Implications of pollination by food and sexual deception for pollinator specificity, fruit set, population genetics and conservation of Caladenia (Orchidaceae)
Ryan D. Phillips A B G , Renate Faast C , Colin C. Bower D , Graham R. Brown E and Rod Peakall FA Kings Park and Botanic Gardens, The Botanic Gardens and Parks Authority, West Perth, WA 6005, Australia.
B School of Plant Biology, The University of Western Australia, Crawley, WA 6009, Australia.
C School of Earth and Environmental Sciences, The University of Adelaide, Adelaide, SA 5005, Australia.
D Florasearch, PO Box 300, Orange, NSW 2800, Australia.
E Museum and Art Gallery of the Northern Territory, GPO Box 4646, Darwin, NT 0801, Australia.
F School of Botany and Zoology, The Australian National University, Canberra, ACT 0200, Australia.
G Corresponding author. Email: Ryan.Phillips@bgpa.wa.gov.au
Australian Journal of Botany 57(4) 287-306 https://doi.org/10.1071/BT08154
Submitted: 17 August 2008 Accepted: 3 February 2009 Published: 29 July 2009
Abstract
Caladenia is very unusual in that it contains species that attract pollinators by two different strategies, food and sexual deception. Among the sexually deceptive species, baiting for pollinators has shown that within populations orchid species are typically pollinated by a single species of thynnine wasp. However, some wasp species can be pollinators of more than one species of orchid usually when their ranges do not overlap. There is a trend for closely related orchids to exploit wasps from the same genus, with different lineages of orchids often pollinated by different genera. Very little is known about pollination of food-deceptive Caladenia species, although it is evident they attract a suite of generalist food-seeking insects. Food-deceptive species have a higher pollination rate than do sexually deceptive species. Studies of population genetics and pollen movements are few, although they suggest a pattern of fine-scale genetic structuring within populations, owing to predominantly restricted seed dispersal and low genetic differentiation among populations as a consequence of rare long-distance seed-dispersal events. Both evolutionary and ecological research of Caladenia will greatly benefit from a better understanding of the insect species involved in pollination, their ecological requirements and the ecological and genetic consequences of food and sexual deception.
Acknowledgements
R. D. Phillips was supported by an Australian Postgraduate Award. Fieldwork by R. D. Phillips was undertaken with financial support of the Australian Orchid Foundation, the Holsworth Wildlife Research Endowment and the School of Plant Biology at the University of Western Australia. Thanks go to Jon See, Nigel Swarts and Eric Chapman for assistance with fieldwork and Andrew Brown, Kingsley Dixon and Steve Hopper for their advice and encouragement. R. Faast was supported by a Faculty of Sciences Divisional Scholarship from The University of Adelaide and an Australian Research Council Linkage Project grant (LP 0560578) with the Department for Environment and Heritage SA, the South Australian Museum, Foundation for Australia’s Most Endangered Species and Biocity Centre for Urban Habitats, University of Adelaide. Thanks go to José Facelli and Andrew Austin for advice and guidance. C. C. Bower received financial support for field studies from the Australian Orchid Foundation. R. Peakall was supported by an Australian Research Council (ARC) Discovery Project grant (DP0451374) and the Australian National University.
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 |
Adams PB,
Bartareau T, Walker KL
(1992) Pollination of Australian orchids by Trigona (Tetragona) jurine bees (Hymenoptera: Apidae). Australian Entomological Magazine 19, 97–101.
Aizen MA, Feinsinger P
(1994) Habitat fragmentation, native insect pollinators, and feral honey bees in Argentina ‘Chaco Serrano’. Ecological Applications 4, 378–392.
| Crossref | GoogleScholarGoogle Scholar |
Aizen MA,
Ashworth L, Leonardo G
(2002) Reproductive success in fragmented habitats: do compatability systems and pollination specialization matter? Journal of Vegetation Science 13, 885–892.
| Crossref | GoogleScholarGoogle Scholar |
Alcock J
(1981) Notes on the reproductive behaviour of some Australian thynnine wasps (Hymenoptera: Tiphiidae). Journal of the Kansas Entomological Society 54, 681–693.
