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15 Jun 2020
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Investigating the rare behavior of male parental care in great-tailed grackles

Studying a rare behavior in a polygamous bird: male parental care in great-tailed grackles

Recommended by based on reviews by Matthieu Paquet and André C Ferreira

The Great-tailed grackle (Quiscalus mexicanus) is a polygamous bird species that is originating from Central America and rapidly expanding its geographic range toward the North, and in which females were long thought to be the sole nest builders and caretakers of the young. In their pre-registration [1], Folsom and collaborators report repeated occurrences of male parental care and develop hypotheses aiming at better understanding the occurrence and the fitness consequences of this very rarely observed male behavior. They propose to assess if male parental care correlates with the circulating levels of several relevant hormones, increases offspring survival, is a local adaptation, and is a mating strategy, in surveying three populations located in Arizona (middle of the geographic range expansion), California (northern edge of the geographic range), and in Central America (core of the range). This study is part of a 5-year bigger project.
Both reviewers and I strongly value Folsom and collaborators’ commitment to program a study, in natural field conditions, of a rare, yet likely evolutionary-important behavior, namely parental care by males of the great-tailed grackle. Yet, we all also recognized that it is a risky endeavor, and as a consequence, we wondered about the authors’ ability to reach a sufficient sample size to statistically test (all) hypotheses and predictions with enough confidence (e.g. risk of type I errors, also known as false positives).
Folsom and collaborators acknowledged these limitations in their pre-registration. (i) They made the exploratory nature of their research work clear to readers. (ii) They adapted their analysis plan in running prior power analyses and in focusing on effect sizes (estimates and confidence intervals). (iii) Last and not least, Folsom and collaborators clearly exposed a priori hypotheses, their associated predictions and alternatives, and ranked the latter based on their plausibility according to knowledge in the current and other study systems. Developing theory about male parental care behavior more generally with regard to a polygamous species that is rapidly expanding its geographic range and that is considered not to provide male parental care is without any doubt an added value to this study.
In summary, while this study will likely be insufficient to fully understand male parental care behavior of great-tailed grackles, it is much needed because it will definitely allow rejecting some predictions (e.g., if this behavior is present in all the studied populations, it would be common across range against expectation; finding only one male providing care to an unrelated offspring would lead to reject the prediction that males only care for their own offspring) and thus it will help laying the foundation of future research directions.
I strongly support the pre-registration system and thank all the contributors for producing a fruitful discussion throughout the review process, which in fine improved the clarity and logic of this pre-registration. Given the positive and encouraging reviews, the detailed and thorough answers to all comments by Folsom and collaborators, and their satisfactory and interesting revisions, I am happy to recommend this pre-registration and I look forward to seeing its outcomes.

References

[1] Folsom MA, MacPherson M, Lukas D, McCune KB, Bergeron L, Bond A, Blackwell A, Rowney C, Logan CJ. 2020. Investigating the rare behavior of male parental care in great-tailed grackles. corinalogan.com/Preregistrations/gmalecare.html In principle acceptance by PCI Ecology of the version on 15 June 2020 corinalogan/grackles/blob/master/Files/Preregistrations/gmalecare.Rmd.

Investigating the rare behavior of male parental care in great-tailed gracklesFolsom MA, MacPherson M, Lukas D, McCune KB, Bergeron L, Bond A, Blackwell A, Rowney C, Logan CJThis is a PREREGISTRATION submitted for pre-study peer review. Our planned data collection START DATE is May 2020, therefore it would be ideal if the peer review process could be completed before then. Abstract: Great-tailed grackles (Quiscalus...Behaviour & Ethology, Biological invasions, Preregistrations, ZoologyMarie-Jeanne Holveck2019-12-05 17:38:47 View
06 Sep 2019
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Assessing metacommunity processes through signatures in spatiotemporal turnover of community composition

On the importance of temporal meta-community dynamics for our understanding of assembly processes

Recommended by ORCID_LOGO based on reviews by Joaquín Hortal and 2 anonymous reviewers

The processes that trigger community assembly are still in the centre of ecological interest. While prior work mostly focused on spatial patterns of co-occurrence within a meta-community framework [reviewed in 1, 2] recent studies also include temporal patterns of community composition [e.g. 3, 4, 5, 6]. In this preprint [7], Franck Jabot and co-workers extend they prior approaches to quasi neutral community assembly [8, 9, 10] and develop an analytical framework of spatial and temporal diversity turnover. A simple and heuristic path model for beta diversity and an extended ecological drift model serve as starting points. The model can be seen as a counterpart to Ulrich et al. [5]. These authors implemented competitive hierarchies into their neutral meta-community model while the present paper focuses on environmental filtering. Most important, the model and parameterization of four empirical data sets on aquatic plant and animal meta-communities used by Jabot et al. returned a consistent high influence of environmental stochasticity on species turnover. Of course, this major result does not come to a surprise. As typical for this kind of models it depends also to a good deal on the initial model settings. It nevertheless makes a strong conceptual point for the importance of environmental variability over dispersal and richness effects. One interesting side effect regards the impact of richness differences (ΔS). Jabot et al. interpret this as a ‘nuisance variable’ as they do not have a stringent explanation. Of course, it might be a pure statistical bias introduced by the Soerensen metric of turnover that is normalized by richness. However, I suspect that there is more behind the ΔS effect. Richness differences are generally associated with respective differences in total abundances and introduce source – sink dynamics that inevitably shape subsequent colonization – extinction processes. It would be interesting to see whether ΔS alone is able to trigger observed patterns of community assembly and community composition. Such an analysis would require partitioning of species turnover into richness and nestedness effects [11]. I encourage Jabot et al. to undertake such an effort.
The present paper is also another call to include temporal population variability into metapopulation models for a better understanding of the dynamics and triggering of community assembly. In a next step, competitive interactions should be included into the model to infer the relative importance of both factors.

