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24 May 2023
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Evolutionary determinants of reproductive seasonality: a theoretical approach

When does seasonal reproduction evolve?

Recommended by ORCID_LOGO based on reviews by Francois-Xavier Dechaume-Moncharmont, Nigel Yoccoz and 1 anonymous reviewer

Have you ever wondered why some species breed seasonally while others do not? You might think it is all down to lattitude and the harshness of winters but it turns out it is quite a bit more complicated than that. A consequence of this is that climate change may result in the evolution of the degree of seasonal reproduction, with some species perhaps becoming less seasonal and others more so even in the same habitat. 

Burtschell et al. (2023) investigated how various factors influence seasonal breeding by building an individual-based model of a baboon population from which they calculated the degree of seasonality for the fittest reproductive strategy. They then altered key aspects of their model to examine how these changes impacted the degree of seasonality in the reproductive strategy. What they found is fascinating. 

The degree of seasonality in reproductive strategy is expected to increase with increased seasonality in the environment, decreased food availability, increased energy expenditure, and how predictable resource availability is. Interestingly, neither female cycle length nor extrinsic infant mortality influenced the degree of seasonality in reproduction.

What this means in reality for seasonal species is more challenging to understand. Some environments appear to be becoming more seasonal yet less predictable, and some species appear to be altering their daily energy budgets in response to changing climate in quite complex ways. As with pretty much everything in biology, Burtschell et al.'s work reveals much nuance and complexity, and that predicting how species might alter their reproductive timing is fraught with challenges.

The paper is very well written. With a simpler model it may have proven possible to achieve analytical solutions, but this is a very minor gripe. The reviewers were positive about the paper, and I have little doubt it will be well-cited. 

REFERENCES

Burtschell L, Dezeure J, Huchard E, Godelle B (2023) Evolutionary determinants of reproductive seasonality: a theoretical approach. bioRxiv, 2022.08.22.504761, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.08.22.504761

Evolutionary determinants of reproductive seasonality: a theoretical approachLugdiwine Burtschell, Jules Dezeure, Elise Huchard, Bernard Godelle<p style="text-align: justify;">Reproductive seasonality is a major adaptation to seasonal cycles and varies substantially among organisms. This variation, which was long thought to reflect a simple latitudinal gradient, remains poorly understood ...Evolutionary ecology, Life history, Theoretical ecologyTim Coulson Nigel Yoccoz2022-08-23 21:37:28 View
05 Apr 2022
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Late-acting self-incompatible system, preferential allogamy and delayed selfing in the heterostylous invasive populations of Ludwigia grandiflora subsp. hexapetala

Water primerose (Ludwigia grandiflora subsp. hexapetala) auto- and allogamy: an ecological perspective

Recommended by ORCID_LOGO based on reviews by Juan Arroyo, Emiliano Mora-Carrera and 1 anonymous reviewer

Invasive plant species are widely studied by the ecologist community, especially in wetlands. Indeed, alien plants are considered one of the major threats to wetland biodiversity (Reid et al., 2019). Ludwigia grandiflora subsp. hexapetala (Hook. & Arn.) G.L.Nesom & Kartesz, 2000 (Lgh) is one of them and has received particular attention for a long time (Hieda et al., 2020; Thouvenot, Haury, & Thiebaut, 2013). The ecology of this invasive species and its effect on its biotic and abiotic environment has been studied in previous works. Different processes were demonstrated to explain their invasibility such as allelopathic interference (Dandelot et al., 2008), resource competition (Gérard et al., 2014), and high phenotypic plasticity (Thouvenot, Haury, & Thiébaut, 2013), to cite a few of them. However, although vegetative reproduction is a well-known invasive process for alien plants like Lgh (Glover et al., 2015), the sexual reproduction of this species is still unclear and may help to understand the Lgh population dynamics.

Portillo Lemus et al. (2021) showed that two floral morphs of Lgh co-exist in natura, involving self-compatibility for short-styled phenotype and self-incompatibility for long-styled phenotype processes. This new article (Portillo Lemus et al., 2022) goes further and details the underlying mechanisms of the sexual reproduction of the two floral morphs.

Complementing their previous study, the authors have described a late self-incompatible process associated with the long-styled morph, which authorized a small proportion of autogamy. Although this represents a small fraction of the L-morph reproduction, it may have a considerable impact on the L-morph population dynamics. Indeed, authors report that “floral morphs are mostly found in allopatric monomorphic populations (i.e., exclusively S-morph or exclusively L-morph populations)” with a large proportion of L-morph populations compared to S-morph populations in the field. It may seem counterintuitive as L-morph mainly relies on cross-fecundation. 

Results show that L-morph autogamy mainly occurs in the fall, late in the reproduction season. Therefore, the reproduction may be ensured if no exogenous pollen reaches the stigma of L-morph individuals. It partly explains the large proportion of L-morph populations in the field. 

