Hervé CAPRA and 1 anonymous reviewer

Population dynamics and stock assessment models are only as good as the data used to parameterise them. For Atlantic salmon (Salmo salar) populations, a critical parameter may be frequency of precocious maturation. Indeed, the young males (parrs) that mature early, before leaving the river to reach the ocean, can contribute to reproduction but have much lower survival rates afterwards. The authors cite evidence of the potentially major consequences of this alternate reproductive strategy. So, to be parameterised correctly, it needs to be assessed correctly. Cue the ultrasound machine.

Through a thorough analysis of data collected on 850 individuals [1], over three years, the authors clearly show that the non-invasive examination of the internal cavity of young fishes to look for gonads, using a portable ultrasound machine, provides reliable and replicable evidence of precocious maturation. They turned into OB-GYN for salmons (albeit for male salmons!) and it worked. While using ultrasounds to detect fish gonads is not a new idea (early attempts for salmonids date back to the 80s [2]), the value here is in the comparison with the classic visual inspection technique (which turns out to be less reliable) and the fact that ultrasounds can now easily be carried out in the field.

Beyond the potentially important consequences of this new technique for the correct assessment of salmon population dynamics, the authors also make the case for the acquisition of more reliable individual-level data in ecological studies, which I applaud.

References.

[1] Nevoux M, Marchand F, Forget G, Huteau D, Tremblay J, and Destouches J-P. (2019). Field assessment of precocious maturation in salmon parr using ultrasound imaging. bioRxiv 425561, ver. 3 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/425561
[2] Reimers E, Landmark P, Sorsdal T, Bohmer E, Solum T. (1987). Determination of salmonids’ sex, maturation and size: an ultrasound and photocell approach. Aquaculture Magazine.13:41-44.

Field assessment of precocious maturation in salmon parr using ultrasound imagingMarie Nevoux, Frédéric Marchand, Guillaume Forget, Dominique Huteau, Julien Tremblay, Jean-Pierre Destouches<p>Salmonids are characterized by a large diversity of life histories, but their study is often limited by the imperfect observation of the true state of an individual in the wild. Challenged by the need to reduce uncertainty of empirical data, re...Conservation biology, Demography, Experimental ecology, Freshwater ecology, Life history, Phenotypic plasticity, Population ecologyJean-Olivier Irisson2018-09-25 17:24:59 View
17 Mar 2021
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Intra and inter-annual climatic conditions have stronger effect than grazing intensity on root growth of permanent grasslands

Resolving herbivore influences under climate variability

Recommended by based on reviews by 3 anonymous reviewers

We know that herbivory can have profound influences on plant communities with respect to their distribution and productivity (recently reviewed by Jia et al. 2018). However, the degree to which these effects are realized belowground in the rhizosphere is far less understood. Indeed, many independent studies and synthesis find that the environmental context can be more important than the direct effects of herbivore activity and its removal of plant biomass (Andriuzzi and Wall 2017, Schrama et al. 2013). In spite of dedicated attention, generalizable conclusions remain a bit elusive (Sitters and Venterink 2015). Picon-Cochard and colleagues (2021) help address this research conundrum in an elegant analysis that demonstrates the interaction between long-term cattle grazing and climatic variability on primary production aboveground and belowground. 

Over the course of two years, Picon-Cochard et al. (2021) measured above and belowground net primary productivity in French grasslands that had been subject to ten years of managed cattle grazing. When they compared these data with climatic trends, they find an interesting interaction among grazing intensity and climatic factors influencing plant growth.  In short, and as expected, plants allocate more resources to root growth in dry years and more to above ground biomass in wet and cooler years. However, this study reveals the degree to which this is affected by cattle grazing. Grazed grasslands support warmer and dryer soils creating feedback that further and significantly promotes root growth over green biomass production.  

The implications of this work to understanding the capacity of grassland soils to store carbon is profound. This study addresses one brief moment in time of the long trajectory of this grazed ecosystem. The legacy of grazing does not appear to influence soil ecosystem functioning with respect to root growth except within the environmental context, in this case, climate. This supports the notion that long-term research in animal husbandry and grazing effects on landscapes is deeded. It is my hope that this study is one of many that can be used to synthesize many different data sets and build a deeper understanding of the long-term effects of grazing and herd management within the context of a changing climate.  Herbivory has a profound influence upon ecosystem health and the distribution of plant communities (Speed and Austrheim 2017), global carbon storage (Chen and Frank 2020) and nutrient cycling (Sitters et al. 2020). The analysis and results presented by Picon-Cochard (2021) help to resolve the mechanisms that underly these complex effects and ultimately make projections for the future.

