Context and the functional use of information in insect sensory ecology.

Context-specific behaviors emerge from the interaction between an animal's internal state and its external environment. Although the importance of context is acknowledged in the field of insect sensory ecology, there is a lack of synthesis on this topic stemming from challenges in conceptualizing 'context'. We address this challenge by gleaning over the recent findings on the sensory ecology of mosquitoes and other insect pollinators. We discuss internal states and their temporal dynamics, from those lasting minutes to hours (host-seeking) to those lasting days to weeks (diapause, migration). Of the many patterns reviewed, at least three were common to all taxa studied. First, different sensory cues gain prominence depending on the insect's internal state. Second, similar sensory circuits between related species can result in different behavioral outcomes. And third, ambient conditions can dramatically alter internal states and behaviors.

Cone humidity is a strong attractant in an obligate cycad pollination system.

Studies of pollination biology often focus on visual and olfactory aspects of attraction, with few studies addressing behavioral responses and morphological adaptation to primary metabolic attributes. As part of an in-depth study of obligate nursery pollination of cycads, we find that Rhopalotria furfuracea weevils show a strong physiological response and behavioral orientation to the cone humidity of the host plant Zamia furfuracea in an equally sensitive manner to their responses to Z. furfuracea-produced cone volatiles. Our results demonstrate that weevils can perceive fine-scale differences in relative humidity (RH) and that individuals exhibit a strong behavioral preference for higher RH in binary choice assays. Host plant Z. furfuracea produces a localized cloud of higher than ambient humidity around both pollen and ovulate cones, and R. furfuracea weevils preferentially land at the zone of maximum humidity on ovulate cones, i.e., the cracks between rows of megasporophylls that provide access to the ovules. Moreover, R. furfuracea weevils exhibit striking antennal morphological traits associated with RH perception, suggesting the importance of humidity sensing in the evolution of this insect lineage. Results from this study suggest that humidity functions in a signal-like fashion in this highly specialized pollination system and help to characterize a key pollination-mediating trait in an ancient plant lineage.

A signal-like role for floral humidity in a nocturnal pollination system.

Previous studies have considered floral humidity to be an inadvertent consequence of nectar evaporation, which could be exploited as a cue by nectar-seeking pollinators. By contrast, our interdisciplinary study of a night-blooming flower, Datura wrightii, and its hawkmoth pollinator, Manduca sexta, reveals that floral relative humidity acts as a mutually beneficial signal in this system. The distinction between cue- and signal-based functions is illustrated by three experimental findings. First, floral humidity gradients in Datura are nearly ten-fold greater than those reported for other species, and result from active (stomatal conductance) rather than passive (nectar evaporation) processes. These humidity gradients are sustained in the face of wind and are reconstituted within seconds of moth visitation, implying substantial physiological costs to these desert plants. Second, the water balance costs in Datura are compensated through increased visitation by Manduca moths, with concomitant increases in pollen export. We show that moths are innately attracted to humid flowers, even when floral humidity and nectar rewards are experimentally decoupled. Moreover, moths can track minute changes in humidity via antennal hygrosensory sensilla but fail to do so when these sensilla are experimentally occluded. Third, their preference for humid flowers benefits hawkmoths by reducing the energetic costs of flower handling during nectar foraging. Taken together, these findings suggest that floral humidity may function as a signal mediating the final stages of floral choice by hawkmoths, complementing the attractive functions of visual and olfactory signals beyond the floral threshold in this nocturnal plant-pollinator system.

Mutualism has its limits: consequences of asymmetric interactions between a well-defended plant and its herbivorous pollinator.

Concern for pollinator health often focuses on social bees and their agricultural importance at the expense of other pollinators and their ecosystem services. When pollinating herbivores use the same plants as nectar sources and larval hosts, ecological conflicts emerge for both parties, as the pollinator's services are mitigated by herbivory and its larvae are harmed by plant defences. We tracked individual-level metrics of pollinator health-growth, survivorship, fecundity-across the life cycle of a pollinating herbivore, the common hawkmoth, Hyles lineata, interacting with a rare plant, Oenothera harringtonii, that is polymorphic for the common floral volatile (R)-(-)-linalool. Linalool had no impact on floral attraction, but its experimental addition suppressed oviposition on plants lacking linalool. Plants showed robust resistance against herbivory from leaf-disc to whole-plant scales, through poor larval growth and survivorship. Higher larval performance on other Oenothera species indicates that constitutive herbivore resistance by O. harringtonii is not a genus-wide trait. Leaf volatiles differed among populations of O. harringtonii but were not induced by larval herbivory. Similarly, elagitannins and other phenolics varied among plant tissues but were not herbivore-induced. Our findings highlight asymmetric plant-pollinator interactions and the importance of third parties, including alternative larval host plants, in maintaining pollinator health. This article is part of the theme issue 'Natural processes influencing pollinator health: from chemistry to landscapes'.

The roles of vision and antennal mechanoreception in hawkmoth flight control.

Flying animals need continual sensory feedback about their body position and orientation for flight control. The visual system provides essential but slow feedback. In contrast, mechanosensory channels can provide feedback at much shorter timescales. How the contributions from these two senses are integrated remains an open question in most insect groups. In Diptera, fast mechanosensory feedback is provided by organs called halteres and is crucial for the control of rapid flight manoeuvres, while vision controls manoeuvres in lower temporal frequency bands. Here, we have investigated the visual-mechanosensory integration in the hawkmoth Macroglossum stellatarum. They represent a large group of insects that use Johnston's organs in their antennae to provide mechanosensory feedback on perturbations in body position. Our experiments show that antennal mechanosensory feedback specifically mediates fast flight manoeuvres, but not slow ones. Moreover, we did not observe compensatory interactions between antennal and visual feedback.

Spatial Representation of Feeding and Oviposition Odors in the Brain of a Hawkmoth.

Female hawkmoths, Manduca sexta, use olfactory cues to locate nectar sources and oviposition sites. We investigated if the behavioral significance of odorants is represented already in the antennal lobe, the first olfactory neuropil of the insect's brain. Using in vivo calcium imaging, we first established a functional map of the dorsal surface of the antennal lobe by stimulating the moths with 80 ecologically relevant and chemically diverse monomolecular odorants. We were able to address 23 olfactory glomeruli, functional subunits of the antennal lobe, in each individual female. Next, we studied the relevance of the same odorants with two-choice experiments (odorant versus solvent) in a wind tunnel. Depending on odorant identity, naive moths made attempts to feed or to oviposit at the scented targets. A correlation of wind tunnel results with glomerular activation patterns revealed that feeding and oviposition behaviors are encoded in the moth's antennal lobe by the activation of distinct groups of glomeruli.