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28 Mar 2019
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Direct and transgenerational effects of an experimental heat wave on early life stages in a freshwater snail

Escargots cooked just right: telling apart the direct and indirect effects of heat waves in freashwater snails

Recommended by based on reviews by Amanda Lynn Caskenette, Kévin Tougeron and arnaud sentis

Amongst the many challenges and forms of environmental change that organisms face in our era of global change, climate change is perhaps one of the most straightforward and amenable to investigation. First, measurements of day-to-day temperatures are relatively feasible and accessible, and predictions regarding the expected trends in Earth surface temperature are probably some of the most reliable we have. It appears quite clear, in particular, that beyond the overall increase in average temperature, the heat waves locally experienced by organisms in their natural habitats are bound to become more frequent, more intense, and more long-lasting [1]. Second, it is well appreciated that temperature is a major environmental factor with strong impacts on different facets of organismal development and life-history [2-4]. These impacts have reasonably clear mechanistic underpinnings, with definite connections to biochemistry, physiology, and considerations on energetics. Third, since variation in temperature is a challenge already experienced by natural populations across their current and historical ranges, it is not a completely alien form of environmental change. Therefore, we already learnt quite a lot about it in several species, and so did the species, as they may be expected to have evolved dedicated adaptive mechanisms to respond to elevated temperatures. Last, but not least, temperature is quite amenable to being manipulated as an experimental factor.
For all these reasons, experimental studies of the consequences of increased temperature hit some of a sweetspot and are a source of very nice research, in many different organisms. The work by Leicht and Seppala [5] complements a sequence of earlier studies by this group, using the freshwater snail Lymnaea stagnalis as their model system [6-7].
In the present study, the authors investigate how a heat wave (a period of abnormally elevated temperature, here 25°C versus a normal 15°C) may have indirect effects on the next generation, through maternal effects. They question whether such indirect effects exist, and if they exist, how they compare, in terms of effect size, with the (more straightforward) direct effects observed in individuals that directly experience a heat wave. Transgenerational effects are well-known to occur following periods of physiological stress, and might thus have non negligible contributions to the overall effect of warming.
In this freshwater snail, heat has very strong direct effects: mortality increases at high temperature, but survivors grow much bigger, with a greater propensity to lay eggs and a (spectacular) three-fold increase in the number of eggs laid [6]. Considering that, it is easy to consider that transgenerational effects should be small game. And indeed, the present study also observes the big and obvious direct effects of elevated temperature: higher mortality, but greater propensity to oviposit. However, it was also found that the eggs were smaller if from mothers exposed to high temperature, with a correspondingly smaller size of hatchlings. This suggests that a heat wave causes the snails to lay more eggs, but smaller ones, reminiscent of a size-number trade-off. Unfortunately, clutch size could not be measured in this experiment, so this cannot be investigated any further. For this trait, the indirect effect may indeed be regarded as small game : eggs and hatchlings were about 15 % smaller, an effect size pretty small compared to the mammoth direct positive effect of temperature on shell length (see Figure 4 ; and also [6]). The same is true for developmental time (Figure 3).
However, for some traits the story was different. In particular, it was found that the (smaller) eggs produced from heated mothers were more likely to hatch by almost 10% (Figure 2). Here the indirect effect not only goes against the direct effect (hatching rate is lower at high temperature), but it also has similar effect size. As a consequence, taking into account both the indirect and direct effects, hatching success is essentially the same at 15°C and 25°C (Figure 2). Survival also had comparable effect sizes for direct and indirect effects. Indeed, survival was reduced by about 20% regardless of whom endured the heat stress (the focal individual or her mother; Figure 4). Interestingly, the direct and indirect effects were not quite cumulative: if a mother experienced a heat wave, heating up the offspring did not do much more damage, as though the offspring were ‘adapted’ to the warmer conditions (but keep in mind that, surprisingly, the authors’ stats did not find a significant interaction; Table 2).
At the end of the day, even though at first heat seems a relatively simple and understandable component of environmental change, this study shows how varied its effects can be effects on different components of individual fitness. The overall impact most likely is a mix of direct and indirect effects, of shifts along allocation trade-offs, and of maladaptive and adaptive responses, whose overall ecological significance is not so easy to grasp. That said, this study shows that direct and indirect (maternal) effects can sometimes go against one another and have similar intensities. Indirect effects should therefore not be overlooked in this kind of studies. It also gives a hint of what an interesting challenge it is to understand the adaptive or maladaptive nature of organism responses to elevated temperatures, and to evaluate their ultimate fitness consequences.

References

[1] Meehl, G. A., & Tebaldi, C. (2004). More intense, more frequent, and longer lasting heat waves in the 21st century. Science (New York, N.Y.), 305(5686), 994–997. doi: 10.1126/science.1098704
[2] Adamo, S. A., & Lovett, M. M. E. (2011). Some like it hot: the effects of climate change on reproduction, immune function and disease resistance in the cricket Gryllus texensis. The Journal of Experimental Biology, 214(Pt 12), 1997–2004. doi: 10.1242/jeb.056531
[3] Deutsch, C. A., Tewksbury, J. J., Tigchelaar, M., Battisti, D. S., Merrill, S. C., Huey, R. B., & Naylor, R. L. (2018). Increase in crop losses to insect pests in a warming climate. Science (New York, N.Y.), 361(6405), 916–919. doi: 10.1126/science.aat3466
[4] Sentis, A., Hemptinne, J.-L., & Brodeur, J. (2013). Effects of simulated heat waves on an experimental plant–herbivore–predator food chain. Global Change Biology, 19(3), 833–842. doi: 10.1111/gcb.12094
[5] Leicht, K., & Seppälä, O. (2019). Direct and transgenerational effects of an experimental heat wave on early life stages in a freshwater snail. BioRxiv, 449777, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/449777
[6] Leicht, K., Seppälä, K., & Seppälä, O. (2017). Potential for adaptation to climate change: family-level variation in fitness-related traits and their responses to heat waves in a snail population. BMC Evolutionary Biology, 17(1), 140. doi: 10.1186/s12862-017-0988-x
[7] Leicht, K., Jokela, J., & Seppälä, O. (2013). An experimental heat wave changes immune defense and life history traits in a freshwater snail. Ecology and Evolution, 3(15), 4861–4871. doi: 10.1002/ece3.874

Direct and transgenerational effects of an experimental heat wave on early life stages in a freshwater snailKatja Leicht, Otto Seppälä<p>Global climate change imposes a serious threat to natural populations of many species. Estimates of the effects of climate change‐mediated environmental stresses are, however, often based only on their direct effects on organisms, and neglect t...Climate changevincent calcagno2018-10-22 22:19:22 View
06 May 2022
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Effects of climate warming on the pine processionary moth at the southern edge of its range: a retrospective analysis on egg survival in Tunisia

Even the current climate change winners could end up being losers

Recommended by based on reviews by Matt Hill, Philippe Louapre, José Hodar and Corentin Iltis

Climate change is accelerating (IPCC 2022), and so applies ever stronger selective pressures on biodiversity (Segan et al. 2016). Possible responses include range shifts or adaptations to new climatic conditions (Bellard et al. 2012), but there is still much uncertainty about the extent of most species' adaptive capacities and the impact of extreme climatic events.
 
