Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
Shopping Cart: ( empty )
You are here: Home > Journals > BT > BT23110
RESEARCH ARTICLE (Open Access)
Contents Vol 72(5)

Pollination by multiple species of nectar foraging Hymenoptera in Prasophyllum innubum, a critically endangered orchid of the Australian Alps

Tobias Hayashi A B C # , Bronwyn M. Ayre https://orcid.org/0000-0001-7553-3491 A B # , Björn Bohman D E , Graham R. Brown F G H , Noushka Reiter https://orcid.org/0000-0001-8450-2769 A B C and Ryan D. Phillips https://orcid.org/0000-0002-3777-9260 A B *
+ Author Affiliations
- Author Affiliations

A Department of Environment and Genetics and the Research Centre for Future Landscapes, La Trobe University, Melbourne, Vic, Australia.

B Royal Botanic Gardens Victoria, Science Division, Corner of Ballarto Road and Botanic Drive, Cranbourne, Vic 3977, Australia.

C Ecology and Evolution, Research School of Biology, The Australian National University, Canberra, ACT 2600, Australia.

D School of Molecular Sciences, The University of Western Australia, Crawley, WA, Australia.

E Department of Plant Protection Biology, Swedish University of Agricultural Sciences, Lomma, Sweden.

F Natural Sciences, Museum and Art Gallery of the Northern Territory, GPO Box 4646, Darwin, NT 0801, Australia.

G CSIRO Land and Water, Private Mail Bag 44, Winnellie, NT 0822, Australia.

H Research Institute for Environment and Livelihoods, Charles Darwin University, Darwin, NT 0909, Australia.

* Correspondence to: R.Phillips@latrobe.edu.au

Handling Editor: James Camac

Australian Journal of Botany 72, BT23110 https://doi.org/10.1071/BT23110
Submitted: 21 December 2023  Accepted: 11 June 2024  Published: 8 July 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context

Australia has numerous threatened species of terrestrial orchid, with a particularly high incidence of rarity in the genus Prasophyllum R.Br. Although there has been research on mycorrhizal associations and propagation, little is known about the reproductive ecology of threatened Prasophyllum. Understanding which animals are responsible for pollination and the impact of herbivores on reproduction may inform conservation actions.

Aims

For the nationally Critically Endangered Prasophyllum innubum, we aimed to determine the pollinator species, test for self-pollination, quantify levels of reproductive success and herbivory, and identify herbivores.

Methods

Pollinator observations were undertaken at wild populations of P. innubum, whereas an experiment testing for self-pollination was undertaken in shadehouse conditions. We quantified reproductive success and herbivory at two populations and attempted to identify herbivores using game cameras.

Key results

Pollination occurred via three species of bee and a sphecid wasp, all of which attempted feeding on floral nectar. Fruit set averaged 72–84% at wild sites, whereas only 6% of flowers set fruit via self-pollination when insects were excluded. Just 4% of inflorescences were completely consumed by herbivores, and no herbivory was captured on camera.

Conclusions

P. innubum has a generalist rewarding pollination system that confers high levels of reproductive success, with herbivory having little impact on reproduction.

Implications

Pollinator availability is unlikely to restrict conservation translocation site selection of P. innubum because of a generalist pollination system. If herbivores are a threat for this species, it is likely to be through alteration of habitat rather than direct grazing.

Keywords: Australia, conservation, Halictidae, Hymenoptera, Lasioglossum, orchid, pollination, Prasophyllum, reproduction, Specidae.

