Orchid conservation: Assessing threats and conservation priorities
Author Wraith, Jenna L
Published 2020-03-10
Thesis Type Thesis (PhD Doctorate)
School School of Environment and Sc
DOI https://doi.org/10.25904/1912/1368
Copyright Statement The author owns the copyright in this thesis, unless stated otherwise.
Downloaded from http://hdl.handle.net/10072/392403
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Orchid conservation: Assessing threats and conservation priorities
Jenna Wraith B.Sc (Hons)
Griffith School of Environment and Science Environmental Futures Research Institute Griffith Sciences
Submitted in the fulfilment of the requirements of the degree of Doctor of Philosophy
December 2019
1 Statement of Originality
This work has not previously been submitted for a degree or diploma in any university.
To the best of my knowledge and belief, the thesis contains no material previously published or written by another person except where due reference is made in the thesis itself.
(Signed)______
Jenna Wraith
2 Abstract
Globally, over a million species are threatened with extinction from habitat loss, climate change, over-exploitation as well as other anthropogenic activities. Orchids are particularly at risk in part due to their distinctive ecology including high species diversity, often limited geographic range for many species, and tight ecological relations with specific symbionts. They are the most diverse group of flowering plants with
~28,000 species and are found on all but one continent. However, due to increasing pressures from humans many orchids are threatened with extinction. It is therefore important to assess what is threatening them and where. Therefore, this thesis assesses threats to orchids at a global and continental scale to highlight the most significant threats to orchids, where orchids are threatened and by what, and to prioritise conservation actions and future research.
The range and diversity of threats to orchids was globally assessed and mapped using data from the International Union for Conservation of Nature (IUCN) Red List
(Chapter 2). For the 442 orchids on the Red List, the most common threats were biological resource use (80% species), agriculture (53%), human intrusion and disturbance (36%) and development (35%) and were most commonly found in Africa
(predominantly Madagascar), South and East Asia and South America. These threats often interacted and co-occurred with four major threat syndromes. Understanding threat syndromes is vital for orchid conservation as they can create more consistent conservation planning and help focus efforts on the specific threats in a given region.
Globally the scale and extent of tourism and recreation is increasing, including nature- based tourism. As a result, tourism and recreation is increasingly recognised as a threat to plants including orchids. Therefore, the extent and nature of tourism and recreation as
3 a threat to orchids globally was also assessed in more detail using data from the IUCN
Red List (Chapter 3). This demonstrated that 149 of the 442 listed orchids were threatened by tourism and recreation including impacts of residential and commercial development for tourism infrastructure (22%), intentional collecting within protected areas (17%), and human intrusion and disturbance from recreational activities (20%).
Tourism and recreation threats were severe, impacting many populations of some orchids and causing rapid decline. These findings highlight how tourism and recreation can threaten specific groups of plants in diverse habitats, but particularly in forests and shrublands and these threats often co-occurred as threat syndromes.
To better facilitate orchid conservation, a more detailed analysis of geographical patterns in threatened orchids and threats to orchids was conducted at a continental scale using a methodology that could be adapted to other threatened taxa (Chapter 4). By utilising data on threatened orchids from the Australian Government, combined with species occurrence data from the Atlas of Living Australia, the distribution of the most severe threats to orchids in Australia were mapped. This included identifying locations where habitat modification, changing fire regimes, grazing, weeds, tourism and recreation and illegal collection occurred, including where they co-occurred as threat syndromes. This study shows that the loss of native vegetation is a key driver of most threats, while increases within protected areas was associated with an increased threat from tourism and recreation. This study also provides critical information for formulating conservation and management strategies for threatened orchids and other species in a changing environment.
To ensure the successful conservation of orchids, researchers need to understand research and conservation priorities at a global scale. Therefore, conservation and research priorities for orchid conservation were assessed (Chapter 5) using data on
4 research publications on orchid conservation from Scopus, data on conservation priorities from the Red List, and species occurrence records from the Global
Biodiversity Information Facility (GBIF). This study highlighted the increase in conservation research and important gaps as well as key conservation priorities which were analysed to guide recommendations on future priorities. Based on the results, orchid conservation and research globally should increasingly focus on monitoring population, trends and distributions including the impacts of climate change, ecology, threats and threat mitigation, protection and management of species and their habitats and increasing education and awareness.
The research in this thesis demonstrated how orchids are significantly threatened by anthropogenic activities at a global and continental scale including impacts from habitat loss, illegal collecting, tourism and recreation, increased fire regimes and invasive species. However, it is also evident that climate change is underrepresented as a threat to orchids and needs to be considered in future research. These studies highlight the prevalence and importance of threat syndromes and provide novel methods for spatially assessing them. It is evident from these studies that orchid conservation will benefit from global collaboration and focussed conservation priorities.
5 Table of Contents Statement of Originality ...... 2 Abstract ...... 3 Table of Contents ...... 6 List of Figures...... 8 List of Appendices ...... 9 Acknowledgements ...... 10 Published papers included in the thesis ...... 11 Glossary ...... 12 References ...... 13 Chapter 1. Introduction ...... 15 1.1 Sixth wave of mass extinction ...... 15 1.2 Threats to global plant biodiversity ...... 15 1.3 Research on plant conservation ...... 19 1.4 Why are orchids important? ...... 21 1.5 Aims...... 24 1.6 Structure of the thesis ...... 25 1.7 Published and submitted papers included as results Chapters in the thesis...... 28 1.7.1 Other publications completed during candidature but not included in this thesis: .. 28 1.7.2 Related published papers ...... 28 1.7.3 Conference presentations and talks to orchid societies ...... 28 1.7.4 Other publications ...... 29 1.8 References ...... 29 Chapter 2. Quantifying global threats to orchids ...... 38 Chapter 3. Tourism and recreation a global threat to orchids ...... 50 Chapter 4. A continental scale analysis of threats to orchids ...... 65 Chapter 5. Research and conservation priorities for globally Red Listed orchids ...... 77 Chapter 6. Discussion and Conclusion ...... 105 6.1 Introduction ...... 105 6.2 Aim 1: What are the major threats to orchids globally? ...... 106 6.3 Aim 2: Where are threats to orchids occurring and which habitats are most at risk?..... 113 6.4 Aim 3: What is the impact of threats on orchid life forms and genera? ...... 116 6.5 Aim 4: Are orchids impacted by threat syndromes? ...... 119 6.6 Aim 5: What are the key priorities for orchid conservation and research? ...... 122 6.7 Contribution to conservation, limitations and future directions ...... 125 6.8 Conclusions ...... 130
6 6.9 References...... 130 Appendices ...... 143
7 List of Figures
Figure 1.1. The most common threats to the ~14,000 plants on the IUCN Red List, with the number of species in green. Adapted from the IUCN Red List (2019) ...... 16 Figure 1.2. The number of research and review articles published per year on plant conservation based on data from Scopus, using the search terms ‘plant’ and ‘conservation’ in October 2019…………………………………………………………………………………….19 Figure 1.3. The number of research and review articles on the conservation of the most diverse families of flowering plants. The numbers of papers per family were identified by searching the family name and synonyms combined with ‘conservation’ on Scopus and cover the period 1969- 2018………………………………………………………………………………….…20 Figure 1.4. The proportion of threatened orchid species on the IUCN Red List (2019) where the numbers to the right of each bar represent the total number of extant species assessed with CR = critically endangered, VU = vulnerable, NT = near threatened, DD = data deficient and LC = least concern………………………………………………………………………………….21 Figure 1.5. Schematic overview of the content and structure of the thesis ….…….….27 Figure 6.1. The most commonly threats for orchids globally (Top) and all plants (Bottom) on the IUCN Red List (2019) and where the same threats occur for both groups of plants, they are given the same colour coding. T & R = tourism and recreation…………………………………………………………………….………..107 Figure 6.2. Schematic overview of the percent of threatened orchids on the IUCN Red List impacted by tourism and recreation threats based on data from Wraith and Pickering (2017) ………….……………………………………………………….….108 Figure 6.3. The most commonly listed threats to orchids in Australia (Top) and globally (Bottom) based on data from the Australian Government, and the IUCN Red List (2019) with the same threats in the two datasets colour coordinated…………………………112 Figure 6.4. Four major threat syndromes affecting orchids on the IUCN Red List using data from Wraith and Pickering (2018) ………………………………………………121 Figure 6.5. Schematic overview of the gaps in orchid conservation research and priorities based on the data on the IUCN Red List adapted from Wraith et al. (In press) …………………………………………………………………...……………………125 Figure 6.6. A schematic overview of the key aspects to consider when developing a conservation or management plan for threatened species…………………...………..128
8 List of Appendices
Appendix 1 Griffith University policy on the inclusion of papers within the thesis.