The pine processionary is a major pest of pine trees in the Mediterranean area. It is notably one of the few species for which a clear link between recent climate change and its northward expansion has been established (Battisti et al. 2005), and as such is often considered as globally benefitting from climate change. However, recent results show a retraction of its range at the southern limit (Bourougaaoui et al. 2021), exposed to high warming (+1.4°C in Tunisia since 1901 as opposed to +1.12°C on average in the Northern hemisphere) and extreme summer temperature events (Verner et al. 2013). Thus, it is possible that the species' adaptive abilities are being challenged at the southern limit of its native range by the magnitude of observed climate change.
 
In this work, Bourougaaoui et al. (2022) investigate how climate change over the last 30 years has impacted the reproductive success of the pine processionary moth in Tunisia. A major methodological interest of this study is that they used data both from historical collections and from recent samplings, which raised a challenge for running a longitudinal analysis as sampling locations differed between the two periods. By applying a grouping method to local climatic data, the authors were able to define several large climatic clusters within the country, and analyze long-term data from different sites within the same clusters. They find that both fecundity and hatching rate decreased over the period, while at the same time both the average temperature increased and climate variability increased. One of the main conclusions is that recurrent episodes of extreme heat during summer might have a larger impact than the long-term increase of average temperature, which strongly echoes how the intensification of weather extremes is currently proving one of the most important dimensions of climate change.
 
However, a most interesting hypothesis also arises from the analysis of the differences between climatic clusters: preexisting adaptations to heat, for instance, phenological shifts that allow the most sensitive stages to develop earlier in the season before the extreme heat events are most likely to occur, might actually reduce impacts in the historically warmest areas. Thus the greatest climate vulnerability might not always stand where one expects it.
 
References

Battisti A, Stastny M, Netherer S, Robinet C, Schopf A, Roques A, Larsson S (2005) Expansion of Geographic Range in the Pine Processionary Moth Caused by Increased Winter Temperatures. Ecological Applications, 15, 2084–2096. https://doi.org/10.1890/04-1903

Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F (2012) Impacts of climate change on the future of biodiversity. Ecology Letters, 15, 365–377. https://doi.org/10.1111/j.1461-0248.2011.01736.x

Bourougaaoui A, Ben Jamâa ML, Robinet C (2021) Has North Africa turned too warm for a Mediterranean forest pest because of climate change? Climatic Change, 165, 46. https://doi.org/10.1007/s10584-021-03077-1

Bourougaaoui A, Robinet C, Jamaa MLB, Laparie M (2022) Effects of climate warming on the pine processionary moth at the southern edge of its range: a retrospective analysis on egg survival in Tunisia. bioRxiv, 2021.08.17.456665, ver. 5 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2021.08.17.456665

IPCC. 2022. Climate Change 2022: Impacts, Adaptation, and Vulnerability. Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change [H.-O. Pörtner, D.C. Roberts, M. Tignor, E.S. Poloczanska, K. Mintenbeck, A. Alegría, M. Craig, S. Langsdorf, S. Löschke, V. Möller, A. Okem, B. Rama (eds.)]. Cambridge University Press. In Press.

Segan DB, Murray KA, Watson JEM (2016) A global assessment of current and future biodiversity vulnerability to habitat loss–climate change interactions. Global Ecology and Conservation, 5, 12–21. https://doi.org/10.1016/j.gecco.2015.11.002

Verner D (2013) Tunisia in a Changing Climate : Assessment and Actions for Increased Resilience and Development. World Bank, Washington, DC. https://doi.org/10.1596/978-0-8213-9857-9  

Effects of climate warming on the pine processionary moth at the southern edge of its range: a retrospective analysis on egg survival in TunisiaAsma Bourougaaoui, Christelle Robinet, Mohamed Lahbib Ben Jamâa, Mathieu Laparie<p style="text-align: justify;">In recent years, ectotherm species have largely been impacted by extreme climate events, essentially heatwaves. In Tunisia, the pine processionary moth (PPM), <em>Thaumetopoea pityocampa</em>, is a highly damaging p...Climate change, Dispersal & Migration, Life history, Phenotypic plasticity, Species distributions, Terrestrial ecology, Thermal ecology, ZoologyElodie Vercken2021-08-19 11:03:13 View
06 Jan 2021
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Comparing statistical and mechanistic models to identify the drivers of mortality within a rear-edge beech population

The complexity of predicting mortality in trees

Recommended by based on reviews by Lisa Hülsmann and 2 anonymous reviewers

One of the main issues of forest ecosystems is rising tree mortality as a result of extreme weather events (Franklin et al., 1987). Eventually, tree mortality reduces forest biomass (Allen et al., 2010), although its effect on forest ecosystem fluxes seems not lasting too long (Anderegg et al., 2016). This controversy about the negative consequences of tree mortality is joined to the debate about the drivers triggering and the mechanisms accelerating tree decline. For instance, there is still room for discussion about carbon starvation or hydraulic failure determining the decay processes (Sevanto et al., 2014) or about the importance of mortality sources (Reichstein et al., 2013). Therefore, understanding and predicting tree mortality has become one of the challenges for forest ecologists in the last decade, doubling the rate of articles published on the topic (*). Although predicting the responses of ecosystems to environmental change based on the traits of species may seem a simplistic conception of ecosystem functioning (Sutherland et al., 2013), identifying those traits that are involved in the proneness of a tree to die would help to predict how forests will respond to climate threatens.
Modelling tree mortality is complex, involving multiple factors acting simultaneously at different scales, from tree genetics to ecosystem dynamics and from microsite conditions to global climatic events. Therefore, taking into account different approaches to reduce uncertainty of the predictions is needed (Bugmann et al., 2019). Petit-Cailleux et al. (2020) uses statistical and process-based models to detect the main mortality drivers of a drought- and frost-prone beech population. Particularly, they assessed the intra-individual characteristics of the population, that may play a decisive role explaining the differences in tree vulnerability to extreme weather events. Comparing the results of both analytical approaches, they find out several key factors, such as defoliation, leaf phenology and tree size, that were consistent between them. Even more, the process-based model showed the physiological mechanisms that may explain the individual vulnerability, for instance higher loss of hydraulic conductance may increase the mortality risk of trees with early budburst phenology and large stem diameter. The authors also successfully model annual mortality rate with a linear relationship including only three parameters: loss of conductance, biomass of reserves and late frost days.
This valuable study is a good example of the complexity in understanding and predicting tree mortality. The authors carried out the ambitious commitment of studying the inter-annual variation in mortality with 14-year dataset. However, it might be not enough time to control for the dependence of temporal data to soundly model mortality rate. The authors also acknowledge that the use of two approaches increases the knowledge from different perspectives, but at the same time comparing their results is difficult because the parameters used are not identical. Particularly, process-based models tend to consider the same microclimatic conditions for every tree in the population, and may produce inconsistences with statistical models. Alternatively, individual-based modelling might overcome some of the incompatibilities between the approaches (Zhu et al., 2019).

(*) Number (and percentage) of articles found in Web of Sciences after searching (December the 10th, 2020) “tree mortality”: from 163 (0.006%) in 2010 to 412 (0.013%) in 2020.