References

Ackerman JD, Montalvo AM (1990) Short- and long-term limitations to fruit production in a tropical orchid. Ecology 71, 263-272.
| Crossref | Google Scholar |

Ackerman JD, Phillips RD, Tremblay RL, Karremans A, Reiter N, Peter CI, Bogarín D, Perez-Escobar OA, Liu H (2023) Beyond the various contrivances by which orchids are pollinated: global patterns in orchid pollination biology. Botanical Journal of the Linnean Society 202, 295-324.
| Crossref | Google Scholar |

Antonelli A, Dahlberg CJ, Carlgren KHI, Appelqvist T (2009) Pollination of the Lady’s slipper orchid (Cypripedium calceolus) in Scandinavia – taxonomic and conservational aspects. Nordic Journal of Botany 27, 266-273.
| Crossref | Google Scholar |

Atlas of Living Australia (2023) Atlas of Living Australia – species: Lasioglossum (Paraspechodes) altichum. Available at https://biocache.ala.org.au/occurrences/search?q=lsid:https://biodiversity.org.au/afd/taxa/321afe67-1274-470c-8ec9-1b0968a5f188#tab_chartsView

Australian Government (2023) Species Profile and Threats Database – EPBC Act List of Threatened Flora. Available at http://www.environment.gov.au/cgi-bin/sprat/public/publicthreatenedlist.pl?wanted=flora

Backhouse GN (2018) ‘Bush Beauties: The Wild Orchids of Victoria, Australia.’ (Published by Gary Backhouse: Mallacoota, Vic., Australia)

Backhouse GN (2023) ‘Guide to Native Orchids of Victoria.’ (CSIRO Publishing: Melbourne, Vic, Australia)

Bates R (1984a) Apomixy in four South Australian species of Prasophyllum R.Br. Journal of the Native Orchid Society of South Australia 6, 37-38.
| Google Scholar |

Bates R (1984b) Pollination of Prasophyllum elatum R.Br. The Orchadian 8, 14-17.
| Google Scholar |

Bernhardt P, Burns-Balogh P (1986) Observations of the floral biology of Prasophyllum odoratum (Orchidaceae, Spiranthoideae). Plant Systematics and Evolution 153, 65-76.
| Google Scholar |

Brown AP, Thomson-Dans C, Marchant N (1998) ‘Western Australia’s Threatened Flora.’ (Department of Conservation and Land Management: Perth, WA, Australia)

Catling PM (1983) Pollination of northeastern North American Spiranthes (Orchidaceae). Canadian Journal of Botany 61, 1080-1093.
| Crossref | Google Scholar |

Davies KL, Stpiczyńska M, Gregg A (2005) Nectar-secreting floral stomata in Maxillaria anceps Ames & C.Schweinf. (Orchidaceae). Annals of Botany 96, 217-227.
| Crossref | Google Scholar | PubMed |

Department of Agriculture, Water and the Environment (2014) Approved Conservation Advice for Prasophyllum innubum (Brandy Mary’s leek-orchid). Department of Agriculture, Water and the Environment, Canberra, ACT, Australia. [Retrieved 20th March 2021]

Department of Climate Change, Energy, Environment and Water (2024) Species Profile and Threats Database – EPBC Act List of Threatened Flora. Available at http://www.environment.gov.au/cgi-bin/sprat/public/publicthreatenedlist.pl?wanted=flora

Driscoll DA, Worboys GL, Allan H, et al. (2019) Impacts of feral horses in the Australian Alps and evidence-based solutions. Ecological Management and Restoration 20, 63-72.
| Crossref | Google Scholar |

Eldridge DJ, Travers SK, Val J, Zaja A, Veblen KE (2019) Horse activity is associated with degraded subalpine grassland structure and reduced habitat for a threatened rodent. Rangeland Ecology & Management 72, 467-473.
| Crossref | Google 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.
| Google Scholar |

Faast R, Facelli JM (2009) Grazing orchids: impact of florivory on two species of Caladenia (Orchidaceae). Australian Journal of Botany 57, 361-372.
| Crossref | Google Scholar |

Freestone MW, Swarts ND, Reiter N, Tomlinson S, Sussmilch FC, Wright MM, Holmes GD, Phillips RD, Linde CC (2021) Continental-scale distribution and diversity of Ceratobasidium orchid mycorrhizal fungi in Australia. Annals of Botany 128, 329-343.
| Crossref | Google Scholar | PubMed |

