Christopher J. Greyson-Gaito, Gabriel Gellner, Kevin S. McCann. 2023. Life history speed, population disappearances, and noise-induced ratchet effects. Proceedings of the Royal Society B 290:20222149. https://doi.org/10.1098/rspb.2022.2149 Ⓒ 2023 The Author(s)
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Life history speed, population disappearances, and noise-induced ratchet effects
Nature is replete with variation in the body sizes, reproductive output and generation times of species that produce life-history responses known to vary from small and fast to large and slow. Although researchers recognize that life-history speed likely dictates fundamental processes in consumer-resource interactions like productivity and stability, theoretical work remains incomplete in this critical area. Here, we examine the role of life-history speed on consumer–resource interactions by using a well-used mathematical approach that manipulates the speed of the consumer's growth rate in a consumer–resource interaction. Importantly, this approach holds the isocline geometry intact, allowing us to assess the impacts of altered life-history speed on stability (coefficient of variation, CV) without changing the underlying qualitative dynamics. Although slowing life history can be initially stabilizing, we find that in stochastic settings slowing ultimately drives highly destabilizing population disappearances, especially under reddened noise. Our results suggest that human-driven reddening of noise may decrease species stability because the autocorrelation of red noise enlarges the period and magnitude of perturbations, overwhelming a species' natural compensatory responses via a ratchet-like effect. This ratchet-like effect then pushes species’ population dynamics far away from equilibria, which can lead to precipitous local extinction.
Phylogenetic community structure and stable isotope analysis of the parasitoid community associated with Eastern spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae)
1. Eastern spruce budworm, Choristoneura fumiferana Clemens (Lepidoptera: Tortricidae), is a major pest of eastern North American forests. Outbreaks of spruce budworm occur every 30–40 years, causing high tree mortality. 2.Researchers have established that higher proportions of hardwood trees within stands (higher hardwood content) may reduce the defoliation and mortality of balsam fir and spruces during spruce budworm outbreaks. One mechanism posited to explain these patterns is that hardwood trees positively impact the parasitoids of spruce budworm. Indeed, parasitism of spruce budworm by parasitoids has been found to be impacted by hardwood content. However, more research is needed to understand how hardwood content impacts the parasitoid community as a whole. 3. In this study, we trialled the use of two analyses, phylogenetic community structure and stable isotope analysis, to examine how hardwood content influenced the parasitoid community associated with spruce budworm. 4. We found that phylogenetic community structure differed between forest stands with different hardwood content. Furthermore, the trophic relationships between several parasitoids and caterpillars on balsam fir or hardwood trees changed within and between years. 5. Our study highlights the potential of these two analyses for understanding how hardwood content influences the parasitoid community associated with spruce budworm.
Marie K. Gutgesell, Kevin S. McCann, Gabriel Gellner, Kevin Cazelles, Christopher J. Greyson-Gaito, Carling Bieg, Matthew M. Guzzo, Connor P. K. Warne, Charlotte Ward, Reilly F. O'Connor, Alexa M. Scott, Brandon C. Graham, Emily J. Champagne, Bailey C. McMeans. 2022. On the Dynamic Nature of Omnivory in a Changing World. BioScience 72:416–430. https://doi.org/10.1093/biosci/biab144 Ⓒ 2022 The Author(s)
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On the Dynamic Nature of Omnivory in a Changing World
Nature's variability plays a major role in maintenance of biodiversity. As global change is altering variability, understanding how key food web structures maintain stability in the face of variation becomes critical. Surprisingly, little research has been undertaken to mechanistically understand how key food web structures are expected to operate in a noisy world and what this means for stability. Omnivory, for example, has been historically well studied but largely from a static perspective. Recent empirical evidence suggests that the strength of omnivory varies in response to changing conditions in ways that may be fundamental to stability. In the present article, we extend existing omnivory theory to predict how omnivory responds to variation and to show that dynamic omnivory responses are indeed a potent stabilizing structure in the face of variation. We end by synthesizing empirical examples within this framework, demonstrating the ubiquity of the theoretical mechanisms proposed across ecosystem types, spatial scales, and taxa.
