Multiple parasitoid species enhance top-down control, but parasitoid performance is context dependent.

Ecological communities are composed of many species, forming complex networks of interactions. Current environmental changes are altering the structure and species composition of ecological networks, which could modify interactions, either directly or indirectly. To predict changes in the functioning of communities, we need to understand whether species interactions are primarily driven by network structure (i.e. topology) or the specific identities of species (i.e. nodes). Yet, this partitioning of effects is challenging and thus rarely explored. Here we disentangled the influence of network structure and the identities of species on the outcome of consumer-resource interactions using a host-parasitoid system. We used four common community modules in host-parasitoid communities to represent network structure (i.e. host-parasitoid, exploitative competition, alternative host and a combination of exploitative competition and alternative host). We assembled nine different species combinations per community module in a laboratory experiment using a pool of three Drosophila hosts and three larval parasitoid species (Leptopilina sp., Ganaspis sp. and Asobara sp.). We compared host suppression and parasitoid performance across community modules and species assemblages to identify general effects linked to network structure and specific effects due to species community composition. We found that multiple parasitoid species enhanced host suppression due to sampling effect, weaker interspecific than intraspecific competition between parasitoids, and synergism. However, the effects of network structure on parasitoid performance were species specific and dependent on the identity of co-occurring species. Consequently, multiple parasitoid species generally strengthen top-down control, but the performance of the parasitoids depends on the identity of either the co-occurring parasitoid species, the alternative host species or both. Our results highlight the importance of preserving parasitoid diversity for ecosystem functioning and show that other effects depend on species community composition, and may therefore be altered by ongoing environmental changes.

More winners than losers over 12 years of monitoring tiger moths (Erebidae: Arctiinae) on Barro Colorado Island, Panama.

Understanding the causes and consequences of insect declines has become an important goal in ecology, particularly in the tropics, where most terrestrial diversity exists. Over the past 12 years, the ForestGEO Arthropod Initiative has systematically monitored multiple insect groups on Barro Colorado Island (BCI), Panama, providing baseline data for assessing long-term population trends. Here, we estimate the rates of change in abundance among 96 tiger moth species on BCI. Population trends of most species were stable (n = 20) or increasing (n = 62), with few (n = 14) declining species. Our analysis of morphological and climatic sensitivity traits associated with population trends shows that species-specific responses to climate were most strongly linked with trends. Specifically, tiger moth species that are more abundant in warmer and wetter years are more likely to show population increases. Our study contrasts with recent findings indicating insect decline in tropical and temperate regions. These results highlight the significant role of biotic responses to climate in determining long-term population trends and suggest that future climate changes are likely to impact tropical insect communities.

Effects of phenological mismatch under warming are modified by community context.

Climate change is altering the relative timing of species interactions by shifting when species first appear in communities and modifying the duration organisms spend in each developmental stage. However, community contexts, such as intraspecific competition and alternative resource species, can prolong shortened windows of availability and may mitigate the effects of phenological shifts on species interactions. Using a combination of laboratory experiments and dynamic simulations, we quantified how the effects of phenological shifts in Drosophila-parasitoid interactions differed with concurrent changes in temperature, intraspecific competition, and the presence of alternative host species. Our study confirmed that warming shortens the window of host susceptibility. However, the presence of alternative host species sustained interaction persistence across a broader range of phenological shifts than pairwise interactions by increasing the degree of temporal overlap with suitable development stages between hosts and parasitoids. Irrespective of phenological shifts, parasitism rates declined under warming due to reduced parasitoid performance, which limited the ability of community context to manage temporally mismatched interactions. These results demonstrate that the ongoing decline in insect diversity may exacerbate the effects of phenological shifts in ecological communities under future global warming temperatures.

The presence of multiple parasitoids decreases host survival under warming, but parasitoid performance also decreases.

Current global changes are reshaping ecological communities and modifying environmental conditions. We need to recognize the combined impact of these biotic and abiotic factors on species interactions, community dynamics and ecosystem functioning. Specifically, the strength of predator-prey interactions often depends on the presence of other natural enemies: it weakens with competition and interference or strengthens with facilitation. Such effects of multiple predators on prey are likely to be affected by changes in the abiotic environment, altering top-down control, a key structuring force in natural and agricultural ecosystems. Here, we investigated how warming alters the effects of multiple predators on prey suppression using a dynamic model coupled with empirical laboratory experiments with Drosophila-parasitoid communities. While multiple parasitoids enhanced top-down control under warming, parasitoid performance generally declined when another parasitoid was present owing to competitive interactions. This could reduce top-down control over multiple generations. Our study highlights the importance of accounting for interactive effects between abiotic and biotic factors to better predict community dynamics in a rapidly changing world and thus better preserve ecosystem functioning and services such as biological control.

