Differences in emergence and flowering in wild, re-introduced and translocated populations of an endangered terrestrial orchid and the influences of climate and orchid mycorrhizal abundance
Brendan Janissen A D , Garry French B , Jamie Selby-Pham C , Ann C. Lawrie A and Tien Huynh AA School of Science, RMIT University, PO Box 71, Bundoora, Vic. 3083, Australia.
B Australasian Native Orchid Society, Victoria Group, PO Box 308, Boronia, Vic. 3155, Australia.
C College of Science, Engineering and Health, RMIT University, GPO Box 2476, Melbourne, Vic. 3001, Australia.
D Corresponding author. Email: bjjanissen@gmail.com
Australian Journal of Botany - https://doi.org/10.1071/BT20102
Submitted: 11 August 2020 Accepted: 25 November 2020 Published online: 11 January 2021
Abstract
Re-introduction and translocation are conservation strategies often employed to circumvent declining wild orchid populations but their efficacy as conservation strategies is widely debated. The aim of this study was to investigate the long-term efficacy of re-introduction and translocation strategies for an endangered orchid as its climate changed. Vital rates of the wild, re-introduced and translocated populations of an endangered terrestrial orchid Caladenia amoena were compared from 2008 to 2019. Emergence and flowering declined at significantly faster rates in the translocated and re-introduced populations than in the wild population. Emergence and flowering declined as mean maximum temperatures rose, whereas flowering increased with rainfall. Both emergence and flowering were positively correlated with the length of the growing period, which decreased by >33% during the study. The relevant orchid mycorrhizal fungi (OMF) (Serendipita sp.) were more abundant in soil at the wild population than at the translocated or re-introduced populations. However, the limited soil sampling used to minimise disturbance may not have detected true fungal heterogeneity. This study suggests that translocation and re-introduction may not be effective long-term solutions for C. amoena. Reduction in above-ground growing period length was probably the over-riding influence in the decline of all populations. Greater OMF abundance in the soil may be the critical factor that renders the wild population more able to withstand the influences of climate change. Future research should consider methods to reduce the impacts of increased temperature and reduced rainfall on threatened orchid taxa.
Keywords: Caladenia amoena, climate change, growing period length, mycorrhizal fungi, orchid, conservation, re-introduction, translocation.
References
Allen MR, Dube OP, Solecki W, Aragón-Durand F, Cramer W, Humphreys S, Kainuma M, Kala J, Mahowald N, Mulugetta Y, Perez R, Wairiu M, Zickfeld K (2018) Framing and context. In ‘Global Warming of 1.5°C. An IPCC Special Report on the Impacts of Global Warming of 1.5°C above Pre-Industrial Levels and Related Global Greenhouse Gas Emission Pathways, in the Context of Strengthening the Global Response to the Threat of Climate Change, Sustainable Development, and Efforts to Eradicate Poverty’. (Eds V Masson-Delmotte, P Zhai, H-O Pörtner, D Roberts, J Skea, PR Shukla, A Pirani, W Moufouma-Okia, C Péan, R Pidcock, S Connors, JBR Matthews, Y Chen, X Zhou, MI Gomis, E Lonnoy, T Maycock, M Tignor, T Waterfield) pp. 41–91. (Intergovernmental Panel on Climate Change) Available at https://www.ipcc.ch/site/assets/uploads/sites/2/2019/05/SR15_Chapter1_Low_Res.pdf [Verified 17 December 2020]Amrit K, Pandey RP, Mishra SK, Daradur M (2018) Relationship of drought frequency and severity with range of annual temperature variation. Natural Hazards 92, 1199–1210.
| Relationship of drought frequency and severity with range of annual temperature variation.Crossref | GoogleScholarGoogle Scholar |
Batty AL, Brundrett MC, Dixon KW, Sivasithamparam K (2006) In situ symbiotic seed germination and propagation of terrestrial orchid seedlings for establishment at field sites. Australian Journal of Botany 54, 375–381.