References

Allen et al. (2010). A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest ecology and management, 259(4), 660-684. doi: https://doi.org/10.1016/j.foreco.2009.09.001
Anderegg et al. (2016). When a tree dies in the forest: scaling climate-driven tree mortality to ecosystem water and carbon fluxes. Ecosystems, 19(6), 1133-1147. doi: https://doi.org/10.1007/s10021-016-9982-1
Bugmann et al. (2019). Tree mortality submodels drive simulated long‐term forest dynamics: assessing 15 models from the stand to global scale. Ecosphere, 10(2), e02616. doi: https://doi.org/10.1002/ecs2.2616
Franklin, J. F., Shugart, H. H. and Harmon, M. E. (1987) Death as an ecological process: the causes, consequences, and variability of tree mortality. BioScience, 37, 550–556. doi: https://doi.org/10.2307/1310665
Petit-Cailleux, C., Davi, H., Lefèvre, F., Garrigue, J., Magdalou, J.-A., Hurson, C., Magnanou, E. and Oddou-Muratorio, S. (2020) Comparing statistical and mechanistic models to identify the drivers of mortality within a rear-edge beech population. bioRxiv, 645747, ver 7 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/645747
Reichstein et al. (2013). Climate extremes and the carbon cycle. Nature, 500(7462), 287-295. doi: https://doi.org/10.1038/nature12350
Sevanto, S., Mcdowell, N. G., Dickman, L. T., Pangle, R., and Pockman, W. T. (2014). How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant, cell & environment, 37(1), 153-161. doi: https://doi.org/10.1111/pce.12141
Sutherland et al. (2013). Identification of 100 fundamental ecological questions. Journal of ecology, 101(1), 58-67. doi: https://doi.org/10.1111/1365-2745.12025
Zhu, Y., Liu, Z., and Jin, G. (2019). Evaluating individual-based tree mortality modeling with temporal observation data collected from a large forest plot. Forest Ecology and Management, 450, 117496. doi: https://doi.org/10.1016/j.foreco.2019.117496

Comparing statistical and mechanistic models to identify the drivers of mortality within a rear-edge beech populationCathleen Petit-Cailleux, Hendrik Davi, François Lefevre, Christophe Hurson, Joseph Garrigue, Jean-André Magdalou, Elodie Magnanou and Sylvie Oddou-Muratorio<p>Since several studies have been reporting an increase in the decline of forests, a major issue in ecology is to better understand and predict tree mortality. The interactions between the different factors and the physiological processes giving ...Climate change, Physiology, Population ecologyLucía DeSoto2019-05-24 11:37:38 View
15 Nov 2023
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The challenges of independence: ontogeny of at-sea behaviour in a long-lived seabird

On the road to adulthood: exploring progressive changes in foraging behaviour during post-fledging immaturity using remote tracking

Recommended by based on reviews by Juliet Lamb and 1 anonymous reviewer

In most vertebrate species, the period of life spanning from departure from the growing site until reaching a more advanced life stage (immature or adult) is critical. During this period, juveniles are often highly vulnerable because they have not reached the morphological, physiological and behavioural maturity levels of adults yet and are therefore at high risk of mortality, e.g. through starvation, depredation or competition (e.g. Marchetti & Price 1989, Wunderle 1991, Naef-Daenzer & Grüebler 2016). In line with this, juvenile survival is most often far lower than adult survival (e.g. Wooller et al. 1992). In species with parental care, juveniles have to acquire behavioural independence from their parents and possibly establish their own territory during this period of life. Very often, this is also the period that is least well-known in the life cycle (Cox et al. 2014, Naef-Daenzer & Grüebler 2016) because of reduced accessibility to individuals and/or adoption of low conspicuous behaviours. Therefore, our understanding of how juveniles acquire typical adult behaviours and how this progressively increases their survival prospects is still very limited (Naef-Daenzer & Grüebler 2016), and questions such as the length of this transition period or the cognitive (e.g. learning, memorization) mechanisms involved remain largely unresolved. This is particularly true regarding the acquisition of independent foraging behaviour (Marchetti & Price 1989).

Because direct observations of juvenile behaviours are usually very difficult except in specific situations or at the cost of an enormous effort, the use of remote tracking devices can be particularly appealing in this context (e.g. Ponchon et al. 2013, Kays et al. 2015). Over the past decades, technical advances have allowed the monitoring of not only individuals’ movements at both large and small spatial scales but also their activities and behaviours based on different parameters recording e.g. speed of movement or diving depth (Whitford & Klimley 2019). Device miniaturization has in particular allowed smaller species to be equipped and/or longer periods of time to be monitored (e.g. Naef-Daenzer et al. 2005). This has opened up whole fields of research, and has been particularly used on marine seabirds. In these species, individuals are most often inaccessible when at sea, representing most of the time outside (and even within) the breeding season, and the life cycle of these long-lived species can include an extended immature period (up to many years) during which most of them will remain unseen, until they come back as breeders or pre-breeders (e.g. Wooller et al. 1992, Oro & Martínez-Abraín 2009). Survival has been found to increase gradually with age in these species before reaching high values characteristic of the adult stage. However, the mechanisms underlying this increase are still to be deciphered.

The study by Delord et al. (2023) builds upon the hypothesis that juveniles gradually learn foraging techniques and movement strategies, improving their foraging efficiency, as previous data on flight parameters seemed to show in different long-lived bird species. Yet, these previous studies obtained data over a limited period of time, i.e. a few months at best. Whether these data could capture the whole dynamics of the progressive acquisition of foraging and movement skills can only be assessed by measuring behaviour over a longer time period and comparing it to similar data in adults, to account for seasonal variation in relation to both resource availability and energetic demands, e.g. due to molt.

The present study (Delord et al. 2023) addresses these questions by taking advantage of longer-lasting recordings of the location and activity of juvenile, immature and adult birds obtained simultaneously to investigate changes over time in juvenile behaviour and thereby provide hints about how young progressively acquire foraging skills. This study is performed on Amsterdam albatrosses, a highly endangered long-lived sea bird, with obvious conservation issues (Thiebot et al. 2015). The results show progressive changes in foraging effort over the first two months after departure from the birth colony, but large differences remain between life stages over a much longer time frame. They also reveal strong variations between sexes and over time in the year. Overall, this study, therefore, confirms the need for very long-term data to be collected in order to address the question of progressive behavioural maturation and associated survival consequences in such species with strongly deferred maturity. Ideally, the same individuals should be monitored over different life stages, from the juvenile period up to adulthood, but this would require further technical development to release the issue of powering duration limitation.

As reviewers emphasized in the first review round, one main challenge now remains to ascertain the outcome of the observed behavioural changes in foraging behaviour: we expect them to reflect improvement in foraging skills and thus performance of juveniles over time, but this would need to be tested. Collecting data on foraging efficiency is yet another challenge, that future technical developments may also help overcome. Importantly also, data were available only for individuals that could be caught again because the tracking device had to be retrieved from the bird. Here, a substantial fraction of the loggers (one-fifth) could not be found again (Delord et al. 2023). To what extent the birds for which no data could be obtained are a random sample of the equipped birds would also need to be assessed. The further development of remote tracking techniques allowing data to be downloaded from a long distance should help further exploration of behavioural ontogeny of juveniles while maturing and its survival consequences. Because the maturation process explored here is likely to show very different characteristics (e.g. timing and speed) in smaller / shorter-lived species (see Cox et al. 2014, Naef-Daenzer & Grüebler 2016), the development of miniaturization is also expected to allow further investigation of post-fledging behavioural maturation in a wider range of bird species. Our understanding of this crucial life phase in different types of species should thus continue to progress in the coming years.