Christopher J. Greyson-Gaito, Kevin S. McCann, Jochen Fründ, Christopher J. Lucarotti, M. Alex Smith, Eldon S. Eveleigh. 2021. Parasitoid community responds indiscriminately to fluctuating spruce budworm and other caterpillars on balsam fir. The Canadian Entomologist 153:482-496. https://doi.org/10.4039/tce.2021.14 Ⓒ The authors, and Her Majesty, the Queen, in right of Canada, 2021. Published by Cambridge University Press on behalf of the Entomological Society of Canada
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Parasitoid community responds indiscriminately to fluctuating spruce budworm and other caterpillars on balsam fir
The world is astoundingly variable, and organisms - from individuals to whole communities - must respond to variability to survive. One example of nature's variability is the fluctuations in populations of spruce budworm, Choristoneura fumiferana Clemens (Lepidoptera: Tortricidae), which cycle every 35 years. In this study, we examined how a parasitoid community altered its parasitism of budworm and other caterpillar species in response to these fluctuations. Budworm and other caterpillar species were sampled from balsam fir (Pinaceae) in three plots for 14 years in Atlantic Canada, then were reared to identify any emerging parasitoids. We found that the parasitoid community generally showed an indiscriminate response (i.e., no preference, where frequencies dictated parasitism rates) to changes in budworm frequencies relative to other caterpillar species on balsam fir. We also observed changes in topology and distributions of interaction strengths between the parasitoids, budworm, and other caterpillar species as budworm frequencies fluctuated. Our study contributes to the hypothesis that hardwood trees are a critical part of the budworm–parasitoid food web, where parasitoids attack other caterpillar species on hardwood trees when budworm populations are low. Taken together, our results show that a parasitoid community collectively alters species interactions in response to variable budworm frequencies, thereby fundamentally shifting food-web pathways.
Matthew A. Barbour, Christopher J. Greyson-Gaito , Arezoo Sotoodeh, Brendan Locke, Jordi Bascompte. 2020. Loss of consumers constrains phenotypic evolution in the resulting food web. Evolution Letters 4:266-277. https://onlinelibrary.wiley.com/doi/10.1002/evl3.170 Ⓒ 2020 The Author(s) CC BY 3.0
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Loss of consumers constrains phenotypic evolution in the resulting food web
The loss of biodiversity is altering the structure of ecological networks; however, we are currently in a poor position to predict howthese altered communities will affect the evolution of remaining populations. Theory on fitness landscapes provides a frameworkfor predicting how selection alters the evolutionary trajectory and adaptive potential of populations, but often treats the networkof interacting populations as a “black box.” Here, we integrate ecological networks and fitness landscapes to examine how changesin food-web structure shape phenotypic evolution. We conducted a field experiment that removed a guild of larval parasitoidsthat imposed direct and indirect selection pressures on an insect herbivore. We then measured herbivore survival as a functionof three key phenotypic traits to estimate directional, quadratic, and correlational selection gradients in each treatment. We usedthese selection gradients to characterize the slope and curvature of the fitness landscape to understand the direct and indirecteffects of consumer loss on phenotypic evolution. We found that the number of traits under directional selection increased withthe removal of larval parasitoids, indicating evolution was more constrained toward a specific combination of traits. Similarly, wefound that the removal of larval parasitoids altered the curvature of the fitness landscape in such a way that tended to decreasethe evolvability of the traits we measured in the next generation. Our results suggest that the loss of trophic interactions canimpose greater constraints on phenotypic evolution. This indicates that the simplification of ecological communities may constrainthe adaptive potential of remaining populations to future environmental change.
Christopher J. Greyson-Gaito , Timothy J. Bartley, Karl Cottenie, Will M.C. Jarvis, Amy E.M. Newman, Mason R. Stothart. 2020. Into the wild: microbiome transplant studies need broader ecological reality. Proceedings of the Royal Society B 287:20192834. https://doi.org/10.1098/rspb.2019.2834 Ⓒ 2020 The Author(s)
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Into the wild: microbiome transplant studies need broader ecological reality
Gut microbial communities (microbiomes) profoundly shape the ecology and evolution of multicellular life. Interactions between host and microbiome appear to be reciprocal, and ecological theory is now being applied to better understand how hosts and their microbiome influence each other. However, some ecological processes that underlie reciprocal host–microbiome interactions may be obscured by the current convention of highly controlled transplantation experiments. Although these approaches have yielded invaluable insights, there is a need for a broader array of approaches to fully understand host–microbiome reciprocity. Using a directed review, we surveyed the breadth of ecological reality in the current literature on gut microbiome transplants with non-human recipients. For 55 studies, we categorized nine key experimental conditions that impact the ecological reality (EcoReality) of the transplant, including host taxon match and donor environment. Using these categories, we rated the EcoReality of each transplant. Encouragingly, the breadth of EcoReality has increased over time, but some components of EcoReality are still relatively unexplored, including recipient host environment and microbiome state. The conceptual framework we develop here maps the landscape of possible EcoReality to highlight where fundamental ecological processes can be considered in future transplant experiments.
