Trait‐based ecology of terrestrial arthropods Wong, Mark K. L.; Guénard, Benoit; Lewis, Owen T.
Biological reviews of the Cambridge Philosophical Society,
June 2019, Letnik:
94, Številka:
3
Journal Article
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ABSTRACT
In focusing on how organisms' generalizable functional properties (traits) interact mechanistically with environments across spatial scales and levels of biological organization, trait‐based ...approaches provide a powerful framework for attaining synthesis, generality and prediction. Trait‐based research has considerably improved understanding of the assembly, structure and functioning of plant communities. Further advances in ecology may be achieved by exploring the trait–environment relationships of non‐sessile, heterotrophic organisms such as terrestrial arthropods, which are geographically ubiquitous, ecologically diverse, and often important functional components of ecosystems. Trait‐based studies and trait databases have recently been compiled for groups such as ants, bees, beetles, butterflies, spiders and many others; however, the explicit justification, conceptual framework, and primary‐evidence base for the burgeoning field of ‘terrestrial arthropod trait‐based ecology’ have not been well established. Consequently, there is some confusion over the scope and relevance of this field, as well as a tendency for studies to overlook important assumptions of the trait‐based approach. Here we aim to provide a broad and accessible overview of the trait‐based ecology of terrestrial arthropods. We first define and illustrate foundational concepts in trait‐based ecology with respect to terrestrial arthropods, and justify the application of trait‐based approaches to the study of their ecology. Next, we review studies in community ecology where trait‐based approaches have been used to elucidate how assembly processes for terrestrial arthropod communities are influenced by niche filtering along environmental gradients (e.g. climatic, structural, and land‐use gradients) and by abiotic and biotic disturbances (e.g. fire, floods, and biological invasions). We also review studies in ecosystem ecology where trait‐based approaches have been used to investigate biodiversity–ecosystem function relationships: how the functional diversity of arthropod communities relates to a host of ecosystem functions and services that they mediate, such as decomposition, pollination and predation. We then suggest how future work can address fundamental assumptions and limitations by investigating trait functionality and the effects of intraspecific variation, assessing the potential for sampling methods to bias the traits and trait values observed, and enhancing the quality and consolidation of trait information in databases. A roadmap to guide observational trait‐based studies is also presented. Lastly, we highlight new areas where trait‐based studies on terrestrial arthropods are well positioned to advance ecological understanding and application. These include examining the roles of competitive, non‐competitive and (multi‐)trophic interactions in shaping coexistence, and macro‐scaling trait–environment relationships to explain and predict patterns in biodiversity and ecosystem functions across space and time. We hope this review will spur and guide future applications of the trait‐based framework to advance ecological insights from the most diverse eukaryotic organisms on Earth.
Abstract
As mean temperatures increase and heatwaves become more frequent, species are expanding their distributions to colonise new habitats. The resulting novel species interactions will ...simultaneously shape the temperature‐driven reorganization of resident communities. The interactive effects of climate change and climate change‐facilitated invasion have rarely been studied in multi‐trophic communities, and are likely to differ depending on the nature of the climatic driver (i.e., climate extremes or constant warming). We re‐created under laboratory conditions a host‐parasitoid community typical of high‐elevation rainforest sites in Queensland, Australia, comprising four
Drosophila
species and two associated parasitoid species. We subjected these communities to an equivalent increase in average temperature in the form of periodic heatwaves or constant warming, in combination with an invasion treatment involving a novel host species from lower‐elevation habitats. The two parasitoid species were sensitive to both warming and heatwaves, while the demographic responses of
Drosophila
species were highly idiosyncratic, reflecting the combined effects of thermal tolerance, parasitism, competition, and facilitation. After multiple generations, our heatwave treatment promoted the establishment of low‐elevation species in upland communities. Invasion of the low‐elevation species correlated negatively with the abundance of one of the parasitoid species, leading to cascading effects on its hosts and their competitors. Our study, therefore, reveals differing, sometimes contrasting, impacts of extreme temperatures and constant warming on community composition. It also highlights how the scale and direction of climate impacts could be further modified by invading species within a bi‐trophic community network.
