Museum records indicate male bias in pollinators of sexually deceptive orchids.

Deception has evolved in a range of taxa. When deception imposes costs, yet persists over generations, exploited species typically have traits to help them bear or minimise costs. The sexually deceptive orchids, Cryptostylis spp., are pollinated by tricking male haplodiploid wasps (Lissopimpla excelsa) into mating with flowers, which offer no reward and often elicit sperm wastage. We hypothesise that by attracting haplodiploid species, orchids have a pollinator ideally suited to withstand the costs of sexual deception-and a selective advantage compared to other orchids. Haplodiploid females can reproduce with or without sperm-albeit when spermless, females can only have sons. Through orchid deception and sperm wastage, deceived haplodiploid populations could become male biased, providing enough males to share between orchids and females. In this way, pollinator populations can persist despite high densities of sexually deceptive orchids. Here, we aim to broadly test this prediction using museum and digital records of the pollinator, L. excelsa, from sites with or without orchids. For robustness, we also analyse the sex ratio of a sister ichneumonid species that occurs in the same areas but is not deceived by orchids. We found that at sites with orchids, L. excelsa was significantly more male biased than at sites without orchids and significantly more male biased than the sister ichneumonid. This survey is the first to test the population-level effects of sexually deceptive orchids on their pollinator. It supports our prediction that orchid deception can drive male-biased sex ratios in exploited pollinators.

Dung beetles in an avian-dominated island ecosystem: feeding and trophic ecology.

Globally, dung beetles (Scarabaeidae: Scarabaeinae) are linked to many critical ecosystem processes involving the consumption and breakdown of mammal dung. Endemic New Zealand dung beetles (Canthonini) are an anomaly, occurring at high abundance and low diversity on an island archipelago historically lacking terrestrial mammals, except bats, and instead dominated by birds. Have New Zealand's dung beetles evolved to specialise on bird dung or carrion, or have they become broad generalist feeders? We test dietary preferences by analysing nitrogen isotope ratios of wild dung beetles and by performing feeding behaviour observations of captive specimens. We also use nitrogen and carbon stable isotopes to determine if the dung beetle Saphobius edwardsi will consume marine-derived carrion. Nitrogen isotope ratios indicated trophic generalism in Saphobius dung beetles and this was supported by behavioural observations where a broad range of food resources were utilised. Alternative food resource use was further illustrated experimentally by nitrogen and carbon stable isotope signatures of S. edwardsi, where individuals provided with decomposed squid had δ(15)N and δ(13)C values that had shifted toward values associated with marine diet. Our findings suggest that, in the absence of native mammal dung resources, New Zealand dung beetles have evolved a generalist diet of dung and carrion. This may include marine-derived resources, as provided by the seabird colonies present in New Zealand forests before the arrival of humans. This has probably enabled New Zealand dung beetles to persist in indigenous ecosystems despite the decline of native birds and the introduction of many mammal species.

Colour mimicry and sexual deception by Tongue orchids (Cryptostylis).

Typically, floral colour attracts pollinators by advertising rewards such as nectar, but how does colour function when pollinators are deceived, unrewarded, and may even suffer fitness costs? Sexually deceptive orchids are pollinated only by male insects fooled into mating with orchid flowers and inadvertently transferring orchid pollinia. Over long distances, sexually deceptive orchids lure pollinators with counterfeit insect sex pheromones, but close-range deception with colour mimicry is a tantalising possibility. Here, for the first time, we analyse the colours of four sexually deceptive Cryptostylis orchid species and the female wasp they mimic (Lissopimpla excelsa, Ichneumonidae), from the perspective of the orchids' single, shared pollinator, male Lissopimpla excelsa. Despite appearing different to humans, the colours of the orchids and female wasps were effectively identical when mapped into a hymenopteran hexagonal colour space. The orchids and wasps reflected predominantly red-orange wavelengths, but UV was also reflected by raised bumps on two orchid species and by female wasp wings. The orchids' bright yellow pollinia contrasted significantly with their overall red colour. Orchid deception may therefore involve accurate and species-specific mimicry of wavelengths reflected by female wasps, and potentially, exploitation of insects' innate attraction to UV and yellow wavelengths. In general, mimicry may be facilitated by exploiting visual vulnerabilities and evolve more readily at the peripheries of sensory perception. Many sexually deceptive orchids are predominantly red, green or white: colours that are all potentially difficult for hymenoptera to detect or distinguish from the background.

Orchid sexual deceit provokes ejaculation.

Sexually deceptive orchids lure pollinators by mimicking female insects. Male insects fooled into gripping or copulating with orchids unwittingly transfer the pollinia. The effect of deception on pollinators has been considered negligible, but we show that pollinators may suffer considerable costs. Insects pollinating Australian tongue orchids (Cryptostylis species) frequently ejaculate and waste copious sperm. The costs of sperm wastage could select for pollinator avoidance of orchids, thereby driving and maintaining sexual deception via antagonistic coevolution or an arms race between pollinator learning and escalating orchid mimicry. However, we also show that orchid species provoking such extreme pollinator behavior have the highest pollination success. How can deception persist, given the costs to pollinators? Sexually-deceptive-orchid pollinators are almost exclusively solitary and haplodiploid species. Therefore, female insects deprived of matings by orchid deception could still produce male offspring, which may even enhance orchid pollination.

