Bees and white spiders: unravelling the pollination syndrome of Caladenia rigida (Orchidaceae)
Renate Faast A C , Lachlan Farrington A B , José M. Facelli A C and Andrew D. Austin A BA School of Earth and Environmental Sciences, The University of Adelaide, SA 5005, Australia.
B Australian Centre for Evolutionary Biology and Biodiversity, The University of Adelaide, SA 5005, Australia.
C Corresponding authors. Email: renate.faast@adelaide.edu.au or jose.facelli@adelaide.edu.au
Australian Journal of Botany 57(4) 315-325 https://doi.org/10.1071/BT08135
Submitted: 30 July 2008 Accepted: 5 February 2009 Published: 29 July 2009
Abstract
Orchids of the genus Caladenia have been shown to utilise two quite different pollination strategies, namely species-specific sexual deception of thynnine wasps and a more generalist strategy attracting a larger spectrum of foraging insects. While baiting techniques have enabled the identification of numerous pollinators of sexually deceptive Caladenia, insects that pollinate food-advertising species have received little attention. The present study employed a multidisciplinary approach to better evaluate the pollination syndrome of the white spider orchid, Caladenia rigida R.S.Rogers, a species previously reported to utilise both food and sexual deception. This included the observation and capture of potential pollinators of C. rigida through direct observation, pantraps, Malaise traps and pollinator-baiting experiments, and the use of molecular techniques to identify orchid pollinia isolated from carrier insects. We describe a suite of generalist insects visiting and bearing pollinia from C. rigida. In addition, samples collected from the labellum and column of C. rigida contained sugars at levels comparable to those of a known nectar-producing orchid, Microtis parviflora R.Br. Potential osmophores in the clubs and calli stained positively with neutral red and although this character is often associated with sexual deception, we found no evidence for this secondary pollination syndrome in C. rigida. The present study is the first one to provide a detailed description of the pollinators and pollination syndrome of a non-sexually deceptive species within the genus Caladenia and the first report to provide evidence of nectar production by a species within this genus.
Acknowledgements
We thank Ken Walker (Museum of Victoria) and Remko Leijs (South Australian Museum) for identification of bees and David Yeates (CSIRO, Canberra) and John Jennings (University of Adelaide) for fly identification. John Conran and Helen Brown (University of Adelaide) assisted with nectar chromatography and Sally Thompson helped with fieldwork. Joe Quarmby and Bob Bates provided locations of orchid populations and Jackie Crompton and Monique Blason arranged access to Forestry SA and SA Water reserves, respectively. We thank two anonymous reviewers for helpful comments on this manuscript. This research was made possible by funding received from the Native Vegetation Council, South Australia and an Australian Research Council Linkage Project (LP0560578) with the Department for Environment and Heritage South Australia, South Australian Museum, Foundation for Australia’s Most Endangered Species and Biocity Centre for Urban Habitats, University of Adelaide. The first author held a Faculty of Sciences Divisional Scholarship from The University of Adelaide.
Adams PB, Lawson SD
(1993) Pollination in Australian orchids: a critical assessment of the literature 1882–1992. Australian Journal of Botany 41, 553–575.
| Crossref | GoogleScholarGoogle Scholar |
Ascensao L,
Francisco A,
Cotrim H, Salome M
(2005) Comparative structure of the labellum in Ophrys fusca and O. lutea (Orchidaceae). American Journal of Botany 92, 1059–1067.
| Crossref | GoogleScholarGoogle Scholar |
Bates R
(1982) Observation of pollen vectors on Caladenia congesta R.Br. Journal of Native Orchid Society of South Australia 6, 37–38.
Bates R
(1984a) The ecology and biology of Caladenia rigida (Orchidaceae). South Australian Naturalist 58, 56–65.
Bates R
(1984b) Pollination of Caladenia: an overview. Orchadian 7, 269–270.
Bates R
(1984c) Pollination of Prasophyllum elatum R.Br. (with notes on associated biology). Orchadian 10, 14–17.
Bates R
(1985) Extra-floral nectaries, pseudo-nectaries and vestigial nectar-spurs in Dipodium punctatum R.Br. Journal of Native Orchid Society of South Australia 9, 7–8.