Beyond the description of late-acting self-incompatibility, which makes the Onagraceae a third family of Myrtales with this reproductive adaptation, the study raises several ecological questions linked to the results presented in the article. First, it seems that even if autogamy is possible, Lgh would favour allogamy, even in S-morph, through the faster development of pollen tubes from other individuals. This may confer an adaptative and evolutive advantage for the Lgh, increasing its invasive potential. The article shows this faster pollen tube development in S-morph but does not test the evolutive consequences. It is an interesting perspective for future research. It would also be interesting to describe cellular processes which recognize and then influence the speed of the pollen tube. Second, the importance of sexual reproduction vs vegetative reproduction would also provide information on the benefits of sexual dimorphism within populations. For instance, how fruit production increases the dispersal potential of Lgh would help to understand Lgh population dynamics and to propose adapted management practices (Delbart et al., 2013; Meisler, 2009).

To conclude, the study proposes a morphological, reproductive and physiological description of the Lgh sexual reproduction process. However, underlying ecological questions are well included in the article and the ecophysiological results enlighten some questions about the role of sexual reproduction in the invasiveness of Lgh. I advise the reader to pay attention to the reviewers’ comments; the debates were very constructive and, thanks to the great collaboration with the authorship, lead to an interesting paper about Lgh reproduction and with promising perspectives in ecology and invasion ecology.

References

Dandelot S, Robles C, Pech N, Cazaubon A, Verlaque R (2008) Allelopathic potential of two invasive alien Ludwigia spp. Aquatic Botany, 88, 311–316. https://doi.org/10.1016/j.aquabot.2007.12.004

Delbart E, Mahy G, Monty A (2013) Efficacité des méthodes de lutte contre le développement de cinq espèces de plantes invasives amphibies : Crassula helmsii, Hydrocotyle ranunculoides, Ludwigia grandiflora, Ludwigia peploides et Myriophyllum aquaticum (synthèse bibliographique). BASE, 17, 87–102. https://popups.uliege.be/1780-4507/index.php?id=9586

Gérard J, Brion N, Triest L (2014) Effect of water column phosphorus reduction on competitive outcome and traits of Ludwigia grandiflora and L. peploides, invasive species in Europe. Aquatic Invasions, 9, 157–166. https://doi.org/10.3391/ai.2014.9.2.04

Glover R, Drenovsky RE, Futrell CJ, Grewell BJ (2015) Clonal integration in Ludwigia hexapetala under different light regimes. Aquatic Botany, 122, 40–46. https://doi.org/10.1016/j.aquabot.2015.01.004

Hieda S, Kaneko Y, Nakagawa M, Noma N (2020) Ludwigia grandiflora (Michx.) Greuter & Burdet subsp. hexapetala (Hook. & Arn.) G. L. Nesom & Kartesz, an Invasive Aquatic Plant in Lake Biwa, the Largest Lake in Japan. Acta Phytotaxonomica et Geobotanica, 71, 65–71. https://doi.org/10.18942/apg.201911

Meisler J (2009) Controlling Ludwigia hexaplata in Northern California. Wetland Science and Practice, 26, 15–19. https://doi.org/10.1672/055.026.0404

Portillo Lemus LO, Harang M, Bozec M, Haury J, Stoeckel S, Barloy D (2022) Late-acting self-incompatible system, preferential allogamy and delayed selfing in the heteromorphic invasive populations of Ludwigia grandiflora subsp. hexapetala. bioRxiv, 2021.07.15.452457, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2021.07.15.452457

Portillo Lemus LO, Bozec M, Harang M, Coudreuse J, Haury J, Stoeckel S, Barloy D (2021) Self-incompatibility limits sexual reproduction rather than environmental conditions in an invasive water primrose. Plant-Environment Interactions, 2, 74–86. https://doi.org/10.1002/pei3.10042

Reid AJ, Carlson AK, Creed IF, Eliason EJ, Gell PA, Johnson PTJ, Kidd KA, MacCormack TJ, Olden JD, Ormerod SJ, Smol JP, Taylor WW, Tockner K, Vermaire JC, Dudgeon D, Cooke SJ (2019) Emerging threats and persistent conservation challenges for freshwater biodiversity. Biological Reviews, 94, 849–873. https://doi.org/10.1111/brv.12480

Thouvenot L, Haury J, Thiebaut G (2013) A success story: water primroses, aquatic plant pests. Aquatic Conservation: Marine and Freshwater Ecosystems, 23, 790–803. https://doi.org/10.1002/aqc.2387