References

Cox W. A., Thompson F. R. III, Cox A. S. & Faaborg J. 2014. Post-fledging survival in passerine birds and the value of post-fledging studies to conservation. Journal of Wildlife Management, 78: 183-193. https://doi.org/10.1002/jwmg.670

Delord K., Weimerskirch H. & Barbraud C. 2023. The challenges of independence: ontogeny of at-sea behaviour in a long-lived seabird. bioRxiv, ver. 6 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2021.10.23.465439

Kays R., Crofoot M. C., Jetz W. & Wikelski M. 2015. Terrestrial animal tracking as an eye on life and planet. Science, 348 (6240). https://doi.org/10.1126/science.aaa2478

Marchetti K: & Price T. 1989. Differences in the foraging of juvenile and adult birds: the importance of developmental constraints. Biological Reviews, 64: 51-70. https://doi.org/10.1111/j.1469-185X.1989.tb00638.x

Naef-Daenzer B., Fruh D., Stalder M., Wetli P. & Weise E. 2005. Miniaturization (0.2 g) and evaluation of attachment techniques of telemetry transmitters. The Journal of Experimental Biology, 208: 4063–4068. https://doi.org/10.1242/jeb.01870

Naef-Daenzer B. & Grüebler M. U. 2016. Post-fledging survival of altricial birds: ecological determinants and adaptation. Journal of Field Ornithology, 87: 227-250. https://doi.org/10.1111/jofo.12157

Oro D. & Martínez-Abraín A. 2009. Ecology and behavior of seabirds. Marine Ecology, pp.364-389.

Ponchon A., Grémillet D., Doligez B., Chambert T., Tveera T., Gonzàles-Solìs J & Boulinier T. 2013. Tracking prospecting movements involved in breeding habitat selection: insights, pitfalls and perspectives. Methods in Ecology and Evolution, 4: 143-150. https://doi.org/10.1111/j.2041-210x.2012.00259.x

Thiebot J.-B., Delord K., Barbraud C., Marteau C. & Weimerskirch H. 2015. 167 individuals versus millions of hooks: bycatch mitigation in longline fisheries underlies conservation of Amsterdam albatrosses. Aquatic Conservation 26: 674-688. https://doi.org/10.1002/aqc.2578

Whitford M & Klimley A. P. An overview of behavioral, physiological, and environmental sensors used in animal biotelemetry and biologging studies. Animal Biotelemetry, 7: 26. https://doi.org/10.1186/s40317-019-0189-z

Wooller R.D., Bradley J. S. & Croxall J. P. 1992. Long-term population studies of seabirds. Trends in Ecology and Evolution, 7: 111-114. https://doi.org/10.1016/0169-5347(92)90143-y

Wunderle J. M. 1991. Age-specific foraging proficiency in birds. Current Ornithology, 8: 273-324.

The challenges of independence: ontogeny of at-sea behaviour in a long-lived seabirdKarine Delord, Henri Weimerskirch, Christophe Barbraud<p style="text-align: justify;">The transition to independent foraging represents an important developmental stage in the life cycle of most vertebrate animals. Juveniles differ from adults in various life history traits and tend to survive less w...Behaviour & Ethology, Foraging, OntogenyBlandine Doligez2021-10-26 07:51:49 View
10 Aug 2023
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Coexistence of many species under a random competition-colonization trade-off

Assembly in metacommunities driven by a competition-colonization tradeoff: more species in, more species out

Recommended by based on reviews by Canan Karakoç and 1 anonymous reviewer

The output of a community model depends on how you set its parameters. Thus, analyses of specific parameter settings hardwire the results to specific ecological scenarios. Because more general answers are often of interest, one tradition is to give models a statistical treatment: one summarizes how model parameters vary across species, and then predicts how changing the summary, instead of the individual parameters themselves, would change model output. Arguably the best-known example is the work initiated by May, showing that the properties of a community matrix, encoding effects species have on each other near their equilibrium, determine stability (1,2). More recently, this statistical treatment has also been applied to one of community ecology’s more prickly and slippery subjects: community assembly, which deals with the question “Given some regional species pool, which species will be able to persist together at some local ecosystem?”. Summaries of how species grow and interact in this regional pool predict the fraction of survivors and their relative abundances, the kind of dynamics, and various kinds of stability (3,4). One common characteristic of such statistical treatments is the assumption of disorder: if species do not interact in too structured ways, simple and therefore powerful predictions ensue that often stand up to scrutiny in relatively ordered systems. 
 
In their recent preprint, Miller, Clenet, et al. (5) subscribe to this tradition and consider tractable assembly scenarios (6) to study the outcome of assembly in a metacommunity. They recover a result of remarkable simplicity: roughly half of the species pool makes it into the final assemblage. Their vehicle is Tilman’s classic metacommunity model (7), where colonization rates are traded off with competitive ability. More precisely, in this model, one ranks species according to their colonization rate and attributes a greater competitive strength to lower-ranked species, which makes competition strictly hierarchical and thus departs from the disorder usually imposed by statistical approaches. The authors then leverage the simplicity of the species interaction network implied by this recursive setting to analytically probe how many species survive assembly. This turns out to be a fixed fraction that is distributed according to a Binomial with a mean of 0.5. While these results should not be extrapolated beyond the system at hand (4), they are important for two reasons. First, they imply that, within the framework of metacommunities driven by competition-colonization tradeoffs, richer species pools will produce richer communities: there is no upper bound on species richness, other than the one set by the raw material available for assembly. Second, this conclusion does not rely on simulation or equation solving and is, therefore, a hopeful sign of the palatability of the problem, if formalized in the right way. Their paper then shows that varying some of the settings does not change the main conclusion: changing how colonization rates distribute across species, and therefore the nature of the tradeoff, or the order with which species invade seems not to disrupt the big picture. Only when invaders are created “de novo” during assembly, a scenario akin to “de novo” mutation, a smaller fraction of species will survive assembly. 
 
As always, logical extensions of this study involve complicating the model and then looking if the results stay on par. The manuscript cites switching to other kinds of competition-colonization tradeoffs, and the addition of spatial heterogeneity as two potential avenues for further research. While certainly of merit, alternative albeit more bumpy roads would encompass models with radically different behavior. Most notably, one wonders how priority effects would play out. The current analysis shows that different invasion orders always lead to the same final composition, and therefore the same final species richness, confirming earlier results from models with similar structures (6). In models with priority effects, different invasion orders will surely lead to different compositions at the end. However, if one only cares about how many (and not which) species survive, it is unsure how much priority effects will qualitatively affect assembly. Because priority effects are varied in their topological manifestation (8), an important first step will be to evaluate which kinds of priority effects are compliant with formal analysis. 
 
References
 
1. May, R. M. (1972). Will a Large Complex System be Stable? Nature 238, 413–414. https://doi.org/10.1038/238413a0

2. Allesina, S. & Tang, S. (2015). The stability–complexity relationship at age 40: a random matrix perspective. Population Ecology, 57, 63–75. https://doi.org/10.1007/s10144-014-0471-0

3. Bunin, G. (2016). Interaction patterns and diversity in assembled ecological communities. Preprint at http://arxiv.org/abs/1607.04734.