References

Andriuzzi WS, Wall DH. 2017. Responses of belowground communities to large aboveground herbivores: Meta‐analysis reveals biome‐dependent patterns and critical research gaps. Global Change Biology 23:3857-3868. doi: https://doi.org/10.1111/gcb.13675

Chen J, Frank DA. 2020. Herbivores stimulate respiration from labile and recalcitrant soil carbon pools in grasslands of Yellowstone National Park. Land Degradation & Development 31:2620-2634. doi: https://doi.org/10.1002/ldr.3656

Jia S, Wang X, Yuan Z, Lin F, Ye J, Hao Z, Luskin MS. 2018. Global signal of top-down control of terrestrial plant communities by herbivores. Proceedings of the National Academy of Sciences 115:6237-6242. doi: https://doi.org/10.1073/pnas.1707984115

Picon-Cochard C, Vassal N, Martin R, Herfurth D, Note P, Louault F. 2021. Intra and inter-annual climatic conditions have stronger effect than grazing intensity on root growth of permanent grasslands. bioRxiv, 2020.08.23.263137, version 6 peer-reviewed and recommended by PCI Ecology. doi: https://doi.org/10.1101/2020.08.23.263137

Schrama M, Veen GC, Bakker EL, Ruifrok JL, Bakker JP, Olff H. 2013. An integrated perspective to explain nitrogen mineralization in grazed ecosystems. Perspectives in Plant Ecology, Evolution and Systematics 15:32-44. doi: https://doi.org/10.1016/j.ppees.2012.12.001

Sitters J, Venterink HO. 2015. The need for a novel integrative theory on feedbacks between herbivores, plants and soil nutrient cycling. Plant and Soil 396:421-426. doi: https://doi.org/10.1007/s11104-015-2679-y

Sitters J, Wubs EJ, Bakker ES, Crowther TW, Adler PB, Bagchi S, Bakker JD, Biederman L, Borer ET, Cleland EE. 2020. Nutrient availability controls the impact of mammalian herbivores on soil carbon and nitrogen pools in grasslands. Global Change Biology 26:2060-2071. doi: https://doi.org/10.1111/gcb.15023

Speed JD, Austrheim G. 2017. The importance of herbivore density and management as determinants of the distribution of rare plant species. Biological Conservation 205:77-84. doi: https://doi.org/10.1016/j.biocon.2016.11.030

Intra and inter-annual climatic conditions have stronger effect than grazing intensity on root growth of permanent grasslandsCatherine Picon-Cochard, Nathalie Vassal, Raphaël Martin, Damien Herfurth, Priscilla Note, Frédérique Louault<p>Background and Aims: Understanding how direct and indirect changes in climatic conditions, management, and species composition affect root production and root traits is of prime importance for the delivery of carbon sequestration services of gr...Agroecology, Biodiversity, Botany, Community ecology, Ecosystem functioningJennifer Krumins2020-08-30 19:27:30 View
26 Mar 2019
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Is behavioral flexibility linked with exploration, but not boldness, persistence, or motor diversity?

Probing behaviors correlated with behavioral flexibility

Recommended by based on reviews by 2 anonymous reviewers

Behavioral plasticity, which is a subset of phenotypic plasticity, is an important component of foraging, defense against predators, mating, and many other behaviors. More specifically, behavioral flexibility, in this study, captures how quickly individuals adapt to new circumstances. In cases where individuals disperse to new environments, which often occurs in range expansions, behavioral flexibility is likely crucial to the chance that individuals can establish in these environments. Thus, it is important to understand how best to measure behavioral flexibility and how measures of such flexibility might vary across individuals and behavioral contexts and with other measures of learning and problem solving.
In this preregistration, Logan and colleagues propose to use a long-term study of the great-tailed grackle to measure how much they can manipulate behavioral flexibility in a reversal learning task, how much behavioral flexibility in one task predicts flexibility in another task and in problem solving a new task, and how robust these patterns are within individuals and across tasks. Logan and colleagues lay out their hypotheses and predictions for each experiment in a clear and concise manner. They also are very clear about the details of their study system, such as how they determined the number of trials they use in their learning reversal experiments, and how those details have influenced their experimental design. Further, given that the preregistration uses RMarkdown and is stored on GitHub (as are other studies in the larger project), their statistical code and its history of modification are easily available. This is a crucial component of making research more reproducible, which is a recent emphasis in behavioral sciences more broadly.
Reviewers of this preregistration found the study of substantial merit. The authors have responded to the reviewers' comments and their revisions have made the preregistration much clearer and cogent. I am happy to recommend this preregistration.

Is behavioral flexibility linked with exploration, but not boldness, persistence, or motor diversity?Kelsey McCune, Carolyn Rowney, Luisa Bergeron, Corina LoganThis is a PREREGISTRATION. The DOI was issued by OSF and refers to the whole GitHub repository, which contains multiple files. The specific file we are submitting is g_exploration.Rmd, which is easily accessible at GitHub at https://github.com/cor...Behaviour & Ethology, Preregistrations, ZoologyJeremy Van Cleve2018-09-27 03:35:12 View
29 Mar 2021
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Temperature predicts the maximum tree-species richness and water and frost shape the residual variation

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

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

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

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

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

References

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Temperature predicts the maximum tree-species richness and water and frost shape the residual variationRicardo A. Segovia<p>The kinetic hypothesis of biodiversity proposes that temperature is the main driver of variation in species richness, given its exponential effect on biological activity and, potentially, on rates of diversification. However, limited support fo...Biodiversity, Biogeography, Botany, Macroecology, Species distributionsJoaquín Hortal2019-11-10 20:56:40 View
18 Dec 2020
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Once upon a time in the far south: Influence of local drivers and functional traits on plant invasion in the harsh sub-Antarctic islands