Orchid pollination by sexual deception: pollinator perspectives.

The extraordinary taxonomic and morphological diversity of orchids is accompanied by a remarkable range of pollinators and pollination systems. Sexually deceptive orchids are adapted to attract specific male insects that are fooled into attempting to mate with orchid flowers and inadvertently acting as pollinators. This review summarises current knowledge, explores new hypotheses in the literature, and introduces some new approaches to understanding sexual deception from the perspective of the duped pollinator. Four main topics are addressed: (1) global patterns in sexual deception, (2) pollinator identities, mating systems and behaviours, (3) pollinator perception of orchid deceptive signals, and (4) the evolutionary implications of pollinator responses to orchid deception, including potential costs imposed on pollinators by orchids. A global list of known and putative sexually deceptive orchids and their pollinators is provided and methods for incorporating pollinator perspectives into sexual deception research are provided and reviewed. At present, almost all known sexually deceptive orchid taxa are from Australia or Europe. A few sexually deceptive species and genera are reported for New Zealand and South Africa. In Central and Southern America, Asia, and the Pacific many more species are likely to be identified in the future. Despite the great diversity of sexually deceptive orchid genera in Australia, pollination rates reported in the literature are similar between Australian and European species. The typical pollinator of a sexually deceptive orchid is a male insect of a species that is polygynous, monandrous, haplodiploid, and solitary rather than social. Insect behaviours involved in the pollination of sexually deceptive orchids include pre-copulatory gripping of flowers, brief entrapment, mating, and very rarely, ejaculation. Pollinator behaviour varies within and among pollinator species. Deception involving orchid mimicry of insect scent signals is becoming well understood for some species, but visual and tactile signals such as colour, shape, and texture remain neglected. Experimental manipulations that test for function, multi-signal interactions, and pollinator perception of these signals are required. Furthermore, other forms of deception such as exploitation of pollinator sensory biases or mating preferences merit more comprehensive investigation. Application of molecular techniques adapted from model plants and animals is likely to deliver new insights into orchid signalling, and pollinator perception and behaviour. There is little current evidence that sexual deception drives any species-level selection on pollinators. Pollinators do learn to avoid deceptive orchids and their locations, but this is not necessarily a response specific to orchids. Even in systems where evidence suggests that orchids do interfere with pollinator mating opportunities, considerable further research is required to determine whether this is sufficient to impose selection on pollinators or generate antagonistic coevolution or an arms race between orchids and their pollinators. Botanists, taxonomists and chemical ecologists have made remarkable progress in the study of deceptive orchid pollination. Further complementary investigations from entomology and behavioural ecology perspectives should prove fascinating and engender a more complete understanding of the evolution and maintenance of such enigmatic plant-animal interactions.

Spider sex pheromones: emission, reception, structures, and functions.

Spiders and their mating systems are useful study subjects with which to investigate questions of widespread interest about sexual selection, pre- and post-copulatory mate choice, sperm competition, mating strategies, and sexual conflict. Conclusions drawn from such studies are broadly applicable to a range of taxa, but rely on accurate understanding of spider sexual interactions. Extensive behavioural experimentation demonstrates the presence of sex pheromones in many spider species, and recent major advances in the identification of spider sex pheromones merit review. Synthesised here are the emission, transmission, structures, and functions of spider sex pheromones, with emphasis on the crucial and dynamic role of sex pheromones in female and male mating strategies generally. Techniques for behavioural, chemical and electrophysiological study are summarised, and I aim to provide guidelines for incorporating sex pheromones into future studies of spider mating. In the spiders, pheromones are generally emitted by females and received by males, but this pattern is not universal. Female spiders emit cuticular and/or silk-based sex pheromones, which can be airborne or received via contact with chemoreceptors on male pedipalps. Airborne pheromones primarily attract males or elicit male searching behaviour. Contact pheromones stimulate male courtship behaviour and provide specific information about the emitter's identity. Male spiders are generally choosy and are often most attracted to adult virgin females and juvenile females prior to their final moult. This suggests the first male to mate with a female has significant advantages, perhaps due to sperm priority patterns, or mated female disinterest. Both sexes may attempt to control female pheromone emission, and thus dictate the frequency and timing of female mating, reflecting the potentially different costs of female signalling and/or polyandry to both sexes. Spider sex pheromones are likely to be lipids or lipid soluble, may be closely related to primary metabolites, and are not necessarily species specific, although they can still assist with species recognition. Newer electrophysiological techniques coupled with chemical analyses assist with the identification of sex pheromone compounds. This provides opportunities for more targeted behavioural experimentation, perhaps with synthetic pheromones, and for theorising about the biosynthesis and evolution of chemical signals generally. Given the intriguing biology of spiders, and the critical role of chemical signals for spiders and many other animal taxa, a deeper understanding of spider sex pheromones should prove productive.