Beardsell DV,
Clements MA,
Hutchinson JF, Williams EG
(1986) Pollination of Diuris maculata R.Br. (Orchidaceae) by floral mimicry of the native legumes Daviesia spp. and Pultenaea scrabra R.Br. Australian Journal of Botany 34, 165–173.
| Crossref | GoogleScholarGoogle Scholar |
Bernhardt P, Burns-Balogh P
(1986a) Observations of the floral biology of Prasophyllum odoratum (Orchidaceae, Spiranthoideae). Plant Systematics and Evolution 153, 65–76.
| Crossref | GoogleScholarGoogle Scholar |
Bernhardt P, Burns-Balogh P
(1986b) Floral mimesis in Thelymitra nuda (Orchidaceae). Plant Systematics and Evolution 151, 187–202.
| Crossref | GoogleScholarGoogle Scholar |
Bond WJ
(1994) Do mutualisms matter? Assessing the impact of pollinator and disperser disruption on plant extinction. Philosophical Transactions of the Royal Society of London. Series B 344, 83–90.
| Crossref | GoogleScholarGoogle Scholar |
Bower CC
(1996) Demonstration of pollinator-mediated reproductive isolation in sexually deceptive species of Chiloglottis (Orchidaceae: Caladeniinae). Australian Journal of Botany 44, 15–33.
| Crossref | GoogleScholarGoogle Scholar |
Dafni A, Bernhardt P
(1990) Pollination of terrestrial orchids of southern Australia and the Mediterranean region: Systematic, ecological, and evolutionary implications. Evolutionary Biology 24, 193–253.
Dafni A, Calder DM
(1987) Pollination by deceit and floral mimesis in Thelymitra antennifera (Orchidaceae). Plant Systematics and Evolution 158, 11–22.
| Crossref | GoogleScholarGoogle Scholar |
Davies KL,
Stpiczynska M, Gregg A
(2005) Nectar-secreting floral stomata in Maxillaria anceps Ames & C.Schweinf. (Orchidaceae). Annals of Botany 96, 217–227.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Davies KL, Turner MP
(2004) Morphology of floral papillae in Maxillaria Ruiz & Pav. (Orchidaceae). Annals of Botany 93, 75–86.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Davis AR
(1997) Influence of floral visitation on nectar-sugar composition and nectary surface changes in Eucalyptus. Apidologie 28, 27–42.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Dickson CR, Petit S
(2006) Effect of individual height and labellum colour on the pollination of Caladenia (syn. Arachnorchis) behrii (Orchidaceae) in the northern Adelaide region, South Australia. Plant Systematics and Evolution 262, 65–74.
| Crossref | GoogleScholarGoogle Scholar |
Farrington L,
Macgillivray P,
Faast R, Austin AD
(2009) Investigating DNA barcoding options for the identification of Caladenia (Orchidaceae) species. Australian Journal of Botany 57, 276–286.
Ferdy JB,
Austerlitz F,
Moret J,
Gouyon PH, Godelle B
(1999) Pollinator-induced density dependence in deceptive species. Oikos 87, 549–560.
| Crossref | GoogleScholarGoogle Scholar |
Hopper SD, Brown AP
(2001) Contributions to Western Australian orchidology: 2. New taxa and circumscriptions in Caladenia. Nuytsia 14, 27–308.
Indsto JO,
Weston PH,
Clements MA,
Dyer AG,
Batley M, Whelan RJ
(2006) Pollination of Diuris maculata (Orchidaceae) by male Trichocolletes venustus bees. Australian Journal of Botany 54, 669–679.
| Crossref | GoogleScholarGoogle Scholar |
Indsto JO,
Weston PH,
Clements MA, Dyer AG
(2007) Generalised pollination of Diuris alba (Orchidaceae) by small bees and wasps. Australian Journal of Botany 55, 628–634.
| Crossref | GoogleScholarGoogle Scholar |
Irwin RE,
Adler LS, Brody AK
(2004) The dual role of floral traits: pollinator attraction and plant defense. Ecology 85, 1503–1511.
| Crossref | GoogleScholarGoogle Scholar |
Ivri Y, Dafni A
(1977) The pollination ecology of Epipactis consimilis Don (Orchidaceae) in Israel. New Phytologist 79, 173–177.
| Crossref | GoogleScholarGoogle Scholar |
Jersakova J, Johnson SD
(2006) Lack of floral nectar reduces self-pollination in a fly-pollinated orchid. Oecologia 147, 60–68.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kevan PG, Baker HG
(1983) Insects as flower visitors and pollinators. Annual Review of Entomology 28, 407–453.
| Crossref | GoogleScholarGoogle Scholar |
Makino TT, Sakai S
(2007) Experience changes pollinator responses to floral display size: from size-based to reward-based foraging. Functional Ecology 21, 854–863.
| Crossref | GoogleScholarGoogle Scholar |
Murza GL, Davis AR
(2003) Comparative flower structure of three species of sundew (Drosera anglica, Drosera linearis, and Drosera rotundifolia) in relation to breeding system. Canadian Journal of Botany 81, 1129–1142.
| Crossref | GoogleScholarGoogle Scholar |
Neiland MR, Wilcock CC
(1998) Fruit set, nectar reward, and rarity in the Orchidaceae. American Journal of Botany 85, 1657–1671.
| Crossref | GoogleScholarGoogle Scholar |
Nilsson LA
(1992) Orchid pollination biology. Trends in Ecology & Evolution 7, 255–259.
