Collateral damage: epiphytic orchids at risk from myrtle rust

Heidi Zimmer; Mark Clements; Endymion Cooper; David Jones; Robert Makinson; Katharina Nargar; Kristy Stevenson

doi:10.1071/BT23047

RESEARCH ARTICLE (Open Access)

Previous Next Contents Vol 71(8)

Collateral damage: epiphytic orchids at risk from myrtle rust

Heidi Zimmer

^A ^* , Mark Clements ^A , Endymion Cooper ^A , David Jones ^B , Robert Makinson ^C , Katharina Nargar ^D and Kristy Stevenson ^E

+ Author Affiliations

- Author Affiliations

^A Centre for Australian National Biodiversity Research (a joint venture between CSIRO and Parks Australia), GPO Box 1700, Canberra, ACT 2601, Australia.

^B Kalaru, NSW 2550, Australia.

^C Australian Network for Plant Conservation Inc., Canberra, ACT 2601, Australia.

^D Australian Tropical Herbarium, James Cook University (JCU) Cairns Campus, P.O. Box 6811, Cairns, Qld 4870, Australia.

^E School of Agriculture and Food Science, The University of Queensland, St Lucia, Qld 4072, Australia.

^* Correspondence to: Heidi.Zimmer@csiro.au

Handling Editor: Ben Gooden

Australian Journal of Botany https://doi.org/10.1071/BT23047

Submitted: 16 June 2023 Accepted: 31 October 2023 Published: 2 December 2023

© 2023 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

Epiphytic orchids rely on the habitat provided by their plant hosts to survive. The naturalisation of Austropuccinia psidii (G. Winter) Beenken (the causal agent for myrtle rust) in Australia means that some of these plant hosts, from the family Myrtaceae, are at risk of serious decline. We aimed to identify orchid species that associate with myrtaceous host plants and determine which, if any, might be susceptible to loss of habitat as a result of myrtle rust. We reviewed species descriptions and herbarium records and identified 73 epiphytic orchid species that are commonly found growing on myrtaceous hosts. At least seven orchid species are predominantly reliant on myrtaceous hosts, are distributed predominantly in the myrtle rust zone, and have host species that are highly or extremely susceptible to myrtle rust. Four of these orchid species are already listed as threatened. The impact of myrtle rust is broader than causing decline of Myrtaceae species, with knock-on effects on other biota, including epiphytic orchids. Moreover, there is the potential for further impact on these orchids through fragmentation (e.g. affecting pollination) and interactive effects with fire. Increased effort is required to identify the relative frequency of myrtaceous and non-myrtaceous hosts for these epiphytic orchid species, especially in relation to the compound effects of myrtle rust and other perturbations, such as fire and climate change. Where this is not possible, ex situ conservation may be required.

Keywords: Austropuccinia psidii, conservation, Durabaculum, Myrtaceae, Orchidaceae, threatened species.

References

ABC News (2023) Most of Lord Howe Island off limits to visitors due to ‘highly infectious’ plant disease myrtle rust. Australian Broadcasting Commission. Available at https://www.abc.net.au/news/2023-03-16/lord-howe-island-partly-closed-due-to-myrtle-rust-nsw/102098242 [Accessed 30 March 2023]

Ai Y-Y, Liu Q, Hu H-X, Shen T, Mo Y-X, Wu X-F, Li J-L, Dossa GGO, Song L (2023) Terrestrial and epiphytic orchids exhibit different diversity and distribution patterns along an elevation gradient of Mt. Victoria, Myanmar. Global Ecology and Conservation 42, e02408.
| Crossref | Google Scholar |

Beenken L (2017) Austropuccinia: a new genus name for the myrtle rust Puccinia psidii placed within the redefined family Sphaerophragmiaceae (Pucciniales). Phytotaxa 297, 53-61.
| Crossref | Google Scholar |

Benzing DH (1987) Vascular epiphytism: taxonomic participation and adaptive diversity. Annals of the Missouri Botanical Garden 74, 183-204.
| Crossref | Google Scholar |

Benzing DH (2004) Vascular epiphytes. Ch. 9. In ‘Forest canopies’. (Eds MD Lowman, HB Rinker) pp. 175–211. (Elsevier)

Benzing DH (2008) ‘Vascular epiphytes: general biology and related biota.’ (Cambridge University Press: Cambridge, UK)

Binskin M, Bennett A, Macintosh A (2020) Royal Commission into National Natural Disaster Arrangements: report (RCNNDA report). The Commission, Canberra.

Bjelke U, Boberg J, Oliva J, Tattersdill K, McKie BG (2016) Dieback of riparian alder caused by the Phytophthora alni complex: projected consequences for stream ecosystems. Freshwater Biology 61, 565-579.
| Crossref | Google Scholar |

Cannon AM (2011) Myrtle Rust – forest industry issues paper. Project No. PRC 218-1011. Forest & Wood Products Australia Limited, Melbourne.