Alcock J
(2000) Interactions between the sexually deceptive orchid Spiculaea ciliata and its wasp pollinator Thynnoturneria sp. (Hymenoptera: Thynninae). Journal of Natural History 34, 629–636.
| Crossref | GoogleScholarGoogle Scholar |
Alcock J, Gwynne DT
(1987) Courtship feeding and mate choice in thynnine wasps (Hymenoptera: Tiphiidae). Australian Journal of Zoology 35, 451–458.
| Crossref | GoogleScholarGoogle Scholar |
Anderson B, Johnson SD
(2006) The effects of floral mimics and models on each others’ fitness. Proceedings of the Royal Society B: Biological Sciences 273, 969–974.
| Crossref |
Ashworth L,
Aguilar R,
Galetto L, Aizen MA
(2004) Why do pollination generalist and specialist plant species show similar reproductive susceptibility to habitat fragmentation? Journal of Ecology 92, 717–719.
| Crossref | GoogleScholarGoogle Scholar |
Bates R
(1978) Pollination of orchids – Part 9. Self pollination. Journal of the Native Orchid Society of South Australia 3, 7–8.
Bates R
(1982) Observations of pollen vectors on Caladenia congesta R.Br. Journal of the Native Orchid Society of South Australia 6, 37–38.
Bates R
(1984a) The ecology and biology of Caladenia rigida (Orchidaceae). South Australian Naturalist 56–59, 63–65. 58,
Bates R
(1984b) Pollination of Caladenia: an overview. Orchadian 7, 269–270.
Bates R
(1996a) Little known South Australian Spider Orchids. Orchadian 12, 29–32.
Batty AL,
Dixon KW,
Brundrett M, Sivasithamparan K
(2001) Constraints to symbiotic germination of terrestrial orchid seed in a mediterranean bushland. New Phytologist 152, 511–520.
| Crossref | GoogleScholarGoogle Scholar |
Bernhardt P
(1987) A comparison of the diversity, density, and foraging behavior of bees and wasps on Australian Acacia. Annals of the Missouri Botanical Garden 74, 42–50.
| Crossref | GoogleScholarGoogle Scholar |
Bickerton D
(1997b) A pollination study of the endangered orchid Caladenia rigida. Part 3: Pollinators. Journal of the Native Orchid Society of South Australia 21, 74–75.
Bower CC
(1992) The use of pollinators in the taxonomy of sexually deceptive orchids in the subtribe Caladeniinae (Orchidaceae). Orchadian 10, 331–338.
Bower CC
(1996) Demonstration of pollinator-mediated reproductive isolation in sexually deceptive species of Chiloglottis (Orchidaceae: Calademiiae). Australian Journal of Botany 44, 15–33.
| Crossref | GoogleScholarGoogle Scholar |
Bower CC
(2006) Specific pollinators reveal a cryptic taxon in the bird orchid, Chiloglottis valida sensu lato (Orchidaceae) in south-eastern Australia. Australian Journal of Botany 54, 53–64.
| Crossref | GoogleScholarGoogle Scholar |
Bower CC, Brown GR
(1997) Hidden biodiversity: detection of cryptic thynnine wasp species using sexually deceptive, female-mimicking orchids. Memoirs of the Museum of Victoria 56, 461–466.
Brown GR
(1993) A new species of Lestricothynnus with notes on miscoupling in Thynninae (Hymenoptea: Tiphiidae). Journal of the Australian Entomological Society 32, 197–199.
| Crossref | GoogleScholarGoogle Scholar |
Brown GR
(1995a) New synonyms and combinations in the genus Zeleboria Saussure (Hymenoptera: Tiphiidae). General and Applied Entomology 26, 9–12.
Brown GR
(1995b) Revision of the Australian wasp genus Macrothynnus Turner (Hymenoptera: Tiphiidae: Thynninae). Records of the Western Australian Museum 17, 267–275.