A meaningful application of species distribution models and functional traits to understand invasion dynamics

Recommended by based on reviews by Paula Matos and Peter Convey

Polar and subpolar regions are fragile environments, where the introduction of alien species may completely change ecosystem dynamics if the alien species become keystone species (e.g. Croll, 2005). The increasing number of human visits, together with climate change, are favouring the introduction and settling of new invaders to these regions, particularly in Antarctica (Hughes et al. 2015). Within this context, the joint use of Species Distribution Models (SDM) –to assess the areas potentially suitable for the aliens– with other measures of the potential to become successful invaders can inform on the need for devoting specific efforts to eradicate these new species before they become naturalized (e.g. Pertierra et al. 2016).
Bazzichetto et al. (2020) use data from a detailed inventory, SDMs and trait data altogether to assess the drivers of invasion success of six alien plants on Possession Island, in the remote sub-Antarctic archipelago of Crozet. SDMs have inherent limitations to describe different aspects of species distributions, including the fundamental niche and, with it, the areas that could host viable populations (Hortal et al. 2012). Therefore, their utility to predict future biological invasions is limited (Jiménez-Valverde et al. 2011). However, they can be powerful tools to describe species range dynamics if they are thoughtfully used by adopting conscious decisions about the techniques and data used, and interpreting carefully the actual implications of their results.
This is what Bazzichetto et al. (2020) do, using General Linear Models (GLM) –a technique well rooted in the original niche-based SDM theory (e.g. Austin 1990)– that can provide a meaningful description of the realized niche within the limits of an adequately sampled region. Further, as alien species share and are similarly affected by several steps of the invasion process (Richardson et al. 2000), these authors model the realized distribution of the six species altogether. This can be done through the recently developed joint-SDM, a group of techniques where the co-occurrence of the modelled species is explicitly taken into account during modelling (e.g. Pollock et al. 2014). Here, the addition of species traits has been identified as a key step to understand the associations of species in space (see Dormann et al. 2018). Bazzichetto et al. (2020) combine their GLM-based SDM for each species with a so-called multi-SDM approach, where they assess together the consistency in the interactions between both species and topographically-driven climate variations, and several plant traits and two key anthropic factors –accessibility from human settlements and distance to hiking paths.
This work is a good example on how a theoretically meaningful SDM approach can provide useful –though perhaps not deep– insights on biological invasions for remote landscapes threatened by biotic homogenization. By combining climate and topographic variables as proxies for the spatial variations in the abiotic conditions regulating plant growth, measures of accessibility, and traits of the plant invaders, Bazzichetto et al. (2020) are able to identify the different effects that the interactions between the potential intensity of propagule dissemination by humans, and the ecological characteristics of the invaders themselves, may have on their invasion success.
The innovation of modelling together species responses is important because it allows dissecting the spatial dynamics of spread of the invaders, which indeed vary according to a handful of their traits. For example, their results show that no all old residents have profited from the larger time of residence in the island, as Poa pratensis is seemingly as dependent of a higher intensity of human activity as the newcomer invaders in general are. According to Bazzichetto et al. trait-based analyses, these differences are apparently related with plant height, as smaller plants disperse more easily. Further, being perennial also provides an advantage for the persistence in areas with less human influence. This puts name, shame and fame to the known influence of plant life history on their dispersal success (Beckman et al. 2018), at least for the particular case of plant invasions in Possession Island.
Of course this approach has limitations, as data on the texture, chemistry and temperature of the soil are not available, and thus were not considered in the analyses. These factors may be critical for both establishment and persistence of small plants in the harsh Antarctic environments, as Bazzichetto et al. (2020) recognize. But all in all, their results provide key insights on which traits may confer alien plants with a higher likelihood of becoming successful invaders in the fragile Antarctic and sub-Antarctic ecosystems. This opens a way for rapid assessments of invasibility, which will help identifying which species in the process of naturalizing may require active contention measures to prevent them from becoming ecological game changers and cause disastrous cascade effects that shift the dynamics of native ecosystems.