Accessed November 2019 https://intranet.secure.griffith.edu.au/research/griffith- graduate-research-school/preparing-your-thesis/inclusion-of-papers-within-the-thesis.
Appendix 2 Chapter 2 supplementary material (appendix 1) for the paper Wraith, J. and
C. Pickering (2018). Quantifying anthropogenic threats to orchids using the IUCN Red
List. Ambio 47(3): 307-317.
9 Acknowledgements
I would like to sincerely thank my principal supervisor Professor Catherine Pickering and Associate supervisor’s Dr Melinda Laidlaw and Dr Willow Hallgren for their encouragement, support and ideas. It has been incredible to work with and learn from inspiring women in science and I have been fortunate to have their thoughtful input and editorial advice, which greatly improved the quality of this thesis and published papers within.
I sincerely thank the staff and fellow postgraduates at the Griffith School of
Environment and Science and the Environmental Futures Research Institute for their friendship, community and advice during my projects. I am particularly grateful for the friendship, support and comradery of Victoria Thomson, Dr Eloise Skinner, Dr
Stephanie Chaousis and Dr Ryan Pearson.
I am also sincerely grateful for my husband Patrick Norman who has been the most supportive and encouraging partner in both science and life. Completing our PhDs side by side has been a wonderful experience. I am also grateful to my supportive and encouraging friends Pippa Skillington, Courtney Cotter and Victoria Thomson.
I express my deepest appreciation to my mum and dad for instilling the belief that I could achieve anything and their unconditional support and encouragement.
I also want to express my immense gratitude to the wonderous world of orchids which not only includes the most fascinating plants but the most passionate, kind and knowledgeable people who welcomed me with open arms into their societies, tours, conferences and circles. I will cherish these friendships, adventures and memories for a lifetime.
10 Published papers included in the thesis
This thesis includes published papers and papers in press with Chapters 2, 3, 4 and 5 consisting of peer reviewed and co-authored papers with other researchers. My contribution to each co-authored paper is outlined at the front of the relevant Chapters.
The bibliographic details (if published or in press) status for these papers including all authors, are:
Chapter 2: Wraith, J., and C. Pickering (2018). Quantifying anthropogenic threats to orchids using the IUCN Red List. Ambio. 47(3): 307-317.
Chapter 3: Wraith, J., and C. Pickering (2017). Tourism and recreation a global threat to orchids. Biodiversity and Conservation 26(14): 3407-3420.
Chapter 4: Wraith, J., and C. Pickering (2019). A continental scale analysis of threats to orchids. Biological Conservation 234: 7-17.
Chapter 5: Wraith, J., P. Norman, and C. Pickering (2019). Orchid conservation and research: an analysis of gaps and priorities for globally Red Listed species. Ambio (In press).
Appropriate acknowledgements of those contributing to the research but did not qualify as authors are also included in each paper.
(Signed):
(Date): 17 December, 2019
Jenna Lee Wraith
(Counter signed):
(Date): 17 December, 2019
Professor Catherine Marina Pickering
11 Glossary
ALA: The Atlas of Living Australia is an online collaborative data portal containing species occurrence records in Australia (Atlas of Living Australia 2019).
CITES: Convention of International Trade in Endangered Species of Wild Fauna and
Flora (Cites 2019).
Endemic: Native species that are restricted to a certain geographic area (Malcolm et al.
2006).
Epiphytic: Orchids that require host trees for growth and derive nutrients from moisture in the air and debris as well as mycorrhizae (Jones 2006).
GBIF: The Global Biodiversity Information Facility is a data portal containing global species occurrence records for plants and animals (GBIF 2019).
GIS: Geographic information systems (Fischer et al. 2019).
GLM: A generalised linear model is a statistical model commonly used for count data
(Li et al. 2017).
IUCN: The International Union for Conservation of Nature’s Red List of Threatened
Species is a comprehensive data portal containing information on the global conservation status of animal, fungi and plant species (IUCN 2019).
Lithophyte: Orchids that predominantly grow on rocks and derive nutrients from moisture in the air and debris as well as mycorrhizae (Jones 2006).
Mycorrhizae: Fungi in the soil which orchids require for growth and nutrients and are often symbiotic (Jones 2006). p.p.m.v: Parts per million by volume (Thomas et al. 2006).
Terrestrial: orchids that predominantly grow on the ground obtaining nutrients from the soil via mycorrhizae (Jones 2006).
12 Threat: An activity or process that causes negative impacts to biodiversity (IUCN
2016).
Threatened species: any species listed as at risk of extinction with the status of vulnerable, endangered or critically endangered on nationally or internationally accredited and recognised list of species under conservation.
Threat syndrome: Interacting threats that often co-occur (Burgman et al. 2007, Wraith and Pickering 2018, 2019).
References
Atlas of Living Australia (2019). Atlas of Living Australia. Accessed December 2019
http://spatial.ala.org.au/.
Burgman, M., D. Keith, S. Hopper, D. Widyatmoko and C. Drill (2007). Threat
syndromes and conservation of the Australian flora. Biological Conservation
134(1): 73-82.
CITES (2019). Convention of International Trade in Endangered Species of Wild Fauna
and Flora. Accessed December 2019 https://www.cites.org/.
Malcolm, J. R., C. Liu, R. P. Neilson, L. Hansen and L. E. Hannah (2006). Global
warming and extinctions of endemic species from biodiversity hotspots.
Conservation Biology 20(2): 538-548.
Jones, D. L. (2006). A complete guide to native orchids of Australia, including the
island territories. Reed New Holland, Sydney.
IUCN (2016). The IUCN Red List of threatened species. Accessed December 2019
https://www.iucnredlist.org/resources/threat-classification-scheme.
IUCN (2019). The IUCN Red List of Threatened Species. Accessed September 2019.
http://www.iucnredlist.org.
13 GBIF (2019). The Global Biodiversity Information Facility. Accessed December 2019
https://www.gbif.org/.
Fischer, M. M., H. J. Scholten and D. Unwin (2019). Geographic information systems,
spatial data analysis and spatial modelling: an introduction. In Spatial
Analytical. Routledge, London 3-20.
Li, J., B. Alvarez, J. Siwabessy, M. Tran, Z. Huang, R. Przeslawski, L. Radke, F.
Howard and S. Nichol (2017). Application of random forest, generalised linear
model and their hybrid methods with geostatistical techniques to count data:
Predicting sponge species richness. Environmental modelling & software
97:112-129.