References

[1] Götzenberger, L. et al. (2012). Ecological assembly rules in plant communities—approaches, patterns and prospects. Biological reviews, 87(1), 111-127. doi: 10.1111/j.1469-185X.2011.00187.x
[2] Ulrich, W., & Gotelli, N. J. (2013). Pattern detection in null model analysis. Oikos, 122(1), 2-18. doi: 10.1111/j.1600-0706.2012.20325.x
[3] Grilli, J., Barabás, G., Michalska-Smith, M. J., & Allesina, S. (2017). Higher-order interactions stabilize dynamics in competitive network models. Nature, 548(7666), 210. doi: 10.1038/nature23273
[4] Nuvoloni, F. M., Feres, R. J. F., & Gilbert, B. (2016). Species turnover through time: colonization and extinction dynamics across metacommunities. The American Naturalist, 187(6), 786-796. doi: 10.1086/686150
[5] Ulrich, W., Jabot, F., & Gotelli, N. J. (2017). Competitive interactions change the pattern of species co‐occurrences under neutral dispersal. Oikos, 126(1), 91-100. doi: 10.1111/oik.03392
[6] Dobramysl, U., Mobilia, M., Pleimling, M., & Täuber, U. C. (2018). Stochastic population dynamics in spatially extended predator–prey systems. Journal of Physics A: Mathematical and Theoretical, 51(6), 063001. doi: 10.1088/1751-8121/aa95c7
[7] Jabot, F., Laroche, F., Massol, F., Arthaud, F., Crabot, J., Dubart, M., Blanchet, S., Munoz, F., David, P., and Datry, T. (2019). Assessing metacommunity processes through signatures in spatiotemporal turnover of community composition. bioRxiv, 480335, ver. 3 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/480335
[8] Jabot, F., & Chave, J. (2011). Analyzing tropical forest tree species abundance distributions using a nonneutral model and through approximate Bayesian inference. The American Naturalist, 178(2), E37-E47. doi: 10.1086/660829
[9] Jabot, F., & Lohier, T. (2016). Non‐random correlation of species dynamics in tropical tree communities. Oikos, 125(12), 1733-1742. doi: 10.1111/oik.03103
[10] Datry, T., Bonada, N., & Heino, J. (2016). Towards understanding the organisation of metacommunities in highly dynamic ecological systems. Oikos, 125(2), 149-159. doi: 10.1111/oik.02922
[11] Baselga, A. (2010). Partitioning the turnover and nestedness components of beta diversity. Global ecology and biogeography, 19(1), 134-143. doi: 10.1111/j.1466-8238.2009.00490.x

Assessing metacommunity processes through signatures in spatiotemporal turnover of community compositionFranck Jabot, Fabien Laroche, Francois Massol, Florent Arthaud, Julie Crabot, Maxime Dubart, Simon Blanchet, Francois Munoz, Patrice David, Thibault Datry<p>Although metacommunity ecology has been a major field of research in the last decades, with both conceptual and empirical outputs, the analysis of the temporal dynamics of metacommunities has only emerged recently and still consists mostly of r...Biodiversity, Coexistence, Community ecology, Spatial ecology, Metacommunities & MetapopulationsWerner Ulrich2018-11-29 14:58:54 View
24 May 2022
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Controversy over the decline of arthropods: a matter of temporal baseline?

Don't jump to conclusions on arthropod abundance dynamics without appropriate data

Recommended by ORCID_LOGO based on reviews by Gabor L Lovei and 1 anonymous reviewer

Humans are dramatically modifying many aspects of our planet via increasing concentrations of carbon dioxide in the atmosphere, patterns of land-use change, and unsustainable exploitation of the planet’s resources. These changes impact the abundance of species of wild organisms, with winners and losers. Identifying how different species and groups of species are influenced by anthropogenic activity in different biomes, continents, and habitats, has become a pressing scientific question with many publications reporting analyses of disparate data on species population sizes. Many conclusions are based on the linear analysis of rather short time series of organismal abundances.
 
There has been particular interest in how arthropods are impacted by environmental change, with several recent papers reporting contradictory results. To investigate why these contradictions might arise, Duchenne et al. (2022) conducted an analysis of four published data sets along with a series of experimental analyses of simulated time series to examine the power of widely used statistical analyses to gain inference on temporal trends. Their important paper reveals that accurate inference on dynamics, particularly of species that exhibit large temporal fluctuations in abundance, requires time series that are substantially longer than are typically collected, as well as careful thought as to whether linear models are appropriate. Linear analyses of short time series are susceptible to providing unreliable inference as trends can be strongly influenced by points at either end of the time series. 
 
Duchenne et al.’s paper provides important insight on the conditions when strong inference on temporal trends of arthropod (and other species) abundances can be made, and when they should be treated with caution. They do not doubt that many insect and arachnid species are changing their abundances, and that patterns in these changes may vary spatially. What their results do say is that we should treat grand claims of population recovery or rapid declines apparently to extinction with caution when they are based on short time series, particularly of species that show significant boom and bust dynamics. In many ways, these results are not unexpected, but it is nice to see such careful and thoughtful analyses and interpretation. More data are required for most arthropod species before clear assessments of abundance trends can be made. Given our reliance on many arthropods for food, pollination, and numerous ecosystem services, and the ability of other species to spread devastating human diseases such as dengue and malaria, it is advisable that we slow our modification of their habitats while additional data are collected to allow us to better characterise the trajectory of arthropod populations to understand what the consequences of our actions on the natural world are likely to be.  
 
References

Duchenne F, Porcher E, Mihoub J-B, Loïs G, Fontaine C (2022) Controversy over the decline of arthropods: a matter of temporal baseline? bioRxiv, 2022.02.09.479422, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.02.09.479422

Controversy over the decline of arthropods: a matter of temporal baseline?François Duchenne, Emmanuelle Porcher, Jean-Baptiste Mihoub, Grégoire Loïs, Colin Fontaine<p style="text-align: justify;">Recently, a number of studies have reported somewhat contradictory patterns of temporal trends in arthropod abundance, from decline to increase. Arthropods often exhibit non-monotonous variation in abundance over ti...Conservation biologyTim Coulson2022-02-11 15:44:44 View
03 Apr 2020
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Body temperatures, life history, and skeletal morphology in the nine-banded armadillo (Dasypus novemcinctus)

Is vertebral count in mammals influenced by developmental temperature? A study with Dasypus novemcinctus

Recommended by based on reviews by Darin Croft and ?