Mariano A. Rodriguez-Cabal, M. Noelia Barrios-Garcia, Christopher J. Greyson-Gaito , Heather L. Slinn, M. Paz Tapella, Agustín Vitali, Gregory M. Crutsinger. 2019. Non-native ungulates indirectly impact foliar arthropods but not soil function. Biological Invasions 21:3077–3084. https://doi.org/10.1007/s10530-019-02030-9 Ⓒ Springer Nature Switzerland AG 2019
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Non-native ungulates indirectly impact foliar arthropods but not soil function
One of the greatest challenges in contemporary ecology is to understand how the homogenization of biodiversity at all levels of organization and spatial scales will influence the assembly of communities and the functioning of ecosystems. Such homogenization can occur through the gain of non-native species and the loss of native species. Here, we show that by disrupting a keystone mutualistic interaction, non-native ungulates indirectly impact foliar arthropod abundance and richness, but not soil properties (soil respiration, temperature and humidity), in a temperate forest of Patagonia. The results of this study show that the gain of non-native ungulates and the loss of a key interaction can trigger unnoticed cascading effects. Our findings highlight the importance of assessing biodiversity not only as the sum of different components but also through the direct and indirect interactions among them.
Christopher J. Greyson-Gaito, Matthew A. Barbour, Mariano A. Rodriguez-Cabal, Gregory M. Crutsinger, and Gregory H.R Henry. 2016. Freedom to move: Arctic caterpillar (Lepidoptera) growth rate increases with access to new willows (Salicaceae). Canadian Entomologist 148:673-682. https://doi.org/10.4039/tce.2016.22 Ⓒ Entomological Society of Canada 2016
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Freedom to move: Arctic caterpillar (Lepidoptera) growth rate increases with access to new willows (Salicaceae)
Movement between host plants during the growing season is a common behaviour among insect herbivores, although the mechanisms promoting these movements are poorly understood for many systems. Two possible reasons why insect herbivores relocate include compensating for host plant quantity and/or quality changes and the avoidance of natural enemies. The Arctic caterpillar (Gynaephora groenlandica (Wocke); Lepidoptera: Lymantriidae) moves several metres each day, feeds on its patchily distributed host plant, Arctic willow (Salix arctica Pallas; Salicaceae), and has two main natural enemies, the parasitoids Exorista thula Wood (Diptera: Tachinidae) and Hyposoter diechmanni (Nielsen) (Hymenoptera: Ichneumonidae). We physically moved caterpillars between Arctic willows and restricted other caterpillar individuals each to a single willow throughout the active period of Arctic caterpillars. We found that growth rate, herbivory rate, and the proportion of available leaf fascicles eaten were higher for experimentally moved caterpillars. Parasitoid abundances were low and did not differ between experimentally moved and stationary caterpillars. Taken together, our study addresses the bottom–up and top–down controls on insect herbivore movement during the short duration of the growing season in the Arctic. Our results suggest that caterpillars are likely moving to new willow shrubs to access high quality resources.
Slower organisms exhibit sudden population disappearances in a reddened world
Sudden population disappearances are a possibility in natural systems. Human-caused reddening of noise — increasing the autocorrelation of noise — may make sudden population disappearances more likely because red noise can enlarge the period and magnitude of perturbations, potentially overwhelming species' natural compensatory responses and pushing species' population dynamics away from equilibria into transient dynamics and close to extinction. Furthermore, species' natural compensatory responses are related to life history along the slow-fast continuum. This interaction of slow-fast life history plus red noise may be a potent factor producing sudden population disappearances. Using a simple mathematical technique with the classic Rozenzweig-MacArthur consumer resource model, we created an experiment varying the consumer's maximum population growth rate, effectively varying the consumer's life history along the slow-fast continuum. Initial slowing of the consumer's growth rate increased the stability of the consumer-resource model with added stochasticity. Slowing the consumer's growth rate further and reddening the noise decreased the stability with population disappearances occurring frequently. Taken together, we have shown that slow life histories can both stabilize or destabilize interactions depending on the relative speeds within the interaction. Disconcertingly with a reddening world, larger and slower organisms may be especially prone to experiencing transient-driven sudden population disappearances.
Ⓒ Christopher J. Greyson-Gaito, Sarah J. Dolson, Glen Forbes, Rosanna Lamb, Wayne E. MacKinnon, Kevin S. McCann, M. Alex Smith, Eldon S. Eveleigh 2021. Hardwood content impacts the parasitoid community associated with Eastern spruce budworm (Lepidoptera: Tortricidae). https://doi.org/10.32942/osf.io/mdua8CC-By Attribution-ShareAlike 4.0 International
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Hardwood content impacts the parasitoid community associated with Eastern spruce budworm (Lepidoptera: Tortricidae)
A major pest of eastern North American forests is spruce budworm, Choristoneura fumiferana Clemens (Lepidoptera: Tortricidae), which outbreaks every 30-40 years and causes large scale tree mortality. Researchers have established that hardwood content reduces the defoliation and mortality of balsam fir and spruces during spruce budworm outbreaks. One mechanism posited to explain these patterns is that hardwood content positively impacts the parasitoids of spruce budworm. Researchers have found that parasitism of spruce budworm by individual parasitoids is impacted by hardwood content. Yet, more research is needed to understand how hardwood content impacts the parasitoid community as a whole. In this study, we used DNA barcoding and stable isotope analysis of Malaise trap sampled parasitoids to examine how hardwood content influenced parasitoid community composition, structure, and trophic interactions. We found that although composition did not significantly differ along a hardwood content gradient, phylogenetic community structure did differ. Furthermore, the trophic relationships between several parasitoids and caterpillars on balsam fir or hardwood trees changed over time. Our study highlights the importance of hardwood trees for spruce budworm dynamics through influencing the parasitoid community.