Thouvenot L, Haury J, Thiébaut G (2013) Seasonal plasticity of Ludwigia grandiflora under light and water depth gradients: An outdoor mesocosm experiment. Flora - Morphology, Distribution, Functional Ecology of Plants, 208, 430–437. https://doi.org/10.1016/j.flora.2013.07.004

Late-acting self-incompatible system, preferential allogamy and delayed selfing in the heterostylous invasive populations of Ludwigia grandiflora subsp. hexapetalaLuis O. Portillo Lemus, Maryline Harang, Michel Bozec, Jacques Haury, Solenn Stoeckel, Dominique Barloy<p style="text-align: justify;">Breeding system influences local population genetic structure, effective size, offspring fitness and functional variation. Determining the respective importance of self- and cross-fertilization in hermaphroditic flo...Biological invasions, Botany, Freshwater ecology, PollinationAntoine Vernay2021-07-16 09:53:50 View
15 Feb 2024
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Sources of confusion in global biodiversity trends

Unraveling the Complexity of Global Biodiversity Dynamics: Insights and Imperatives

Recommended by ORCID_LOGO based on reviews by Pedro Cardoso and 1 anonymous reviewer

Biodiversity loss is occurring at an alarming rate across terrestrial and marine ecosystems, driven by various processes that degrade habitats and threaten species with extinction. Despite the urgency of this issue, empirical studies present a mixed picture, with some indicating declining trends while others show more complex patterns.

In a recent effort to better understand global biodiversity dynamics, Boennec et al. (2024) conducted a comprehensive literature review examining temporal trends in biodiversity. Their analysis reveals that reviews and meta-analyses, coupled with the use of global indicators, tend to report declining trends more frequently. Additionally, the study underscores a critical gap in research: the scarcity of investigations into the combined impact of multiple pressures on biodiversity at a global scale. This lack of understanding complicates efforts to identify the root causes of biodiversity changes and develop effective conservation strategies.

This study serves as a crucial reminder of the pressing need for long-term biodiversity monitoring and large-scale conservation studies. By filling these gaps in knowledge, researchers can provide policymakers and conservation practitioners with the insights necessary to mitigate biodiversity loss and safeguard ecosystems for future generations.

References

Boennec, M., Dakos, V. & Devictor, V. (2023). Sources of confusion in global biodiversity trend. bioRxiv, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.32942/X29W3H

 

Sources of confusion in global biodiversity trendsMaelys Boennec, Vasilis Dakos, Vincent Devictor<p>Populations and ecological communities are changing worldwide, and empirical studies exhibit a mixture of either declining or mixed trends. Confusion in global biodiversity trends thus remains while assessing such changes is of major social, po...Biodiversity, Conservation biology, Meta-analysesPaulo Borges2023-09-20 11:10:25 View
14 Jul 2023
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Field margins as substitute habitat for the conservation of birds in agricultural wetlands

Searching for conservation opportunities at the margins

Recommended by based on reviews by Scott Wilson and Elena D Concepción

In a progressively human-dominated planet (Venter et al., 2016), the fate of many species will depend on the extent to which they can persist in anthropogenic landscapes. In Western Europe, where only small areas of primary habitat remain (e.g. Sabatini et al., 2018), semi-natural areas are crucial habitats to many native species, yet they are threatened by the expansion of human activities, including agricultural expansion and intensification (Rigal et al., 2023). 

A new study by Mallet and colleagues (Mallet et al., 2023) investigates the extent to which bird species in the Camargue region are able to use the margins of agricultural fields as substitutes for their preferred semi-natural habitats. Located in the delta of the Rhône River in Southern France, the Camargue is internationally recognized for its biodiversity value, classified as a Biosphere Reserve by UNESCO and as a Wetland of International Importance under the Ramsar Convention (IUCN & UN-WCMC, 2023). Mallet and colleagues tested three specific hypotheses: that grass strips (grassy field boundaries, including grassy tracks or dirt roads used for moving agricultural machinery) can function as substitute habitats for grassland species; that reed strips along drainage ditches (common in the rice paddy landscapes of the Camargue) can function as substitute habitats to wetland species; and that hedgerows can function as substitute habitats to species that favour woodland edges. They did so by measuring how the local abundances of 14 bird species (nine typical of forest edges, 3 of grasslands, and two of reedbeds) respond to increasing coverage of either the three types of field margins or of the three types of semi-natural habitat. 

This is an elegant study design, yet – as is often the case with real field data – results are not as simple as expected. Indeed, for most species (11 out of 14) local abundances did not increase significantly with the area of their supposed primary habitat, undermining the assumption that they are strongly associated with (or dependent on) those habitats. Among the three species that did respond positively to the area of their primary habitat, one (a forest edge species) responded positively but not significantly to the area of field margins (hedgerows), providing weak evidence to the habitat compensation hypothesis. For the other two (grassland and a wetland species), abundance responded even more strongly to the area of field margins (grass and reed strips, respectively) than to the primary habitat, suggesting that the field margins are not so much a substitute but valuable habitats in their own right. 