Mammals show a very low level of variation in vertebral count, both among and within species, in comparison to other vertebrates [1]. Jordan’s rule for fishes states that the vertebral number among species increases with latitude, due to ambient temperatures during development [2]. Temperature has also been shown to influence vertebral count within species in fish [3], amphibians [4], and birds [5]. However, in mammals the count appears to be constrained, on the one hand, by a possible relationship between the development of the skeleton and the proliferations of cell lines with associated costs (neural malformations, cancer etc., [6]), and on the other by the cervical origin of the diaphragm [7].
Knight et al. [8] investigate the effect of intrauterine temperature variation on skeletal morphology during development, and focus on a particular mammal, Dasypus novemcinctus, or nine-banded armadillo. Armadillos (Xenarthra) and are characterized by relatively low body temperatures and low basal rates of metabolism. Dasypus novemcinctus is the only xenarthran mammal to have naturally expanded its range into the middle latitudes of the U.S., and one of the few mammals that invaded North America from South America. It is one of few placentals that withstand considerable decrease of body temperature without torpor. It presents a resting body temperature that is low and variable for a placental mammal of its size [9] and is the only vertebrate that gives birth to monozygotic quadruplets. Among 42 monotreme, marsupial and placental genera, Dasypus novemcinctus shows the highest variation of thoracolumbar vertebral count [10].
The particularities of Dasypus novemcinctus regarding vertebral count variation and ability to withstand variable temperature qualify it as a target organism for study of the relationship between skeleton morphology and temperature in mammals.
Knight et al. [8] explored variability in vertebral count within Dasypus novemcinctus to understand whether temperature during development determines skeleton morphology. To this end they experimented with 22 armadillos (19 with data) and litters from 12 pregnant females, in two environments, for three years — an impressive effort and experimental setup. Moreover, they used a wide variety of advanced experimental and analytical techniques. For example, they implanted intra-abdominal, long-term temperature recorders, which recorded data every 6 to 120 minutes for up to several months. They analysed body temperature periodicity by approximation of the recordings with Fourier series, and they CT-scanned fetuses.
All 19 individuals (from which data could be gathered) exhibited substantial daily variation in body temperature. Several intriguing results emerged such as the counter-intuitive finding that the mammals’ body temperature fluctuates more indoors than outdoors. Furthermore, three females (out of 12) were found to have offspring with atypical skeletons, and two of these mothers presented an extremely low internal temperature early in pregnancy. Additionally, genetically identical quadruplets differed skeletally among themselves within two litters.
Results are not yet definitive about the relationship of temperature during development and vertebral count in Dasypus novemcinctus. However, Knight et al. [8] demonstrated that nine-banded armadillos survive with high daily internal temperature fluctuations and successfully bring to term offspring which vary in skeletal morphology among and within genetically identical litters despite major temperature extremes.

References

[1] Hautier L, Weisbecker V, Sánchez-Villagra MR, Goswami A, Asher RJ (2010) Skeletal development in sloths and the evolution of mammalian vertebral patterning. Proceedings of the National Academy of Sciences, 107, 18903–18908. doi: 10.1073/pnas.1010335107
[2] Jordan, D.S. (1892) Relations of temperature to vertebrae among fishes. Proceedings of the United States National Museum, 1891, 107-120. doi: 10.5479/si.00963801.14-845.107
[3] Tibblin P, Berggren H, Nordahl O, Larsson P, Forsman A (2016) Causes and consequences of intra-specific variation in vertebral number. Scientific Reports, 6, 1–12. doi: 10.1038/srep26372
[4] Peabody RB, Brodie ED (1975) Effect of temperature, salinity and photoperiod on the number of trunk vertebrae in Ambystoma maculatum. Copeia, 1975, 741–746. doi: 10.2307/1443326
[5] Lindsey CC, Moodie GEE (1967) The effect of incubation temperature on vertebral count in the chicken. Canadian Journal of Zoology, 45, 891–892. doi: 10.1139/z67-099
[6] Galis F, Dooren TJMV, Feuth JD, Metz JAJ, Witkam A, Ruinard S, Steigenga MJ, Wunaendts LCD (2006) Extreme selection in humans against homeotic transformations of cervical vertebrae. Evolution, 60, 2643–2654. doi: 10.1111/j.0014-3820.2006.tb01896.x
[7] Buchholtz EA, Stepien CC (2009) Anatomical transformation in mammals: developmental origin of aberrant cervical anatomy in tree sloths. Evolution and Development, 11, 69–79. doi: 10.1111/j.1525-142X.2008.00303.x
[8] Knight F, Connor C, Venkataramanan R, Asher RJ. (2020). Body temperatures, life history, and skeletal morphology in the nine-banded armadillo (Dasypus novemcinctus). PCI-Ecology. doi: 10.17863/CAM.50971
[9] McNab BK (1980) Energetics and the limits to a temperate distribution in armadillos. Journal of Mammalogy, 61, 606–627. doi: 10.2307/1380307
[10] Asher RJ, Lin KH, Kardjilov N, Hautier L (2011) Variability and constraint in the mammalian vertebral column. Journal of Evolutionary Biology, 24, 1080–1090. doi: 10.1111/j.1420-9101.2011.02240.x

Body temperatures, life history, and skeletal morphology in the nine-banded armadillo (Dasypus novemcinctus)Frank Knight, Cristin Connor, Ramji Venkataramanan, Robert J. Asher<p>The nine banded armadillo (*Dasypus novemcinctus*) is the only xenarthran mammal to have naturally expanded its range into the middle latitudes of the USA. It is not known to hibernate, but has been associated with unusually labile core body te...Behaviour & Ethology, Evolutionary ecology, Life history, Physiology, ZoologyMar Sobral2019-11-22 22:57:31 View
09 Nov 2023
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Mark loss can strongly bias estimates of demographic rates in multi-state models: a case study with simulated and empirical datasets

Marks lost in action, biased estimations

Recommended by ORCID_LOGO based on reviews by Olivier Gimenez, Devin Johnson and 1 anonymous reviewer

Capture-Mark-Recapture (CMR) data are commonly used to estimate ecological variables such as abundance, survival probability, or transition rates from one state to another (e.g. from juvenile to adult, or migration from one site to another). Many studies have shown how estimations can be affected by neglecting one aspect of the population under study (e.g. the heterogeneity in survival between individuals) or one limit of the methodology itself (e.g. the fact that observers might not detect an individual although it is still alive). Strikingly, very few studies have yet assessed the robustness of one fundamental assumption of all CMR-based inferences: marks are supposed definitive and immutable. If they are not, how are estimations affected? Addressing this issue is the main goal of the paper by Touzalin et al. (2023), and they did a very nice work. But, because the answer is not that simple, it also calls for further investigations.