4. Barbier, M., Arnoldi, J.-F., Bunin, G. & Loreau, M. (2018). Generic assembly patterns in complex ecological communities. Proceeding of the National Academy of Sciences, 115, 2156–2161. https://doi.org/10.1073/pnas.1710352115

5. Miller, Z. R., Clenet, M., Libera, K. D., Massol, F. & Allesina, S. (2023). Coexistence of many species under a random competition-colonization trade-off. bioRxiv 2023.03.23.533867, ver 3 peer-reviewed and recommended by PCI Ecology. https://doi.org/10.1101/2023.03.23.533867

6. Serván, C. A. & Allesina, S. (2021). Tractable models of ecological assembly. Ecology Letters, 24, 1029–1037. https://doi.org/10.1111/ele.13702

7. Tilman, D. (1994). Competition and Biodiversity in Spatially Structured Habitats. Ecology, 75, 2–16. https://doi.org/10.2307/1939377

8. Song, C., Fukami, T. & Saavedra, S. (2021). Untangling the complexity of priority effects in multispecies communities. Ecolygy Letters, 24, 2301–2313. https://doi.org/10.1111/ele.13870

Coexistence of many species under a random competition-colonization trade-offZachary R. Miller, Maxime Clenet, Katja Della Libera, François Massol, Stefano Allesina<p>The competition-colonization trade-off is a well-studied coexistence mechanism for metacommunities. In this setting, it is believed that coexistence of all species requires their traits to satisfy restrictive conditions limiting their similarit...Biodiversity, Coexistence, Colonization, Community ecology, Competition, Population ecology, Spatial ecology, Metacommunities & Metapopulations, Theoretical ecologyFrederik De Laender2023-03-30 20:42:48 View
25 Oct 2021
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The taxonomic and functional biogeographies of phytoplankton and zooplankton communities across boreal lakes

The difficult interpretation of species co-distribution

Recommended by based on reviews by Anthony Maire and Emilie Macke ?

Ecology is the study of the distribution of organisms in space and time and their interactions. As such, there is a tradition of studies relating abiotic environmental conditions to species distribution, while another one is concerned by the effects of consumers on the abundance of their resources.  Interestingly, joining the dots appears more difficult than it would suggest: eluding the effect of species interactions on distribution remains one of the greatest challenges to elucidate nowadays (Kissling et al. 2012). Theory suggests that yes, species interactions such as predation and competition should influence range limits (Godsoe et al. 2017), but the common intuition among many biogeographers remains that over large areas such as regions and continents, environmental drivers like temperature and precipitation overwhelm their local effects. Answering this question is of primary importance in the context where species are moving around with climate warming.  Inconsistencies in food web structure may arise with asynchronized movements of consumers and their resources, leading to a major disruption in regulation and potentially ecosystem functioning. Solving this problem, however, remains very challenging because we have to rely on observational data since experiments are hard to perform at the biogeographical scale. 

The study of St-Gelais is an interesting step forward to solve this problem. Their main objective was to assess the strength of the association between phytoplankton and zooplankton communities at a large spatial scale, looking at the spatial covariation of both taxonomic and functional composition. To do so, they undertook a massive survey of more than 100 lakes across three regions of the boreal region of Québec. Species and functional composition were recorded, along with a set of abiotic variables. Classic community ecology at this point. The difficulty they faced was to disentangle the multiple causal relationships involved in the distribution of both trophic levels. Teasing apart bottom-up and top-down forces driving the assembly of plankton communities using observational data is not an easy task. On the one hand, both trophic levels could respond to variations in temperature, nutrient availability and dissolved organic carbon. The interpretation is fairly straightforward if the two levels respond to different factors, but the situation is much more complicated when they do respond similarly. There are potentially three possible underlying scenarios. First, the phyto and zooplankton communities may share the same environmental requirements, thereby generating a joint distribution over gradients such as temperature and nutrient availability. Second, the abiotic environment could drive the distribution of the phytoplankton community, which would then propagate up and influence the distribution of the zooplankton community. Alternatively, the abiotic environment could constrain the distribution of the zooplankton, which could then affect the one of phytoplankton. In addition to all of these factors, St-Gelais et al also consider that dispersal may limit the distribution, well aware of previous studies documenting stronger dispersal limitations for zooplankton communities. 

Unfortunately, there is not a single statistical approach that could be taken from the shelf and used to elucidate drivers of co-distribution. Joint species distribution was once envisioned as a major step forward in this direction (Warton et al. 2015), but there are several limits preventing the direct interpretation that co-occurrence is linked to interactions (Blanchet et al. 2020). Rather, St-Gelais used a variety of multivariate statistics to reveal the structure in their observational data. First, using a Procrustes analysis (a method testing if the spatial variation of one community is correlated to the structure of another community), they found a significant correlation between phytoplankton and zooplankton communities, indicating a taxonomic coupling between the groups. Interestingly, this observation was maintained for functional composition only when interaction-related traits were considered. At this point, these results strongly suggest that interactions are involved in the correlation, but it's hard to decipher between bottom-up and top-down perspectives. A complementary analysis performed with a constrained ordination, per trophic level, provided complementary pieces of information. First observation was that only functional variation was found to be related to the different environmental variables, not taxonomic variation. Despite that trophic levels responded to water quality variables, spatial autocorrelation was more important for zooplankton communities and the two layers appear to respond to different variables. 

It is impossible with those results to formulate a strong conclusion about whether grazing influence the co-distribution of phytoplankton and zooplankton communities. That's the mere nature of observational data. While there is a strong spatial association between them, there are also diverging responses to the different environmental variables considered. But the contrast between taxonomic and functional composition is nonetheless informative and it seems that beyond the idiosyncrasies of species composition, trait distribution may be more informative and general. Perhaps the most original contribution of this study is the hierarchical approach to analyze the data, combined with the simultaneous analysis of taxonomic and functional distributions. Having access to a vast catalog of multivariate statistical techniques, a careful selection of analyses helps revealing key features in the data, rejecting some hypotheses and accepting others. Hopefully, we will see more and more of such multi-trophic approaches to distribution because it is now clear that the factors driving distribution are much more complicated than anticipated in more traditional analyses of community data. Biodiversity is more than a species list, it is also all of the interactions between them, influencing their distribution and abundance (Jordano 2016).