It would have been good conservation news if field margins were found to be suitable habitat substitutes to semi-natural habitats, or at least reasonable approximations, to most species. Given that these margins have functional roles in agricultural landscapes (marking boundaries, access areas, water drainage), they could constitute good win-win solutions for reconciling biodiversity conservation with agricultural production. Alas, the results are more complicated than that, with wide variation in species responses that could not have been predicted from presumed habitat affinities. These results illustrate the challenges of conservation practice in complex landscapes formed by mosaics of variable land use types. With species not necessarily falling neatly into habitat guilds, it becomes even more challenging to plan strategically how to manage landscapes to optimize their conservation. The results presented here suggest that species’ abundances may be responding to landscape variables not taken into account in the analyses, such as connectivity between habitat patches, or maybe positive and negative edge effects between land use types. That such uncertainties remain even in a well-studied region as the Camargue, and for such a well-studied taxon such as birds, only demonstrates the continued importance of rigorous field studies testing explicit hypotheses such as this one by Mallet and colleagues. 

References

IUCN, & UN-WCMC (2023). Protected Planet. Protected Planet. https://www.protectedplanet.net/en 

Mallet, P., Béchet, A., Sirami, C., Mesléard, F., Blanchon, T., Calatayud, F., Dagonet, T., Gaget, E., Leray, C., & Galewski, T. (2023). Field margins as substitute habitat for the conservation of birds in agricultural wetlands. bioRxiv, 2022.05.05.490780, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.05.05.490780 

Rigal, S., Dakos, V., Alonso, H., Auniņš, A., Benkő, Z., Brotons, L., Chodkiewicz, T., Chylarecki, P., de Carli, E., del Moral, J. C. et al. (2023). Farmland practices are driving bird population decline across Europe. Proceedings of the National Academy of Sciences, 120, e2216573120. https://doi.org/10.1073/pnas.2216573120 

Sabatini, F. M., Burrascano, S., Keeton, W. S., Levers, C., Lindner, M., Pötzschner, F., Verkerk, P. J., Bauhus, J., Buchwald, E., Chaskovsky, O., Debaive, N. et al. (2018). Where are Europe’s last primary forests? Diversity and Distributions, 24, 1426–1439. https://doi.org/10.1111/ddi.12778 

Venter, O., Sanderson, E. W., Magrach, A., Allan, J. R., Beher, J., Jones, K. R., Possingham, H. P., Laurance, W. F., Wood, P., Fekete, B. M., Levy, M. A., & Watson, J. E. M. (2016). Sixteen years of change in the global terrestrial human footprint and implications for biodiversity conservation. Nature Communications, 7, 12558. https://doi.org/10.1038/ncomms12558 

Field margins as substitute habitat for the conservation of birds in agricultural wetlandsMallet Pierre, Béchet Arnaud, Sirami Clélia, Mesléard François, Blanchon Thomas, Calatayud François, Dagonet Thomas, Gaget Elie, Leray Carole, Galewski Thomas<p style="text-align: justify;">Breeding birds in agricultural landscapes have declined considerably since the 1950s and the beginning of agricultural intensification in Europe. Given the increasing pressure on agricultural land, it is necessary t...Agroecology, Biodiversity, Conservation biology, Landscape ecologyAna S. L. Rodrigues2022-05-09 10:48:49 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
07 Aug 2023
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Being a tree crop increases the odds of experiencing yield declines irrespective of pollinator dependence

The complexities of understanding why yield is declining

Recommended by ORCID_LOGO based on reviews by Nicolas Deguines and 1 anonymous reviewer

Despite the repeated mantra that "correlation does not imply causation", ecological studies not amenable to experimental settings often rely on correlational patterns to infer the causes of observed patterns. In this context, it's of paramount importance to build a plausible hypothesis and take into account potential confounding factors. The paper by Aizen and collaborators (2023) is a beautiful example of how properly unveil the complexities of an intriguing pattern: The decline in yield of some crops over the last few decades. This is an outstanding question to solve given the need to feed a growing population without destroying the environment, for example by increasing the area under cultivation. Previous studies suggested that pollinator-dependent crops were more susceptible to suffering yield declines than non-pollinator-dependent crops (Garibaldi et al 2011). Given the actual population declines of some pollinators, especially in agricultural areas, this correlative evidence was quite appealing to be interpreted as a causal effect. However, as elegantly shown by Aizen and colleagues in this paper, this first analysis did not account for other alternative explanations, such as the effect of climate change on other plant life-history traits correlated with pollinator dependence. Plant life-history traits do not vary independently. For example, trees are more likely to be pollinator-dependent than herbs (Lanuza et al 2023), which can be an important confounding factor in the analysis. With an elegant analysis and an impressive global dataset, this paper shows that the declining trend in the yield of some crops is most likely associated with their life form than with their dependence on pollinators. This does not imply that pollinators are not important for crop yield, but that the decline in their populations is not leaving a clear imprint in the global yield production trends once accounted for the technological and agronomic improvements. All in all, this paper makes a key contribution to food security by elucidating the factors beyond declining yield trends, and is a brave example of how science can self-correct itself as new knowledge emerges.   