When and why would mark loss bias estimation? In at least two situations. First, when estimating survival rates: if an individual loses its mark, it will be considered as dead, hence death rates will be overestimated. Second, more subtly, when estimating transition rates: if one individual loses its mark at the specific moment where its state changes, then a transition will be missed in data. The history of the marked individual would then be split into two independent CMR sequences as if there were two different individuals, including one which died.

Touzalin et al. (2023) thoroughly studied these two situations by estimating ecological parameters on 1) well-thought simulated datasets, that cover a large range of possible situations inspired from a nice compilation of hundreds of estimations from fish and bats studies, and 2) on their own bats dataset, for which they had various sources of information about mark losses, i.e. different mark types on the same individuals, including mark based on genotypes, and marks found on the soil in the place where bats lived. Their main findings from the simulated datasets are that there is a general trend for underestimation of survival and transition rates if mark loss is not accounting for in the model, as it would be intuitively expected. However, they also showed from the bats dataset that biases do not show any obvious general trend, suggesting complex interactions between different ecological processes and/or with the estimation procedure itself.

The results by Touzalin et al. (2023) strongly suggest that mark loss should systematically be included in models estimating parameters from CMR data. In addition to adapt the inferential models, the authors also recommend considering either a double marking, or even a single but ‘permanent’ mark such as one based on the genotypes. However, the potential gain of a double marking or of the use of genotypes is still to be evaluated both in theory and practice, and it seems to be not that obvious at first sight. First because double marking can be costly for experimenters but also for the marked animals, especially as several studies showed that marks can significantly affect survival or recapture rates. Second because multiple sources of errors can affect genotyping, which would result in wrong individual assignations especially in populations with low genetic diversity or high inbreeding, or no individual assignation at all, which would increase the occurrence of missing data in CMR datasets. Touzalin et al. (2023) supposed in their paper that there were no genotyping errors, but one can doubt it to be true in most situations. They have now important and interesting other issues to address.

References

Frédéric Touzalin, Eric J. Petit, Emmanuelle Cam, Claire Stagier, Emma C. Teeling, Sébastien J. Puechmaille (2023) Mark loss can strongly bias demographic rates in multi-state models: a case study with simulated and empirical datasets. BioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.03.25.485763

Mark loss can strongly bias estimates of demographic rates in multi-state models: a case study with simulated and empirical datasetsFrédéric Touzalin, Eric J. Petit, Emmanuelle Cam, Claire Stagier, Emma C. Teeling, Sébastien J. Puechmaille<p style="text-align: justify;">1. The development of methods for individual identification in wild species and the refinement of Capture-Mark-Recapture (CMR) models over the past few decades have greatly improved the assessment of population demo...Conservation biology, DemographySylvain Billiard2022-04-12 18:49:34 View
24 Nov 2023
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Consistent individual positions within roosts in Spix's disc-winged bats

Consistent individual differences in habitat use in a tropical leaf roosting bat

Recommended by based on reviews by Annemarie van der Marel and 2 anonymous reviewers

Consistent individual differences in habitat use are found across species and can play a role in who an individual mates with, their risk of predation, and their ability to compete with others (Stuber et al. 2022). However, the data informing such hypotheses come primarily from temperate regions (Stroud & Thompson 2019, Titley et al. 2017). This calls into question the generalizability of the conclusions from this research until further investigations can be conducted in tropical regions.

Giacomini and colleagues (2023) tackled this task in an investigation of consistent individual differences in habitat use in the Central American tropics. They explored whether Spix’s disc-winged bats form positional hierarchies in roosts, which is an excellent start to learning more about the social behavior of this species - a species that is difficult to directly observe. They found that individual bats use their roosting habitat in predictable ways by positioning themselves consistently either in the bottom, middle, or top of the roost leaf. Individuals chose the same positions across time and across different roost sites. They also found that age and sex play a role in which sections individuals are positioned in.

Their research shows that consistent individual differences in habitat use are present in a tropical system, and sets the stage for further investigations into social behavior in this species, particularly whether there is a dominance hierarchy among individuals and whether some positions in the roost are more protective and sought after than others.

References

Giacomini G, Chaves-Ramirez S, Hernandez-Pinson A, Barrantes JP, Chaverri G. (2023). Consistent individual positions within roosts in Spix's disc-winged bats. bioRxiv, https://doi.org/10.1101/2022.11.04.515223 

Stroud, J. T., & Thompson, M. E. (2019). Looking to the past to understand the future of tropical conservation: The importance of collecting basic data. Biotropica, 51(3), 293-299. https://doi.org/10.1111/btp.12665

Stuber, E. F., Carlson, B. S., & Jesmer, B. R. (2022). Spatial personalities: a meta-analysis of consistent individual differences in spatial behavior. Behavioral Ecology, 33(3), 477-486. https://doi.org/10.1093/beheco/arab147 

Titley, M. A., Snaddon, J. L., & Turner, E. C. (2017). Scientific research on animal biodiversity is systematically biased towards vertebrates and temperate regions. PloS one, 12(12), e0189577. https://doi.org/10.1371/journal.pone.0189577