Brown GR
(1997a) Chilothynnus, a new genus of Australian Thynninae (Hymenoptera: Tiphiidae) associated with orchids. The Beagle. Records of the Museums and Art Galleries of the Northern Territory 13, 61–71.
Brown GR
(1997b) The identity of Aeolothynnus Ashmead and notes on Iswaroides Ashmead (Hymenoptera: Tiphiidae: Thynninae). Australian Entomologist 24, 87–92.
Brundrett MC,
Scade A,
Batty AL,
Dixon KW, Sivasithamparam K
(2003) Development of in situ and ex situ seed baiting techniques to detect mycorrhizal fungi from terrestrial orchid habitats. Mycological Research 107, 1210–1220.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Burrell RW
(1935) Notes on the habits of certain Australian Thynnidae. New York Entomological Society Journal 43, 19–29.
Chung MY,
Nason JD, Chung MG
(2005) Spatial genetic structure in populations of the terrestrial orchid Orchis cyclochila (Orchidaceae). Plant Systematics and Evolution 254, 209–219.
| Crossref | GoogleScholarGoogle Scholar |
Cunningham SA
(2000) Depressed pollination in habitat fragments causes low fruit set. Proceedings of the Royal Society of London. Series B. Biological Sciences 267, 1149–1152.
| 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 |
Devey DS,
Bateman RM,
Fay MF, Hawkins JA
(2008) Friends or relatives? Phylogenetics and species delimitation in the controversial European orchid genus Ophrys. Annals of Botany 101, 385–402.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Diez JM
(2007) Hierarchical patterns of symbiotic orchid germination linked to adult plant proximity and environmental gradients. Journal of Ecology 95, 159–170.
| Crossref | GoogleScholarGoogle Scholar |
Dixon KW, Tremblay RL
(2009) Biology and natural history of Caladenia. Australian Journal of Botany in press. 57,
Ebert D, Peakall R
(2009a) A new set of universal de novo sequencing primers for extensive coverage of non-coding chloroplast DNA: new opportunities for phylogenetic studies and cpSSR discovery. Molecular Ecology Resources in press. ,
| Crossref | GoogleScholarGoogle Scholar |
Ebert D, Peakall R
(2009b) Chloroplast simple sequence repeats (cpSSRs): technical resources and recommendations for expanding cpSSR discovery and applications to a wide array of plant species. Molecular Ecology Resources in press. ,
| Crossref | GoogleScholarGoogle Scholar |
Ebert D,
Hayes C, Peakall R
(2009) Chloroplast simple sequence repeat (cpSSRs) markers for evolutionary studies in the sexually deceptive orchid genus Chiloglottis. Molecular Ecology Resources in press. ,
| Crossref | GoogleScholarGoogle Scholar |
Elliott CP, Ladd PG
(2002) Pollen limitation of fruit set in Western Australian terrestrial orchids. Journal of the Royal Society of Western Australia 85, 165–168.
Faast R,
Farrington L,
Faceli JM, Austin AD
(2009) Bees and white spiders: unraveling the pollination syndrome of Caladenia rigida (Orchidaceae). Australian Journal of Botany 57, 315–325.
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.
| Crossref | GoogleScholarGoogle Scholar |
Fritz A-L, Nilsson LA
(1994) How pollinator-mediated mating varies with population size in plants. Oecologia 100, 451–462.
| Crossref | GoogleScholarGoogle Scholar |
Gaskett AC,
Winnick CG, Herberstein ME
(2008) Orchid sexual deceit provokes ejaculation. American Naturalist 171, E206–E212.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gumbert A, Kunze J
(2001) Colour similarity to rewarding model plants affects pollination in a food deceptive orchid, Orchis boryi. Biological Journal of the Linnean Society 72, 419–433.
| Crossref | GoogleScholarGoogle Scholar |
Hopper SD, Brown AP
(2001) Contributions to Western Australian orchidology: 2. New taxa and circumscriptions in Caladenia. Nuytsia 14, 27–308.