| In situ symbiotic seed germination and propagation of terrestrial orchid seedlings for establishment at field sites.Crossref | GoogleScholarGoogle Scholar |
Bernardo HL, Albrecht MA, Knight TM (2016) Increased drought frequency alters the optimal management strategy of an endangered plant. Biological Conservation 203, 243–251.
| Increased drought frequency alters the optimal management strategy of an endangered plant.Crossref | GoogleScholarGoogle Scholar |
Bureau of Meteorology (2020) Climate change in Australia: projections for Australia’s NRM regions. Southern slopes (Victoria west). Available at https://www.climatechangeinaustralia.gov.au/en/climate-projections/future-climate/regional-climate-change-explorer/sub-clusters/?current=SSVWC&popup=true&tooltip=true [Verified 17 December 2020]
Bustam BM, Dixon KW, Bunn E (2014) In vitro propagation of temperate Australian terrestrial orchids: revisiting asymbiotic compared with symbiotic germination. Botanical Journal of the Linnean Society 176, 556–566.
| In vitro propagation of temperate Australian terrestrial orchids: revisiting asymbiotic compared with symbiotic germination.Crossref | GoogleScholarGoogle Scholar |
Clements MA, Muir H, Cribb PJ (1986) A preliminary report on the symbiotic germination of European terrestrial orchids. Kew Bulletin 41, 437–445.
| A preliminary report on the symbiotic germination of European terrestrial orchids.Crossref | GoogleScholarGoogle Scholar |
Coates F, Lunt ID, Tremblay RL (2006) Effects of disturbance on population dynamics of the threatened orchid Prasophyllum correctum D.L. Jones and implications for grassland management in south-eastern Australia. Biological Conservation 129, 59–69.
| Effects of disturbance on population dynamics of the threatened orchid Prasophyllum correctum D.L. Jones and implications for grassland management in south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Collins M, Knutti R, Arblaster JM, Dufresnse J-L, Fichefet T, Friedlingstein P, Gao X, Gutowski WJ, Johns T, Krinner G, Shongwe M, Tebaldi C, Weaver AJ, Wehner M (2013) Long-term climate change: projections, commitments and irreversibility. In ‘Climate Change 2013. The Physical Science Basis’. (Eds TF Stocker, D Qin, G-K Plattner, M Tignor, SK Allen, J Boschung, A Nauels, Y Xia, V Bex, PM Midgley) pp. 1029–1136. (Cambridge University Press: Cambridge, UK)
Department of Natural Resources and Environment (2000) Recovery plan for twelve threatened spider-orchid Caladenia taxa of Victoria and South Australia 2000–2004. Available at https://www.environment.gov.au/system/files/resources/5673cd4d-1802-4927-85e5-4bdbf947ba58/files/12-orchid.pdf [Verified 17 December 2020]
Downing JL, Liu H, Shao S, Wang X, McCormick M, Deng R, Gao J (2017) Contrasting changes in biotic interactions of orchid populations subject to conservation introduction vs conventional translocation in tropical China. Biological Conservation 212, 29–38.
| Contrasting changes in biotic interactions of orchid populations subject to conservation introduction vs conventional translocation in tropical China.Crossref | GoogleScholarGoogle Scholar |
Duncan M, Moloney PD (2018) Comparing wild and reintroduced populations of the threatened orchid Diuris fragrantissima (Orchidaceae) in south-eastern Australia. Australian Journal of Botany 66, 459–467.
| Comparing wild and reintroduced populations of the threatened orchid Diuris fragrantissima (Orchidaceae) in south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Gandin A, Gutjahr S, Dizengremel P, Lapointe L (2011) Source–sink imbalance increases with growth temperature in the spring geophyte Erythronium americanum. Journal of Experimental Botany 62, 3467–3479.
| Source–sink imbalance increases with growth temperature in the spring geophyte Erythronium americanum.Crossref | GoogleScholarGoogle Scholar | 21335435PubMed |
Gaskett AC, Gallagher RV (2018) Orchid diversity: spatial and climatic patterns from herbarium records. Ecology and Evolution 8, 11235–11245.