References

Aizen, M.A., Gleiser, G., Kitzberger T. and Milla R. 2023. Being A Tree Crop Increases the Odds of Experiencing Yield Declines Irrespective of Pollinator Dependence. bioRxiv, 2023.04.27.538617, ver 2, peer-reviewed and recommended by PCI Ecology. https://doi.org/10.1101/2023.04.27.538617

Lanuza, J.B., Rader, R., Stavert, J., Kendall, L.K., Saunders, M.E. and Bartomeus, I. 2023. Covariation among reproductive traits in flowering plants shapes their interactions with pollinators. Functional Ecology 37: 2072-2084. https://doi.org/10.1111/1365-2435.14340

Garibaldi, L.A., Aizen, M.A., Klein, A.M., Cunningham, S.A. and Harder, L.D. 2011. Global growth and stability of agricultural yield decrease with pollinator dependence. Proceedings of the National Academy of Sciences, 108: 5909-5914. https://doi.org/10.1073/pnas.1012431108

Being a tree crop increases the odds of experiencing yield declines irrespective of pollinator dependenceMarcelo A. Aizen, Gabriela Gleiser, Thomas Kitzberger, and Rubén Milla<p>Crop yields, i.e., harvestable production per unit of cropland area, are in decline for a number of crops and regions, but the drivers of this process are poorly known. Global decreases in pollinator abundance and diversity have been proposed a...Agroecology, Climate change, Community ecology, Demography, Facilitation & Mutualism, Life history, Phenotypic plasticity, Pollination, Terrestrial ecologyIgnasi Bartomeus2023-05-02 18:54:44 View
16 Sep 2019
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Blood, sweat and tears: a review of non-invasive DNA sampling

Words matter: extensive misapplication of "non-invasive" in describing DNA sampling methods, and proposed clarifying terms

Recommended by based on reviews by 2 anonymous reviewers

The ability to successfully sequence trace quantities of environmental DNA (eDNA) has provided unprecedented opportunities to use genetic analyses to elucidate animal ecology, behavior, and population structure without affecting the behavior, fitness, or welfare of the animal sampled. Hair associated with an animal track in the snow, the shed exoskeleton of an insect, or a swab of animal scat are all examples of non-invasive methods to collect eDNA. Despite the seemingly uncomplicated definition of "non-invasive" as proposed by Taberlet et al. [1], Lefort et al. [2] highlight that its appropriate application to sampling methods in practice is not so straightforward. For example, collecting scat left behind on the forest floor by a mammal could be invasive if feces is used by that species to mark territorial boundaries. Other collection strategies such as baited DNA traps to collect hair, capturing and handling an individual to swab or stimulate emission of a body fluid, or removal of a presumed non essential body part like a feather, fish scale, or even a leg from an insect are often described as "non-invasive" sampling methods. However, such methods cannot be considered truly non-invasive. At a minimum, attracting or capturing and handling an animal to obtain a DNA sample interrupts its normal behavioral routine, but additionally can cause both acute and long-lasting physiological and behavioral stress responses and other effects. Even invertebrates exhibit long-term hypersensitization after an injury, which manifests as heightened vigilance and enhanced escape responses [3-5].
Through an extensive analysis of 380 papers published from 2013-2018, Lefort et al. [2] document the widespread misapplication of the term "non-invasive" to methods used to sample DNA. An astonishing 58% of these papers employed the term incorrectly. A big part of the problem is that "non-invasive" is usually used by authors in the medical or veterinary sense of not breaking the skin or entering the body [6], rather than in the broader, ecological sense of Taberlet et al. [1]. The authors argue that correct use of the term matters, because it may lead naive readers – one can imagine students, policy makers, and the general public – to incorrectly assume a particular method is safe to use in a situation where disturbing the animal could affect experimental results or raise animal welfare concerns. Such assumptions can affect experimental design, as well as interpretations of one's own or others' data.
The importance of the Lefort et al. [2] paper lies in part on the authors' call for the research community to be much more careful when applying the term "non-invasive" to methods of DNA sampling. This call cannot be shrugged off as a minor problem in a few papers – as their literature review demonstrates, "non-invasive" is being applied incorrectly more often than not. The authors recognize that not all DNA sampling must be non-invasive to be useful or ethical. Examples include taking samples for DNA extraction from museum specimens, or opportunistically from carcasses of animals hunted either legally or seized by authorities from poachers. In many cases, there may be no viable non-invasive method to obtain DNA, but a researcher strives to collect samples using methods that, although they may involve taking a sample directly from the animal's body, do not disrupt, or only slightly disrupt behavior, fitness, or welfare of the animal. Thus, the other important contribution by Lefort et al. [2] is to propose the terms "non-disruptive" and "minimally-disruptive" to describe such sampling methods, which are not strictly non-invasive. While gray areas undoubtedly remain, as acknowledged by the authors, answering the call for correct use of "non-invasive" and applying the proposed new terms for certain types of invasive sampling with a focus on level of disruption, will go a long way in limiting misconceptions and misinterpretations caused by the current confusion in terminology.