Hopper SD, Brown AP
(2004) Robert Brown’s Caladenia revisited, including a revision of its sister genera Cyanicula, Ericksonella and Pheladenia (Caladeniinae: Orchidaceae). Australian Systematic Botany 17, 171–240.
| Crossref | GoogleScholarGoogle Scholar |
Hopper SD, Brown AP
(2006) Australia’s wasp-pollinated flying duck orchids revised (Paracaleana: Orchidaceae). Australian Systematic Botany 19, 211–244.
| Crossref |
Hopper SD, Brown AP
(2007) A revision of Australia’s hammer orchids (Drakaea: Orchidaceae), with some field data on species-specific sexually deceived wasp pollinators. Australian Systematic Botany 20, 252–285.
| Crossref | GoogleScholarGoogle Scholar |
Hopper SD, Gioia P
(2004) The southwest Australian floristic region: Evolution and conservation of a global diversity hotspot. Annual Review of Ecology Evolution and Systematics 35, 623–650.
| Crossref |
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 |
Internicola AI,
Juillet N,
Smithson A, Gigord LDB
(2006) Experimental investigation of the effect of spatial aggregation on reproductive success in a rewardless orchid. Oecologia 150, 435–441.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Internicola AI,
Page PA,
Bernasconi G, Gigord L
(2007) Competition for pollinator visitation between deceptive and rewarding artificial inflorescences: an experimental test of the effects of floral colour similarity and spatial mingling. Functional Ecology 21, 864–872.
| Crossref | GoogleScholarGoogle Scholar |
Johnson SD,
Neal PR, Harder LD
(2005) Pollen fates and the limits on male reproductive success in an orchid population. Biological Journal of the Linnean Society 86, 175–190.
| Crossref | GoogleScholarGoogle Scholar |
Johnson SD,
Peter CI,
Nilsson LA, Ågren J
(2003) Pollination success in a deceptive orchid is enhanced by co-occurring rewarding magnet plants. Ecology 84, 2919–2927.
| Crossref | GoogleScholarGoogle Scholar |
Juillet N,
Gonzalez MA,
Page PA, Gigord LDB
(2007) Pollination of the European food deceptive Traunsteinera globosa (Orchidaceae): the importance of nectar-producing neighbouring plants. Plant Systematics and Evolution 265, 123–129.
| Crossref | GoogleScholarGoogle Scholar |
Kropf M, Renner SS
(2008) Pollinator-mediated selfing in two deceptive orchids and a review of pollinium tracking studies addressing geitonogamy. Oecologia 155, 497–508.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kruess A, Tscharntke T
(2000) Species richness and parasitism in a fragmented landscape: experiments and field studies with insects on Vicia sepium. Oecologia 122, 129–137.
| Crossref | GoogleScholarGoogle Scholar |
Kunze J, Gumbert A
(2001) The combined effect of color and odor on flower choice behavior of bumble bees in flower mimicry systems. Behavioral Ecology 12, 447–456.
| Crossref | GoogleScholarGoogle Scholar |
Lammi A, Kuitunen MT
(1995) Deceptive pollination of Dactylorhiza incarnata: an experimental test of the magnet species hypothesis. Oecologia 101, 500–503.
| Crossref | GoogleScholarGoogle Scholar |
Laurance WF
(1994) Rain-forest fragmentation and the structure of small mammal communities in tropical Queensland. Biological Conservation 69, 23–32.
| Crossref | GoogleScholarGoogle Scholar |
Laverty TM
(1992) Plant interactions for pollinator visits: a test of the magnet species effect. Oecologia 89, 502–508.