DROP: Molecular voucher database for identification of Drosophila parasitoids.

Molecular identification is increasingly used to speed up biodiversity surveys and laboratory experiments. However, many groups of organisms cannot be reliably identified using standard databases such as GenBank or BOLD due to lack of sequenced voucher specimens identified by experts. Sometimes a large number of sequences are available, but with too many errors to allow identification. Here, we address this problem for parasitoids of Drosophila by introducing a curated open-access molecular reference database, DROP (Drosophila parasitoids). Identifying Drosophila parasitoids is challenging and poses a major impediment to realize the full potential of this model system in studies ranging from molecular mechanisms to food webs, and in biological control of Drosophila suzukii. In DROP, genetic data are linked to voucher specimens and, where possible, the voucher specimens are identified by taxonomists and vetted through direct comparison with primary type material. To initiate DROP, we curated 154 laboratory strains, 856 vouchers, 554 DNA sequences, 16 genomes, 14 transcriptomes, and six proteomes drawn from a total of 183 operational taxonomic units (OTUs): 114 described Drosophila parasitoid species and 69 provisional species. We found species richness of Drosophila parasitoids to be heavily underestimated and provide an updated taxonomic catalogue for the community. DROP offers accurate molecular identification and improves cross-referencing between individual studies that we hope will catalyse research on this diverse and fascinating model system. Our effort should also serve as an example for researchers facing similar molecular identification problems in other groups of organisms.

Experimental warming influences species abundances in a Drosophila host community through direct effects on species performance rather than altered competition and parasitism.

Global warming is expected to have direct effects on species through their sensitivity to temperature, and also via their biotic interactions, with cascading indirect effects on species, communities, and entire ecosystems. To predict the community-level consequences of global climate change we need to understand the relative roles of both the direct and indirect effects of warming. We used a laboratory experiment to investigate how warming affects a tropical community of three species of Drosophila hosts interacting with two species of parasitoids over a single generation. Our experimental design allowed us to distinguish between the direct effects of temperature on host species performance, and indirect effects through altered biotic interactions (competition among hosts and parasitism by parasitoid wasps). Although experimental warming significantly decreased parasitism for all host-parasitoid pairs, the effects of parasitism and competition on host abundances and host frequencies did not vary across temperatures. Instead, effects on host relative abundances were species-specific, with one host species dominating the community at warmer temperatures, irrespective of parasitism and competition treatments. Our results show that temperature shaped a Drosophila host community directly through differences in species' thermal performance, and not via its influences on biotic interactions.

Chemical cues and genetic divergence in insects on plants: conceptual cross pollination between mutualistic and antagonistic systems.

Cascading or reciprocal genetic diversification of herbivores, parasitoids, and pollinators can track chemotypic variation in host resources, and can lead to non-overlapping communities. Because plants simultaneously interact with both pollinators and herbivores, models investigating the genetic divergence of antagonistic herbivores and mutualistic pollinators should be merged in order to study how both processes interact using a common conceptual and methodological approach. We expect insects to mediate divergence in many systems, with outcomes depending on the level of pollinator or herbivore specialisation, and the relative selective pressures they impose. Applying approaches widely used to study insect pollinators, for example genomic tools and integration of behavioural, genetic and chemical data, to both pollinators and herbivores in the same system will facilitate our understanding of patterns of genetic divergence across multiple interacting species.

Simulated tri-trophic networks reveal complex relationships between species diversity and interaction diversity.

Most of earth's biodiversity is comprised of interactions among species, yet it is unclear what causes variation in interaction diversity across space and time. We define interaction diversity as the richness and relative abundance of interactions linking species together at scales from localized, measurable webs to entire ecosystems. Large-scale patterns suggest that two basic components of interaction diversity differ substantially and predictably between different ecosystems: overall taxonomic diversity and host specificity of consumers. Understanding how these factors influence interaction diversity, and quantifying the causes and effects of variation in interaction diversity are important goals for community ecology. While previous studies have examined the effects of sampling bias and consumer specialization on determining patterns of ecological networks, these studies were restricted to two trophic levels and did not incorporate realistic variation in species diversity and consumer diet breadth. Here, we developed a food web model to generate tri-trophic ecological networks, and evaluated specific hypotheses about how the diversity of trophic interactions and species diversity are related under different scenarios of species richness, taxonomic abundance, and consumer diet breadth. We investigated the accumulation of species and interactions and found that interactions accumulate more quickly; thus, the accumulation of novel interactions may require less sampling effort than sampling species in order to get reliable estimates of either type of diversity. Mean consumer diet breadth influenced the correlation between species and interaction diversity significantly more than variation in both species richness and taxonomic abundance. However, this effect of diet breadth on interaction diversity is conditional on the number of observed interactions included in the models. The results presented here will help develop realistic predictions of the relationships between consumer diet breadth, interaction diversity, and species diversity within multi-trophic communities, which is critical for the conservation of biodiversity in this period of accelerated global change.