References

Austin, M. P., Nicholls, A. O., and Margules, C. R. (1990). Measurement of the realized qualitative niche: environmental niches of five Eucalyptus species. Ecological Monographs, 60(2), 161-177. doi: https://doi.org/10.2307/1943043
Bazzichetto, M., Massol, F., Carboni, M., Lenoir, J., Lembrechts, J. J. and Joly, R. (2020) Once upon a time in the far south: Influence of local drivers and functional traits on plant invasion in the harsh sub-Antarctic islands. bioRxiv, 2020.07.19.210880, ver. 3 peer-reviewed and recommended by PCI Ecology. doi: https://doi.org/10.1101/2020.07.19.210880
Beckman, N. G., Bullock, J. M., and Salguero-Gómez, R. (2018). High dispersal ability is related to fast life-history strategies. Journal of Ecology, 106(4), 1349-1362. doi: https://doi.org/10.1111/1365-2745.12989
Croll, D. A., Maron, J. L., Estes, J. A., Danner, E. M., and Byrd, G. V. (2005). Introduced predators transform subarctic islands from grassland to tundra. Science, 307(5717), 1959-1961. doi: https://doi.org/10.1126/science.1108485
Dormann, C. F., Bobrowski, M., Dehling, D. M., Harris, D. J., Hartig, F., Lischke, H., Moretti, M. D., Pagel, J., Pinkert, S., Schleuning, M., Schmidt, S. I., Sheppard, C. S., Steinbauer, M. J., Zeuss, D., and Kraan, C. (2018). Biotic interactions in species distribution modelling: 10 questions to guide interpretation and avoid false conclusions. Global Ecology and Biogeography, 27(9), 1004-1016. doi: https://doi.org/10.1111/geb.12759
Jiménez-Valverde, A., Peterson, A., Soberón, J., Overton, J., Aragón, P., and Lobo, J. (2011). Use of niche models in invasive species risk assessments. Biological Invasions, 13(12), 2785-2797. doi: https://doi.org/10.1007/s10530-011-9963-4
Hortal, J., Lobo, J. M., and Jiménez-Valverde, A. (2012). Basic questions in biogeography and the (lack of) simplicity of species distributions: Putting species distribution models in the right place. Natureza & Conservação – Brazilian Journal of Nature Conservation, 10(2), 108-118. doi: https://doi.org/10.4322/natcon.2012.029
Hughes, K. A., Pertierra, L. R., Molina-Montenegro, M. A., and Convey, P. (2015). Biological invasions in terrestrial Antarctica: what is the current status and can we respond? Biodiversity and Conservation, 24(5), 1031-1055. doi: https://doi.org/10.1007/s10531-015-0896-6
Pertierra, L. R., Baker, M., Howard, C., Vega, G. C., Olalla-Tarraga, M. A., and Scott, J. (2016). Assessing the invasive risk of two non-native Agrostis species on sub-Antarctic Macquarie Island. Polar Biology, 39(12), 2361-2371. doi: https://doi.org/10.1007/s00300-016-1912-3
Pollock, L. J., Tingley, R., Morris, W. K., Golding, N., O'Hara, R. B., Parris, K. M., Vesk, P. A., and McCarthy, M. A. (2014). Understanding co-occurrence by modelling species simultaneously with a Joint Species Distribution Model (JSDM). Methods in Ecology and Evolution, 5(5), 397-406. doi: https://doi.org/10.1111/2041-210X.12180
Richardson, D. M., Pyšek, P., Rejmánek, M., Barbour, M. G., Panetta, F. D., and West, C. J. (2000). Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions, 6(2), 93-107. doi: https://doi.org/10.1046/j.1472-4642.2000.00083.x

Once upon a time in the far south: Influence of local drivers and functional traits on plant invasion in the harsh sub-Antarctic islandsManuele Bazzichetto, François Massol, Marta Carboni, Jonathan Lenoir, Jonas Johan Lembrechts, Rémi Joly, David Renault<p>Aim Here, we aim to: (i) investigate the local effect of environmental and human-related factors on alien plant invasion in sub-Antarctic islands; (ii) explore the relationship between alien species features and their dependence on anthropogeni...Biogeography, Biological invasions, Spatial ecology, Metacommunities & Metapopulations, Species distributionsJoaquín Hortal2020-07-21 21:13:08 View
27 Apr 2021
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Joint species distributions reveal the combined effects of host plants, abiotic factors and species competition as drivers of species abundances in fruit flies

Understanding the interplay between host-specificity, environmental conditions and competition through the sound application of Joint Species Distribution Models

Recommended by based on reviews by Joaquín Calatayud and Carsten Dormann

Understanding why and how species coexist in local communities is one of the central questions in ecology. There is general agreement that species distribution and coexistence are determined by a number of key mechanisms, including the environmental requirements of species, dispersal, evolutionary constraints, resource availability and selection, metapopulation dynamics, and biotic interactions (e.g. Soberón & Nakamura 2009; Colwell & Rangel 2009; Ricklefs 2015). These factors are however intricately intertwined in a scale-structured fashion (Hortal et al. 2010; D’Amen et al. 2017), making it particularly difficult to tease apart the effects of each one of them. This could be addressed by the novel field of Joint Species Distribution Modelling (JSDM; Okasvainen & Abrego 2020), as it allows assessing the effects of several sets of factors and the co-occurrence and/or covariation in abundances of potentially interacting species at the same time (Pollock et al. 2014; Ovaskainen et al. 2016; Dormann et al. 2018). However, the development of JSDM has been hampered by the general lack of good-quality detailed data on species co-occurrences and abundances (see Hortal et al. 2015).

Facon et al. (2021) use a particularly large compilation of field surveys to study the abundance and co-occurrence of Tephritidae fruit flies in c. 400 orchards, gardens and natural areas throughout the island of Réunion. Further, they combine such information with lab data on their host-selection fundamental niche (i.e. in the absence of competitors), codifying traits of female choice and larval performances in 21 host species. They use Poisson Log-Normal models, a type of mixed model that allows one to jointly model the random effects associated with all species, and retrieve the covariations in abundance that are not explained by environmental conditions or differences in sampling effort. Then, they use a series of models to evaluate the effects on these matrices of ecological covariates (date, elevation, habitat, climate and host plant), species interactions (by comparing with a constrained residual variance-covariance matrix) and the species’ host-selection fundamental niches (through separate models for each fly species).