| Crossref | GoogleScholarGoogle Scholar |
Ordano M, Ornelas JF
(2005) The cost of nectar replenishment in two epiphytic bromeliads. Journal of Tropical Ecology 21, 541–547.
| Crossref | GoogleScholarGoogle Scholar |
Peakall R
(1989) A new technique for monitoring pollen flow in orchids. Oecologia 79, 361–365.
| Crossref | GoogleScholarGoogle Scholar |
Peakall R
(1990) Responses of male Zaspilothynnus trilobatus Turner wasps to females and the sexually deceptive orchid it pollinates. Functional Ecology 4, 159–167.
| Crossref | GoogleScholarGoogle Scholar |
Peakall R, Beattie AJ
(1989) Pollination of the orchid Microtis parviflora R.Br. by flightless worker ants. Functional Ecology 3, 515–522.
| Crossref | GoogleScholarGoogle Scholar |
Peakall R, Beattie AJ
(1996) Ecological and genetic consequences of pollination by sexual deception in the orchid Caladenia tentaculata. Evolution 50, 2207–2220.
| Crossref | GoogleScholarGoogle Scholar |
Percival MS
(1961) Types of nectar in angiosperms. New Phytologist 60, 235–281.
| Crossref | GoogleScholarGoogle Scholar |
Phillips R,
Faast R,
Bower CC,
Brown GR, Peakall R
(2009) Implications of pollination by food and sexual deception for pollinator specificity, fruit set, population genetics and conservation of Caladenia (Orchidaceae). Australian Journal of Botany 57, 287–306.
Pyke GH
(1991) What does it cost a plant to produce floral nectar? Nature 350, 58–59.
| Crossref | GoogleScholarGoogle Scholar |
Rymer PD,
Whelan RJ,
Ayre DJ,
Weston PH, Russell KG
(2005) Reproductive success and pollinator effectiveness differ in common and rare Persoonia species (Proteaceae). Biological Conservation 123, 521–532.
| Crossref | GoogleScholarGoogle Scholar |
Sih A, Baltus M
(1987) Patch size, pollinator behaviour, and pollinator limitation in catnip. Ecology 68, 1679–1690.
| Crossref | GoogleScholarGoogle Scholar |
Smithson A
(2005) Pollinator limitation and inbreeding depression in orchid species with and without nectar rewards. New Phytologist 169, 419–430.
| Crossref |
Smithson A, Gigord LDB
(2001) Are there fitness advantages in being a rewardless orchid? Reward supplementation experiments with Barlia robertiana. Proceedings of the Royal Society of London. Series B. Biological Sciences 268, 1435–1441.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Stern WL,
Curry KJ, Whitten WM
(1986) Staining fragrance glands in orchid flowers. Bulletin of the Torrey Botanical Club 113, 288–297.
| Crossref | GoogleScholarGoogle Scholar |
Stoutamire WP
(1979) Australian terrestrial orchids, thynnid wasps, and pseudocopulation. Orchadian 6, 110–111.
Stoutamire WP
(1983) Wasp-pollinated species of Caladenia (Orchidaceae) in south-western Australia. Australian Journal of Botany 31, 383–394.
| Crossref | GoogleScholarGoogle Scholar |
Stpiczynska M,
Davies KL, Gregg A
(2004) Nectary structure and nectar secretion in Maxillaria coccinea (Jacq.) L.O.Williams ex Hodge (Orchidaceae). Annals of Botany 93, 87–95.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Sugiura N
(1996) Pollination of the orchid Epipactis thunbergii by syrphid flies (Diptera: Syrphidae). Ecological Research 11, 249–255.
| Crossref | GoogleScholarGoogle Scholar |
Townes H
(1972) A lightweight malaise trap. Entomological News 83, 239–247.
Tremblay RL,
Ackerman JD,
Zimmerman JK, Calvo RN
(2005) Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biological Journal of the Linnean Society 84, 1–54.
| Crossref | GoogleScholarGoogle Scholar |
Turner D, Conran JG
(2004) The reproductive ecology of two naturalised Erica species (Ericaceae) in the Adelaide hills: the rise and fall of two ‘would-be’ weeds? Transactions of the Royal Society of South Australia 128, 23–31.
Weston PH,
Perkins AJ, Entwisle TJ
(2005) More than symbioses: orchid ecology, with examples from the Sydney Region. Cunninghamia 9, 1–15.
Widmer A,
Cozzolino S,
Pellegrino G,
Soliva M, Dafni A
(2000) Molecular analysis of orchid pollinaria and pollinaria-remains found on insects. Molecular Ecology 9, 1911–1914.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wong BB, Schiestl FP
(2002) How an orchid harms its pollinator. Proceedings of the Royal Society of London. Series B. Biological Sciences 269, 1529–1532.
| Crossref | GoogleScholarGoogle Scholar |