Tropical forests are important reservoirs of biodiversity, but the processes that maintain this diversity remain poorly understood. The Janzen-Connell hypothesis suggests that specialized natural ...enemies such as insect herbivores and fungal pathogens maintain high diversity by elevating mortality when plant species occur at high density (negative density dependence; NDD). NDD has been detected widely in tropical forests, but the prediction that NDD caused by insects and pathogens has a community-wide role in maintaining tropical plant diversity remains untested. We show experimentally that changes in plant diversity and species composition are caused by fungal pathogens and insect herbivores. Effective plant species richness increased across the seed-to-seedling transition, corresponding to large changes in species composition. Treating seeds and young seedlings with fungicides significantly reduced the diversity of the seedling assemblage, consistent with the Janzen-Connell hypothesis. Although suppressing insect herbivores using insecticides did not alter species diversity, it greatly increased seedling recruitment and caused a marked shift in seedling species composition. Overall, seedling recruitment was significantly reduced at high conspecific seed densities and this NDD was greatest for the species that were most abundant as seeds. Suppressing fungi reduced the negative effects of density on recruitment, confirming that the diversity-enhancing effect of fungi is mediated by NDD. Our study provides an overall test of the Janzen-Connell hypothesis and demonstrates the crucial role that insects and pathogens have both in structuring tropical plant communities and in maintaining their remarkable diversity.
Species turnover with elevation is a widespread phenomenon and provides valuable information on why and how ecological communities might reorganize as the climate warms. It is commonly assumed that ...species interactions are more likely to set warm range limits, while physiological tolerances determine cold range limits. However, most studies are from temperate systems and rely on correlations between thermal physiological traits and range limits; little is known about how physiological traits and biotic interactions change simultaneously along continuous thermal gradients. We used a combination of correlational and experimental approaches to investigate communities of Drosophila flies in rainforests of the Australian Wet Tropics, where there is substantial species turnover with elevation. Our experiments quantified individual‐level and population‐level responses to temperature, as well as the impact of interspecific competition under different temperature regimes. Species' distributions were better explained by their performance at extreme temperatures than by their thermal optima. Upper thermal limits varied less among species than lower thermal limits. Nonetheless, these small differences were associated with differences in the centered elevation of distribution. Low‐elevation species were not those with the lowest tolerance to cold, suggesting that cold temperatures were not limiting their abundance at high elevations. Instead, under upland temperature regimes, abundances of these low‐elevation species were reduced by competition with a high‐elevation species, in both short‐ and long‐term competition experiments. Our results demonstrate that high‐elevation species are confined to their current ranges by high temperatures at lower elevations, indicating that their ranges will be highly sensitive to future warming. Counter to expectation, species interactions strongly influenced community composition at cooler, high‐elevation sites. Together, these results raise the possibility that tropical communities differ from better‐studied temperate communities in terms of the relative importance of biotic interactions and abiotic factors in shaping community composition and how the impact of these factors will change as temperatures increase.
An increase in species richness with decreasing latitude is a prominent pattern in nature. However, it remains unclear whether there are corresponding latitudinal gradients in the properties of ...ecological interaction networks. We investigated the structure of 216 quantitative antagonistic networks comprising insect hosts and their parasitoids, drawn from 28 studies from the High Arctic to the tropics. Key metrics of network structure were strongly affected by the size of the interaction matrix (i.e. the total number of interactions documented between individuals) and by the taxonomic diversity of the host taxa involved. After controlling for these sampling effects, quantitative networks showed no consistent structural patterns across latitude and host guilds, suggesting that there may be basic rules for how sets of antagonists interact with resource species. Furthermore, the strong association between network size and structure implies that many apparent spatial and temporal variations in network structure may prove to be artefacts.