Thomas, C. D., A. Cameron, R. E. Green, M. Bakkenes, L. J. Beaumont, Y. C.
Collingham, B. F. Erasmus, M. F. De Siqueira, A. Grainger, L. Hannah and L.
Hughes (2004). Extinction risk from climate change. Nature 427(6970): 145.
Wraith, J. and C. Pickering (2018). Quantifying anthropogenic threats to orchids using
the IUCN Red List. Ambio 47(3): 307-317.
Wraith, J. and C. Pickering (2019). A continental scale analysis of threats to orchids.
Biological Conservation 234: 7-17.
14 Chapter 1. Introduction
1.1 Sixth wave of mass extinction
Global biodiversity is currently experiencing a sixth wave of mass extinction with rates predicted to be thousands of times greater than the natural background rate (Pimm and
Raven 2000, Wake and Vredenburg 2008, Swarts and Dixon 2009, Ceballos et al. 2010,
Ceballos et al. 2015, Ceballos et al. 2017). The International Union for the Conservation of Nature (IUCN) Red List, for example, currently includes 873 species as extinct and over 28,000 species at risk of extinction, but as the List only covers 27% of species, the loss of biodiversity is likely to be even greater (Ceballos et al. 2010, IUCN 2019). Other estimates using different methodology give even higher rates with over a million species at risk of extinction (Ceballos et al. 2017). With the exponential increase in the human population, and the increasing impact of climate change, there will be further impacts to the environment (Thomas et al. 2004, Elmhagen et al. 2015). With estimates of this magnitude and rate of extinction only increasing, it is critically important to understand which species are at risk, what threatens them and where, so action can be taken to conserve global biodiversity.
1.2 Threats to global plant biodiversity
The IUCN Red List is the most comprehensive global database of threatened species as it uses a standardised set of criteria for listing species and threats and, as such, is a valuable resource for understanding global patterns in biodiversity and threats, particularly for flowering plants (Brummitt et al. 2015). The Red List currently includes
~14,000 plants, affected by anthropogenic activities (IUCN 2019). The most common threats are development for housing (26% species on the list), agricultural processes such as small holder farming (21%), livestock farming (16%), logging (19%),
15 increasing fire intensity (16%), plant collecting (15%) and shifting agriculture (14%)
(Figure 1.1). Threats such as these will only grow as the human population increases and as such it is important that we understand how they are affecting plants at a global scale in order to better conserve biodiversity.
Figure 1.1. The most common threats to the ~14,000 plants on the IUCN Red List, with the number of species in green. Adapted from the IUCN Red List (2019).
Habitat loss due to land clearing and fragmentation is a common threat to plants globally and the leading cause of extinction (Pimm and Raven 2000, Keil et al. 2015,
Tilman et al. 2017 ). This reflects the extensive loss of natural vegetation in many regions of the world, with 2.3 million km2 of forest lost between 2000-2010 globally
(Krauss et al. 2010, Hansen et al. 2013). Forest loss is expected to increase due to activities such as land clearing for development and agriculture (Krauss et al. 2010,
Hansen et al. 2013) as well as climate change (Thomas et al. 2004, Mitchard 2018). The loss of forests and other habitat has devastating impacts on many plants, particularly locally endemic species and those with niche ecosystem requirements dependent on functioning forests (Keil et al. 2015, Orsenigo et al. 2018).
16 Overexploitation is also a common threat to plants globally, including impacts from logging and the illegal collection of plants from the wild (Brummitt et al. 2015,
Maxwell et al. 2016, IUCN 2019). For instance, it was estimated that approximately
1,200 km2 of forest were logged within conservation areas each year, contributing to plant extinctions (Asner et al. 2005). These activities, even though detrimental to the environment, are lucrative and thus continue to thrive. For example, wild plant collection is estimated to be worth $21 billion per year and is driven by the use of plants in medicine, horticulture and food (Oldfield 2003, Rosen and Smith 2010). Rare and threatened species are seen as more desirable than common species by plant collectors, further contributing to the risk of extinction for some rare species (Flores-Palacios and
Valencia-Diaz 2007, Challender et al. 2015, Goettsch et al. 2015). To restrict the illegal wildlife trade, the Convention on International Trade in Endangered Species (CITES) was implemented, and it includes strict guidelines and regulations on the global trade in threatened species (Challender et al. 2019). However, even with these guidelines in place, threatened species are still collected in the wild and traded, including from protected areas (Rivalan et al. 2007, Challender et al. 2019, Lawson et al. 2019).
Tourism and recreation is increasingly recognised as a threat to many plants, including those in protected areas (Ballantyne and Pickering 2012, Ballantyne and Pickering
2013, Rankin et al. 2015). Although a significant contributor to the global economy, there are a wide range of environmental impacts from tourism and recreation that contribute to species decline and extinction (Pickering et al. 2007, Balmford et al. 2009,
Newsome et al. 2012, Monz et al. 2013, UNWTO 2015). Impacts from tourism and recreation on plants include those associated with the construction and use of tourism facilities, those from transport and accommodation, as well as those associated with specific tourism activities, such as trampling from hikers, mountain bikers, horses and
17 recreational vehicles (Liddle 1997, Kelly et al. 2003, Pickering et al. 2007, Holden
2016). Currently outdoor recreation is the single most common threat to the 2,733 rare and vulnerable plants listed as at risk of extinction within the United States, negatively affecting 35% of species (Hernández-Yáñez et al. 2016). In Europe, tourism and recreation threatens 42% of the 194 vascular plants on the IUCN Red List (Ballantyne and Pickering 2013), while in Australia, tourism and recreation threatens 42% of the
659 vascular plants listed as at risk of extinction by the Australian Government (Rankin et al. 2015).
The major threat to plant diversity is increasingly climate change (Bakkenes et al. 2002,
Jump and Penuelas 2005, Dullinger et al. 2012, Parmesan and Hanley 2015). Modelling indicates that that even mid-range temperature increases of 1.8–2.0°C and CO2 increases of 500–550 p.p.m.v will cause the extinction of 15-37% of locally endemic species by 2050, including 56,000 endemic plant species from biodiversity hotspots
(Thomas et al. 2004, Malcolm et al. 2006). Extinction rates this severe will have a lasting impact on global biodiversity, particularly for already threatened species and their ecosystems which are already at two times higher risk of extinction than non- threatened species (Bitencourt et al. 2016).
Threats to biodiversity often interact and hence occur as threat syndromes (Burgman et al. 2007, Wraith and Pickering 2018, Wraith and Pickering 2019). This includes when there are complex interactions between different threatening processes and ecological factors such as habitat types and/or species growth forms (Burgman et al. 2007). For example, 424 threatened plants in Australia were impacted by threat syndromes incorporating land clearing for roads, weeds and fire (Burgman et al. 2007).
Characterising threats and threat syndromes can help identify appropriate conservation and management strategies leading to more efficient and effective conservation.
18 However, there is limited research analysing threats spatially, including at a large scale and hence identifying complex large-scale threat syndromes is important (Evans et al.
2011).
1.3 Research on plant conservation
With the scale and severity of damage to natural ecosystems increasing, particularly from specific types of anthropogenic activities, there is increasing interest in plant conservation research. This can be seen in databases of academic literature, with over
48,600 research and review articles (on plant conservation) listed on the large academic database Scopus, with the number of articles increasing dramatically in the last few years (Figure 1.2).
4000
3500
3000
2500
2000
1500
1000
500
0 1969 1974 1979 1984 1989 1994 1999 2004 2009 2014 2019
Figure 1.2. The number of research and review articles published per year on plant conservation based on data from Scopus, using the search terms ‘plant’ and
‘conservation’ in October 2019.