Carnegie AJ, Pegg GS (2018) Lessons from the incursion of myrtle rust in Australia. Annual Review of Phytopathology 56, 457-478.
| Crossref | Google Scholar | PubMed |

Carnegie AJ, Kathuria A, Pegg GS, Entwistle P, Nagel M, Giblin FR (2016) Impact of the invasive rust Puccinia psidii (myrtle rust) on native Myrtaceae in natural ecosystems in Australia. Biological Invasions 18, 127-144.
| Crossref | Google Scholar |

Cobb RC, Chan MN, Meentemeyer RK, Rizzo DM (2012) Common factors drive disease and coarse woody debris dynamics in forests impacted by sudden oak death. Ecosystems 15, 242-255.
| Crossref | Google Scholar |

Fensham RJ, Radford-Smith J (2021) Unprecedented extinction of tree species by fungal disease. Biological Conservation 261, 109276.
| Crossref | Google Scholar |

Fensham RJ, Carnegie AJ, Laffineur B, Makinson RO, Pegg GS, Wills J (2020) Imminent extinction of Australian Myrtaceae by fungal disease. Trends in Ecology & Evolution 35(7), 554-557.
| Crossref | Google Scholar | PubMed |

Fernandez-Winzer L, Berthon KA, Entwistle P, Manea A, Winzer N, Pegg GS, Carnegie AJ, Leishman MR (2020) Direct and indirect community effects of the invasive plant pathogen Austropuccinia psidii (myrtle rust) in eastern Australian rainforests. Biological Invasions 22, 2357-2369.
| Crossref | Google Scholar |

Gale SW, Fischer GA, Cribb PJ, Fay MF (2018) Orchid conservation: bridging the gap between science and practice. Botanical Journal of the Linnean Society 186(4), 425-434.
| Crossref | Google Scholar |

Givnish TJ, Spalink D, Ames M, Lyon SP, Hunter SJ, Zuluaga A, IIes WJD, Clements MA, Arroyo MTK, Leebens-Mack J, Endara L, Kriebel R, Neubig KM, Whitten WM, Williams NH, Cameron KM (2015) Orchid phylogenomics and multiple drivers of their extraordinary diversification. Proceedings of the Royal Society B: Biological Sciences 282(1814), 20151553.
| Crossref | Google Scholar |

Godfree RC, Knerr N, Encinas-Viso F, Albrecht D, Bush D, Christine Cargill D, Clements M, Gueidan C, Guja LK, Harwood T, Joseph L, Lepschi B, Nargar K, Schmidt-Lebuhn A, Broadhurst LM (2021) Implications of the 2019–2020 megafires for the biogeography and conservation of Australian vegetation. Nature Communications 12, 1023.
| Crossref | Google Scholar | PubMed |

Gowland KM, van der Merwe MM, Linde CC, Clements MA, Nicotra AB (2013) The host bias of three epiphytic Aeridinae orchid species is reflected, but not explained, by mycorrhizal fungal associations. American Journal of Botany 100, 764-777.
| Crossref | Google Scholar | PubMed |

Gravendeel B, Smithson A, Slik FJW, Schuiteman A (2004) Epiphytism and pollinator specialization: drivers for orchid diversity? Philosophical Transactions of the Royal Society. Series B: Biological Sciences 359(1450), 1523-1535.
| Crossref | Google Scholar | PubMed |

Jones D (2021) ‘A complete guide to native orchids of Australia.’ (Reed New Holland Pty Ltd: Sydney, NSW)

Laube S, Zotz G (2006) Neither host-specific nor random: vascular epiphytes on three tree species in a Panamanian lowland forest. Annals of Botany 97(6), 1103-1114.
| Crossref | Google Scholar | PubMed |

Leishman MR, Gallagher RV, Catford JA, Morgan JW, Grice AC, Setterfield SA (2017) Invasive plants and pathogens in Australia. In ‘Australian vegetation’. (Ed. D Keith) pp. 207–229. (Cambridge University Press: Cambridge, UK)

Makinson RO (2018) Myrtle rust reviewed: the impacts of the invasive pathogen Austropuccinia psidii on the Australian environment. Plant Biosecurity Cooperative Research Centre, Canberra, ACT, Australia.

Martín-Forés I, Bywaters SL, Sparrow B, Guerin GR (2022) Simultaneous effect of habitat remnancy, exotic species, and anthropogenic disturbance on orchid diversity in South Australia. Conservation Science and Practice 4(4), e12652.
| Crossref | Google Scholar |

Mitchell RJ, Bellamy PE, Broome A, Ellis CJ, Hewison RL, Iason GR, Littlewood NA, Newey S, Pozsgai G, Ray D, Stockan JA, Stokes V, Taylor AFS (2022) Cumulative impact assessments of multiple host species loss from plant diseases show disproportionate reductions in associated biodiversity. Journal of Ecology 110, 221-231.
| Crossref | Google Scholar |

Murren CJ (2002) Effects of habitat fragmentation on pollination: pollinators, pollinia viability and reproductive success. Journal of Ecology 90, 100-107.
| Crossref | Google Scholar |