Consistent individual positions within roosts in Spix's disc-winged batsGiada Giacomini, Silvia Chaves-Ramirez, Andres Hernandez-Pinson, Jose Pablo Barrantes, Gloriana Chaverri<p style="text-align: justify;">Individuals within both moving and stationary groups arrange themselves in a predictable manner; for example, some individuals are consistently found at the front of the group or in the periphery and others in the c...Behaviour & Ethology, Social structure, ZoologyCorina Logan2022-11-05 17:39:35 View
29 Dec 2018
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The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web

From deserts to avocado orchards - understanding realized trophic interactions in communities

Recommended by based on reviews by Owen Petchey and 2 anonymous reviewers

The late eminent ecologist Gary Polis once stated that “most catalogued food-webs are oversimplified caricatures of actual communities” and are “grossly incomplete representations of communities in terms of both diversity and trophic connections.” Not content with that damning indictment, he went further by railing that “theorists are trying to explain phenomena that do not exist” [1]. The latter critique might have been push back for Robert May´s ground-breaking but ultimately flawed research on the relationship between food-web complexity and stability [2]. Polis was a brilliant ecologist, and his thinking was clearly influenced by his experiences researching desert food webs. Those food webs possess an uncommon combination of properties, such as frequent omnivory, cannibalism, and looping; high linkage density (L/S); and a nearly complete absence of apex consumers, since few species completely lack predators or parasites [3]. During my PhD studies, I was lucky enough to visit Joshua Tree National Park on the way to a conference in New England, and I could immediately see the problems posed by desert ecosystems. At the time, I was ruminating on the “harsh-benign” hypothesis [4], which predicts that the relative importance of abiotic and biotic forces should vary with changes in local environmental conditions (from harsh to benign). Specifically, in more “harsh” environments, abiotic factors should determine community composition whilst weakening the influence of biotic interactions. However, in the harsh desert environment I saw first-hand evidence that species interactions were not diminished; if anything, they were strengthened. Teddy-bear chollas possessed murderously sharp defenses to protect precious water, creosote bushes engaged in belowground “chemical warfare” (allelopathy) to deter potential competitors, and rampant cannibalism amongst scorpions drove temporal and spatial ontogenetic niche partitioning. Life in the desert was hard, but you couldn´t expect your competition to go easy on you.
If that experience colored my thinking about nature’s reaction to a capricious environment, then the seminal work by Robert Paine on the marine rocky shore helped further cement the importance of biotic interactions. The insights provided by Paine [5] brings us closer to the research reported in the preprint “The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web” [6], given that the authors in that study hold the environment constant and test the interactions between different permutations of a simple community. Paine [5] was able to elegantly demonstrate using the chief protagonist Pisaster ochraceus (a predatory echinoderm also known as the purple sea star) that a keystone consumer could exert strong top-down control that radically reshaped the interactions amongst other community members. What was special about this study was that the presence of Pisaster promoted species diversity by altering competition for space by sedentary species, providing a rare example of an ecological network experiment combining trophic and non-trophic interactions. Whilst there are increasing efforts to describe these interactions (e.g., competition and facilitation) in multiplex networks [7], the authors of “The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web” [6] have avoided strictly competitive interactions for the sake of simplicity. They do focus on two trophic forms of competition, namely intraguild predation and apparent competition. These two interaction motifs, along with prey switching are relevant to my own research on the influence of cross-ecosystem prey subsidies to receiving food webs [8]. In particular, the apparent competition motif may be particularly important in the context of emergent adult aquatic insects as prey subsidies to terrestrial consumers. This was demonstrated by Henschel et al. [9] where the abundances of emergent adult aquatic midges in riparian fields adjacent to a large river helped stimulate higher abundances of spiders and lower abundances of herbivorous leafhoppers, leading to a trophic cascade. The aquatic insects had a bottom-up effect on spiders and this subsidy facilitated a top-down effect that cascaded from spiders to leafhoppers to plants. The apparent competition motif becomes relevant because the aquatic midges exerted a negative indirect effect on leafhoppers mediated through their common arachnid predators.
In the preprint “The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web” [6], the authors have described different permutations of a simple mite community present in avocado orchards (Persea americana). This community comprises of two predators (Euseius stipulatus and Neoseiulus californicus), one herbivore as shared prey (Oligonychus perseae), and pollen of Carpobrotus edulis as alternative food resource, with the potential for the intraguild predation and apparent competition interaction motifs to be expressed. The authors determined that these motifs should be realized based off pairwise feeding trials. It is common for food-web researchers to depict potential food webs, which contain all species sampled and all potential trophic links based on laboratory feeding trials (as demonstrated here) or from observational data and literature reviews [10]. In reality, not all these potential feeding links are realized because species may partition space and time, thus driving alternative food-web architectures. In “The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web” [6], the authors are able to show that placing species in combinations that should yield more complex interaction motifs based off pairwise feeding trials fails to deliver – the predators revert to their preferred prey resulting in modular and simple trophic chains to be expressed. Whilst these realized interaction motifs may be stable, there might also be a tradeoff with function by yielding less top-down control than desirable when considering the potential for ecosystem services such as pest management. These are valuable insights, although it should be noted that here the fundamental niche is described in a strictly Eltonian sense as a trophic role [11]. Adding additional niche dimensions (sensu [12]), such as a thermal gradient could alter the observed interactions, although it might be possible to explain these contingencies through metabolic and optimal foraging theory combined with species traits. Nonetheless, the results of these experiments further demonstrate the need for ecologists to cross-validate theory with empirical approaches to develop more realistic and predictive food-web models, lest they invoke the wrath of Gary Polis´ ghost by “trying to explain phenomena that do not exist”.