Into the wild: microbiome transplant studies need broader ecological reality
Resident gut microbial communities (microbiomes) have profound impacts on the ecology and evolution of multicellular life, shaping host physiology, behaviour, and community interactions. We are beginning to understand that ecological theories can be applied to the interactions between hosts and their microbiomes. However, the ecological processes that govern host-microbiome interactions may be obscured by current experimental protocols that rely on highly controlled transplantation of microbiomes. We surveyed current studies that used gut microbiome transplants with non-human recipients, and categorized the 9 key experimental conditions that impact the ecological reality (EcoReality) of the transplant. Using these categories, we rated the EcoReality of all transplants and assessed the breadth of EcoReality in the microbiome transplant literature. Encouragingly, we found an increase in EcoReality over time, but EcoReality was still lacking in the host environment and in the state of the recipient host microbiome. From this process, we have created a novel conceptual framework for future researchers to adapt as necessary to incorporate fundamental ecological processes in their transplant experiments and employ broader ranges of EcoReality.
Ⓒ Christopher J. Greyson-Gaito, Kevin S. McCann, Jochen Fründ, Christopher J. Lucarotti, M. Alex Smith, Eldon S. Eveleigh 2019. Parasitoid community responds indiscriminately to fluctuating spruce budworm and other caterpillars on balsam fir. https://doi.org/10.1101/615799CC-BY-NC 4.0 International license
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Parasitoid community responds indiscriminately to fluctuating spruce budworm and other caterpillars on balsam fir
The world is astoundingly variable, and individuals to whole communities must respond to variability to survive. One example of nature's variability is the massive fluctuations in spruce budworm (Choristoneura fumiferana Clemens, Lepidoptera: Tortricidae) populations that occur over 35 years. We examined how the parasitoid community altered its parasitism ofbudworm and other caterpillar species in response to these fluctuations. Budworm and other caterpillar species were sampled from balsam fir in three plots for 14 years in Atlantic Canada, and then reared to identify any emerging parasitoids. We found that the parasitoid community showed a simple linear, indiscriminate response (i.e., no preference, where densities purely dictated parasitism rates) to changes in budworm densities relative to other caterpillar species on balsam fir. We also observed strong changes in topology and distributions of interaction strengths between the parasitoids, budworm and other caterpillar species as budworm densities fluctuated. Our study contributes to the suggestion that hardwood trees are a critical part of the budworm-parasitoid food web, where parasitoids attack other caterpillar species on hardwood trees when budworm populations are low. Taken together, our study shows that a parasitoid community collectively alters species interactions in response to variable budworm densities, fundamentally shifting food web pathways.
Loss of consumers constrains phenotypic evolution in the resulting food web
The loss of biodiversity is altering the structure of ecological networks; however, we are currently in a poor position to predict how these altered communities will affect the evolutionary potential of remaining populations. Theory on adaptive landscapes provides a framework for predicting how selection constrains phenotypic evolution, but often treats the network context of evolving populations as a “black box”. Here, we integrate ecological networks and adaptive landscapes to examine how changes in food-web structure shape evolutionary constraints. We conducted a field experiment that removed a guild of larval parasitoids that imposed direct and indirect selection pressures on an insect herbivore. We then measured herbivore survival as a function of three key phenotypic traits to estimate directional, quadratic, and correlational selection gradients in each treatment. We used these selection gradients to characterize the slope and curvature of the adaptive landscape to understand the direct and indirect effects of consumer loss on evolutionary constraints. We found that the number of traits under directional selection increased with the removal of larval parasitoids, indicating greater selective constraints on the trajectory of evolutionary change. Similarly, we found that the removal of larval parasitoids altered the curvature of the adaptive landscape in such a way that tended to decrease the evolvability of the traits we measured in the next generation. Our results suggest that the loss of trophic interactions can impose greater constraints on phenotypic evolution. This indicates that the simplification of ecological communities may constrain the adaptive potential of remaining populations to future environmental change.