When the data from Scopus was analysed, the diversity of research on plant conservation was apparent. This includes a diversity of researchers, with authors from
19 159 countries contributing, although it is dominated by researchers from the United
States of America (17%), China (8%), the United Kingdom (8%), Germany (5%) and
Australia (4.5%). Much of the research falls within the broad disciplines of agricultural and biological sciences (30,857 articles), environmental science (20, 234), biochemistry, genetics and molecular biology (10,879) and earth and planetary sciences (2,709). The four most diverse families of flowering plants are the focus of much of this research, including articles examining Poaceae (2,667 articles), Orchidaceae (1,449), Fabaceae
(1,393), and Asteraceae (1,076) (Figure 1.3).
Figure 1.3. The number of research and review articles on the conservation of the most diverse families of flowering plants. The number of papers per family were identified by searching the family name and synonyms combined with ‘conservation’ on Scopus and cover the period 1969-2018.
Although the literature on plant conservation is extensive, there are few studies looking at large scale patterns in threats (Brummitt et al. 2015, Orsenigo et al. 2018, Schulze et al. 2018). As plant biodiversity is rapidly declining it is important to focus research on large scale patterns in threats so we can understand where and why species are threatened, what is threatening them, what is the impact of threat syndromes and how
20 we can conserve species more effectively. This is particularly important for taxonomic groups where large numbers of species are at risk of extinction such as orchids.
1.4 Why are orchids important?
Orchidaceae is a highly diverse group of flowering plants accounting for ~10% of angiosperms worldwide, with ~28,000 species in 850-1,000 genera (Cribb et al. 2003,
Jones 2006, WCSP 2016). Unfortunately, they are also among taxa most at risk of extinction, with the Orchidaceae having the highest proportion of threatened genera of all plant families (Swarts and Dixon 2009). At least 5% of orchids are threatened, with
1,399 species on the IUCN Red List, many of which are critically endangered or endangered (Figure 1.4). The true scale of the threats to orchids is likely to be even greater, with the IUCN Red List known to underestimate the total number of orchids threatened, including in specific regions such as Australia and much of Africa (Wraith et al. In press).
Total CR EN VU DD NT LC extant Orchids 1399
0 0.2 0.4 0.6 0.8 1 Proportion of extant orchid species
Figure 1.4. The proportion of threatened orchid species on the IUCN Red List (2019) where the numbers to the right of each bar represent the total number of extant species assessed with CR = critically endangered, VU = vulnerable, NT = near threatened, DD
= data deficient and LC = least concern.
The orchid family is widespread with species found on every continent except
Antarctica (Jones 2006). They also occupy a range of habitats and climatic zones from high alpine tundras to woodlands, although the greatest diversity is found in tropics,
21 particularly in rainforests (Jones 2006). As a result hotspots of orchid diversity include some parts of South America, meso-America, Madagascar, Indo-China and South-west
China, Sumatra, Borneo, Papua New Guinea, and Australia (Cribb et al. 2003). In
Australia there are ~1,794 orchid species, with a high diversity of ground orchids, including in temperate as well as tropical parts of Australia (Jones 2006). Many of the orchids in Australia are at risk of extinction, with 184 listed as threatened by the
Australian Government, although very few of these are currently included on the IUCN
Red list (Wraith and Pickering 2019). Unfortunately, globally and in Australia, most ecosystems rich in orchid diversity are also affected by habitat loss, climate change and exploitation of natural resources (Kull and Hutchings 2006, Swarts and Dixon 2009).
Even though orchids are highly diverse, many species are also inherently rare due to small population sizes, narrow ranges and specific symbiotic associations with fungi and pollinators, resulting in specialised habitat requirements (Nilsson 1992, Cozzolino and Widmer 2005, Roberts and Dixon 2008). These factors create a complex ecology that relies on the success of a range of species-specific interactions and abiotic factors
(Shefferson et al. 2019). Unfortunately, with the current scale of environmental change, many of these interactions as well as abiotic factors are changing rapidly, increasing the risk of extinction for orchids and, in some cases, their symbionts as well (Swarts and
Dixon 2009, Liu et al. 2010, Seaton et al. 2010, Wraith and Pickering 2019). The high diversity, occurrence across much of the globe, but also a high proportion of threatened species, makes orchids an important plant family to conserve. This includes assessing threatening processes including where species are threatened, by what and what can be done to conserve them.
Many orchids are charismatic with large and unusual flowers highly prized for their beauty as well as rarity (Nash 2003, Ballantyne and Pickering 2012). There is a long
22 history of people collecting orchids from the wild. This obsession with rare orchids known as ‘orchidelirium’ peaked in the 19th century in Europe and North America
(Ghorbani et al. 2014). Orchid collecting continues to be an issue, with popular books such as the Orchid Thief (Orlean 2000) and Orchid Fever (Hansen 2016) highlighting the scale and peculiar nature of the hunt for orchids in the wild and how they are valued by collectors.
Wild orchids are also collected for medicinal purposes with many species used in
Chinese, African and North American traditional medicine and as such are traded globally (Hinsley et al. 2017). Some orchids are also used as a food source with around
35 species harvested to produce Salep, a traditional tea and dessert in the Middle East contributing to declines in these species (Ghorbani et al. 2014, Hinsley et al. 2017). The global interest in orchids can also be seen in the scale and size of orchid societies, and orchid specific events such as conferences, with major international conferences held every three years, for example, the World Orchid Conference and Exhibition which attracts thousands of people to both a conference and exhibition showcasing displays on orchid conservation and propagation.
The economic value of the trade in orchids is large, with their export from the
Netherlands worth around 65 million Euros per year (Statista 2017). In the USA potted orchids are worth nearly $US300 million per year, while cut orchid flowers are worth another $US8 million (National Agricultural Statistics Service 2016). Orchids such as
Vanilla, which are used as flavouring, are also valuable and currently represent 20% of
Madagascan exports, worth around $US600 million (The Economist 2018). Orchid species made up ~19% of all commercially traded plants between 2006-2015 and hybrids another ~29% (Hinsley et al. 2017). Unfortunately, due to this popularity in commercial trade there is also an intense illegal collecting and harvesting culture,
23 contributing to rapid declines in many species including members of the Paphiopedilum and Cypripedium genera (Cribb and Sandison 1998, Liu et al. 2006).
To combat threats from overharvesting, the trade in all wild orchids among countries is restricted under the Convention on International Trade in Endangered Species (CITES)
(Lawson et al. 2019). However, even with strict regulations, there are still black markets trading wild orchids within and between countries (Roberts and Dixon 2008, Lawson et al. 2019). For example, 347 orchid species in South East Asia are illegally collected and sold, contributing to population declines (Phelps and Webb 2015). The effectiveness of the current CITES regulations and other protocols require revision and stricter implementation to successfully reduce the illegal orchid trade (Lawson et al. 2019).
With orchid numbers continuing to decline as a result of human activities it is increasingly important that we understand specifically what is threatening them and where, if they are impacted by threat syndromes and to establish conservation and research priorities.
1.5 Aims
Orchids are not only highly diverse, but also among the most threatened plants globally.
With orchid numbers declining due to anthropogenic threats, it is important to better understand what is threatening them and where. This includes mapping orchids and their threats, identifying which habitats contain threatened orchids, which life forms and genera of orchids are particularly at risk and if and where threats co-occur as threat syndromes. This thesis uses authoritative data sources such as the IUCN Red List and the Australian Government species listings to analyse threats to orchids, including spatial patterns of threats, and identifies research and conservation priorities.