Freestone M, Linde C, Swarts N, Reiter N (2022) Ceratobasidium orchid mycorrhizal fungi reveal intraspecific variation and interaction with different nutrient media in symbiotic germination of Prasophyllum (Orchidaceae). Symbiosis 87, 255-268.
| Crossref | Google Scholar |

Freestone M, Linde C, Swarts N, Reiter N (2023) Asymbiotic germination of Prasophyllum (Orchidaceae) requires low mineral concentration. Australian Journal of Botany 71, 67-78.
| Crossref | Google Scholar |

Galetto C, Bernardello G, Rivera GL (1997) Nectar, nectaries, flower visitors, and breeding system in five terrestrial Orchidaceae from central Argentina. Journal of Plant Research 110, 393-403.
| Crossref | Google Scholar |

Griffin AR, Hingston AB, Ohmart CP (2009) Pollinators of Eucalyptus regnans (Myrtaceae), the world’s tallest flowering plant species. Australian Journal of Botany 57, 18-25.
| Crossref | Google Scholar |

Hall M (2018) Blue and yellow vane traps differ in their sampling effectiveness for wild bees in both open and wooded habitats. Agricultural and Forest Entomology 20, 487-495.
| Crossref | Google Scholar |

Huber FK, Kaiser R, Sauter W, Schiestl FP (2005) Floral scent emission and pollinator attraction in two species of Gymnadenia (Orchidaceae). Oecologia 142, 564-575.
| Crossref | Google Scholar | PubMed |

Inouye DW, Pyke GH (1988) Pollination biology in the Snowy Mountains of Australia: comparisons with montane Colorado, USA. Australian Journal of Ecology 13, 191-205.
| Crossref | Google Scholar |

Johanson LG, Hoffman AA, Walker KL, Nash MA (2019) Bees of the Victorian Alps: network structure and interactions of introduced species. Austral Ecology 44, 245-254.
| Crossref | Google Scholar |

Johnson SD (1996) Bird pollination in South African species of Satyrium (Orchidaceae). Plant Systematics and Evolution 203, 91-98.
| Crossref | Google Scholar |

Jones DL (1972) The Pollination of Prasophyllum alpinum R.Br. Victorian Naturalist 89, 260-263.
| Google Scholar |

Jones DL (2007) Two endangered new species of Prasophyllum R.Br. (Orchidacaea) from southern New South Wales. The Orchadian 15, 373-374.
| Google Scholar |

Jones DL (2021) ‘A complete guide to native Orchids of Australia,’ 3rd edn. (Reed New Holland Publishers)

Karremans AP, Bogarín D, Fernández Otárola M, Sharma J, Watteyn C, Warner J, Rodríguez Herrera B, Chinchilla IF, Carman E, Rojas Valerio E, Pillco Huarcaya R, Whitworth A (2023) First evidence for multimodal animal seed dispersal in orchids. Current Biology 33, 364-371.e3.
| Crossref | Google Scholar | PubMed |

Kuiter RH (2018) ‘Orchid pollinators of Victoria,’ 4th edn. (Aquatic Photographics: Seaford, Vic, Australia)

Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protocols 1, 387-396.
| Crossref | Google Scholar | PubMed |

Nilsson LA, Jonsson L, Rason L, Randrianjohany E (1986) The pollination of Cymbidiella flabellata (Orchidaceae) in Madagascar: a system operated by sphecid wasps. Nordic Journal of Botany 6, 411-422.
| Crossref | Google Scholar |

Nunes CEP, Peñaflor MFGV, Bento JMS, Salvador MJ, Sazima M (2016) The dilemma of being a fragrant flower: the major floral volatile attracts pollinators and florivores in the euglossine-pollinated orchid Dichaea pendula. Oecologia 182, 933-946.
| Crossref | Google Scholar | PubMed |

Patt JM, Merchant MW, Williams DRE, Meeuse BJD (1989) Pollination biology of Platanthera stricta (Orchidaceae) in Olympic National Park, Washington. American Journal of Botany 76, 1097–-1106.
| Google Scholar |

Peakall R (1987) Genetic systems of Australian terrestrial orchids. PhD Thesis, The University of Western Australia, Botany Department, Perth, WA, Australia.

