Sexual attraction with pollination during feeding behaviour: implications for transitions between specialized strategies

Abstract

Background and aims: Understanding the origin of pollination by sexual deception has proven challenging, as sexually deceptive flowers are often highly modified, making it hard to resolve how any intermediate forms between sexual deception and an ancestral strategy might have functioned. Here, we report the discovery in Caladenia (Orchidaceae) of sexual attraction with pollination during feeding behaviour, which may offer important clues for understanding shifts in pollination strategy.

Methods: For Caladenia robinsonii, we observed the behaviour of its male wasp pollinator, Phymatothynnus aff. nitidus (Thynnidae), determined the site of release of the sexual attractant, and experimentally evaluated if the position of the attractant influences rates of attempted copulation and feeding behaviour. We applied GC-MS to test for surface sugar on the labellum. To establish if this pollination strategy is widespread in Caladenia, we conducted similar observations and experiments for four other Caladenia species.

Key results: In C. robinsonii, long-range sexual attraction of the pollinator is via semiochemicals emitted from the glandular sepal tips. Of the wasps landing on the flower, 57 % attempted copulation with the sepal tips, while 27 % attempted to feed from the base of the labellum, the behaviour associated with pollen transfer. A similar proportion of wasps exhibited feeding behaviour when the site of odour release was manipulated. A comparable pollination strategy occurs in another phylogenetically distinct clade of Caladenia.

Conclusions: We document a previously overlooked type of sexual deception for orchids involving long-distance sexual attraction, but with pollination occurring during feeding behaviour at the labellum. We show this type of sexual deception operates in other Caladenia species and predict that it is widespread across the genus. Our findings may offer clues about how an intermediate transitional strategy from a food-rewarding or food-deceptive ancestor operated during the evolution of sexual deception.

Keywords: Orchidaceae; Sexual deception; evolution; nectar; pollination.

Fig. 1.

Caladenia robinsonii showing the flower, nectar and attempted copulation by Phymatothynnus aff. nitidus. (A) A flower with floral parts labelled, (B) a close-up of the labellum, showing liquid that has been exuded onto the upper surface, and (C) male P. aff. nitidus attempting copulation with the clubs of a C. robinsonii flower. These clubs are the source of sexual attractant. Images (A) and (B) by Rod Peakall, and image (C) by Noushka Reiter.

Fig. 2.

A summary of pollination behaviour on Caladenia robinsonii illustrated using flow diagrams. Numbers represent the proportion of individuals transitioning from one behaviour to the next. Size of the circles represents the total number of individuals exhibiting that behaviour. (A) A summary across the control flowers for all experiments (the natural state), and (B) the experimental treatment when the source of the sexual attractant is moved under the labellum. A = approach only, L = landed, Cclubs = copulated with clubs, Clab = copulated with labellum, F = attempted to feed, pP = potential pollination (contacted the column). In the flow diagrams, data on the order of feeding and copulatory behaviour were extrapolated from the subset of observations where these details were recorded.

Fig. 3.

Summary of pollinator behaviour for each of the five study species. Column 1 – the proportion of individuals exhibiting copulatory behaviours per flower, with behaviours expressed in mutually exclusive categories: A = approached without landing; L = landed without exhibiting further behaviour; C = landed then copulated. Column 2 – the proportion of pollinators copulating with different floral parts. Column 3 – the proportion of pollinators engaging in copulatory and/or feeding behaviour: C only = copulation; C + F = copulation and feeding; F only = feeding. Column 4 – the proportion of individuals that potentially pollinated the flower (contact with the column) for different behaviours: C = copulation; C + F = copulation and feeding; F = feeding; N = no visible copulatory or feeding behaviour. Note, due to the low proportion of individuals potentially pollinating the flower (graphs in column 4), this axis is on a different scale to the graphs in columns 1–3. White diamonds represent the mean. Images by Rod Peakall.