References

[1] Polis, G. A. (1991). Complex trophic interactions in deserts: an empirical critique of food-web theory. The American Naturalist, 138(1), 123-155. doi: 10.1086/285208
[2] May, R. M. (1973). Stability and complexity in model ecosystems. Princeton University Press, Princeton, NJ, USA
[3] Dunne, J. A. (2006). The network structure of food webs. In Pascual, M., & Dunne, J. A. (eds) Ecological Networks: Linking Structure to Dynamics in Food Webs. Oxford University Press, New York, USA, 27-86
[4] Menge, B. A., & Sutherland, J. P. (1976). Species diversity gradients: synthesis of the roles of predation, competition, and temporal heterogeneity. The American Naturalist, 110(973), 351-369. doi: 10.1086/283073
[5] Paine, R. T. (1966). Food web complexity and species diversity. The American Naturalist, 100(910), 65-75. doi: 10.1086/282400
[6] Torres-Campos, I., Magalhães, S., Moya-Laraño, J., & Montserrat, M. (2018). The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food web. bioRxiv, 324178, ver. 5 peer-reviewed and recommended by PCI Ecol. doi: 10.1101/324178
[7] Kéfi, S., Berlow, E. L., Wieters, E. A., Joppa, L. N., Wood, S. A., Brose, U., & Navarrete, S. A. (2015). Network structure beyond food webs: mapping non‐trophic and trophic interactions on Chilean rocky shores. Ecology, 96(1), 291-303. doi: 10.1890/13-1424.1
[8] Burdon, F. J., & Harding, J. S. (2008). The linkage between riparian predators and aquatic insects across a stream‐resource spectrum. Freshwater Biology, 53(2), 330-346. doi: 10.1111/j.1365-2427.2007.01897.x
[9] Henschel, J. R., Mahsberg, D., & Stumpf, H. (2001). Allochthonous aquatic insects increase predation and decrease herbivory in river shore food webs. Oikos, 93(3), 429-438. doi: 10.1034/j.1600-0706.2001.930308.x
[10] Brose, U., Pavao-Zuckerman, M., Eklöf, A., Bengtsson, J., Berg, M. P., Cousins, S. H., Mulder, C., Verhoef, H. A., & Wolters, V. (2005). Spatial aspects of food webs. In de Ruiter, P., Wolters, V., Moore, J. C., & Melville-Smith, K. (eds) Dynamic Food Webs. vol 3. Academic Press, Burlington, 463-469
[11] Elton, C. (1927). Animal Ecology. Sidgwick and Jackson, London, UK
[12] Hutchinson, G. E. (1957). Concluding Remarks. Cold Spring Harbor Symposia on Quantitative Biology, 22, 415-427. doi: 10.1101/sqb.1957.022.01.039

The return of the trophic chain: fundamental vs realized interactions in a simple arthropod food webInmaculada Torres-Campos, Sara Magalhães, Jordi Moya-Laraño, Marta Montserrat<p>The mathematical theory describing small assemblages of interacting species (community modules or motifs) has proved to be essential in understanding the emergent properties of ecological communities. These models use differential equations to ...Community ecology, Experimental ecologyFrancis John Burdon2018-05-16 19:34:10 View
20 Feb 2024
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Functional trade-offs: exploring the temporal response of field margin plant communities to climate change and agricultural practices

Unravelling plant diversity in agricultural field margins in France: plant species better adapted to climate change need other agricultures to persist

Recommended by ORCID_LOGO based on reviews by Ignasi Bartomeus, Clelia Sirami and Diego Gurvich

Agricultural field margin plants, often referred to as “spontaneous” species, are key for the stabilization of several social-ecological processes related to crop production such as pollination or pest control (Tamburini et al. 2020). Because of its beneficial function, increasing the diversity of field margin flora becomes as important as crop diversity in process-based agricultures such as agroecology. Contrary, supply-dependent intensive agricultures produce monocultures and homogenized environments that might benefit their productivity, which generally includes the control or elimination of the field margin flora (Emmerson et al. 2016, Aligner 2018). Considering that different agricultural practices are produced by (and produce) different territories (Moore 2020) and that they are also been shaped by current climate change, we urgently need to understand how agricultural intensification constrains the potential of territories to develop agriculture more resilient to such change (Altieri et al., 2015). Thus, studies unraveling how agricultural practices' effects on agricultural field margin flora interact with those of climate change is of main importance, as plant strategies better adapted to such social-ecological processes may differ.        
 
In this vein, the study of Poinas et al. (2024) can be considered a key contribution. It exemplifies how agricultural intensification practiced in the context of climate change can constrain the potential of agricultural field margin flora to cope with climatic variations. The authors found that the incidence of plant strategies better adapted to climate change (conservative/stress-tolerant and Mediterranean species) increased with higher temperatures and lower soil moisture, and with lower intensity of margin management. In contrast, the incidence of ruderal species decreased with climate change. Thus, increasing or even maintaining current levels of agricultural intensification may affect the potential of French agriculture to move to sustainable process-based agricultures because of the reduction of plant diversity, particularly of vegetation better adapted to climate change. 
 
By using an impressive dataset spanning 9 years and 555 agricultural margins in continental France, Poinas et al. (2024) investigated temporal changes in climatic variables (temperature and soil moisture), agricultural practices (herbicide and fertilizers quantity, the frequency of margin mowing or grinding), plant taxonomical and functional diversity, plant strategies (Grime 1977, 1988) and relationships between these temporal changes. Temporal changes in plant strategies were associated with those observed in climatic variables and agricultural practices. Even such associations seem to be mediated by spatial changes, as described in the supplementary material and in their most recent article (Poinas et al. 2023), changes in climatic variables registered in a decade shaped plant strategies and therefore the diversity and functional potential of agricultural field margins. These results are clearly synthesized in Figures 6 and 7 of the present contribution.
 
As shown by Poinas et al. (2024), in the context of climate change, decreasing agricultural intensification will produce more diverse agricultural field margins by promoting the persistence of plant species better adapted to higher temperatures and lower soil moisture. Thus, adopting other agricultural practices (e.g., agroforestry, agroecology) will produce territories with a higher potential to move to sustainable processes-based agricultures that may better cope with climate change by harboring higher biocultural diversity (Altieri et al. 2015).