| Orchid diversity: spatial and climatic patterns from herbarium records.Crossref | GoogleScholarGoogle Scholar | 30519440PubMed |
Herath SM, Sarukkalige R, Nguyen VTV (2018) Evaluation of empirical relationships between extreme rainfall and daily maximum temperature in Australia. Journal of Hydrology 556, 1171–1181.
| Evaluation of empirical relationships between extreme rainfall and daily maximum temperature in Australia.Crossref | GoogleScholarGoogle Scholar |
Hutchings MJ (1987) The population biology of the early spider orchid, Ophrys sphegodes Mill. I. A demographic study from 1975 to 1984. Journal of Ecology 75, 711–727.
| The population biology of the early spider orchid, Ophrys sphegodes Mill. I. A demographic study from 1975 to 1984.Crossref | GoogleScholarGoogle Scholar |
Huynh TT, Thomson R, Mclean CB, Lawrie AC (2009) Functional and genetic diversity of mycorrhizal fungi from single plants of Caladenia formosa (Orchidaceae). Annals of Botany 104, 757–765.
| Functional and genetic diversity of mycorrhizal fungi from single plants of Caladenia formosa (Orchidaceae).Crossref | GoogleScholarGoogle Scholar | 19561011PubMed |
Inghe O, Tamm CO (1988) Survival and flowering of perennial herbs. 5 Patterns of flowering. Oikos 51, 203–219.
| Survival and flowering of perennial herbs. 5 Patterns of flowering.Crossref | GoogleScholarGoogle Scholar |
Izuddin M, Yam TW, Webb EL (2018) Specific niche requirements drive long-term survival and growth of translocated epiphytic orchids in an urbanised tropical landscape. Urban Ecosystems 21, 531–540.
| Specific niche requirements drive long-term survival and growth of translocated epiphytic orchids in an urbanised tropical landscape.Crossref | GoogleScholarGoogle Scholar |
Jasinge NU, Huynh T, Lawrie AC (2018) Changes in orchid populations and endophytic fungi with rainfall and prescribed burning in Pterostylis revoluta in Victoria, Australia. Annals of Botany 121, 321–334.
| Changes in orchid populations and endophytic fungi with rainfall and prescribed burning in Pterostylis revoluta in Victoria, Australia.Crossref | GoogleScholarGoogle Scholar | 29300863PubMed |
Kéry M, Gregg KB (2004) Demographic analysis of dormancy and survival in the terrestrial orchid Cypripedium reginae. Journal of Ecology 92, 686–695.
| Demographic analysis of dormancy and survival in the terrestrial orchid Cypripedium reginae.Crossref | GoogleScholarGoogle Scholar |
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.
| MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms.Crossref | GoogleScholarGoogle Scholar | 29722887PubMed |
Light MH, MacConnaill M (1991) Patterns of appearance in Epipactis helleborine (L.) Crantz. In ‘Population Ecology of Terrestrial Orchids’. (Eds TCE Wells, JH Willems) pp. 77–87. (SPB Academic Publishing: The Hague, Netherlands)
Marchin R, Dunn R, Hoffmann W (2014) Are winter-active species vulnerable to climate warming? A case study with the wintergreen terrestrial orchid, Tipularia discolor. Oecologia 176, 1161–1172.
| Are winter-active species vulnerable to climate warming? A case study with the wintergreen terrestrial orchid, Tipularia discolor.Crossref | GoogleScholarGoogle Scholar | 25255853PubMed |
McCormick MK, Taylor DL, Whigham DF, Burnett RK (2016) Germination patterns in three terrestrial orchids relate to abundance of mycorrhizal fungi. Journal of Ecology 104, 744–754.
| Germination patterns in three terrestrial orchids relate to abundance of mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |
McCormick MK, Whigham DF, Canchani‐Viruet A (2018) Mycorrhizal fungi affect orchid distribution and population dynamics. New Phytologist 219, 1207–1215.