The eight Tephritidae species inhabiting Réunion include both generalists and specialists in Solanaceae and Cucurbitaceae with a known history of interspecific competition. Facon et al. (2021) use a comprehensive JSDM approach to assess the effects of different factors separately and altogether. This allows them to identify large effects of plant hosts and the fundamental host-selection niche on species co-occurrence, but also to show that ecological covariates and weak –though not negligible– species interactions are necessary to account for all residual variance in the matrix of joint species abundances per site. Further, they also find evidence that the fitness per host measured in the lab has a strong influence on the abundances in each host plant in the field for specialist species, but not for generalists. Indeed, the stronger effects of competitive exclusion were found in pairs of Cucurbitaceae specialist species. However, these analyses fail to provide solid grounds to assess why generalists are rarely found in Cucurbitaceae and Solanaceae. Although they argue that this may be due to Connell’s (1980) ghost of competition past (past competition that led to current niche differentiation), further data on the evolutionary history of these fruit flies is needed to assess this hypothesis.

Finding evidence for the effects of competitive interactions on species’ occurrences and spatial distributions is often difficult, perhaps because these effects occur over longer time scales than the ones usually studied by ecologists (Yackulic 2017). The work by Facon and colleagues shows that weak effects of competition can be detected also at the short ecological timescales that determine coexistence in local communities, under the virtuous combination of good-quality data and sound analytical designs that account for several aspects of species’ niches, their biotopes and their joint population responses. This adds a new dimension to the application of Hutchinson’s (1978) niche framework to understand the spatial dynamics of species and communities (see also Colwell & Rangel 2009), although further advances to incorporate dispersal-driven metacommunity dynamics (see, e.g., Ovaskainen et al. 2016; Leibold et al. 2017) are certainly needed. Nonetheless, this work shows the potential value of in-depth analyses of species coexistence based on combining good-quality field data with well-thought out JSDM applications. If many studies like this are conducted, it is likely that the uprising field of Joint Species Distribution Modelling will improve our understanding of the hierarchical relationships between the different factors affecting species coexistence in ecological communities in the near future.

 

References

Colwell RK, Rangel TF (2009) Hutchinson’s duality: The once and future niche. Proceedings of the National Academy of Sciences, 106, 19651–19658. https://doi.org/10.1073/pnas.0901650106

Connell JH (1980) Diversity and the Coevolution of Competitors, or the Ghost of Competition Past. Oikos, 35, 131–138. https://doi.org/10.2307/3544421

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

Dormann CF, Bobrowski M, Dehling DM, Harris DJ, Hartig F, Lischke H, Moretti MD, Pagel J, Pinkert S, Schleuning M, Schmidt SI, Sheppard CS, Steinbauer MJ, Zeuss D, Kraan C (2018) Biotic interactions in species distribution modelling: 10 questions to guide interpretation and avoid false conclusions. Global Ecology and Biogeography, 27, 1004–1016. https://doi.org/10.1111/geb.12759

Facon B, Hafsi A, Masselière MC de la, Robin S, Massol F, Dubart M, Chiquet J, Frago E, Chiroleu F, Duyck P-F, Ravigné V (2021) Joint species distributions reveal the combined effects of host plants, abiotic factors and species competition as drivers of community structure in fruit flies. bioRxiv, 2020.12.07.414326. ver. 4 peer-reviewed and recommended by Peer community in Ecology. https://doi.org/10.1101/2020.12.07.414326

Hortal J, de Bello F, Diniz-Filho JAF, Lewinsohn TM, Lobo JM, Ladle RJ (2015) Seven Shortfalls that Beset Large-Scale Knowledge of Biodiversity. Annual Review of Ecology, Evolution, and Systematics, 46, 523–549. https://doi.org/10.1146/annurev-ecolsys-112414-054400

Hortal J, Roura‐Pascual N, Sanders NJ, Rahbek C (2010) Understanding (insect) species distributions across spatial scales. Ecography, 33, 51–53. https://doi.org/10.1111/j.1600-0587.2009.06428.x

Hutchinson, G.E. (1978) An introduction to population biology. Yale University Press, New Haven, CT.

Leibold MA, Chase JM, Ernest SKM (2017) Community assembly and the functioning of ecosystems: how metacommunity processes alter ecosystems attributes. Ecology, 98, 909–919. https://doi.org/10.1002/ecy.1697

Ovaskainen O, Abrego N (2020) Joint Species Distribution Modelling: With Applications in R. Cambridge University Press, Cambridge. https://doi.org/10.1017/9781108591720

Ovaskainen O, Roy DB, Fox R, Anderson BJ (2016) Uncovering hidden spatial structure in species communities with spatially explicit joint species distribution models. Methods in Ecology and Evolution, 7, 428–436. https://doi.org/10.1111/2041-210X.12502

Pollock LJ, Tingley R, Morris WK, Golding N, O’Hara RB, Parris KM, Vesk PA, McCarthy MA (2014) Understanding co-occurrence by modelling species simultaneously with a Joint Species Distribution Model (JSDM). Methods in Ecology and Evolution, 5, 397–406. https://doi.org/10.1111/2041-210X.12180

