Carbonyl products of ozone oxidation of volatile organic compounds can modulate olfactory choice behavior in insects.

Insects are a diverse group of organisms that provide important ecosystem services like pollination, pest control, and decomposition and rely on olfaction to perform these services. In the Anthropocene, increasing concentrations of oxidant pollutants such as ozone have been shown to corrupt odor-driven behavior in insects by chemically degrading e.g. flower signals or insect pheromones. The degradation, however, does not only result in a loss of signals, but also in a potential enrichment of oxidation products, predominantly small carbonyls. Whether and how these oxidation products affect insect olfactory perception remains unclear. We examined the effects of ozone-generated small carbonyls on the olfactory behavior of the vinegar fly Drosophila melanogaster. We compiled a broad collection of neurophysiologically relevant odorants for the fly from databases and literature and predicted the formation of the types of stable small carbonyl products resulting from the odorant's oxidation by ozone. Based on these predictions, we evaluated the olfactory detection and behavioral impact of the ten most frequently predicted carbonyl products in the fly using single sensillum recordings (SSRs) and behavioral tests. Our results demonstrate that the fly's olfactory system can detect the oxidation products, which then elicit either attractive or neutral behavioral responses, rather than repulsion. However, certain products alter behavioral choices to an attractive odor source of balsamic vinegar. Our findings suggest that the enrichment of small carbonyl oxidation products due to increased ozone levels can affect olfactory guided insect behavior. Our study underscores the implications for odor-guided foraging in insects and the essential ecosystem services they offer under carbonyl enriched environments.

Functional Interaction Between Drosophila Olfactory Sensory Neurons and Their Support Cells.

Insects detect volatile chemicals using antennae, which house a vast variety of olfactory sensory neurons (OSNs) that innervate hair-like structures called sensilla where odor detection takes place. In addition to OSNs, the antenna also hosts various support cell types. These include the triad of trichogen, tormogen, and thecogen support cells that lie adjacent to their respective OSNs. The arrangement of OSN supporting cells occurs stereotypically for all sensilla and is widely conserved in evolution. While insect chemosensory neurons have received considerable attention, little is known about the functional significance of the cells that support them. For instance, it remains unknown whether support cells play an active role in odor detection, or only passively contribute to homeostasis, e.g., by maintaining sensillum lymph composition. To investigate the functional interaction between OSNs and support cells, we used optical and electrophysiological approaches in Drosophila. First, we characterized the distribution of various supporting cells using genetic markers. By means of an ex vivo antennal preparation and genetically-encoded Ca2+ and K+ indicators, we then studied the activation of these auxiliary cells during odor presentation in adult flies. We observed acute responses and distinct differences in Ca2+ and K+ fluxes between support cell types. Finally, we observed alterations in OSN responses upon thecogen cell ablation in mature adults. Upon inducible ablation of thecogen cells, we notice a gain in mechanical responsiveness to mechanical stimulations during single-sensillum recording, but a lack of change to the neuronal resting activity. Taken together, these results demonstrate that support cells play a more active and responsive role during odor processing than previously thought. Our observations thus reveal that support cells functionally interact with OSNs and may be important for the extraordinary ability of insect olfactory systems to dynamically and sensitively discriminate between odors in the turbulent sensory landscape of insect flight.

Staying in the club: Exploring criteria governing metacommunity membership for obligate symbionts under host-symbiont feedback.

Metacommunity membership is influenced by habitat availability and trophic requirements. However, for multitrophic horizontally transmitted symbiont communities that are closely associated with hosts, symbiont-host interactions may affect membership criteria in novel ways. For example, failure of beneficial services from symbionts could influence the host, and in turn, the entire community. Understanding such host-symbiont feedback effects on symbiont community membership, symbiont community structure, and function is important for understanding if host-symbiont communities are fundamentally different from more traditional ecological communities. We investigate the membership criteria for a multitrophic insect symbiont community that colonizes host inflorescences at specific developmental stages termed colonization windows. The inflorescences serve as microcosm habitats. Symbionts exhibit a range of interactions from mutualism to parasitism. Hosts exhibit feedback by aborting inflorescences not pollinated by mutualistic symbionts. Habitats are consequently lost for all other symbiont species in such host-derived organs whose development is mutualist-dependent. Using empirical measurements to characterize inflorescence development, we simulate symbiont dispersal colonization across hosts. We vary host densities and lengths of symbiont colonization windows, and track the persistence of each symbiont species in the metacommunity based on its trophic requirements and resource availability within the microcosm. Since the persistence of the microcosm habitat is dictated by pollination performed by the mutualist, the mutualist fared better than all other symbionts. The length of symbiont colonization windows was positively related with colonization success and symbiont persistence. The cumulative length of the colonization windows of prey dictated predator success; diet breadth or prey colonization success did not influence predator persistence. Predators also had a greater host-plant density requirement than prey for persistence in the community. These results offer valuable insights into host densities required for maintaining symbionts, and have implications for multitrophic symbiont community stability. Special constraints can govern symbiont community membership, function and structure and symbiont persistence when host-symbiont feedback impacts host microcosm development.