24 The aims of this thesis are to determine:
1) The major threats to orchids at a global and continental scale using data from the
IUCN Red List, threatened species listings and species occurrence records (Chapters 2,
3, 4).
2) If orchids are impacted by threat syndromes (Chapters 2, 3, 4).
3) Where threats to orchids occur and which habitats are most at risk (Chapters 2, 3, 4).
4) The impact of threats on orchid life forms and genera (Chapters 2, 3, 4).
5) Trends and gaps in orchid conservation and research to identify key priorities for future work using bibliometric data from Scopus, data from the IUCN Red List and species occurrence records (Chapter 5).
1.6 Structure of the thesis
This thesis has been prepared as a series of published and unpublished papers in accordance with Griffith University’s Policy on the form of thesis (Appendix A). The thesis therefore consists of six Chapters: A general introduction (Chapter 1), two studies at a global scale using data from the IUCN Red List, the first which assesses all threats to orchids (Chapter 2), and a second which looks specifically at tourism and recreation as a threat (Chapter 3), a continental scale analysis of threats to orchids including a spatial analysis of threats using data from the Australian Government and the Atlas of Living Australia (Chapter 4), an analysis of research on orchid conservation using the research database Scopus combined with an analysis of conservation and research priorities using data from the IUCN Red List (Chapter 5), and finally a general discussion and conclusion synthesising the results in relation to the broader thesis aims and literature (Chapter 6) (Figure 1.5).
25 The four results Chapters (Chapters 2-5) are in the form of manuscripts formatted to meet the requirements of the peer-reviewed academic journals where they have been published. As a result, there is some repetition among the Chapters, and each contains its own reference lists. Tables and figures are also formatted in accordance with the requirements of the journals. The details of the papers, authors’ contributions, and publication status are also given at the beginning of each results Chapter. This thesis includes published papers and papers in press with Chapters 2, 3, 4 and 5 consisting of peer reviewed and co-authored papers with other researchers. Also, some research has also already been presented at national and international academic conferences as well as to orchid societies.
26
Introduction (Chapter 1)
Global threats to orchids
Quantifying global threats to orchids Tourism and recreation as a global (Chapter 2) threat to orchids Paper published in (Chapter 3) Ambio Paper published in Biodiversity & Conservation
Continental threats and spatial analyses
A continental scale analysis of threats to orchids (Chapter 4) Paper published in Biological Conservation
Conservation and research priorities
Research and conservation priorities for globally Red Listed orchids
(Chapter 5) Paper In press in Ambio
Discussion and Conclusions (Chapter 6)
Figure 1.5. Schematic overview of the content and structure of the thesis.
27 1.7 Published and submitted papers included as results Chapters in the thesis.
Chapter 2: Wraith, J., and C. Pickering (2018). Quantifying anthropogenic threats to orchids using the IUCN Red List. Ambio. 47(3), 307-317.
Chapter 3: Wraith, J., and C. Pickering (2017). Tourism and recreation a global threat to orchids. Biodiversity and Conservation. 26(14), 3407-3420.
Chapter 4: Wraith, J., and C. Pickering (2019). A continental scale analysis of threats to orchids. Biological Conservation. 234, 7-17.
Chapter 5: Wraith, J., P. Norman, and C. Pickering (2019). Orchid conservation and research: an analysis of gaps and priorities for globally Red Listed species. Ambio (In press).
1.7.1 Other publications completed during candidature but not included in this thesis:
1.7.2 Related published papers
Lawson, C., J. Wraith, and C.M. Pickering (2019). Regulating wild collected orchids?
The CBD, Nagoya Protocol and CITES overlaps. Environmental and Planning Law
Journal. 36: 339-361.
1.7.3 Conference presentations and talks to orchid societies
Wraith, J., and C. Pickering (2019). A continental scale analysis of threats to orchids
(Lecture and Newsletter publication). Australasian Native Orchid Society, Melbourne,
Australia (Invited speaker). 5th July 2019.
Wraith, J., and C. Pickering (2019). A continental scale analysis of threats to orchids
(Conference and abstract). Orchid Conservation Symposium, Melbourne, Australia
(Invited speaker).18th-19th June 2019.
28 Wraith, J., and C. Pickering (2019). A continental scale analysis of threats to orchids
(Conference and abstract). 7th International Orchid Conservation Congress, Kew
Gardens, United Kingdom. 28th May-1st June 2019.
Wraith, J., and C. Pickering (2018). A continental scale analysis of threats to orchids
(Conference and abstract). Ecological Society of Australia Annual Conference,
Brisbane, Australia. 25th-29th November 2018.
Wraith., J and C. Pickering (2017). Tourism and Recreation a global threat to orchids
(poster presentation and abstract). 22nd World Orchid Conference, Guayaquil, Ecuador.
8th-12th November 2017.
Wraith, J., and C. Pickering (2017). Orchid Conservation: Assessing Impacts from
Tourism and Recreation (Lecture and newsletter publication). W.A. Orchid Spectacular
Conference and Show, Perth, Australia. 5th-6th August 2017.
1.7.4 Other publications
Wraith., J. (2019). Orchid conservation and a continental scale analysis of threats to orchids in Australia. Australasian Native Orchid Society (Victorian Group) Inc
Bulletin. 52(2):5-6.
Wraith., J. (2018). Orchid research news and quantifying anthropogenic threats to orchids using the IUCN Red List. Australasian Native Orchid Society Newsletter. 7.
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37 Chapter 2. Quantifying global threats to orchids
The previous Chapter presents the background, aims and structure of the thesis. The current Chapters is the first results Chapter of the thesis and presents a systematic quantitative analysis of threats to orchids at a global scale using data from the IUCN
Red List. It examines the different types of threats to orchids, including spatial patterns in where orchids are threatened, and how some threats occur as syndromes. It also examines, patterns in threats and threatened orchids between habitats, life forms and genera. In doing so it provides an overview of the diversity and severity of different threats to orchids, while also assessing the benefits and limitations of data from the
IUCN Red List.
This Chapter consists of the published version of a paper co-author with my principle supervisor. The bibliographic details of the paper, including all authors, are: Wraith, J., and C. M. Pickering (2018) Quantifying anthropogenic threats to orchids using the
IUCN Red List. Ambio 47(3): 307-317.
My contribution to the paper involved: research design, methodology, data collection and the compilation of the threatened orchid database, data analyses, drafting of the manuscript, tables and figures and submission to the journal.
(Signed): (Date): 17 December, 2019 Jenna Lee Wraith (Counter signed): (Date): 17 December, 2019 Professor Catherine Marina Pickering
A full copy of this paper is available at the publisher’s website via the following link: https://link.springer.com/article/10.1007/s13280-017-0964-0
38 39 Chapter 3. Tourism and recreation a global threat to orchids
The previous Chapter presented an overview of key threats to orchids globally based on the
IUCN Red List including highlighting that tourism and recreation threatens orchids. This second results Chapter provides a more detailed analysis of tourism and recreation as a threat to orchids. It again uses the IUCN Red List data, but examines the severity, scope and timing of tourism and recreation as a threat at a global scale in more detail. This includes examining three types of tourism and recreation threats including development for tourism and recreation, recreational activities and plant collecting in protected areas. Spatial patterns in where these three threats occur is assessed along with correlations between habitat, life form and genera.
This Chapter consists of the published version of a paper co-author with my principle supervisor. The bibliographic details of the paper, including all authors, are: Wraith, J., and
C. M. Pickering (2017). Tourism and recreation a global threat to orchids. Biodiversity and
Conservation 26(14): 3407-3420.
My contribution to the paper involved: research design, methodology, data collection and the compilation of the threatened orchid database, data analyses, drafting of the manuscript, tables and figures and submission to the journal.