References

Alignier, A., 2018. Two decades of change in a field margin vegetation metacommunity as a result of field margin structure and management practice changes. Agric., Ecosyst. & Environ., 251, 1–10. https://doi.org/10.1016/j.agee.2017.09.013 

Altieri, M.A., Nicholls, C.I., Henao, A., Lana, M.A., 2015. Agroecology and the design of climate change-resilient farming systems. Agron. Sustain. Dev. 35, 869–890. https://doi.org/10.1007/s13593-015-0285-2

Emmerson, M., Morales, M. B., Oñate, J. J., Batary, P., Berendse, F., Liira, J., Aavik, T., Guerrero, I., Bommarco, R., Eggers, S., Pärt, T., Tscharntke, T., Weisser, W., Clement, L. & Bengtsson, J. (2016). How agricultural intensification affects biodiversity and ecosystem services. In Adv. Ecol. Res. 55, 43-97. https://doi.org/10.1016/bs.aecr.2016.08.005

Grime, J. P., 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. The American Naturalist, 111(982), 1169–1194. https://doi.org/10.1086/283244

Grime, J. P., 1988. The C-S-R model of primary plant strategies—Origins, implications and tests. In L. D. Gottlieb & S. K. Jain, Plant Evolutionary Biology (pp. 371–393). Springer Netherlands. https://doi.org/10.1007/978-94-009-1207-6_14

Moore, J., 2020. El capitalismo en la trama de la vida (Capitalism in The Web of Life). Traficantes de sueños, Madrid, Spain. 

Poinas, I., Fried, G., Henckel, L., & Meynard, C. N., 2023. Agricultural drivers of field margin plant communities are scale-dependent. Bas. App. Ecol. 72, 55-63. https://doi.org/10.1016/j.baae.2023.08.003

Poinas, I., Meynard, C. N., Fried, G., 2024. Functional trade-offs: exploring the temporal response of field margin plant communities to climate change and agricultural practices, bioRxiv, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2023.03.03.530956

Tamburini, G., Bommarco, R., Wanger, T.C., Kremen, C., Van Der Heijden, M.G., Liebman, M., Hallin, S., 2020. Agricultural diversification promotes multiple ecosystem services without compromising yield. Sci. Adv. 6, eaba1715. https://doi.org/10.1126/sciadv.aba1715

Functional trade-offs: exploring the temporal response of field margin plant communities to climate change and agricultural practicesIsis Poinas, Christine N Meynard, Guillaume Fried<p style="text-align: justify;">Over the past decades, agricultural intensification and climate change have led to vegetation shifts. However, functional trade-offs linking traits responding to climate and farming practices are rarely analyzed, es...Agroecology, Biodiversity, Botany, Climate change, Community ecologyJulia Astegiano2023-03-04 15:40:35 View
21 Oct 2020
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Why scaling up uncertain predictions to higher levels of organisation will underestimate change

Uncertain predictions of species responses to perturbations lead to underestimate changes at ecosystem level in diverse systems

Recommended by based on reviews by Carlos Melian and 1 anonymous reviewer

Different sources of uncertainty are known to affect our ability to predict ecological dynamics (Petchey et al. 2015). However, the consequences of uncertainty on prediction biases have been less investigated, especially when predictions are scaled up to higher levels of organisation as is commonly done in ecology for instance. The study of Orr et al. (2020) addresses this issue. It shows that, in complex systems, the uncertainty of unbiased predictions at a lower level of organisation (e.g. species level) leads to a bias towards underestimation of change at higher level of organisation (e.g. ecosystem level). This bias is strengthened by larger uncertainty and by higher dimensionality of the system.
This general result has large implications for many fields of science, from economics to energy supply or demography. In ecology, as discussed in this study, these results imply that the uncertainty of predictions of species’ change increases the probability of underestimation of changes of diversity and stability at community and ecosystem levels, especially when species richness is high. The uncertainty of predictions of species’ change also increases the probability of underestimation of change when multiple ecosystem functions are considered at once, or when the combined effect of multiple stressors is considered.
The consequences of species diversity on ecosystem functions and stability have received considerable attention during the last decades (e.g. Cardinale et al. 2012, Kéfi et al. 2019). However, since the bias towards underestimation of change increases with species diversity, future studies will need to investigate how the general statistical effect outlined by Orr et al. might affect our understanding of the well-known relationships between species diversity and ecosystem functioning and stability in response to perturbations.

References

Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S (2012) Biodiversity loss and its impact on humanity. Nature, 486, 59–67. https://doi.org/10.1038/nature11148
Kéfi S, Domínguez‐García V, Donohue I, Fontaine C, Thébault E, Dakos V (2019) Advancing our understanding of ecological stability. Ecology Letters, 22, 1349–1356. https://doi.org/10.1111/ele.13340
Orr JA, Piggott JJ, Jackson A, Arnoldi J-F (2020) Why scaling up uncertain predictions to higher levels of organisation will underestimate change. bioRxiv, 2020.05.26.117200. https://doi.org/10.1101/2020.05.26.117200
Petchey OL, Pontarp M, Massie TM, Kéfi S, Ozgul A, Weilenmann M, Palamara GM, Altermatt F, Matthews B, Levine JM, Childs DZ, McGill BJ, Schaepman ME, Schmid B, Spaak P, Beckerman AP, Pennekamp F, Pearse IS (2015) The ecological forecast horizon, and examples of its uses and determinants. Ecology Letters, 18, 597–611. https://doi.org/10.1111/ele.12443

Why scaling up uncertain predictions to higher levels of organisation will underestimate changeJames Orr, Jeremy Piggott, Andrew Jackson, Jean-François Arnoldi<p>Uncertainty is an irreducible part of predictive science, causing us to over- or underestimate the magnitude of change that a system of interest will face. In a reductionist approach, we may use predictions at the level of individual system com...Community ecology, Ecosystem functioning, Theoretical ecologyElisa ThebaultAnonymous2020-06-02 15:41:12 View
01 Apr 2019
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The inherent multidimensionality of temporal variability: How common and rare species shape stability patterns

Diversity-Stability and the Structure of Perturbations

Recommended by ORCID_LOGO and based on reviews by Frederic Barraquand and 1 anonymous reviewer

