Pollinator attractiveness increases with distance from flowering orchids

Abstract

Orchids are extraordinary among plants because many species are pollinated through sexual duplicity by producing flowers that mimic female insects to lure unsuspecting males. Previous work showed that sexual deception by the orchid Chiloglottis trapeziformis can have a negative impact on its wasp pollinator Neozeleboria cryptoides. We report that female wasps may be capable of mitigating the cost of the orchids' deception. Although male wasps quickly habituated to areas planted with unrewarding flower decoys, we found that the effectiveness of the chemical cue used by the wingless females to attract males increases with increasing distance from an orchid patch. The apparent specif icity of the males' sitebased avoidance strategy means that females emerging in areas occupied by flowering orchids could, potentially, leave the orchid colony by walking to increase their attractiveness.

Deceptive Behavior in Plants. I. Pollination by Sexual Deception in Orchids: A Host–Parasite Perspective

“…From recent studies on the mating behavior of solitary bees and wasps, we now know that female insects attract patrolling males by releasing specific chemical compounds (either in blends or specific compounds) that are capable of triggering genuine copulation attempts by the male insects when tested for their attractiveness on dummies. Besides, comparative analyses of the orchids' floral scent and the female insect sex pheromone have shown that the parasitic orchids use the same odor compounds as the females to deceive the males into pollinating the flowers (Schiestl et al 1999Ayasse et al 2003 ;Schiestl 2004 ;Mant et al 2005a ;Vereecken and Schiestl 2008) . In short, this interaction seems to constitute an illustrative case of mimicry that is primarily mediated by chemical signals.…”

“…a The orchid parasite attracts its male insect host briefly without an attempt at copulation ( Pterostylis ; Taylor 1999 ; Lehnebach et al 2005) ; b The orchid parasite attracts its male insect host and triggers inspection behavior or a precopulatory routine ( Caladenia , Chiloglottis , Drakaea ;Peakall 1990 ;Peakall and Handel 1993 ;Schiestl 2004 ;Dickson and Petit 2006) ; c The orchid parasite triggers a host copulation attempt only ( Ophrys : Darwin 1862 ; Correvon and Pouyanne 1916 ;Kullenberg 1961 ;Ayasse et al 1997 ;Neiland and Wilcock 1998 ;Ayasse et al 2000 ;Vandewoestijne et al 2008 ;Vereecken, unpublished data;Geoblasta : Ciotek et al 2006) ; d The orchid parasite triggers host copulation attempt and ejaculation ( Cryptostylis: Schiestl et al 2004;Gaskett and Herberstein 2006 ;Gaskett et al 2008) . (Modified from Gaskett et al 2008) …”

“…In a series of experiments, Wong and Schiestl (2002) provided evidence that the hosts (males of the Thynnine wasp Neozeleboria cryptoides ) learn to avoid their associated orchid parasite ( Chiloglottis trapeziformis ) after subsequent and unsuccessful copulation attempts, and that the hosts' wingless females experience a significant decrease in attractiveness when they are "calling" for mates from inside an orchid patch (Wong and Schiestl 2002) . The female wasps are only capable of restoring their original attractiveness towards the hosts as the distance between their calling spot and the parasite colony increases (Wong et al 2004) . In another recent study on the ichneumonid host Lissopimpla excelsa and its orchid parasites Cryptostylis erecta and C. leptochila from Australia , Gaskett et al (2008) confirmed Coleman's (1928 earlier findings that the hosts regularly ejaculate in the flowers during pseudocopulations.…”

Floral Scent Emission and Pollination Syndromes: Evolutionary Changes from Food to Sexual Deception

“…Higher outcrossing rates might be particularly advantageous to orchids because the packaging of pollen into pollinia effects high pollination efficiency in a single transfer, thus rendering orchids susceptible to geitonogamy and inbreeding depression. Comparative studies on outcrossing rates between food-deceptive and sexually deceptive species are lacking, but studies on thynnine wasp behavior have shown that males show an explicit site-based avoidance strategy after unsuccessful visits to female flower decoys (Peakall 1990;Wong et al 2004). This strategic avoidance of orchid patches might result in higher outcrossing rates in sexually deceptive species in comparison with food-deceptive ones, where foodseeking insects are duped and search for another nectar or pollen source (Peakall and Beattie 1996).…”

On the success of a swindle: pollination by deception in orchids

“…if the wingless females of the pollinator species are unable to obtain a mate when calling from within a patch of orchids (Wong and Schiestl 2002). The model may therefore be selected to avoid orchids, and field experiments suggest that females can respond by walking out of an orchid patch, which will resume their attractiveness for males (Wong et al 2004). Walking a few meters after unsuccessful calling may have evolved specifically in species exploited by orchids, however, experimental tests are lacking.…”