Peakall R (1989) A new technique for monitoring pollen flow in orchids. Oecologia 79, 361-365.
| Crossref | Google Scholar |

Peakall R, Ebert D, Poldy J, Barrow RA, Francke W, Bower CC, Schiestl FP (2010) Pollinator specificity, floral odour chemistry and the phylogeny of Australian sexually deceptive Chiloglottis orchid: implications for pollinator-driven speciation. New Phytologist 188, 437-450.
| Crossref | Google Scholar | PubMed |

Pedersen HÆ, Srimuang K, Bänziger H, Watthana S (2018) Pollination‑system diversity in Epipactis (Orchidaceae): new insights from studies of E. flava in Thailand. Plant Systematics and Evolution 304, 895-909.
| Crossref | Google 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 | Google Scholar |

Phillips RD, Batley M (2020) Evidence for a food-deceptive pollination system using Hylaeus bees in Caladenia hildae (Orchidaceae). Australian Journal of Botany 68, 146-152.
| Crossref | Google Scholar |

Phillips RD, Peakall R, Hutchinson HF, Linde CC, Xu T, Dixon KW, Hopper SD (2014a) Specialized ecological interactions and plant species rarity: the role of pollinators and mycorrhizal fungi across multiple spatial scales. Biological Conservation 169, 285-295.
| Crossref | Google Scholar |

Phillips RD, Scaccabarozzi D, Retter BA, Hayes C, Brown GR, Dixon K, Peakall R (2014b) Caught in the act: pollination of sexually deceptive trap-flowers by fungus gnats in Pterostylis (Orchidaceae). Annals of Botany 113, 629-641.
| Crossref | Google Scholar |

Phillips RD, Brown GR, Dixon KW, Hayes C, Linde CC, Peakall R (2017) Evolutionary relationships among pollinators and repeated pollinator sharing in sexually deceptive orchids. Journal of Evolutionary Biology 30, 1674-1691.
| Crossref | Google Scholar |

Phillips RD, Reiter N, Peakall R (2020a) Orchid conservation: from theory to practice. Annals of Botany 126, 345-362.
| Crossref | Google Scholar | PubMed |

Phillips RD, Bohman B, Brown GR, Tomlinson S, Peakall R (2020b) A specialised pollination system using nectar-seeking thynnine wasps in Caladenia nobilis (Orchidaceae). Plant Biology 22, 157-166.
| Crossref | Google Scholar | PubMed |

Phillips RD, Ayre BM, Hayashi T, Reiter N (2021a) Preventing Extinction in Bushfire Affected Orchids. Unpublished Report to the Australian Federal Government. La Trobe University, Melbourne, Vic, Australia.

Phillips RD, Bohman B, Peakall R (2021b) Pollination by nectar-foraging pompilid wasps: a new specialised pollination strategy for the Australian flora. Plant Biology 23, 702-710.
| Crossref | Google Scholar | PubMed |

Phillips RD, Hatley J, Li X, Dimon RJ, Reiter N (2024) Resilience to summer bushfire in the threatened orchid, Caladenia tessellata, in terms of pollination success, herbivory and mycorrhizal associations. Botanical Journal of the Linnean Society in press.
| Google Scholar |

Pluskal T, Castillo S, Villar-Briones A, Orešič M (2010) MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinformatics 11, 395.
| Crossref | Google Scholar | PubMed |

Pridgeon AM, Cribb PJ, Chase MW, Rasmussen FN (2001) ‘Genera Orchidacearum. Vol. 2. Orchidoideae (Part One).’ (Oxford University Press: Oxford, UK)

Reiter N, Whitfield J, Pollard G, Bedggood W, Argall M, Dixon K, Davis B, Swarts N (2016) Orchid re-introductions: an evaluation of success and ecological considerations using key comparative studies from Australia. Plant Ecology 217, 81-95.
| Crossref | Google Scholar |