In his 1972 paper “Will a Large Complex System Be Stable?” [1], May challenges the idea that large communities are more stable than small ones. This was the beginning of a fundamental debate that still structures an entire research area in ecology: the diversity-stability debate [2]. The most salient strength of May’s work was to use a mathematical argument to refute an idea based on the observations that simple communities are less stable than large ones. Using the formalism of dynamical systems and a major results on the distribution of the eigen values for random matrices, May demonstrated that the addition of random interactions destabilizes ecological communities and thus, rich communities with a higher number of interactions should be less stable. But May also noted that his mathematical argument holds true only if ecological interactions are randomly distributed and thus concluded that this must not be true! This is how the contradiction between mathematics and empirical observations led to new developments in the study of ecological networks.
Since 1972, the theoretical corpus of ecology has advanced, building on the formalism of dynamical systems, ecologists have revealed that ecological interactions are indeed not randomly distributed [3,4], but general rules are still missing and we are far from understanding what determine the exact network topology of a given community. One promising avenue is to understand the relationship between different facets of the concept of stability [5,6]. Indeed, the classical approach to determine whether a system is stable is qualitative: if a system returns to its equilibrium when it is slightly moved away from it, then the system is considered stable. But there are several other aspects that are worth scrutinizing. For instance, when a system returns to its equilibrium, one can characterize the corresponding transient dynamics [7,8], that is asking fundamental questions such as: what is the trajectory of return? How long does it take to return to the equilibrium? Another fundamental question is whether the system remains qualitatively stable when the distributions of interactions strengths change? From a biological standpoint, all of these questions matter as all these aspects of stability may partially explain the actual structure of ecological networks, and hence, frameworks that integrate several facets of stability are much needed.
The study by Arnoldi et al. [9] is a significant step towards such a framework. The strength of their formalism is threefold. First, instead of considering separately the system and its perturbations, they considering the fluctuations of a perturbed ecological systems and thus, perturbations are parts of the ecological system. Second, they use of a broad definition of perturbation that encompasses the types of perturbations (whether the individual respond synchronously or not), their intensity and their direction (how the perturbations are correlated across species). Third, they quantify the instability of the system using variability which integrates the consequences of perturbations over the whole set of species of a community: such a measure is comparable across communities and accounts for the trivial effect of the perturbations on the system dynamics.
Using this framework, the authors show that interactions within a stable community leads to a general relationship between variability and the abundance of individually perturbed species: if individuals of species respond in synchrony to a perturbation, then the more abundant the species perturbed the higher the variability of the system, but the relationship is reverse when individual respond asynchronously. A direct implications of these results for the classical debate is that the diversity-stability relationship is negative for the former type of perturbations (as in May’s seminal paper) but positive for the latter type. Hence, the rigorous work of Arnoldi and colleagues sheds a new light upon the classical debate: the nature of the perturbation regime prevailing within a community affects the slope of the diversity-stability relationships and given the vast diversity of ecological communities, this may very well be one of the reasons why the debate still endures.
From a historical perspective, it is interesting that ecologists have gone from looking at random webs to structured webs and now, in a sense, Arnoldi et al. are unpacking the role of differentially structured perturbations. The work they achieved will doubtlessly be followed by further theoretical investigations. One natural research avenue is to revisit the role of the topology of ecological networks with this framework: how the distribution of interactions and their strength affect the general relationship they unravel? Finally, this study demonstrate that the impact of the abundance of a species on the variability of the system depends on the nature of the perturbation regime and so the distribution of species abundances within a community should be determined by the prevailing perturbation regime which is a prediction that remains to be tested.

References

[1] May, Robert M (1972). Will a Large Complex System Be Stable? Nature 238, 413–414. doi: 10.1038/238413a0
[2] McCann, Kevin Shear (2000). The Diversity–Stability Debate. Nature 405, 228–233. doi: 10.1038/35012234
[3] Rooney, Neil, Kevin McCann, Gabriel Gellner, and John C. Moore (2006). Structural Asymmetry and the Stability of Diverse Food Webs. Nature 442, 265–269. doi: 10.1038/nature04887
[4] Jacquet, Claire, Charlotte Moritz, Lyne Morissette, Pierre Legagneux, François Massol, Philippe Archambault, and Dominique Gravel (2016). No Complexity–Stability Relationship in Empirical Ecosystems. Nature Communications 7, 12573. doi: 10.1038/ncomms12573
[5] Donohue, Ian, Helmut Hillebrand, José M. Montoya, Owen L. Petchey, Stuart L. Pimm, Mike S. Fowler, Kevin Healy, et al. (2016). Navigating the Complexity of Ecological Stability. Ecology Letters 19, 1172–1185. doi: 10.1111/ele.12648
[6] Arnoldi, Jean-François, and Bart Haegeman (2016). Unifying Dynamical and Structural Stability of Equilibria. Proceedings of the Royal Society A: Mathematical, Physical and Engineering Science 472, 20150874. doi: 10.1098/rspa.2015.0874
[7] Caswell, Hal, and Michael G. Neubert (2005). Reactivity and Transient Dynamics of Discrete-Time Ecological Systems. Journal of Difference Equations and Applications 11, 295–310. doi: 10.1080/10236190412331335382
[8] Arnoldi, J-F., M. Loreau, and B. Haegeman (2016). Resilience, Reactivity and Variability: A Mathematical Comparison of Ecological Stability Measures. Journal of Theoretical Biology 389, 47–59. doi: 10.1016/j.jtbi.2015.10.012
[9] Arnoldi, Jean-Francois, Michel Loreau, and Bart Haegeman. (2019). The Inherent Multidimensionality of Temporal Variability: How Common and Rare Species Shape Stability Patterns.” BioRxiv, 431296, ver. 3 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/431296

The inherent multidimensionality of temporal variability: How common and rare species shape stability patternsJean-François Arnoldi, Michel Loreau, Bart Haegeman<p>Empirical knowledge of ecosystem stability and diversity-stability relationships is mostly based on the analysis of temporal variability of population and ecosystem properties. Variability, however, often depends on external factors that act as...Biodiversity, Coexistence, Community ecology, Competition, Interaction networks, Theoretical ecologyKevin Cazelles2018-10-02 14:01:03 View