Mant JG,
Schiestl FP,
Peakall R, Weston PH
(2002) A phylogenetic study of pollinator conservatism among sexually deceptive orchids. Evolution 56, 888–898.
| PubMed |
Mant J,
Bower CC,
Weston PH, Peakall R
(2005a) Phylogeography of pollinator-specific sexually deceptive Chiloglottis taxa (Orchidaceae): evidence for sympatric divergence? Molecular Ecology 14, 3067–3076.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mant J,
Brown GR, Weston PH
(2005b) Opportunistic pollinator shifts among sexually deceptive orchids indicated by a phylogeny of pollinating and non-pollinating thynnine wasps (Tiphiidae). Biological Journal of the Linnean Society 86, 381–395.
| Crossref | GoogleScholarGoogle Scholar |
Mant J,
Peakall R, Schiestl FP
(2005c) Does selection on floral odor promote differentiation among populations and species of the sexually deceptive orchid genus Ophrys? Evolution 59, 1449–1463.
| PubMed |
McElhinny C,
Gibbons P,
Brack C, Bauhus J
(2006) Fauna-habitat relationships: a basis for identifying key stand structural attributes in temperate Australian eucalypt forests and woodlands. Pacific Conservation Biology 12, 90–110.
Neiland MRM, 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 |
Paulus HF, Gack C
(1990) Pollination of Ophrys (Orchidaceae) in Cyprus. Plant Systematics and Evolution 169, 177–207.
| Crossref | GoogleScholarGoogle Scholar |
Pauw A
(2007) Collapse of a pollination web in small conservation areas. Ecology 88, 1759–1769.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Peakall R
(1989a) A new technique for monitoring pollen flow in orchids. Oecelogia 79, 361–365.
| Crossref | GoogleScholarGoogle Scholar |
Peakall R
(1989b) The unique pollination of Leporella fimbriata (Orchidaceae): pollination by pseudocopulating male ants (Myrmecia urens, Formicidae). Plant Systematics and Evolution 167, 137–148.
| 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
(2007) Speciation in the Orchidaceae: confronting the challenges. Molecular Ecology 16, 2834–2837.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 |
Peakall R, Handel SN
(1993) Pollinators discriminate among heights of a sexually deceptive orchid: implications for selection. Evolution 47, 1681–1687.
| Crossref | GoogleScholarGoogle Scholar |
Peakall R, Schiestl FP
(2004) A mark-recapture study of male Colletes cunicularius bees: implications for pollination by sexual deception. Behavioral Ecology and Sociobiology 56, 579–584.
| Crossref | GoogleScholarGoogle Scholar |
Peakall R,
Beattie AJ, James SH
(1987) Pseudocopulation of an orchid by male ants: a test of two hypotheses accounting for the rarity of ant pollination. Oecologica 73, 522–524.
| Crossref | GoogleScholarGoogle Scholar |
Peakall R,
Bower CC,
Logan AE, Nicol HI
(1997) Confirmation of the hybird origin of Chiloglottis × perscottiana (Orchidaceae: Diuridae). 1. Genetic and morphological evidence. Australian Journal of Botany 45, 839–855.
| Crossref | GoogleScholarGoogle Scholar |
Peakall R,
Jones L,
Bower CC, Mackey BG
(2002) Bioclimatic assessment of the geographic and climatic limits to hybridisation in a sexually deceptive orchid system. Australian Journal of Botany 50, 21–30.
| Crossref | GoogleScholarGoogle Scholar |
Petit S, Dickson CR
(2005) Grass tree (Xanthorrhoea semiplana, Liliaceae) facilitation of the endangered pink-lipped spider orchid (Caladenia syn. Arachnorchis behrii, Orchidaceae) varies in South Australia. Australian Journal of Botany 53, 455–464.
| Crossref | GoogleScholarGoogle Scholar |
Phillips RD,
Backhouse G,
Brown AP, Hopper SD
(2009) Biogeography of Caladenia (Orchidaceae), with special reference to the Southwest Australian Floristic Region. Australian Journal of Botany 57, 259–275.