| Mycorrhizal fungi affect orchid distribution and population dynamics.Crossref | GoogleScholarGoogle Scholar |
Molnár A, Tökölyi J, Végvári Z, Sramkó G, Sulyok J, Barta Z (2012) Pollination mode predicts phenological response to climate change in terrestrial orchids: a case study from central Europe. Journal of Ecology 100, 1141–1152.
| Pollination mode predicts phenological response to climate change in terrestrial orchids: a case study from central Europe.Crossref | GoogleScholarGoogle Scholar |
Nikabadi S, Bunn E, Stevens J, Newman B, Turner SR, Dixon KW (2014) Germination responses of four native terrestrial orchids from south-west Western Australia to temperature and light treatments. Plant Cell, Tissue and Organ Culture 118, 559–569.
| Germination responses of four native terrestrial orchids from south-west Western Australia to temperature and light treatments.Crossref | GoogleScholarGoogle Scholar |
Parthibhan S, Senthil Kumar T, Rao MV (2015) Phenology and reintroduction strategies for Dendrobium aqueum Lindley – an endemic, near threatened orchid. Journal for Nature Conservation 24, 68–71.
| Phenology and reintroduction strategies for Dendrobium aqueum Lindley – an endemic, near threatened orchid.Crossref | GoogleScholarGoogle Scholar |
PerkinElmer (1995) ‘ABI PRISM dye terminator cycle sequencing ready reaction kit with AmpliTaq DNA polymerase. Protocol number 402078, revision A.’ (PerkinElmer Corp.: Waltham, MA, USA)
Perkins AJ, McGee PA (1995) Distribution of the orchid mycorrhizal fungus, Rhizoctonia solani, in relation to its host, Pterostylis acuminata, in the field. Australian Journal of Botany 43, 565–575.
| Distribution of the orchid mycorrhizal fungus, Rhizoctonia solani, in relation to its host, Pterostylis acuminata, in the field.Crossref | GoogleScholarGoogle Scholar |
Rasmussen HN (1995) ‘Terrestrial Orchids: from Seed to Mycotrophic Plant.’ (Cambridge University Press: Cambridge, 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.
| Orchid re-introductions: an evaluation of success and ecological considerations using key comparative studies from Australia.Crossref | GoogleScholarGoogle Scholar |
Reiter N, Lawrie AC, Linde CC (2018) Matching symbiotic associations of an endangered orchid to habitat to improve conservation outcomes. Annals of Botany 122, 947–959.
| Matching symbiotic associations of an endangered orchid to habitat to improve conservation outcomes.Crossref | GoogleScholarGoogle Scholar | 29897399PubMed |
Reiter N, Phillips RD, Swarts ND, Wright M, Holmes G, Sussmilch FC, Davis BJ, Whitehead MR, Linde CC (2020) Specific mycorrhizal associations involving the same fungal taxa in common and threatened Caladenia (Orchidaceae): implications for conservation. Annals of Botany 126, 943–955.
| Specific mycorrhizal associations involving the same fungal taxa in common and threatened Caladenia (Orchidaceae): implications for conservation.Crossref | GoogleScholarGoogle Scholar | 32574356PubMed |
Risbey JS, Pook MJ, McIntosh PC (2013) Spatial trends in synoptic rainfall in southern Australia. Geophysical Research Letters 40, 3781–3785.
| Spatial trends in synoptic rainfall in southern Australia.Crossref | GoogleScholarGoogle Scholar |
Rock‐Blake R, McCormick MK, Brooks HEA, Jones CS, Whigham DF (2017) Symbiont abundance can affect host plant population dynamics. American Journal of Botany 104, 72–82.
| Symbiont abundance can affect host plant population dynamics.Crossref | GoogleScholarGoogle Scholar | 28062407PubMed |
Sieg CH, King RM (1995) Influence of environmental factors and preliminary demographic analyses of a threatened orchid, Platanthera praeclara. American Midland Naturalist 134, 307–323.
| Influence of environmental factors and preliminary demographic analyses of a threatened orchid, Platanthera praeclara.Crossref | GoogleScholarGoogle Scholar |
Silcock JL, Simmons CL, Monks L, Dillon R, Reiter N, Jusaitis M, Vesk PA, Byrne M, Coates DJ (2019) Threatened plant translocation in Australia: a review. Biological Conservation 236, 211–222.