(Signed):
(Date): 17 December, 2019
Jenna Lee Wraith
(Counter signed):
(Date): 17 December, 2019
Professor Catherine Marina Pickering
A full copy of this paper is available at the publisher’s website via the following link: https://link.springer.com/article/10.1007/s10531-017-1412-y
50 51 Chapter 4. A continental scale analysis of threats to orchids
The previous Chapters highlighted threats to orchids globally including from tourism and recreation. This Chapter looks at a continental scale and provides more detailed mapping of threatening processes to orchids. Specifically, it examines threats to orchids in Australia by coding threat data from the Australian Government and species occurrence records from the
Atlas of Living Australia. This data is used to map the distribution of threats using an interpolation analyses to highlight where there are threats and threat syndromes within
Australian. Statistical analysis is also used to highlights key drivers for common threats. As a result, the study provides a novel approach to understanding threats to orchids including how to determine at risk areas for orchids and appropriate habitats for orchid translocations.
This Chapter consists of the published version of a paper co-author with my principle supervisor. The bibliographic details of the paper, including all authors, are: Wraith, J., and
C. M. Pickering (2019). A continental scale analysis of threats to orchids. Biological
Conservation 234: 7-17.
My contribution to the paper involved: research design, methodology, data collection, data analyses, spatial analyses, drafting of the manuscript, tables and figures and submission to the journal.
(Signed): (Date): 17 December, 2019 Jenna Lee Wraith (Counter signed):
(Date): 17 December, 2019 Professor Catherine Marina Pickering
A full copy of this paper is available at the publisher’s website via the following link: https://www.sciencedirect.com/science/article/abs/pii/S0006320718315179
65 66 Chapter 5. Research and conservation priorities for globally Red Listed orchids
The previous Chapters determined the major threats to orchids including at a global and
continental scale and mapped the distribution of threats to orchids. These Chapters identified
important threat syndromes and interactions between threats and habitats, life form and
genera of orchids. Having done so, it was important to the assess global priorities to mitigate
threats to orchids.
The fourth results Chapter of the thesis therefore analyses IUCN Red List data, global species
occurrence records and bibliometric data on orchid conservation to highlight trends in orchid
conservation research and spatially assess priorities for orchid conservation globally. This
Chapter analyses the data to make key recommendations for future orchid conservation and
research at a global scale to be utilised by orchid researchers and conservationists.
This Chapter consists of the version of a paper in press co-authored with my principle
supervisor and another co-author who assisted with guidance on spatial analysis and species
occurrence data collection. The bibliographic details of the paper, including all authors, are:
Wraith, J., P. Norman and C. M. Pickering (2019). Research and conservation priorities for
globally Red Listed orchids. Ambio (In press).
My contribution to the paper involved: research design, methodology, data collection, data
and statistical analyses, spatial analysis, drafting of the manuscript, tables and figures and
submission to the journal.
A full copy of this paper is available at the publisher’s website via the following link: https://link.springer.com/article/10.1007/s13280-019-01306-7
77 (Signed):
(Date): 17 December, 2019
Jenna Lee Wraith
(Counter signed):
(Date): 17 December, 2019
Professor Catherine Marina Pickering
(Counter signed):
(Date): 17 December, 2019
Patrick Norman
78 Title:
Orchid conservation and research: an analysis of gaps and priorities for globally Red Listed species
Abstract:
Orchids are among the most threatened taxa globally due to increasing anthropogenic threats, inherent rarity and specific conservation needs. But what are the global research and conservation priorities for this charismatic group of plants? Using information for 595 orchids on the IUCN Red List we reviewed past research and identified key research and conservation priorities. These included understanding threats, monitoring orchid populations and habitats, species management in ex-situ conservation, genome resource banks and artificial propagation, land and habitat protection and education and awareness through communication. Based on the available data we recommend future orchid conservation and research should focus on the current gaps in knowledge and practice including monitoring population trends and distributions, ecology, threats, protection and management of species and their habitats and increasing education and awareness.
Keywords:
Anthropogenic threats, Conservation, Global biodiversity, IUCN Red List, Threatened species.
Introduction:
Species conservation is increasingly important globally as biodiversity is declining rapidly, with over a million species currently threatened with extinction (Ceballos et al. 2010, Ceballos et al. 2015, Díaz et al. 2019). Threats to global biodiversity are widespread, diverse and mostly stem from anthropogenic activities such habitat loss as a result of land clearing and development, climate change, pollution and over-exploitation (Brook et al. 2008, Stork 2010, Hanski 2011, Urban 2015,
Valiente‐Banuet et al. 2015, Díaz et al. 2019). The rate at which species are declining is only increasing as is the scale and extent of threats (Larsen et al. 2011, Wraith and Pickering 2019). With such a time crisis, it is critical that we prioritise research and conservation, including for at risk taxa such as orchids (Larsen et al. 2011).
79 Orchids are highly diverse with over 27, 000 species in ~1000 genera with populations found on all continents across the globe other than Antarctica (Swarts and Dixon 2009a). They occupy a vast range of habitats from high alpine tundra to tropical rainforests, with their success in part attributed to their ability to grow in the soil (terrestrial form), on trees (epiphytic form) or on rocks (lithophytic form).
However, they are also one of the worlds most threatened taxonomic groups (Wraith and Pickering
2018) with over 600 species of orchids listed as threatened on the global database of threatened species maintained by the International Union for the Conservation of Nature, known as the IUCN
Red List (IUCN 2019).
The threatened status of many orchids is partly a result of their intrinsic rarity due to factors such as small population sizes, limited distributions and species-specific symbioses with pollinators and mycorrhizal fungi (Swarts and Dixon 2009a, Seaton et al. 2013). This creates a complex ecology that relies on the success of a range of species specific interactions and abiotic factors which are being eroded by climate change, habitat modification and altered land use (Swarts and Dixon 2009a, Liu et al. 2010a, Seaton et al. 2010, Wraith and Pickering 2019). These threats, along with increasing impacts of invasive species, changes in fire regimes and illegal collecting are the most common threats to orchids globally and often co-occur as threat syndromes (Wraith and Pickering 2018, Wraith and Pickering 2019). Orchids are highly charismatic, with a long history as the objects of desire for collectors, contributing to population and species declines (Ghorbani et al. 2014, Hinsley et al. 2017b,
Wraith and Pickering 2017). Due to the specialised biotic factors and threat syndromes, successful conservation of orchids in the wild is often difficult and requires the input of a range of research disciplines.
Historically research on orchid conservation has focused on taxonomy including identifying and describing new species (Swarts and Dixon 2009a). More recently with emerging technology there has been a shift in research examining the molecular biology of orchids, including orchid mycorrhizal associations (Liu et al. 2010b, McCormick et al. 2012, McCormick and Jacquemyn 2014) contributing to conservation by facilitating successful propagation of many threatened orchids. Other emerging research fields in orchid conservation include pollination biology, species distributions and methods
80 for translocating orchids for both in-situ and ex-situ conservation. As the success of orchid conservation relies on all these fields an integrated approach has been suggested to incorporate factors such as threats with species specific associations, and ex-situ and in-situ conservation (Swarts and
Dixon 2009a, Liu et al. 2010b).
With orchid numbers continuing to decline in most regions globally (Fay 2018, Wraith and Pickering
2018, Wraith and Pickering 2019), it is important to review current research, and identify research priorities and conservation goals. We assist this process using data from the IUCN Red List and other sources to answer the following questions: 1) what are the trends in orchid conservation research? 2) what are key research priorities for orchid conservation globally? 3) what are the key conservation priorities for threatened orchids globally? 4) what factors influenced conservation priorities?