Ricklefs RE (2015) Intrinsic dynamics of the regional community. Ecology Letters, 18, 497–503. https://doi.org/10.1111/ele.12431

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

Yackulic CB (2017) Competitive exclusion over broad spatial extents is a slow process: evidence and implications for species distribution modeling. Ecography, 40, 305–313. https://doi.org/10.1111/ecog.02836

Joint species distributions reveal the combined effects of host plants, abiotic factors and species competition as drivers of species abundances in fruit fliesBenoit Facon, Abir Hafsi, Maud Charlery de la Masselière, Stéphane Robin, François Massol, Maxime Dubart, Julien Chiquet, Enric Frago, Frédéric Chiroleu, Pierre-François Duyck & Virginie Ravigné<p style="text-align: justify;">The relative importance of ecological factors and species interactions for phytophagous insect species distributions has long been a controversial issue. Using field abundances of eight sympatric Tephritid fruit fli...Biodiversity, Coexistence, Community ecology, Competition, Herbivory, Interaction networks, Species distributionsJoaquín Hortal Carsten Dormann, Joaquín Calatayud2020-12-08 06:44:25 View
16 Jun 2023
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Colonisation debt: when invasion history impacts current range expansion

Combining stochastic models and experiments to understand dispersal in heterogeneous environments

Recommended by based on reviews by 2 anonymous reviewers

Dispersal is a key element of the natural dynamics of meta-communities, and plays a central role in the success of populations colonizing new landscapes. Understanding how demographic processes may affect the speed at which alien species spread through environmentally-heterogeneous habitat fragments is therefore of key importance to manage biological invasions. This requires studying together the complex interplay of dispersal and population processes, two inextricably related phenomena that can produce many possible outcomes. Stochastic models offer an opportunity to describe this kind of process in a meaningful way, but to ensure that they are realistic (sensu Levins 1966) it is also necessary to combine model simulations with empirical data (Snäll et al. 2007).

Morel-Journel et al. (2023) put together stochastic models and experimental data to study how population density may affect the speed at which alien species spread through a heterogeneous landscape. They do it by focusing on what they call ‘colonisation debt’, which is merely the impact that population density at the invasion front may have on the speed at which the species colonizes patches of different carrying capacities. They investigate this issue through two largely independent approaches. First, a stochastic model of dispersal throughout the patches of a linear, 1-dimensional landscape, which accounts for different degrees of density-dependent growth. And second, a microcosm experiment of a parasitoid wasp colonizing patches with different numbers of host eggs. In both cases, they compare the velocity of colonization of patches with lower or higher carrying capacity than the previous one (i.e. what they call upward or downward gradients).

Their results show that density-dependent processes influence the speed at which new fragments are colonized is significantly reduced by positive density dependence. When either population growth or dispersal rate depend on density, colonisation debt limits the speed of invasion, which turns out to be dependent on the strength and direction of the gradient between the conditions of the invasion front, and the newly colonized patches. Although this result may be quite important to understand the meta-population dynamics of dispersing species, it is important to note that in their study the environmental differences between patches do not take into account eventual shifts in the scenopoetic conditions (i.e. the values of the environmental parameters to which species niches’ respond to; Hutchinson 1978, see also Soberón 2007). Rather, differences arise from variations in the carrying capacity of the patches that are consecutively invaded, both in the in silico and microcosm experiments. That is, they account for potential differences in the size or quality of the invaded fragments, but not on the costs of colonizing fragments with different environmental conditions, which may also determine invasion speed through niche-driven processes. This aspect can be of particular importance in biological invasions or under climate change-driven range shifts, when adaptation to new environments is often required (Sakai et al. 2001; Whitney & Gabler 2008; Hill et al. 2011).

The expansion of geographical distribution ranges is the result of complex eco-evolutionary processes where meta-community dynamics and niche shifts interact in a novel physical space and/or environment (see, e.g., Mestre et al. 2020). Here, the invasibility of native communities is determined by niche variations and how similar are the traits of alien and native species (Hui et al. 2023). Within this context, density-dependent processes will build upon and heterogeneous matrix of native communities and environments (Tischendorf et al. 2005), to eventually determine invasion success. What the results of Morel-Journel et al. (2023) show is that, when the invader shows density dependence, the invasion process can be slowed down by variations in the carrying capacity of patches along the dispersal front. This can be particularly useful to manage biological invasions; ongoing invasions can be at least partially controlled by manipulating the size or quality of the patches that are most adequate to the invader, controlling host populations to reduce carrying capacity. But further, landscape manipulation of such kind could be used in a preventive way, to account in advance for the effects of the introduction of alien species for agricultural exploitation or biological control, thereby providing an additional safeguard to practices such as the introduction of parasitoids to control plagues. These practical aspects are certainly worth exploring further, together with a more explicit account of the influence of the abiotic conditions and the characteristics of the invaded communities on the success and speed of biological invasions.