| Threatened plant translocation in Australia: a review.Crossref | GoogleScholarGoogle Scholar |
Slaviero A, Del Vecchio S, Pierce S, Fantinato E, Buffa G (2016) Plant community attributes affect dry grassland orchid establishment. Plant Ecology 217, 1533–1543.
| Plant community attributes affect dry grassland orchid establishment.Crossref | GoogleScholarGoogle Scholar |
Sletvold N, Ågren J (2015) Climate-dependent costs of reproduction: survival and fecundity costs decline with length of the growing season and summer temperature. Ecology Letters 18, 357–364.
| Climate-dependent costs of reproduction: survival and fecundity costs decline with length of the growing season and summer temperature.Crossref | GoogleScholarGoogle Scholar | 25711515PubMed |
Solomon S (2007) ‘Climatic Change 2007. The Physical Science Basis: Working Group I Contribution to the Fourth Assessment Report of the IPCC.’ (Cambridge University Press: Cambridge, UK)
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526.
| Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees.Crossref | GoogleScholarGoogle Scholar | 8336541PubMed |
Waud M, Busschaert P, Lievens B, Jacquemyn H (2016) Specificity and localised distribution of mycorrhizal fungi in the soil may contribute to co-existence of orchid species. Fungal Ecology 20, 155–165.
| Specificity and localised distribution of mycorrhizal fungi in the soil may contribute to co-existence of orchid species.Crossref | GoogleScholarGoogle Scholar |
Weiß M, Waller F, Zuccaro A, Selosse M-A (2016) Sebacinales – one thousand and one interactions with land plants. New Phytologist 211, 20–40.
| Sebacinales – one thousand and one interactions with land plants.Crossref | GoogleScholarGoogle Scholar |
Wells TCE, Rothery P, Cox R, Bamford S (1998) Flowering dynamics of Orchis morio L. and Herminium monorchis (L.) R.Br. at two sites in eastern England. Botanical Journal of the Linnean Society 126, 39–48.
| Flowering dynamics of Orchis morio L. and Herminium monorchis (L.) R.Br. at two sites in eastern England.Crossref | GoogleScholarGoogle Scholar |
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA Genes for phylogenetics. In ‘PCR Protocol Guide Methods Application’. pp. 315–322. (Academic Press: San Diego, CA, USA)
Whitehead MR, Catullo RA, Ruibal M, Dixon KW, Peakall R, Linde CC (2017) Evaluating multilocus Bayesian species delimitation for discovery of cryptic mycorrhizal diversity. Fungal Ecology 26, 74–84.
| Evaluating multilocus Bayesian species delimitation for discovery of cryptic mycorrhizal diversity.Crossref | GoogleScholarGoogle Scholar |
Wright M, Cousens R, Andrusiak S, McLean CB, French G, Cross R (2007) Site amelioration for direct seeding of Caladenia tentaculata improves seedling recruitment and survival in natural habitat. Lankesteriana 7, 430–432.
| Site amelioration for direct seeding of Caladenia tentaculata improves seedling recruitment and survival in natural habitat.Crossref | GoogleScholarGoogle Scholar |
Wright M, Cross R, Dixon K, Huynh T, Lawrie A, Nesbitt L, Pritchard A, Swarts N, Thomson R (2009) Propagation and reintroduction of Caladenia. Australian Journal of Botany 57, 373–387.
| Propagation and reintroduction of Caladenia.Crossref | GoogleScholarGoogle Scholar |
Wu K, Zeng S, Lin D, da Silva JAT, Bu Z, Zhang J, Duan J (2014) In vitro propagation and reintroduction of the endangered Renanthera imschootiana Rolfe. PLoS One 9, e110033
| In vitro propagation and reintroduction of the endangered Renanthera imschootiana Rolfe.Crossref | GoogleScholarGoogle Scholar | 25506700PubMed |