Synchronous population dynamics in California butterflies explained by climatic forcing.

A long-standing challenge for population biology has been to understand why some species are characterized by populations that fluctuate in size independently, while populations of other species fluctuate synchronously across space. The effects of climatic variation and dispersal have been invoked to explain synchronous population dynamics, however an understanding of the relative influence of these drivers in natural populations is lacking. Here we compare support for dispersal- versus climate-driven models of interspecific variation in synchrony using 27 years of observations of 65 butterfly species at 10 sites spanning 2750 m of elevation in Northern California. The degree of spatial synchrony exhibited by each butterfly species was used as a response in a unique approach that allowed us to investigate whether interspecific variation in response to climate or dispersal propensity was most predictive of interspecific variation in synchrony. We report that variation in sensitivity to climate explained 50% of interspecific variation in synchrony, whereas variation in dispersal propensity explained 23%. Sensitivity to the El Niño Southern Oscillation, a primary driver of regional climate, was the best predictor of synchrony. Combining sensitivity to climate and dispersal propensity into a single model did not greatly increase model performance, confirming the primacy of climatic sensitivity for driving spatial synchrony in butterflies. Finally, we uncovered a relationship between spatial synchrony and population decline that is consistent with theory, but small in magnitude, which suggests that the degree to which populations fluctuate in synchrony is of limited use for understanding the ongoing decline of the Northern California butterfly fauna.

Global weather and local butterflies: variable responses to a large-scale climate pattern along an elevational gradient.

Understanding the spatial and temporal scales at which environmental variation affects populations of plants and animals is an important goal for modern population biology, especially in the context of shifting climatic conditions. The El Niño Southern Oscillation (ENSO) generates climatic extremes of interannual variation, and has been shown to have significant effects on the diversity and abundance of a variety of terrestrial taxa. However, studies that have investigated the influence of such large-scale climate phenomena have often been limited in spatial and taxonomic scope. We used 23 years (1988-2010) of a long-term butterfly monitoring data set to explore associations between variation in population abundance of 28 butterfly species and variation in ENSO-derived sea surface temperature anomalies (SSTA) across 10 sites that encompass an elevational range of 2750 m in the Sierra Nevada mountain range of California. Our analysis detected a positive, regional effect of increased SSTA on butterfly abundance (wetter and warmer years predict more butterfly observations), yet the influence of SSTA on butterfly abundances varied along the elevational gradient, and also differed greatly among the 28 species. Migratory species had the strongest relationships with ENSO-derived SSTA, suggesting that large-scale climate indices are particularly valuable for understanding biotic-abiotic relationships of the most mobile species. In general, however, the ecological effects of large-scale climatic factors are context dependent between sites and species. Our results illustrate the power of long-term data sets for revealing pervasive yet subtle climatic effects, but also caution against expectations derived from exemplar species or single locations in the study of biotic-abiotic interactions.

The global distribution of diet breadth in insect herbivores.

Understanding variation in resource specialization is important for progress on issues that include coevolution, community assembly, ecosystem processes, and the latitudinal gradient of species richness. Herbivorous insects are useful models for studying resource specialization, and the interaction between plants and herbivorous insects is one of the most common and consequential ecological associations on the planet. However, uncertainty persists regarding fundamental features of herbivore diet breadth, including its relationship to latitude and plant species richness. Here, we use a global dataset to investigate host range for over 7,500 insect herbivore species covering a wide taxonomic breadth and interacting with more than 2,000 species of plants in 165 families. We ask whether relatively specialized and generalized herbivores represent a dichotomy rather than a continuum from few to many host families and species attacked and whether diet breadth changes with increasing plant species richness toward the tropics. Across geographic regions and taxonomic subsets of the data, we find that the distribution of diet breadth is fit well by a discrete, truncated Pareto power law characterized by the predominance of specialized herbivores and a long, thin tail of more generalized species. Both the taxonomic and phylogenetic distributions of diet breadth shift globally with latitude, consistent with a higher frequency of specialized insects in tropical regions. We also find that more diverse lineages of plants support assemblages of relatively more specialized herbivores and that the global distribution of plant diversity contributes to but does not fully explain the latitudinal gradient in insect herbivore specialization.