REFERENCES

Hill, J.K., Griffiths, H.M. & Thomas, C.D. (2011) Climate change and evolutionary adaptations at species' range margins. Annual Review of Entomology, 56, 143-159. https://doi.org/10.1146/annurev-ento-120709-144746

Hui, C., Pyšek, P. & Richardson, D.M. (2023) Disentangling the relationships among abundance, invasiveness and invasibility in trait space. npj Biodiversity, 2, 13. https://doi.org/10.1038/s44185-023-00019-1

Hutchinson, G.E. (1978) An introduction to population biology. Yale University Press, New Haven, CT.

Levins, R. (1966) The strategy of model building in population biology. American Scientist, 54, 421-431. 

Mestre, A., Poulin, R. & Hortal, J. (2020) A niche perspective on the range expansion of symbionts. Biological Reviews, 95, 491-516. https://doi.org/10.1111/brv.12574

Morel-Journel, T., Haond, M., Duan, L., Mailleret, L. & Vercken, E. (2023) Colonisation debt: when invasion history impacts current range expansion. bioRxiv, 2022.11.13.516255, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.11.13.516255

Snäll, T., B. O'Hara, R. & Arjas, E. (2007) A mathematical and statistical framework for modelling dispersal. Oikos, 116, 1037-1050. https://doi.org/10.1111/j.0030-1299.2007.15604.x

Sakai, A.K., Allendorf, F.W., Holt, J.S., Lodge, D.M., Molofsky, J., With, K.A., Baughman, S., Cabin, R.J., Cohen, J.E., Ellstrand, N.C., McCauley, D.E., O'Neil, P., Parker, I.M., Thompson, J.N. & Weller, S.G. (2001) The population biology of invasive species. Annual Review of Ecology and Systematics, 32, 305-332. https://doi.org/10.1146/annurev.ecolsys.32.081501.114037

Soberón, J. (2007) Grinnellian and Eltonian niches and geographic distributions of species. Ecology Letters, 10, 1115-1123. https://doi.org/10.1111/j.1461-0248.2007.01107.x

Tischendorf, L., Grez, A., Zaviezo, T. & Fahrig, L. (2005) Mechanisms affecting population density in fragmented habitat. Ecology and Society, 10, 7. https://doi.org/10.5751/ES-01265-100107

Whitney, K.D. & Gabler, C.A. (2008) Rapid evolution in introduced species, 'invasive traits' and recipient communities: challenges for predicting invasive potential. Diversity and Distributions, 14, 569-580. https://doi.org/10.1111/j.1472-4642.2008.00473.x

Colonisation debt: when invasion history impacts current range expansionThibaut Morel-Journel, Marjorie Haond, Lana Duan, Ludovic Mailleret, Elodie Vercken<p>Demographic processes that occur at the local level, such as positive density dependence in growth or dispersal, are known to shape population range expansion, notably by linking carrying capacity to invasion speed. As a result of these process...Biological invasions, Colonization, Dispersal & Migration, Experimental ecology, Landscape ecology, Population ecology, Spatial ecology, Metacommunities & Metapopulations, Theoretical ecologyJoaquín HortalAnonymous, Anonymous2022-11-16 15:52:08 View
25 Nov 2022
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Positive fitness effects help explain the broad range of Wolbachia prevalences in natural populations

Population dynamics of Wolbachia symbionts playing Dr. Jekyll and Mr. Hyde

Recommended by based on reviews by 3 anonymous reviewers

"Good and evil are so close as to be chained together in the soul"
Robert Louis Stevenson, Dr. Jekyll and Mr. Hyde


Maternally inherited symbionts—microorganisms that pass from a female host to her progeny—have two main ways of increasing their own fitness. First, they can increase the fecundity or viability of infected females. This “positive fitness effects” strategy is the one commonly used by mutualistic symbionts, such as Buchnera aphidicola—the bacterial endosymbiont of the pea aphid, Acyrthosiphon pisum [4]. Second, maternally inherited symbionts can manipulate the reproduction of infected females in a way that enhances symbiont transmission at the expense of host fitness. A famous example of this “reproductive parasitism” strategy is the cytoplasmic incompatibility (CI) [3] induced by bacteria of the genus Wolbachia in their arthropod and nematode hosts. CI works as a toxin-antidote system, whereby the sperm of infected males is modified in a lethal way (toxin) that can only be reverted if the egg is also infected (antidote) [1]. As a result, CI imposes a kind of conditional sterility on their hosts: while infected females are compatible with both infected and uninfected males, uninfected females experience high offspring mortality if (and only if) they mate with infected males [7].

These two symbiont strategies (positive fitness effects versus reproductive parasitism) have been traditionally studied separately, both empirically and theoretically. However, it has become clear that the two strategies are not mutually exclusive, and that a reproductive parasite can simultaneously act as a mutualist—an infection type that has been dubbed “Jekyll and Hyde” [6], after the famous novella by Robert Louis Stevenson about kind scientist Dr. Jekyll and his evil alter ego, Mr. Hyde. In important previous work, Zug and Hammerstein [7] analyzed the consequences of positive fitness effects on the dynamics of different kind of infections, including “Jekyll and Hyde” infections characterized by CI and other reproductive parasitism strategies. Building on this and related modeling framework, Karisto et al. [2] re-investigate and expand on the interplay between positive fitness effects and reproductive parasitism in Wolbachia infections by focusing on CI in both diplodiploid and haplodiploid populations, and by paying particular attention to the mathematical assumption structure underlying their results.