Reiter N, Vlcek K, O’Brien N, Gibson M, Pitts D, Brown GR, Bower CC, Phillips RD (2017) Pollinator rarity limits reintroduction sites in anendangered sexually deceptive orchid (Caladenia hastata): implicationsfor plants with specialized pollination systems. Botanical Journal of the Linnean Society 184, 122-136.
| Crossref | Google Scholar |

Reiter N, Bohman B, Flematti GR, Phillips RD (2018) Pollination by nectar-foraging thynnine wasps: evidence of a new specialized pollination system for Australian orchids. Botanical Journal of the Linnean Society 188, 327-337.
| Crossref | Google Scholar |

Reiter N, Bohman B, Batley M, Phillips RD (2019a) Pollination of an endangered Caladenia species (Orchidaceae) by nectar-foraging behaviour of a widespread species of colletid bee. Botanical Journal of the Linnean Society 189, 83-98.
| Crossref | Google Scholar |

Reiter N, Bohman B, Freestone M, Brown GR, Phillips RD (2019b) Pollination by nectar-foraging thynnine wasps in the endangered Caladenia arenaria and Caladenia concolor (Orchidaceae). Australian Journal of Botany 67, 490-500.
| Crossref | Google Scholar |

Reiter N, Dimon R, Freestone MW (2021) Saving orchids from extinction: the RBGV Orchid Conservation Program ‘ex situ’ collection. Australasian Plant Conservation 29, 11-13.
| Crossref | Google Scholar |

Robertson IC, Klemash D (2003) Insect-mediated pollination in slickspot peppergrass, Lepidium papilliferum L. (Brassicaeae), and its implications for population viability. Western North American Naturalist 63, 333-342.
| Google Scholar |

Scaccabarozzi D, Cozzolino S, Guzzetti L, Galimberti A, Milne L, Dixon KW, Phillips RD (2018) Masquerading as pea plants: behavioural and morphological evidence for mimicry of multiple models in an Australian orchid. Annals of Botany 122, 1061-1073.
| Crossref | Google Scholar | PubMed |

Sletvold N, Grindeland JM, Ågren J (2010) Pollinator-mediated selection on floral display, spur length and flowering phenology in the deceptive orchid Dactylorhiza lapponica. New Phytologist 188, 385-392.
| Crossref | Google Scholar | PubMed |

Steiner KE, Whitehead VB, Johnson SD (1994) Floral and pollinator divergence in two sexually deceptive South African orchids. American Journal of Botany 81, 185-194.
| Crossref | Google Scholar |

Van der Niet T, Cozien RJ, Johnson SD (2015) Experimental evidence for specialized bird pollination in the endangered South African orchid Satyrium rhodanthum and analysis of associated floral traits. Botanical Journal of the Linnean Society 177, 141-150.
| Crossref | Google Scholar |

Williams GA, Adam P (1998) Pollen loads collected from large insects in Australian subtropical rainforests. Proceedings of the Linnean Society of New South Wales 120, 49-67.
| Google Scholar |

Williams NSG, Morgan JW (2015) The native temperate grasslands of south-eastern Australia. In ‘Land of sweeping plains: managing and restoring the native grasslands of South-Eastern Australia’. (Eds NSG Williams, A Marshall, JW Morgan) pp. 27–60. (CSIRO Publishing: Melbourne, Vic, Australia)

Winkler M, Hülber K, Mehltreter K, Franco JG, Hietz P (2005) Herbivory in epiphytic bromeliads, orchids and ferns in a Mexican montane forest. Journal of Tropical Ecology 21, 147-154.
| Crossref | Google Scholar |

Zhou X, Liu Q, Han JY, Gao JY (2016) Different pollinator assemblages ensure reproductive success of Cleisostoma linearilobatum (Orchidaceae) in fragmented holy hill forest and traditional tea garden. Scientific Reports 6, 21435.
| Crossref | Google Scholar | PubMed |