Methods:
Data collection:
To determine trends in orchid conservation research, bibliometric data was collected from the online academic literature database Scopus in July 2019. This well-regarded database covers ~70 million publications globally and can be searched using keywords and authors (Martín-Martín et al. 2018).
Scopus was searched for all articles and reviews containing the terms orchid, orchids or Orchidaceae and conservation, conserve or conserved in the title, abstract or key words. The search was limited to
English only publications and excluded publications that did not relate to orchid plants including those in medicine and pharmacology, toxicology and pharmaceutics. Information on publications was downloaded from Scopus including authors names, the organisations they are associated with, including in which countries, the year published, publisher, source and author keywords.
To assess global research and conservation priorities for threatened orchids, data was collected from the IUCN Red List in May 2019. It was searched for all threatened orchids listed as critically endangered (CR), endangered (EN) and vulnerable (VU) and then data transferred over into a personal database. This included taxonomic data for all 595 orchid species listed as CR, EN and VU
(IUCN 2019). Additional data included information for each species, threats, land regions and growth
81 form as well as all listed research priorities (three broad categories and 13 subcategories) and conservation priorities (six broad categories and 36 subcategories) (Figure 2). Then to determine if there were taxonomic patterns in the data, the tribes for each genus were included using data from the
NCBI taxonomy database and accompanying literature (Sayers et al. 2009).
82
a. 1.1. ResearchResearch 1.1.1.1. TaxonomyTaxonomy 1.2.1.2. PopulationPopulation size,size, distributiondistribution && trendstrends 1.3.1.3. LifeLife historyhistory && ecologyecology 1.4.1.4. Harvest,Harvest, useuse && livelihoodslivelihoods 1.5.1.5. ThreatsThreats 1.6.1.6. ActionsActions 2.2. ConservationConservation PlanningPlanning 2.1.2.1. SpeciesSpecies Action/RecoveryAction/Recovery PlanPlan 2.2.2.2. Area-basedArea-based ManagementManagement PlanPlan 2.3.2.3. HarvestHarvest && TradeTrade ManagementManagement PlanPlan
3.3. MonitoringMonitoring Research prioritiesResearch Research prioritiesResearch 3.1.3.1. PopulationPopulation trendstrends 3.2.3.2. HarvestHarvest levellevel trendstrends 3.3.3.3. TradeTrade trendstrends 3.4.3.4. HabitatHabitat trendstrends 00 200200 400400 600600 NumberNumber ofof orchidorchid speciesspecies b. 1. Land/water protection 1.1. Site/area protection 1.2. Resource & habitat protection 2. Land/water management 2.1. Site/area management 2.2. Invasive/problematic species control 2.3. Habitat & natural process restoration 3. Species management 3.1. Species management 3.1.1. Harvest management 3.1.2. Trade management 3.2 Species recovery 3.3. Species re-introduction 3.3.1. Reintroduction 3.3.2. Benign introduction 3.4 Ex-situ conservation 3.4.1. Artificial propagation 3.4.2. Genome resource bank 4. Education & awareness 4.1. Formal education 4.2. Training 4.3. Awareness & communications 5. Law & policy 5.1. Legislation 5.1.1. International level
Conservation priorities Conservation 5.1.2. National level 5.1.3. Sub-national level 5.1.4. Scale unspecified 5.2. Policies and regulations 5.3. Private sector standards & codes 5.4. Compliance and enforcemen 5.4.1. International level 5.4.2. National level 5.4.3. Sub-national level 6 Livelihood, economic & other incentives 6.1. Linked enterprises & livelihood alternatives 6.2. Substitution 6.3. Market forces 6.4. Conservation payments 0 200 400 600 Number of orchid species
Figure 2. A summary of the 491 threatened orchids on the IUCN Red List for and (a) their future research priorities (1-3) and subcategories and (b) their conservation priorities (1-6) and subcategories.
83 To highlight spatial patterns in conservation priorities data on the distribution of each of the species was collected where available. This included 18 464 occurrence records for 565 of the 595 threatened orchid species from the Global Biodiversity Information Facility (GBIF) obtained using the rgbif package using R and RStudio (RStudioTeam 2016, Chamberlain et al 2019, Team 2019). After removing duplicates, occurrences with missing or suspect coordinates and those collected before
1969, the total data was reduced to 6471 unique occurrence records covering 432 species.
Data analysis:
To highlight trends in orchid conservation research, the bibliometric data from Scopus was analysed and the results visually presented as networks using VOSviewer software tool which supports in constructing and visualizing bibliometric networks (Centre for Science and Technology Studies
2019). Specifically, we analysed co-occurrences of all keywords listed by authors that occurred in 10 or more publications. For threatened orchids on the IUCN Red List descriptive statistics were calculated to identify the most common research and conservation actions listed for the most common orchid tribes. Chi-square (χ2 ) analyses were conducted to determine if there were significant differences in Conservation status depending on the tribe using R (R Core Team 2019). Bray Curtis cluster analyses were then conducted to determine patterns between threats to orchids and specific conservation priorities (Clarke and Gorley 2006).
To determine the geographical pattern in threatened orchids and conservation priorities, occurrence records for each species were linked with the corresponding conservation priorities using R (R Core
Team 2019). Then species richness of threatened orchids was calculated per country and mapped using QGIS (QGIS Development Team 2019). Finally pie charts showing conservation priorities were overlayed for the 20 counties with the largest number of threatened orchids.
Results:
What are the trends in orchid conservation research?
Research on orchid conservation had increased over the past 20 years, but mainly in the last few years with an average of 118 publications per year from 2010-2018 (Figure 1a). The overall literature is
84 large with 1449 documents published since 1969 and is diverse in terms of the range of authors, where they are from, and the topics they examined. For example, authors from more than 93 countries have contributed to the literature, but many authors are from the United States of America (17%),
Brazil (12%), China (11%), the United Kingdom (10%) or Australia (9%). Some organisations were heavily involved in orchid research including the Royal Botanic Gardens, Kew in the United
Kingdom, which is responsible for 6% of the publications, while the Chinese Academy of Sciences
(5.5%), the University of Western Australia (3%), the University of Florida in the USA (2%) and
Kings Park and Botanic Gardens, also in Western Australia (2%) have also contributed. Orchid conservation attracts a wide range of researchers with more than 150 authors authoring four or more publications, and one author, K. Dixon, authoring 2% of all the research. In terms of disciplines, research was mainly in agricultural and biological sciences (1270 articles), biochemistry, genetics and molecular biology (338) and environmental science (314).
There were four broad themes to orchid research to-date: genetics, fungi, propagation and pollination
(Figure 1b). Genetic research included conservation and population genetics, genetic structure and microsatellite markers and was linked with research on the mycorrhizal fungi of terrestrial and epiphytic orchids. Much of the research on fungi examined species-specific interactions between fungi and orchids, including the fungal genus, Tulasnella. A second theme was orchid propagation including seed germination, protocorms, micropropagation including Phalaenopsis orchids. Research on pollination focussed on specific orchids and/or euglossine bees, with many articles conducted in the Atlantic forest of Brazil. Less common was research on habitat fragmentation and climate change.
85
a. b. 160
140
120
100
80
60 Number of articles & reviews & articles of Number
40
20
0 1968 1978 1988 1998 2008 2018 Year
Figure 6. The number of research articles per year (a) and common themes in orchid conservation based on author keywords (b) using data from Scopus.