Resource dispersion influences dispersal evolution of highly insulated insect communities.

Communities in which species are obligately associated with a single host are ideal to test adaptive responses of community traits to host-imposed selection because such communities are often highly insulated. Fig species provide oviposition resources to co-evolved fig-wasp communities. Dispersing fig-wasp communities move from one host plant to another for oviposition. We compared the spatial dispersion of two fig species and the dispersal capacities of their multitrophic wasp communities. Dispersal capacities were assessed by measuring vital dispersal correlates, namely tethered flight durations, somatic lipid contents and resting metabolic rates. We suggest that dispersal-trait distributions of congeneric wasp species across the communities are an adaptive response to host plant dispersion. Larger dispersal capacities of the entire multitrophic community are related to more widely dispersed resources. Our results provide evidence and a novel perspective for understanding the potential role of adaptation in whole-community dispersal-trait distributions.

Life-history strategy, resource dispersion and phylogenetic associations shape dispersal of a fig wasp community.

BACKGROUND: The combined influence of life-history strategy and resource dispersion on dispersal evolution of a biological community, and by extension, on community assemblage, has received sparse attention. Highly specialized fig wasp communities are ideal for addressing this question since the life-history strategies that affect their pace of life and the dispersion of their oviposition resources vary. We compared dispersal capacities of the wasp community of a widespread tropical fig, Ficus racemosa, by measuring flight durations, somatic lipid content and resting metabolic rates. RESULTS: Wasp species exhibiting greater flight durations had higher energy reserves and resting metabolic rates. "Fast"-paced species showed higher dispersal capacities reflecting requirements for rapid resource location within short adult lifespans. Longer-lived "slow"-paced species exhibited lower dispersal capacities. Most dispersal traits were negatively related with resource dispersion while their variances were positively related with this variable, suggesting that resource dispersion selects for dispersal capacity. Dispersal traits exhibited a phylogenetic signal. CONCLUSIONS: Using a combination of phylogeny, trait functionality and community features, we explain how dispersal traits may have co-evolved with life-history strategies in fig wasps and influenced a predisposition for dispersal. We speculate how processes influencing dispersal trait expression of community members may affect resource occupancy and community assemblage.

High temperatures result in smaller nurseries which lower reproduction of pollinators and parasites in a brood site pollination mutualism.

In a nursery pollination mutualism, we asked whether environmental factors affected reproduction of mutualistic pollinators, non-mutualistic parasites and seed production via seasonal changes in plant traits such as inflorescence size and within-tree reproductive phenology. We examined seasonal variation in reproduction in Ficus racemosa community members that utilise enclosed inflorescences called syconia as nurseries. Temperature, relative humidity and rainfall defined four seasons: winter; hot days, cold nights; summer and wet seasons. Syconium volumes were highest in winter and lowest in summer, and affected syconium contents positively across all seasons. Greater transpiration from the nurseries was possibly responsible for smaller syconia in summer. The 3-5°C increase in mean temperatures between the cooler seasons and summer reduced fig wasp reproduction and increased seed production nearly two-fold. Yet, seed and pollinator progeny production were never negatively related in any season confirming the mutualistic fig-pollinator association across seasons. Non-pollinator parasites affected seed production negatively in some seasons, but had a surprisingly positive relationship with pollinators in most seasons. While within-tree reproductive phenology did not vary across seasons, its effect on syconium inhabitants varied with season. In all seasons, within-tree reproductive asynchrony affected parasite reproduction negatively, whereas it had a positive effect on pollinator reproduction in winter and a negative effect in summer. Seasonally variable syconium volumes probably caused the differential effect of within-tree reproductive phenology on pollinator reproduction. Within-tree reproductive asynchrony itself was positively affected by intra-tree variation in syconium contents and volume, creating a unique feedback loop which varied across seasons. Therefore, nursery size affected fig wasp reproduction, seed production and within-tree reproductive phenology via the feedback cycle in this system. Climatic factors affecting plant reproductive traits cause biotic relationships between plants, mutualists and parasites to vary seasonally and must be accorded greater attention, especially in the context of climate change.