References

[1] Taberlet P., Waits L. P. and Luikart G. 1999. Noninvasive genetic sampling: look before you leap. Trends Ecol. Evol. 14: 323-327. doi: 10.1016/S0169-5347(99)01637-7
[2] Lefort M.-C., Cruickshank R. H., Descovich K., Adams N. J., Barun A., Emami-Khoyi A., Ridden J., Smith V. R., Sprague R., Waterhouse B. R. and Boyer S. 2019. Blood, sweat and tears: a review of non-invasive DNA sampling. bioRxiv, 385120, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/385120
[3] Khuong T. M., Wang Q.-P., Manion J., Oyston L. J., Lau M.-T., Towler H., Lin Y. Q. and Neely G. G. 2019. Nerve injury drives a heightened state of vigilance and neuropathic sensitization in Drosophila. Science Advances 5: eaaw4099. doi: 10.1126/sciadv.aaw4099
[4] Crook, R. J., Hanlon, R. T. and Walters, E. T. 2013. Squid have nociceptors that display widespread long-term sensitization and spontaneous activity after bodily injury. Journal of Neuroscience, 33(24), 10021-10026. doi: 10.1523/JNEUROSCI.0646-13.2013
[5] Walters E. T. 2018. Nociceptive biology of molluscs and arthropods: evolutionary clues about functions and mechanisms potentially related to pain. Frontiers in Physiololgy 9: doi: 10.3389/fphys.2018.01049
[6] Garshelis, D. L. 2006. On the allure of noninvasive genetic sampling-putting a face to the name. Ursus 17: 109-123. doi: 10.2192/1537-6176(2006)17[109:OTAONG]2.0.CO;2

Blood, sweat and tears: a review of non-invasive DNA samplingMarie-Caroline Lefort, Robert H Cruickshank, Kris Descovich, Nigel J Adams, Arijana Barun, Arsalan Emami-Khoyi, Johnaton Ridden, Victoria R Smith, Rowan Sprague, Benjamin Waterhouse, Stephane Boyer<p>The use of DNA data is ubiquitous across animal sciences. DNA may be obtained from an organism for a myriad of reasons including identification and distinction between cryptic species, sex identification, comparisons of different morphocryptic ...Behaviour & Ethology, Conservation biology, Molecular ecology, ZoologyThomas Wilson Sappington2018-11-30 13:33:31 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
02 Dec 2021
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Metabarcoding faecal samples to investigate spatiotemporal variation in the diet of the endangered Westland petrel (Procellaria westlandica)

The promise and limits of DNA based approach to infer diet flexibility in endangered top predators

Recommended by based on reviews by Francis John Burdon and Babett Günther

There is growing evidence of worldwide decline of populations of top predators, including marine ones (Heithaus et al, 2008, Mc Cauley et al., 2015), with cascading effects expected at the ecosystem level, due to global change and human activities, including habitat loss or fragmentation, the collapse or the range shifts of their preys. On a global scale, seabirds are among the most threatened group of birds, about one-third of them being considered as threatened or endangered (Votier& Sherley, 2017). The large consequences of the decrease of the populations of preys they feed on (Cury et al, 2011) points diet flexibility as one important element to understand for effective management (McInnes et al, 2017).  Nevertheless, morphological inventory of preys requires intrusive protocols, and the differential digestion rate of distinct taxa may lead to a large bias in morphological-based diet assessments. The use of DNA metabarcoding on feces (or diet DNA, dDNA) now allows non-invasive approaches facilitating the recollection of samples and the detection of multiple preys independently of their digestion rates (Deagle et al., 2019). Although no gold standard exists yet to avoid bias associated with metabarcoding (primer bias, gaps in reference databases, inability to differentiate primary from secondary predation…), the use of these recent techniques has already improved the knowledge of the foraging behaviour and diet of many animals (Ando et al., 2020).

