Pollinator-mediated selfing in two deceptive orchids and a review of pollinium tracking studies addressing geitonogamy

Abstract

Among the factors thought to have favoured the evolution of deception (rewardlessness) in orchids is the reduction of pollinator-mediated selfing when unrewarded pollinators visit fewer flowers per inflorescence. We obtained data on natural levels of geitonogamy in the deceptive orchids Dactylorhiza sambucina and Himantoglossum hircinum by monitoring the dispersal and receipt of colour-coded pollinia. As donors, we marked 185 flowers of D. sambucina and 956 flowers of H. hircinum. In D. sambucina, 30% of the pollinator-visited flowers and 62% of the marked inflorescences experienced geitonogamous pollination events. In H. hircinum, the respective percentages were 36 and 71%. The furthest pollen transport distance in the Andrena-pollinated H. hircinum was 6.9 m (median 1.27 m), while the furthest transport in the bumblebee-pollinated D. sambucina was 176 m (median 1.23 m), a record in Orchidaceae. An analysis of pollen-tracking studies in orchids revealed geitonogamy levels of around 40% (based on individuals; 19-37% based on flowers) in both rewardless species and rewarding ones. This is similar to geitonogamy levels in other animal-pollinated angiosperms, although the data basis for comparison may still be too small. So far, however, it is not evident that rewardless orchids experience particularly low levels of geitonogamy.

Pollination ecology and the possible impacts of environmental change in the Southwest Australian Biodiversity Hotspot

“…Studies elsewhere directly tracking pollen and using molecular markers to assign pollen to parental plants have revealed that there is no simple dichotomy between bird pollination and insect pollination in terms of pollen movement, with several groups of insects moving pollen considerable distances (Nason et al 1998;Hanson et al 2008;Pasquet et al 2008). However, those species where small pollen movement distances have been reported are predominantly insect-pollinated herbs (Kropf & Renner 2008;Llaurens et al 2008).…”

Himantoglossum hircinum(Lizard Orchid) reviewed in the light of new morphological and molecular observations

“…In addition, Vöth (1990) argued that the dense papillae that partially obscure the spur entrance may secrete tiny drops of nectar, and several subsequent authors have also at least tentatively inferred the presence of a small nectar reward in H. hircinum (Neiland et al, 2001;Bournérias & Prat, 2005;Inda et al, 2012). In truth, such allegations could be levelled against any food-deceitful species of Orchidinae; there is little doubt that pollinators of Himantoglossum species receive no meaningful reward Kropf & Renner, 2008;Claessens & Kleynen, 2011;Bateman, 2013).…”

“…However, the occurrence of at least some geitonogamy (cross-pollination of genetically identical flowers occupying the same inflorescence) was confirmed long ago by the fact that even solitary flowering plants often set seed (Summerhayes, 1951). More recently, detailed observations by Kropf & Renner (2008) estimated a geitonogamy frequency of 36% in three populations of Lizard Orchid in southern Germany. As concluded by Kropf & 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 Renner (2006, p. 506), "foraging behaviour results in a mix of geitonogamy, nearneighbour pollination, and occasional long-distance outcrossing not fundamentally different from the situation in many other insect-pollinated perfect-flowered rewarding angiosperms."…”

“…In their comprehensive summary of pollinators of European orchid species, Claessens & Kleynen (2011) reported that 13 bee species (seven belonging to the genus Andrena: see also Teschner, 1980;Vöth, 1990;Kropf & Renner, 2008) and one species of Oedemera beetle have been observed removing pollinaria from plants of H. hircinum. Davies et al (1983) and suggested that flies or hoverflies may also act as pollinators; certainly, taxonomically broader spectra of pollinators have been recorded in other species of Himantoglossum (Delforge, 2006;Claessens & Kleynen, 2011).…”

“…There have been a few studies of pollination in H. hircinum but these include one that used this species as a model system for the study of geitonogamy -transfer of pollinaria between genetically identical flowers occupying the same inflorescence (Kropf & Renner, 2008). A few populations have also been subjected to unusually detailed studies of annual demographics (Carey, 1998(Carey, , 1999Heinrich, 2003;Pfeifer, 2004;Pfeifer et al, 2006a).…”