References

Blanchet FG, Cazelles K, Gravel D (2020) Co-occurrence is not evidence of ecological interactions. Ecology Letters, 23, 1050–1063. https://doi.org/10.1111/ele.13525

Godsoe W, Jankowski J, Holt RD, Gravel D (2017) Integrating Biogeography with Contemporary Niche Theory. Trends in Ecology & Evolution, 32, 488–499. https://doi.org/10.1016/j.tree.2017.03.008

Jordano P (2016) Chasing Ecological Interactions. PLOS Biology, 14, e1002559. https://doi.org/10.1371/journal.pbio.1002559

Kissling WD, Dormann CF, Groeneveld J, Hickler T, Kühn I, McInerny GJ, Montoya JM, Römermann C, Schiffers K, Schurr FM, Singer A, Svenning J-C, Zimmermann NE, O’Hara RB (2012) Towards novel approaches to modelling biotic interactions in multispecies assemblages at large spatial extents. Journal of Biogeography, 39, 2163–2178. https://doi.org/10.1111/j.1365-2699.2011.02663.x

St-Gelais NF, Vogt RJ, Giorgio PA del, Beisner BE (2021) The taxonomic and functional biogeographies of phytoplankton and zooplankton communities across boreal lakes. bioRxiv, 373332, ver. 4 peer-reviewed and recommended by Peer community in Ecology. https://doi.org/10.1101/373332

Warton DI, Blanchet FG, O’Hara RB, Ovaskainen O, Taskinen S, Walker SC, Hui FKC (2015) So Many Variables: Joint Modeling in Community Ecology. Trends in Ecology & Evolution, 30, 766–779. https://doi.org/10.1016/j.tree.2015.09.007

Wisz MS, Pottier J, Kissling WD, Pellissier L, Lenoir J, Damgaard CF, Dormann CF, Forchhammer MC, Grytnes J-A, Guisan A, Heikkinen RK, Høye TT, Kühn I, Luoto M, Maiorano L, Nilsson M-C, Normand S, Öckinger E, Schmidt NM, Termansen M, Timmermann A, Wardle DA, Aastrup P, Svenning J-C (2013) The role of biotic interactions in shaping distributions and realised assemblages of species: implications for species distribution modelling. Biological Reviews, 88, 15–30. https://doi.org/10.1111/j.1469-185X.2012.00235.x

The taxonomic and functional biogeographies of phytoplankton and zooplankton communities across boreal lakesNicolas F St-Gelais, Richard J Vogt, Paul A del Giorgio, Beatrix E Beisner<p>Strong trophic interactions link primary producers (phytoplankton) and consumers (zooplankton) in lakes. However, the influence of such interactions on the biogeographical distribution of the &nbsp;taxa and functional traits of planktonic organ...Biogeography, Community ecology, Species distributionsDominique Gravel2018-07-24 15:01:51 View
12 Jun 2019
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Environmental heterogeneity drives tsetse fly population dynamics and control

Modeling jointly landscape complexity and environmental heterogeneity to envision new strategies for tsetse flies control

Recommended by based on reviews by Timothée Vergne and 1 anonymous reviewer

Today, understanding spatio-temporal dynamics of pathogens is pivotal to understand their transmission and controlling them. First, understanding this dynamics can reveal the ecology of their transmission [1]. Indeed, such knowledge, based on data that are quite easy to access, can shed light on transmission modes, which could rely on different animal species that can be spatially distributed in a non-uniform way [2]. This is especially true for pathogens with complex life-cycles, despite that investigating such dynamics is very challenging and rely mostly on mathematical models.
Moreover, this knowledge can also highlight some weak points in a complex web of transmission and therefore allowing us to envision new innovative control strategies. This has been first proposed on human pathogens, where connectivity among populations can be analyzed to identify which connections need to be targeted to stop or slow down an epidemics [3]. However, this idea is increasingly recognized as a promising new approach for pathogens involving vector populations, especially regarding the complexity to decrease on a long-term the abundance of these vector populations [4].
In "Environmental heterogeneity drives tsetse fly population dynamics and control" [5], Cecilia and co-authors have developed a sophisticated spatio-temporal mechanistic model to figure out how local environment, involved within landscape of different complexities, can impact the population dynamics of tsetse flies, an invertebrate species that can serve as a vector for many pathogens of animal and human importance. They found that spatial patches with the lowest temperature mean and the lowest environmental fluctuations can act as refuge for this species, representing therefore preferential targets for disease control.
The reviewers and I agree that the mathematical framework developed address very well an important topic for both ecological and public health literature. More importantly, it shows how fundamental ecological knowledge can drive pathogen control strategies, opening an interesting avenue for cross-disciplinary research on vector-borne diseases.

References

[1] Grenfell, B. T., Bjørnstad, O. N., & Kappey, J. (2001). Travelling waves and spatial hierarchies in measles epidemics. Nature, 414(6865), 716-723. doi: 10.1038/414716a
[2] Perkins, S. E., Cattadori, I. M., Tagliapietra, V., Rizzoli, A. P., & Hudson, P. J. (2003). Empirical evidence for key hosts in persistence of a tick-borne disease. International journal for parasitology, 33(9), 909-917. doi: 10.1016/S0020-7519(03)00128-0
[3] Colizza, V., Barrat, A., Barthélemy, M., & Vespignani, A. (2006). The role of the airline transportation network in the prediction and predictability of global epidemics. Proceedings of the National Academy of Sciences, 103(7), 2015-2020. doi: 10.1073/pnas.0510525103
[4] Pepin, K. M., Leach, C. B., Marques-Toledo, C., Laass, K. H., Paixao, K. S., et al. (2015) Utility of mosquito surveillance data for spatial prioritization of vector control against dengue viruses in three Brazilian cities. Parasites & Vectors 8, 1–15. doi: 10.1186/s13071-015-0659-y
[5] Cecilia, H., Arnoux, S., Picault, S., Dicko, A., Seck, M. T., Sall, B., Bassène, M., Vreysen, M., Pagabeleguem, S., Bancé, A., Bouyer, J. and Ezanno, P.(2019). Environmental heterogeneity drives tsetse fly population dynamics and control. bioRxiv 493650, ver. 3 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/493650

Environmental heterogeneity drives tsetse fly population dynamics and controlCecilia H, Arnoux S, Picault S, Dicko A, Seck MT, Sall B, Bassene M, Vreysen M, Pagabeleguem S, Bance A, Bouyer J, Ezanno P<p>A spatially and temporally heterogeneous environment may lead to unexpected population dynamics. Knowledge still is needed on which of the local environment properties favour population maintenance at larger scale. For pathogen vectors, such as...Biological control, Population ecology, Spatial ecology, Metacommunities & MetapopulationsBenjamin Roche2018-12-14 12:13:39 View
23 Mar 2020
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Intraspecific difference among herbivore lineages and their host-plant specialization drive the strength of trophic cascades

Tell me what you’ve eaten, I’ll tell you how much you’ll eat (and be eaten)

Recommended by and based on reviews by Bastien Castagneyrol and 1 anonymous reviewer