Both promise and shortcomings of this approach are illustrated in the article “Metabarcoding faecal samples to investigate spatiotemporal variation in the diet of the endangered Westland petrel (Procellaria westlandica)” by Quereteja et al. (2021). In this work, the authors assessed the nature and spatio-temporal flexibility of the foraging behaviour and consequent diet of the endangered petrel Procellaria westlandica from New-Zealand through metabarcoding of faeces samples.

The results of this dDNA, non-invasive approach, identify some expected and also unexpected prey items, some of which require further investigation likely due to large gaps in the reference databases. They also reveal the temporal (before and after hatching) and spatial (across colonies only 1.5km apart) flexibility of the foraging behaviour, additionally suggesting a possible influence of fisheries activities in the surroundings of the colonies. This study thus both underlines the power of the non-invasive metabarcoding approach on faeces, and the important results such analysis can deliver for conservation, pointing a potential for diet flexibility that may be essential for the resilience of this iconic yet endangered species.

References

Ando H, Mukai H, Komura T, Dewi T, Ando M, Isagi Y (2020) Methodological trends and perspectives of animal dietary studies by noninvasive fecal DNA metabarcoding. Environmental DNA, 2, 391–406. https://doi.org/10.1002/edn3.117

Cury PM, Boyd IL, Bonhommeau S, Anker-Nilssen T, Crawford RJM, Furness RW, Mills JA, Murphy EJ, Österblom H, Paleczny M, Piatt JF, Roux J-P, Shannon L, Sydeman WJ (2011) Global Seabird Response to Forage Fish Depletion—One-Third for the Birds. Science, 334, 1703–1706. https://doi.org/10.1126/science.1212928

Deagle BE, Thomas AC, McInnes JC, Clarke LJ, Vesterinen EJ, Clare EL, Kartzinel TR, Eveson JP (2019) Counting with DNA in metabarcoding studies: How should we convert sequence reads to dietary data? Molecular Ecology, 28, 391–406. https://doi.org/10.1111/mec.14734

Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends in Ecology & Evolution, 23, 202–210. https://doi.org/10.1016/j.tree.2008.01.003

McCauley DJ, Pinsky ML, Palumbi SR, Estes JA, Joyce FH, Warner RR (2015) Marine defaunation: Animal loss in the global ocean. Science, 347, 1255641. https://doi.org/10.1126/science.1255641

McInnes JC, Jarman SN, Lea M-A, Raymond B, Deagle BE, Phillips RA, Catry P, Stanworth A, Weimerskirch H, Kusch A, Gras M, Cherel Y, Maschette D, Alderman R (2017) DNA Metabarcoding as a Marine Conservation and Management Tool: A Circumpolar Examination of Fishery Discards in the Diet of Threatened Albatrosses. Frontiers in Marine Science, 4, 277. https://doi.org/10.3389/fmars.2017.00277

Querejeta M, Lefort M-C, Bretagnolle V, Boyer S (2021) Metabarcoding faecal samples to investigate spatiotemporal variation in the diet of the endangered Westland petrel (Procellaria westlandica). bioRxiv, 2020.10.30.360289, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2020.10.30.360289

Votier SC, Sherley RB (2017) Seabirds. Current Biology, 27, R448–R450. https://doi.org/10.1016/j.cub.2017.01.042

Metabarcoding faecal samples to investigate spatiotemporal variation in the diet of the endangered Westland petrel (Procellaria westlandica)Marina Querejeta, Marie-Caroline Lefort, Vincent Bretagnolle, Stéphane Boyer<p style="text-align: justify;">As top predators, seabirds can be indirectly impacted by climate variability and commercial fishing activities through changes in marine communities. However, high mobility and foraging behaviour enables seabirds to...Conservation biology, Food webs, Marine ecology, Molecular ecologySophie Arnaud-Haond2020-10-30 20:14:50 View
20 Sep 2018
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When higher carrying capacities lead to faster propagation

When the dispersal of the many outruns the dispersal of the few

Recommended by ORCID_LOGO based on reviews by Yuval Zelnik and 1 anonymous reviewer