Ridsdill Smith TJ
(1970a) The biology of Hemithynnus hyalinatus (Hymenoptera: Tiphiidae), a parasite on scarabaeid larvae. Journal of the Australian Entomological Society 9, 183–195.
| Crossref | GoogleScholarGoogle Scholar |
Ridsdill Smith TJ
(1970b) The behaviour of Hemithynnus hyalinatus (Hymenoptera: Tiphiidae), with notes on some other Thynninae. Journal of the Australian Entomological Society 9, 196–208.
| Crossref | GoogleScholarGoogle Scholar |
Salzmann CC,
Brown A, Schiestl FP
(2006) Floral scent emission and pollination syndromes: Evolutionary changes from food to sexual deception. International Journal of Plant Sciences 167, 1197–1204.
| Crossref | GoogleScholarGoogle Scholar |
Salzmann CC,
Nardella AM,
Cozzolino S, Schiestl FP
(2007) Variability in floral scent in rewarding and deceptive orchids: the signature of pollinator-imposed selection? Annals of Botany 100, 757–765.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schemske DW
(1980) Evolution of floral display in the orchid Brassavola nodosa. Evolution 34, 489–493.
| Crossref | GoogleScholarGoogle Scholar |
Schiestl FP, Peakall R
(2005) Two orchids attract different pollinators with the same floral odour compound: ecological and evolutionary implications. Functional Ecology 19, 674–680.
| Crossref | GoogleScholarGoogle Scholar |
Schiestl FP,
Peakall R, Mant J
(2004) Chemical communication in the sexually deceptive orchid genus Cryptostylis. Botanical Journal of the Linnean Society 144, 199–205.
| Crossref | GoogleScholarGoogle Scholar |
Schiestl FP,
Ayasse M,
Paulus HF,
Lofstedt C,
Hansson BS,
Ibarra F, Francke W
(1999) Orchid pollination by sexual swindle. Nature 399, 421–422.
| Crossref | GoogleScholarGoogle Scholar |
Schiestl FP,
Peakall R,
Mant JG,
Ibarra F,
Schulz C,
Franke S, Francke W
(2003) The chemistry of sexual deception in an orchid–wasp pollination system. Science 302, 437–438.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Smouse PE, Peakall R
(1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82, 561–573.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Smouse PE, Sork VL
(2004) Measuring pollen flow in forest trees: an exposition of alternative approaches. Forest Ecology and Management 197, 21–38.
| Crossref | GoogleScholarGoogle Scholar |
Sork VL,
Nason J,
Campbell DR, Fernandez JF
(1999) Landscape approaches to historical and contemporary gene flow in plants. Trends in Ecology & Evolution 14, 219–224.
| Crossref | GoogleScholarGoogle Scholar |
Stoutamire WP
(1975) Pseudocopulation in Australian terrestrial orchids. American Orchid Society Bulletin 44, 226–233.
Stoutamire WP
(1983) Wasp-pollinated species of Caladenia (Orchidaceae) in south-western Australia. Australian Journal of Botany 31, 383–394.
| Crossref | GoogleScholarGoogle Scholar |
Swarts ND,
Sinclair EA,
Krauss SL, Dixon KW
(2008) Genetic diversity in fragmented populations of the critically endangered spider orchid Caladenia huegelii: implications for conservation. Conservation Genetics Published online 28 August 2008. ,
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Trapnell DW, Hamrick JL
(2004) Partitioning nuclear and chloroplast variation at multiple spatial scales in the neotropical epiphytic orchid, Laelia rubescens. Molecular Ecology 13, 2655–2666.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 |
Ulherr J
(1967) A note on the pollination of Caladenia alba R.Br. Orchadian 2, 94–108.
Watson JEM,
Whittaker RJ, Freudenberger D
(2005) Bird community responses to habitat fragmentation: how consistent are they across landscapes? Journal of Biogeography 32, 1353–1370.
Wooller RD,
Russel EM,
Renfree MB, Towers PA
(1983) A comparison of seasonal changes in the pollen loads of nectarivorous marsupials and birds. Australian Wildlife Research 10, 311–317.
| Crossref | GoogleScholarGoogle Scholar |