Tritrophic interactions have a central role in ecological theory and applications [1-3]. Particularly, systems comprised of plants, herbivores and predators have historically received wide attention given their ubiquity and economic importance [4]. Although ecologists have long aimed to understand the forces that govern alternating ecological effects at successive trophic levels [5], several key open questions remain (at least partially) unanswered [6]. In particular, the analysis of complex food webs has questioned whether ecosystems can be viewed as a series of trophic chains [7,8]. Moreover, whether systems are mostly controlled by top-down (trophic cascades) or bottom-up processes remains an open question [6].
Traditionally, studies have addressed how species diversity at different food chain compartments affect the strength and direction of trophic cascades [9]. For example, many studies have tested whether biological control was more efficient with more than one species of natural enemies [10-12]. Much less attention has been given to the role of within-species variation in shaping trophic cascades [13]. In particular, whereas the impact of trait variation within species of plants or predators on successive trophic levels has been recently addressed [14,15], the impact of intraspecific herbivore variation is in its infancy (but see [16]). This is at odds with the resurgent acknowledgment of the importance of individual variation for several ecological processes operating at higher levels of biological organization [17].
Sources of variation within species can come in many flavours. In herbivores, striking ecological variation can be found among populations occurring on different host plants, which become genetically differentiated, thus forming host races [18,19]. Curiously, the impact of variation across host races on the strength of trophic cascades has, to date, not been explored. This is the gap that the manuscript by Sentis and colleagues [20] fills. They experimentally studied a curious tri-trophic system where the primary consumer, pea aphids, specializes in different plant hosts, creating intraspecific variation across biotypes. Interestingly, there is also ecological variation across lineages from the same biotype. The authors set up experimental food chains, where pea aphids from different lineages and biotypes were placed in their universal legume host (broad bean plants) and then exposed to a voracious but charming predator, ladybugs. The full factorial design of this experiment allowed the authors to measure vertical effects of intraspecific variation in herbivores on both plant productivity (top-down) and predator individual growth (bottom-up).
The results nicely uncover the mechanisms by which intraspecific differences in herbivores precipitates vertical modulation in food chains. Herbivore lineage and host-plant specialization shaped the strength of trophic cascades, but curiously these effects were not modulated by density-dependence. Further, ladybugs consuming pea aphids from different lineages and biotypes grew at distinct rates, revealing bottom-up effects of intraspecific variation in herbivores.
These findings are novel and exciting for several reasons. First, they show how intraspecific variation in intermediate food chain compartments can simultaneously reverberate both top-down and bottom-up effects. Second, they bring an evolutionary facet to the understanding of trophic cascades, providing valuable insights on how genetically differentiated populations play particular ecological roles in food webs. Finally, Sentis and colleagues’ findings [20] have critical implications well beyond their study systems. From an applied perspective, they provide an evident instance on how consumers’ evolutionary specialization matters for their role in ecosystems processes (e.g. plant biomass production, predator conversion rate), which has key consequences for biological control initiatives and invasive species management. From a conceptual standpoint, their results ignite the still neglected value of intraspecific variation (driven by evolution) in modulating the functioning of food webs, which is a promising avenue for future theoretical and empirical studies.

References

[1] Price, P. W., Bouton, C. E., Gross, P., McPheron, B. A., Thompson, J. N., & Weis, A. E. (1980). Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual review of Ecology and Systematics, 11(1), 41-65. doi: 10.1146/annurev.es.11.110180.000353
[2] Olff, H., Brown, V.K. & Drent, R.H. (1999). Herbivores: between plants and predators. Blackwell Science, Oxford.
[3] Tscharntke, T. & Hawkins, B.A. (2002). Multitrophic level interactions. Cambridge University Press. doi: 10.1017/CBO9780511542190
[4] Agrawal, A. A. (2000). Mechanisms, ecological consequences and agricultural implications of tri-trophic interactions. Current opinion in plant biology, 3(4), 329-335. doi: 10.1016/S1369-5266(00)00089-3
[5] Pace, M. L., Cole, J. J., Carpenter, S. R., & Kitchell, J. F. (1999). Trophic cascades revealed in diverse ecosystems. Trends in ecology & evolution, 14(12), 483-488. doi: 10.1016/S0169-5347(99)01723-1
[6] Abdala‐Roberts, L., Puentes, A., Finke, D. L., Marquis, R. J., Montserrat, M., Poelman, E. H., ... & Mooney, K. (2019). Tri‐trophic interactions: bridging species, communities and ecosystems. Ecology letters, 22(12), 2151-2167. doi: 10.1111/ele.13392
[7] Polis, G.A. & Winemiller, K.O. (1996). Food webs. Integration of patterns and dynamics. Chapmann & Hall, New York. doi: 10.1007/978-1-4615-7007-3
[8] Torres‐Campos, I., Magalhães, S., Moya‐Laraño, J., & Montserrat, M. (2020). The return of the trophic chain: Fundamental vs. realized interactions in a simple arthropod food web. Functional Ecology, 34(2), 521-533. doi: 10.1111/1365-2435.13470
[9] Polis, G. A., Sears, A. L., Huxel, G. R., Strong, D. R., & Maron, J. (2000). When is a trophic cascade a trophic cascade?. Trends in Ecology & Evolution, 15(11), 473-475. doi: 10.1016/S0169-5347(00)01971-6
[10] Sih, A., Englund, G., & Wooster, D. (1998). Emergent impacts of multiple predators on prey. Trends in ecology & evolution, 13(9), 350-355. doi: 10.1016/S0169-5347(98)01437-2
[11] Diehl, E., Sereda, E., Wolters, V., & Birkhofer, K. (2013). Effects of predator specialization, host plant and climate on biological control of aphids by natural enemies: a meta‐analysis. Journal of Applied Ecology, 50(1), 262-270. doi: 10.1111/1365-2664.12032
[12] Snyder, W. E. (2019). Give predators a complement: conserving natural enemy biodiversity to improve biocontrol. Biological control, 135, 73-82. doi: 10.1016/j.biocontrol.2019.04.017
[13] Des Roches, S., Post, D. M., Turley, N. E., Bailey, J. K., Hendry, A. P., Kinnison, M. T., ... & Palkovacs, E. P. (2018). The ecological importance of intraspecific variation. Nature Ecology & Evolution, 2(1), 57-64. doi: 10.1038/s41559-017-0402-5
[14] Bustos‐Segura, C., Poelman, E. H., Reichelt, M., Gershenzon, J., & Gols, R. (2017). Intraspecific chemical diversity among neighbouring plants correlates positively with plant size and herbivore load but negatively with herbivore damage. Ecology Letters, 20(1), 87-97. doi: 10.1111/ele.12713
[15] Start, D., & Gilbert, B. (2017). Predator personality structures prey communities and trophic cascades. Ecology letters, 20(3), 366-374. doi: 10.1111/ele.12735
[16] Turcotte, M. M., Reznick, D. N., & Daniel Hare, J. (2013). Experimental test of an eco-evolutionary dynamic feedback loop between evolution and population density in the green peach aphid. The American Naturalist, 181(S1), S46-S57. doi: 10.1086/668078
[17] Bolnick, D. I., Amarasekare, P., Araújo, M. S., Bürger, R., Levine, J. M., Novak, M., ... & Vasseur, D. A. (2011). Why intraspecific trait variation matters in community ecology. Trends in ecology & evolution, 26(4), 183-192. doi: 10.1016/j.tree.2011.01.009
[18] Drès, M., & Mallet, J. (2002). Host races in plant–feeding insects and their importance in sympatric speciation. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 357(1420), 471-492. doi: 10.1098/rstb.2002.1059
[19] Magalhães, S., Forbes, M. R., Skoracka, A., Osakabe, M., Chevillon, C., & McCoy, K. D. (2007). Host race formation in the Acari. Experimental and Applied Acarology, 42(4), 225-238. doi: 10.1007/s10493-007-9091-0
[20] Sentis, A., Bertram, R., Dardenne, N., Simon, J.-C., Magro, A., Pujol, B., Danchin, E. and J.-L. Hemptinne (2020) Intraspecific difference among herbivore lineages and their host-plant specialization drive the strength of trophic cascades. bioRxiv, 722140, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/722140