Global conversion of natural habitats to agriculture has led to marked changes in species diversity and composition. However, it is less clear how habitat modification affects interactions among ...species. Networks of feeding interactions (food webs) describe the underlying structure of ecological communities, and might be crucially linked to their stability and function. Here, we analyse 48 quantitative food webs for cavity-nesting bees, wasps and their parasitoids across five tropical habitat types. We found marked changes in food-web structure across the modification gradient, despite little variation in species richness. The evenness of interaction frequencies declined with habitat modification, with most energy flowing along one or a few pathways in intensively managed agricultural habitats. In modified habitats there was a higher ratio of parasitoid to host species and increased parasitism rates, with implications for the important ecosystem services, such as pollination and biological control, that are performed by host bees and wasps. The most abundant parasitoid species was more specialized in modified habitats, with reduced attack rates on alternative hosts. Conventional community descriptors failed to discriminate adequately among habitats, indicating that perturbation of the structure and function of ecological communities might be overlooked in studies that do not document and quantify species interactions. Altered interaction structure therefore represents an insidious and functionally important hidden effect of habitat modification by humans.
1. In natural communities, multiple host and parasitoid species are linked to form complex networks of trophic and non‐trophic interactions. Understanding how these networks will respond to global ...warming is of wide relevance for agriculture and conservation.
2. This study synthesises the emerging evidence surrounding host–parasitoid networks in the context of global warming. The suite of direct and indirect interaction types within host–parasitoid networks is summarised, as well as their sensitivity to temperature changes. The study also compiles and reviews studies investigating the responses of whole host–parasitoid networks to increasing temperatures or proxy variables. The findings reveal there is limited evidence overall for the prediction that parasitism will be reduced under global warming: approximately equal numbers of studies show elevated and reduced parasitism.
3. Increasingly, endosymbiotic bacteria are recognised as influential mediators of host–parasitoid interactions. These endosymbionts can change how individual species respond to global warming, and their effects can cascade to affect whole host–parasitoid networks. The evidence that symbiotic bacteria are likely to affect the response of host–parasitoid networks to global warming is reviewed. Symbionts can protect hosts from their parasitoids or influence thermal tolerance of their host species. Furthermore, the symbionts themselves can be impacted by global warming.
4. Finally, the study considers the most promising avenues for future research into the mechanisms structuring host–parasitoid networks in the context of global warming. Alongside the increasing availability of modern molecular methods to document the structure of real, species‐rich host–parasitoid networks, the study highlights the utility of manipulative experiments and mathematical models.
Research into mechanisms that have long been considered important in host–parasitoid networks (e.g. apparent competition) has increased relevance in the context of global warming.
Important additional mechanisms structuring host–parasitoid networks are emerging, such as endosymbiotic bacteria that can mediate host–parasitoid interactions and species' response to global warming, with cascading effects on network structure.
Laboratory and field experiments that investigate the effects of temperature on host–parasitoid networks are providing new insights, and predictive mathematical models are being developed and refined.
A key challenge for tropical conservation biologists is to assess how forest management practices affect biodiversity and associated ecosystem functions. Dung beetles (Scarabaeidae: Scarabaeinae) ...provide an ideal focal guild for such studies. We compared dung beetle assemblages and experimentally assessed rates of dung removal and seed burial in undisturbed forest, low-intensity selectively logged forest under sustainable forest management, and high-intensity logged forest, not under sustainable management in Malaysian Borneo. In total, 7923 individuals from 39 species of dung beetle were collected. There were no significant differences in abundance, biomass or diversity across sites. Species richness was significantly lower in the high-intensity logged sites. Beta diversity was low: of 35 species recorded in undisturbed forest sites, 32 were also captured in low-intensity sites and 29 in high-intensity sites. The environmental and vegetation variables measured had little influence on species composition. An average of 63–99% of dung was removed over 24
h. Mean dung and seed removal were significantly lower in the high-intensity logged sites. Dung removal rates were significantly and positively correlated with dung beetle species richness, but not with dung beetle biomass or abundance. However, the biomass of large-bodied, nocturnal dung beetles was positively correlated with dung removal. In contrast to previous studies, dung beetle biomass and abundance were not correlated with species richness, indicative of density compensation. Overall, dung beetle communities and associated ecosystem functions were robust to low-intensity but not high-intensity selective logging. These differences may be related to changes in the abundance and biomass of particular dung beetle species or guilds rather than community-wide measures of abundance and biomass, highlighting the need to move beyond simplistic biodiversity-ecosystem functioning correlations to understand the functional consequences of habitat modification in high-diversity ecosystems.