Karisto et al. begin by reviewing classic models of Wolbachia infections in diplodiploid populations that assume a “negative fitness effect” (modeled as a fertility penalty on infected females), characteristic of a pure strategy of reproductive parasitism. Together with the positive frequency-dependent effects due to CI (whereby the fitness benefits to symbionts infecting females increase with the proportion of infected males in the population) this results in population dynamics characterized by two stable equilibria (the Wolbachia-free state and an interior equilibrium with a high frequency of Wolbachia-carrying hosts) separated by an unstable interior equilibrium. Wolbachia can then spread once the initial frequency is above a threshold or an invasion barrier, but is prevented from fixing by a proportion of infections failing to be passed on to offspring. Karisto et al. show that, given the assumption of negative fitness effects, the stable interior equilibrium can never feature a Wolbachia prevalence below one-half. Moreover, they convincingly argue that a prevalence greater than but close to one-half is difficult to maintain in the presence of stochastic fluctuations, as in these cases the high-prevalence stable equilibrium would be too close to the unstable equilibrium signposting the invasion barrier.

Karisto et al. then relax the assumption of negative fitness effects and allow for positive fitness effects (modeled as a fertility premium on infected females) in a diplodiploid population. They show that positive fitness effects may result in situations where the original invasion threshold is now absent, the bistable coexistence dynamics are transformed into purely co-existence dynamics, and Wolbachia symbionts can now invade when rare. Karisto et al. conclude that positive fitness effects provide a plausible and potentially testable explanation for the low frequencies of symbiont-carrying hosts that are sometimes observed in nature, which are difficult to reconcile with the assumption of negative fitness effects. 

Finally, Karisto et al. extend their analysis to haplodiploid host populations (where all fertilized eggs develop as females). Here, they investigate two types of cytoplasmic incompatibility: a female-killing effect, similar to the CI effect studied in diplodiploid populations (the “Leptopilina type” of Vavre et al. [5]) and a masculinization effect, where CI leads to the loss of paternal chromosomes and to the development of the offspring as a male (the “Nasonia type” of Vavre et al. [5]). The models are now two-sex, which precludes a complete analytical treatment, in particular regarding the stability of fixed points. Karisto et al. compensate by conducting large numerical analyses that support their claims. Importantly, all main conclusions regarding the interplay between positive fitness effects and reproductive parasitism continue to hold under haplodiploidy. 

All in all, the analysis and results by Karisto et al. suggest that it is not necessary to resort to classical (but depending on the situation, unlikely) mechanisms, such as ongoing invasion or source-sink dynamics, to explain arthropod populations featuring low-prevalent Wolbachia infections. Instead, low-frequency equilibria might be simply due to reproductive parasites conferring beneficial fitness effects, or Wolbachia symbionts playing Dr. Jekyll (positive fitness effects) and Mr. Hyde (cytoplasmatic incompatibility). 

References

[1] Beckmann JF, Bonneau M, Chen H, Hochstrasser M, Poinsot D, Merçot H, Weill M, Sicard M, Charlat S (2019) The Toxin–Antidote Model of Cytoplasmic Incompatibility: Genetics and Evolutionary Implications. Trends in Genetics, 35, 175–185. https://doi.org/10.1016/j.tig.2018.12.004

[2] Karisto P, Duplouy A, Vries C de, Kokko H (2022) Positive fitness effects help explain the broad range of Wolbachia prevalences in natural populations. bioRxiv, 2022.04.11.487824, ver. 5 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.04.11.487824

[3] Laven H (1956) Cytoplasmic Inheritance in Culex. Nature, 177, 141–142. https://doi.org/10.1038/177141a0

[4] Perreau J, Zhang B, Maeda GP, Kirkpatrick M, Moran NA (2021) Strong within-host selection in a maternally inherited obligate symbiont: Buchnera and aphids. Proceedings of the National Academy of Sciences, 118, e2102467118. https://doi.org/10.1073/pnas.2102467118

[5] Vavre F, Fleury F, Varaldi J, Fouillet P, Bouletreau M (2000) Evidence for Female Mortality in Wolbachia-Mediated Cytoplasmic Incompatibility in Haplodiploid Insects: Epidemiologic and Evolutionary Consequences. Evolution, 54, 191–200. https://doi.org/10.1111/j.0014-3820.2000.tb00019.x

[6] Zug R, Hammerstein P (2015) Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biological Reviews, 90, 89–111. https://doi.org/10.1111/brv.12098

[7] Zug R, Hammerstein P (2018) Evolution of reproductive parasites with direct fitness benefits. Heredity, 120, 266–281. https://doi.org/10.1038/s41437-017-0022-5

Positive fitness effects help explain the broad range of Wolbachia prevalences in natural populationsPetteri Karisto, Anne Duplouy, Charlotte de Vries, Hanna Kokko<p style="text-align: justify;">The bacterial endosymbiont <em>Wolbachia</em> is best known for its ability to modify its host’s reproduction by inducing cytoplasmic incompatibility (CI) to facilitate its own spread. Classical models predict eithe...Host-parasite interactions, Population ecologyJorge Peña2022-04-12 12:52:55 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

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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