Are biological invasions driven by a few pioneers, running ahead of their conspecifics? Or are these pioneers constantly being caught up by, and folded into, the larger flux of propagules from the established populations behind them?
In ecology and beyond, these two scenarios are known as "pulled" and "pushed" fronts, and they come with different expectations. In a pushed front, invasion speed is not just a matter of how good individuals are at dispersing and settling new locations. It becomes a collective, density-dependent property of population fluxes. And in particular, it can depend on the equilibrium abundance of the established populations inside the range, i.e. the species’ carrying capacity K, factoring in its abiotic environment and biotic interactions.
This realization is especially important because it can flip around our expectations about which species expand fast, and how to manage them. We tend to think of initial colonization and long-term abundance as two independent axes of variation among species or indeed as two ends of a spectrum, in the classic competition-colonization tradeoff [1]. When both play into invasion speed, good dispersers might not outrun good competitors. This is useful knowledge, whether we want to contain an invasion or secure a reintroduction.
In their study "When higher carrying capacities lead to faster propagation", Haond et al [2] combine mathematical analysis, Individual-Based simulations and experiments to show that various mechanisms can cause pushed fronts, whose speed increases with the carrying capacity K of the species. Rather than focus on one particular angle, the authors endeavor to demonstrate that this qualitative effect appears again and again in a variety of settings.
It is perhaps surprising that this notable and general connection between K and invasion speed has managed to garner so little fame in ecology. A large fraction of the literature employs the venerable Fisher-KPP reaction-diffusion model, which combines local logistic growth with linear diffusion in space. This model has prompted both considerable mathematical developments [3] and many applications to modelling real invasions [4]. But it only allows pulled fronts, driven by the small populations at the edge of a species range, with a speed that depends only on their initial growth rate r.
This classic setup is, however, singular in many ways. Haond et al [2] use it as a null model, and introduce three mechanisms or factors that each ensure a role of K in invasion speed, while giving less importance to the pioneers at the border.
Two factors, the Allee effect and demographic stochasticity, make small edge populations slower to grow or less likely to survive. These two factors are studied theoretically, and to make their claims stronger, the authors stack the deck against K. When generalizing equations or simulations beyond the null case, it is easy to obtain functional forms where the parameter K does not only play the role of equilibrium carrying capacity, but also affects dynamical properties such as the maximum or mean growth rate. In that case, it can trivially change the propagation speed, without it meaning anything about the role of established populations behind the front. Haond et al [2] avoid this pitfall by disentangling these effects, at the cost of slightly more peculiar expressions, and show that varying essentially nothing but the carrying capacity can still impact the speed of the invasion front.
The third factor, density-dependent dispersal, makes small populations less prone to disperse. It is well established empirically and theoretically that various biological mechanisms, from collective organization to behavioral switches, can prompt organisms in denser populations to disperse more, e.g. in such a way as to escape competition [5]. The authors demonstrate how this effect induces a link between carrying capacity and invasion speed, both theoretically and in a dispersal experiment on the parasitoid wasp, Trichogramma chilonis.
Overall, this study carries a simple and clear message, supported by valuable contributions from different angles. Although some sections are clearly written for the theoretical ecology crowd, this article has something for everyone, from the stray physicist to the open-minded manager. The collaboration between theoreticians and experimentalists, while not central, is worthy of note. Because the narrative of this study is the variety of mechanisms that can lead to the same qualitative effect, the inclusion of various approaches is not a gimmick, but helps drive home its main message. The work is fairly self-contained, although one could always wish for further developments, especially in the direction of more quantitative testing of these mechanisms.
In conclusion, Haond et al [2] effectively convey the widely relevant message that, for some species, invading is not just about the destination, it is about the many offspring one makes along the way.

References

[1] Levins, R., & Culver, D. (1971). Regional Coexistence of Species and Competition between Rare Species. Proceedings of the National Academy of Sciences, 68(6), 1246–1248. doi: 10.1073/pnas.68.6.1246
[2] Haond, M., Morel-Journel, T., Lombaert, E., Vercken, E., Mailleret, L., & Roques, L. (2018). When higher carrying capacities lead to faster propagation. BioRxiv, 307322. doi: 10.1101/307322
[3] Crooks, E. C. M., Dancer, E. N., Hilhorst, D., Mimura, M., & Ninomiya, H. (2004). Spatial segregation limit of a competition-diffusion system with Dirichlet boundary conditions. Nonlinear Analysis: Real World Applications, 5(4), 645–665. doi: 10.1016/j.nonrwa.2004.01.004
[4] Shigesada, N., & Kawasaki, K. (1997). Biological Invasions: Theory and Practice. Oxford University Press, UK.
[5] Matthysen, E. (2005). Density-dependent dispersal in birds and mammals. Ecography, 28(3), 403–416. doi: 10.1111/j.0906-7590.2005.04073.x

When higher carrying capacities lead to faster propagationMarjorie Haond, Thibaut Morel-Journel, Eric Lombaert, Elodie Vercken, Ludovic Mailleret & Lionel Roques<p>This preprint has been reviewed and recommended by Peer Community In Ecology (https://dx.doi.org/10.24072/pci.ecology.100004). Finding general patterns in the expansion of natural populations is a major challenge in ecology and invasion biology...Biological invasions, Colonization, Dispersal & Migration, Experimental ecology, Population ecology, Spatial ecology, Metacommunities & Metapopulations, Theoretical ecologyMatthieu Barbier Yuval Zelnik2018-04-25 10:18:48 View