Intraspecific difference among herbivore lineages and their host-plant specialization drive the strength of trophic cascadesArnaud Sentis, Raphaël Bertram, Nathalie Dardenne, Jean-Christophe Simon, Alexandra Magro, Benoit Pujol, Etienne Danchin and Jean-Louis Hemptinne<p>Trophic cascades, the indirect effect of predators on non-adjacent lower trophic levels, are important drivers of the structure and dynamics of ecological communities. However, the influence of intraspecific trait variation on the strength of t...Community ecology, Eco-evolutionary dynamics, Food webs, Population ecologySara Magalhães2019-08-02 09:11:03 View
10 Oct 2018
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Detecting within-host interactions using genotype combination prevalence data

Combining epidemiological models with statistical inference can detect parasite interactions

Recommended by based on reviews by Samuel Díaz Muñoz, Erick Gagne and 1 anonymous reviewer

There are several important topics in the study of infectious diseases that have not been well explored due to technical difficulties. One such topic is pursued by Alizon et al. in “Modelling coinfections to detect within-host interactions from genotype combination prevalences” [1]. Both theory and several important examples have demonstrated that interactions among co-infecting strains can have outsized impacts on disease outcomes, transmission dynamics, and epidemiology. Unfortunately, empirical data on pathogen interactions and their outcomes is often correlational making results difficult to decipher.
The analytical framework developed by Alizon et al. [1] infers the presence and strength of pathogen interactions through their impact on transmission dynamics using a novel application of Approximate Bayesian Computation (ABC)-regression to epidemiological data. Traditional analytic approaches identify pathogen interactions when the observed distribution of pathogens among hosts differ from ‘neutral’ expectations. However, deviations from this expectation are not only a result of inter-strain interactions but can be caused by many ecological interactions, such as heterogeneity in host contact networks. To overcome this difficulty, Alizon et al [1] develop an analytical framework that incorporates explicit epidemiological models to allow inference of interactions among strains of Human Papillomaviruses (HPV) even with other ecological interactions that impact the distribution of strains among hosts. Alizon et al also demonstrate that using more of the available data, including the specific combination of strains present in hosts and knowledge of the connectivity of the hosts (i.e., super-spreaders), leads to more accurate inferences of the strength and direction of within-host interactions among coinfecting strains. This method successfully identified data generated from models with high and moderate inter-strain interaction intensity when the host population was homogeneous and was only slightly less successful when the host population was heterogeneous (super-spreaders present). By comparison, some previously published analytical methods could identify only some inter-strain interactions in datasets generated from models with homogeneous host populations, but host heterogeneity obscured these interactions.
This manuscript makes seamless connections between basic viral biology and its epidemiological consequences by tying them together with realistic models, illustrating the fundamental utility of biological modeling. This analytical framework provides crucial tools for experimentalists, facilitating collaborations with theoreticians to better understand the epidemiological consequences of co-infections. In addition, the method is simple enough to be applied by a broad base of experimentalists to the many pathogens where co-infections are common. Thus, this paper has the potential to impact several research fields and public health practice. Those attempting to apply this method should note the potential limitations noted by the authors. For example, it is not designed to detect the mechanisms of inter-strain interactions (there is no within host component of the models) but to identify the existence of interactions through patterns indicative of these interactions while ruling out other sources that could cause the pattern. This approach is likely to be most accurate when strain identification within hosts is precise and unbiased - which is unlikely in many systems where samples are taken only from symptomatic cases and strain detection is not sufficiently sensitive – and when host contact networks can be reasonably estimated. Importantly, a priori knowledge of the set of possible epidemiological models is needed for accurate parameter estimates, which may be true for several prominent pathogens, but not be so for many other pathogens and symbionts. We look forward to future extensions of this framework where this restriction is relaxed. Alizon et al. [1] have provided a framework that will facilitate theoretical and empirical work on the impact of coinfections on infectious disease and should shape future public health data collection standards.

References

[1] Alizon, S., Murall, C.L., Saulnier, E., & Sofonea, M.T. (2018). Detecting within-host interactions using genotype combination prevalence data. bioRxiv, 256586, ver. 3 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/256586

Detecting within-host interactions using genotype combination prevalence dataSamuel Alizon, Carmen Lía Murall, Emma Saulnier, Mircea T Sofonea<p>Parasite genetic diversity can provide information on disease transmission dynamics but most methods ignore the exact combinations of genotypes in infections. We introduce and validate a new method that combines explicit epidemiological modelli...Eco-immunology & Immunity, Epidemiology, Host-parasite interactions, Statistical ecologyDustin Brisson Samuel Díaz Muñoz, Erick Gagne2018-02-01 09:23:26 View
27 Feb 2025
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Mineral fertilization reduces the drought resistance of soil multifunctionality in a mountain grassland system through plant-soil interactions

Complex interactions between fertilization, drought and plants impact soil functioning

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

The ingredients of this study are classic in soil ecology and in the study of belowground-aboveground interactions: the presence of plants, draught and mineral fertilization (for the experimental treatments) and microbial carbon, microbial nitrogen, microbial phosphorus, substrate-induced respiration, cumulative extracellular enzyme activity, nitrogen mineralization potential, nitrification potential, denitrification potential (as a result of the treatments). It is interesting and useful to have tested all the combinations of the three treatments and the height variables (also in the form of a soil multifunctionality index) in the same study and to have been able to express hypotheses on the underlying mechanisms of interaction.

 

A key result is that mineral fertilization can reduce the soil ability to withstand draughts in terms of soil multifunctionality. This effect would be due to the increase in plant growth associated with fertilization, which reduces the availability of soil resources. This subsequently affects microbial diversity and soil multifunctionality. This confirms that the interactions between plants and soil microorganisms are complex and relevant for understanding and predicting the impact of climate and fertilization on soil functioning and the sustainability of plant-soil systems.

 

Although the study is rather fundamental, it has been designed to be relevant to grassland management and points to very general mechanisms that are likely to be relevant to arable land management. It would therefore be useful to repeat this work for interactions between a crop and its soil. Finally, it would be crucial to test the impact of heavy fertilization in intensive cropping systems on the resistance and resilience of soil functions to climate variability and climate changes.

 

A slightly disturbing fact is that the underlying interactions are probably so complicated that it seems so far impossible to me to make predictions about the ranking of the height combinations of treatments on each soil variable. But this complexity is clearly inherent to ecology and, in particular, plant-soil interactions.

 

References

Gabin Piton, Arnaud Foulquier, Lionel Bernard, Aurelie Bonin, Thomas Pommier, Sandra Lavorel, Roberto Geremia, Jean Christophe Clement (2025) Mineral fertilization reduces the drought resistance of soil multifunctionality in a mountain grassland system through plant-soil interactions. bioRxiv, ver.2 peer-reviewed and recommended by PCI Ecology https://doi.org/10.1101/2024.09.19.613911

Mineral fertilization reduces the drought resistance of soil multifunctionality in a mountain grassland system through plant-soil interactionsGabin Piton, Arnaud Foulquier, Lionel Bernard, Aurelie Bonin, Thomas Pommier, Sandra Lavorel, Roberto Geremia, Jean Christophe Clement<p>Increasing droughts threaten soil microbial communities and the multiple functions they control in agricultural soils. These soils are often fertilized with mineral nutrients, but it remains unclear how this fertilization may alter the capacity...Agroecology, Climate change, Ecological stoichiometry, Ecosystem functioning, Experimental ecology, Microbial ecology & microbiology, Soil ecologySébastien Barot2024-09-19 18:55:06 View