NSW Government (2022) NSW fire and the environment 2019–20 summary. Available at https://www.environment.nsw.gov.au/-/media/OEH/Corporate-Site/Documents/Parks-reserves-and-protected-areas/Fire/fire-and-the-environment-2019-20-summary-200108.pdf

Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences 11, 1633-1644.
| Crossref | Google Scholar |

Pegg GS, Giblin FR, McTaggart AR, Guymer GP, Taylor H, Ireland KB, Shivas RG, Perry S (2014) Puccinia psidii in Queensland, Australia: disease symptoms, distribution and impact. Plant Pathology 63, 1005-1021.
| Crossref | Google Scholar |

Pegg G, Carnegie A, Giblin F, Perry S (2018) Final report – managing myrtle rust in Australia CRC2063. Plant Biosecurity Cooperative Research Centre, Bruce, ACT. Available at http://www.pbcrc.com.au/publications/pbcrc2206

Pegg GS, Entwistle P, Giblin FR, Carnegie AJ (2020) Fire and rust – the impact of Austropuccinia psidii (myrtle rust) on regeneration of Myrtaceae in coastal heath following wildfire. Southern Forests: A Journal of Forest Science 82, 280-291.
| Crossref | Google Scholar |

POWO (2023) Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. Available at http://www.plantsoftheworldonline.org/ [Accessed 17 September 2023]

Sanger JC (2016) The distribution of epiphytes over environmental and habitat gradients in tropical and subtropical Australia. PhD Thesis, University of Tasmania, Hobart, Australia. Available at https://eprints.utas.edu.au/23443/7/Sanger_whole_thesis_ex_pub_mat.pdf [Accessed 30 March 2023]

Shaw DC, Woolley T, Kelsey RG, McPherson BA, Westlind D, Wood DL, Peterson EK (2017) Surface fuels in recent Phytophthora ramorum created gaps and adjacent intact Quercus agrifolia forests, East Bay Regional Parks, California, USA. Forest Ecology and Management 384, 331-338.
| Crossref | Google Scholar |

Stewart JE, Ross-Davis AL, Graca RN, Alfenas AC, Peever TL, Hanna JW, Uchida JY, Hauff RD, Kadooka CY, Kim M-S, Cannon PG, Namba S, Simeto S, Pérez CA, Rayamajhi MB, Lodge DJ, Arguedas M, Medel-Ortiz R, López-Ramirez MA, Tennant P, Glen M, Machado PS, McTaggart AR, Carnegie AJ, Klopfenstein NB (2017) Genetic diversity of the myrtle rust pathogen (Austropuccinia psidii) in the Americas and Hawaii: global implications for invasive threat assessments. Forest Pathology 48, e12378.
| Crossref | Google Scholar |

Teixeira da Silva JA, Tsavkelova EA, Ng TB, Parthibhan S, Dobránszki J, Cardoso JC, Rao MV, Zeng S (2015) Asymbiotic in vitro seed propagation of Dendrobium. Plant Cell Reports 34, 1685-1706.
| Crossref | Google Scholar | PubMed |

Thuiller W, Albert C, Araújo MB, Berry PM, Cabeza M, Guisan A, Hickler T, Midgley GF, Paterson J, Schurr FM, Sykes MT, Zimmermann NE (2008) Predicting global change impacts on plant species’ distributions: future challenges. Perspectives in Plant Ecology, Evolution and Systematics 9(3–4), 137-152.
| Crossref | Google Scholar |

Vasconcelos TNC, Proença CEB, Ahmad B, Aguilar DS, Aguilar R, Amorim BS, Campbell K, Costa IR, De-Carvalho PS, Faria JEQ, Giaretta A, Kooij PW, Lima DF, Mazine FF, Peguero B, Prenner G, Santos MF, Soewarto J, Wingler A, Lucas EJ (2017) Myrteae phylogeny, calibration, biogeography and diversification patterns: increased understanding in the most species rich tribe of Myrtaceae. Molecular Phylogenetics and Evolution 109, 113-137.
| Crossref | Google Scholar |

Wagner K, Mendieta-Leiva G, Zotz G (2015) Host specificity in vascular epiphytes: a review of methodology, empirical evidence and potential mechanisms. AoB Plants 7, plu092.
| Crossref | Google Scholar |

Wallace BJ (1983) The Australian vascular epiphytes: flora and ecology. PhD Thesis, University of New England, NSW, Australia. Available at https://rune.une.edu.au/web/bitstream/1959.11/23348/6/open/SOURCE05.pdf [Accessed 4 May 2023]

Zotz G (2016) ‘Plants on plants – the biology of vascular epiphytes.’ (Springer International Publishing: Switzerland)

Zotz G, Weigelt P, Kessler M, Kreft H, Taylor A (2021) EpiList 1.0: a global checklist of vascular epiphytes. Ecology 102, e03326.
| Crossref | Google Scholar | PubMed |