Anthropogenic influences of the functional efficiency of Australian insect antennae.

Particulate material (PM) derived from air pollution is a major risk factor affecting human health globally [1]. Industrial and automobile emissions are a major source of PM [2], as is the smoke from bushfires [3]. Research on air pollution has typically addressed its direct impact on human health. We take a novel perspective by considering the potential impact of air pollution on disrupting insect olfactory perception, which has significant practical implications: first, it may contribute to the global decline in insect populations [4], which may also have an impact on maintaining ecosystem services— through the regulation of pests and disease, crop pollination, and nutrient recycling [5]. The aim of this project was to investigate the impact of air pollution on insect olfactory perception by combining advanced aerodynamic simulation techniques with antennal morphology and behavioural assays of key insects of both economic and ecological significance.

Insects live in a sensory world dominated by odours, which are detected only when they physically interact with receptors, located on sensilla supported by the antennae. The factors that influence these odorant-receptor interactions are poorly understood, but presumably include odour chemistry and antennal morphology [6]. The very numerous olfactory (odour detecting) sensilla on insect antennae suggests there is little redundancy— every sensilla matters for odour detection. Indeed, insects frequently groom their antennae, apparently to improve olfactory detection [7], and ants with fewer sensilla fail to respond appropriately to social signals [8]. Perhaps the accumulation of PM on insect antennae similarly compromises their capacity to detect odours that reveal the source and nature of food, mates, and oviposition sites, thereby reducing the viability of insect populations and the provision of ecosystem services. While PM most commonly derives from urban environments, they can be dispersed far beyond the city boundaries. In Australia, bushfires may be a more significant source of PM than anthropogenic sources. Nevertheless, our understanding of the ecological impact of air pollution is confined to its effects on pheromone dispersal [9], but not detection.

Our research addressed two broad issues. First, to identify the nature of PM that is found on the antennae of insects; and second, to determine whether the ability of insects to detect odours and respond appropriately is compromised by the accumulation of PM deposits on the antennae. Our research, conducted in Australia and China, involved three model insect species (houseflies Musca domestica, honeybees Apis melliphera, and diamond back moths Plutella xylostella).

We obtained images of insect antennae using a scanning electron microscope (SEM), which revealed the nature of accumulated PM. The concentration of PM found on houseflies and moths collected from central Beijing is consistently higher on the antennae than other body parts, indicating that their olfactory function particularly may be compromised. We found PM on the antennae of several insects collected downwind of a Victorian bushfire, and subsequently found higher densities on the antennae of houseflies collected downwind than upwind of bushfires in Western Australia. The PM on the antennae of houseflies corresponded with their source, which in Beijing are dust, exhausts from motor vehicles, and heavy industry, while that on houseflies in WA were consistent with a bushfire source. In Beijing, contaminated antennae had a higher proportion of the smaller PM2.5 and a lower proportion of larger PM10 than expected from the proportion in the air. Smaller PM2.5 is common in bushfire smoke [3].

The rate of PM accumulation differed between flies and moths, whose antennae differ in both size and the presence of antennal scales. The rate of PM deposition on the small antennae of flies increases over time, but the effects of different densities of pollution are only seen for long exposure times. In contrast, while the rate of PM deposition on moth antennae, which have scales, similarly increases with exposure time, it is not affected by the level of air pollution.

We used a modelling technique called Computational Flow Dynamics (CFD) to investigate the process by which flies are contaminated by air borne PM. This showed that the location of the antennae on houseflies increases its efficiency in capturing both informative odour molecules in the air flow and PM. However, the exact level of contamination depends on both the probability of intercepting PM, and the microscopic interaction between PM and the surface of the insect. The force that PM interacts with the surface of the insect body can be measured using an Atomic Force Microscope (AFM). This revealed that silicate particles (a common PM species) have much higher attraction force to the antennae of flies, than to the scales of moth antenna. This means that fly antennae are more likely than moths to retain PM particles as they are encountered.

We confirmed experimentally that the accumulation of PM on the antennae of male and female houseflies compromised their ability to detect and respond to crucial chemical signals and cues. Using Y-maze behavioural assays, we discovered that uncontaminated houseflies and moths can identify the source of food and mate location odours. However, houseflies and moths contaminated by air pollution in Beijing, and houseflies contaminated by bushfire smoke failed to respond to these odours.

The differences in the response of contaminated and uncontaminated flies in the behavioural experiments reflected a diminished capacity to detect the odours, rather than a decline in physical activity level. Electroantennogram (EAG) assays revealed that the nervous response of houseflies to a key sex pheromone and food odour was much more prominent in uncontaminated than contaminated antennae.

Finally, we found little evidence that houseflies respond to air pollution by cleaning their antennae. Many insects clean their antennae using bristles on the front leg. SEM micrographs confirmed that a small amount of PM can be removed by grooming behaviour. Nevertheless, contaminated flies do not groom more frequently than uncontaminated flies. Perhaps grooming has little effect since the bristles on the tibia of flies are generally much wider than the size of PM.

References

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