The role of natural enemies in promoting coexistence of competing species has generated substantial debate. Modern coexistence theory provides a detailed framework to investigate this topic, but ...there have been remarkably few empirical applications to the impact of natural enemies.
We tested experimentally the capacity for a generalist enemy to promote coexistence of competing insect species, and the extent to which any impact can be predicted by trade‐offs between reproductive rate and susceptibility to natural enemies.
We used experimental mesocosms to conduct a fully factorial pairwise competition experiment for six rainforest Drosophila species, with and without a generalist pupal parasitoid. We then parameterised models of competition and examined the coexistence of each pair of Drosophila species within the framework of modern coexistence theory.
We found idiosyncratic impacts of parasitism on pairwise coexistence, mediated through changes in fitness differences, not niche differences. There was no evidence of an overall reproductive rate–susceptibility trade‐off. Pairwise reproductive rate–susceptibility relationships were not useful shortcuts for predicting the impact of parasitism on coexistence.
Our results exemplify the value of modern coexistence theory in multi‐trophic contexts and the importance of contextualising the impact of generalist natural enemies to determine their impact. In the set of species investigated, competition was affected by the higher trophic level, but the overall impact on coexistence cannot be easily predicted just from knowledge of relative susceptibility. Methodologically, our Bayesian approach highlights issues with the separability of model parameters within modern coexistence theory and shows how using the full posterior parameter distribution improves inferences. This method should be widely applicable for understanding species coexistence in a range of systems.
摘要
同生态位物种间的共存受到它们共同天敌的调控。这一调控的影响仍备受争议。现代共存理论为这一问题提供了量化的研究框架, 但相关的实证研究还远远落后于理论进展。
我们通过实验探究了非特异性寄生蜂如何调控其宿主之间的竞争性共存, 并尝试用宿主的繁殖力与免疫力间的关系对共存结果加以解释。
在实验室的模拟实验中, 我们将六个热带雨林果蝇物种两两组合后放置于有或者没有寄生蜂的环境下, 记录子代果蝇的数量。我们用这些实验数据拟合出宿主间的物种竞争模型, 再通过现代共存理论推导宿主间的共存关系。
我们发现非特异性寄生蜂改变了不同宿主物种间的适合度差异, 但并没有改变它们的生态位差异。非特异性寄生蜂最终的调控效果依宿主组合的不同而不同, 并没有统一的规律。宿主的繁殖力和免疫力间并不普遍存在此消彼长的关系。即使在某几对宿主间存在负相关性, 寄生蜂的调控也并不总是促进共存。
我们的研究示范了如何将现代共存理论应用于多营养级生态网络,强调了寄生蜂对宿主间共存的影响依具体情况而定: 宿主物种间的竞争受到更高营养级的调控, 而此调控对宿主间共存的影响并不能简单地通过它们的对寄生蜂的免疫能力进行预测。另外, 我们的统计分析指出了在应用现代共存理论到实际系统时将面临的参数协变性问题, 并展示了如何利用贝叶斯统计方法完善对物种共存关系的推测。我们推荐这一方法被更广泛地应用于物种间共存的研究。
Using a large competition experiment and a modern coexistence theory framework, the authors tested the impact of a generalist parasitoid wasp on competition between Drosophila hosts. They found the generalist natural enemy could alter the fitness differences between Drosophila species, but that the impact on pairwise coexistence was mixed.
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