86 What are key research priorities for orchid conservation globally?
Research is a priority for 82.5% of the 595 orchids on the IUCN Red List. Most often this was research on population size, distribution and trends (390 species). Research on threats (282) and potential actions (223) were also important, in contrast to taxonomy which was only listed for 49 species. Monitoring was a priority for 333 species with the monitoring of populations (311) and habitats (241) commonly listed. Research on conservation planning was a priority for 107 species with species action and recovery plans the main focus (97) (Figure 2a).
What are the key conservation priorities for threatened orchids globally?
The four main conservation priorities for orchids were: 1) land/water protection (455 species), 2) land/water management (309), 3) species management (455) and 4) education and awareness (300)
(Figure 2b). At a finer scale (sub categories), the most common priorities were species management in ex-situ conservation (435 species), genome resource banks (400) and artificial propagation (284), land protection for the site/area (233) and habitat protection (233), management for the site/area (309) and education and awareness through communications (293).
What factors influenced conservation priorities?
There were clear patterns in the taxonomic affiliation of orchids on the Red List. Although orchids on the IUCN Red List represent 26 different tribes, most on the list belong to one of six tribes. The most common was Vandeae (116 species) and Orchideae (93), most of which were endangered.
Cypripedilinae (84) were mostly critically endangered, Dendrobieae (77) were most vulnerable,
Cypripedieae (47) were mostly endangered, and Epidendreae (34 species) included some vulnerable, some endangered and some critically endangered species (Table 1). As a result, the proportion of species listed as critically endangered, endangered and vulnerable varied significantly among these six orchid tribes (χ2 test, p < 0.001).
87 Table 1. Orchid tribes with the largest number of species on the IUCN Red List and their specific conservation status which varied significantly among each of the orchid tribes (χ2, p<0.001).
Vulnerable Endangered Critically endangered Total Vandeae 19 64 33 116 Orchideae 15 49 29 93 Cypripedilinae 2 37 45 84 Dendrobieae 31 28 18 77 Cypripedieae 13 22 6 41 Epidendreae 10 15 9 34
There was a complex relationship between orchid tribes and conservation priorities (Figure 3).
Priorities for orchids from the Cypripedieae were diverse and included land management, education and awareness, land protection, law and policy, species management and economic incentives. For orchids from Cypripedilinae, Dendrobieae and Vandeae there were similar priorities, although economic incentives were less important. In contrast, economic incentives were important for orchids in Epidendreae, Malaxideae and Phragmipedieae. For some tribes there were specific priorities, such as for Cranichideae orchids land protection and management were the main priorities for conservation.
88
Figure 3. Number of orchids per tribe (bottom) compared to the listed conservation priorities (top) based on data from the IUCN Red List, displayed as a chord diagram created using the circlize package in R (Zuguang et al 2014). Tribes with few species are labelled as (a) Cranichideae (yellow),
(b) Cymbidieae (dark purple), (c) Malaxideae (light purple), (d) Neottieae (light blue), and (e)
Vanilleae (khaki).
There were clear links between certain types of threats and conservation priorities for the orchids
(Figure 4). For orchids threatened by biological resource use conservation priorities included land management (75% similarity), protection (93% similarity) and species management (93% similarity).
For orchids threatened by human intrusion and disturbance conservation priorities included education and awareness, law and policy (75% similarity). For orchids threatened by pollution conservation priorities included livelihood, economic and other incentives (76% similarity), which were also important for orchids threatened by climate change and severe weather (55% similarity) and transportation and service corridors (65% similarity) (Figure 4).
89
Figure 4. The relationship between the most commonly listed threats (bold lines) and listed conservation priorities (narrow lines) for orchids on the IUCN Red
List. Data was analysed using Bray Curtis cluster analysis (similarity) for threats and conservation priorities affecting over 20 species with the number of species in parentheses.
90 Although conservation priorities for orchids varied among many countries and regions, for most countries with many threatened orchids, land protection was important (Figure 5).
Madagascar, China, Vietnam, United States of America and Mexico have the largest number of threatened orchids and vary in their conservation priorities (Figure 5). Land protection and species management were important for orchids in Madagascar, as was land management, education and awareness, while livelihood, economic and other incentives as well as law and policy were not important. For orchids in China, Vietnam and most countries in South East Asia all six conservation priorities were important, while for orchids in North America and Canada, land protection and management, law and policy, species management and education were most important. Conservation priorities for orchids in Mexico included land protection, law and policy and education and awareness while for orchids in South America and Australia livelihood, economic and other incentives were not as important (Figure 5).
Figure 5. Global pattern is species richness of threatened orchids on the IUCN Red List and their associated conservation priorities (pie charts) for the 20 countries with the largest number of threatened orchids.
91 Discussion
Current research on orchid conservation
With orchids declining due to threats such as habitat loss, climate change and illegal collecting, research on orchids including their conservation is crucial (Reiter et al. 2016, Fay 2018, Wraith and Pickering 2018). Positively, research on orchid conservation has increased including due to the work of a wide range of researchers from many countries and institutions and as a result there is now a large body of literature, most produced in the last 10 years. To date most of the research has focussed on (1) genetics and taxonomy, (2) mycorrhizal associations, (3) propagation and (4) pollination, which all contribute to orchid conservation.
The focus on research into genetic diversity, structure and variation in orchids has been vital for understanding orchid taxonomy, population viability and the threatened status of species contributing to the development of appropriate conservation priorities (Case et al. 1998, Chung et al. 2004, Forrest et al. 2004, Pillon et al. 2007, Swarts and Dixon 2009a, Swarts et al. 2009,
Fay 2018). Studies have successfully linked factors such as a lack of gene flow and increasing levels of inbreeding with threatening processes, highlighting the negative effects of habitat fragmentation as seen for Australian threatened orchids such as Caladenia huegelii and Phaius australis (Swarts et al. 2009, Simmons et al. 2018). Our knowledge of mycorrhizal associations has increased with the development of molecular techniques such as DNA sequencing. This includes information about fungal associates within the genus Tulasnella and Rhizoctonia that are important for the survival of many rare and endangered terrestrial species (Linde et al. 2017,
Reiter et al. 2018). Understanding mycorrhiza associations is particularly important as orchids, unlike most other plants, rely on these relationships for seed germination (Swarts and Dixon
2009b, Yeung 2017, Fay 2018).
Seed germination is one of the most important, yet inherently difficult, challenges in orchid conservation (Reiter et al. 2016). For many orchids, ex situ conservation is important, and the propagation relies on artificial seed germination and therefore mycorrhizal research, for success
92 (Swarts and Dixon 2009b, Reiter et al. 2016). Recently research has focused on protocorm development and cryopreservation techniques particularly for Dendrobium and Phalaenopsis and other attractive species in horticulture, as well as other threatened orchids (Liu et al. 2010b).
Propagation including germination is also important for translocations and/or re-introduction of species into natural habitats. For successful re-introductions information on many aspects of the orchid’s ecology is required including the role of pollinators (Reiter et al. 2016, Reiter et al.
2017, Brundrett 2019). Research into pollination, has focused mainly on euglossine bees.
Although interesting, focussing on this one group of orchids and pollinators that only occur in
South and Central America, is not always useful for orchid conservation more broadly.
Research on pollinators in other regions would be valuable as highly specific pollination syndromes in orchids remains an important issue in conservation (Peakall et al. 2010, Phillips et al. 2015, Reiter et al. 2017) and the loss of pollinators is often listed as a key threat (Wraith and
Pickering 2018). More research on pollination strategies, pollinator species and their distributions facilitate the success of many more orchid re-introductions and translocations
(Phillips et al. 2015, Reiter et al. 2017).
Research priorities
Our analysis of orchids on the IUCN Red List highlighted four major research priorities. The most frequently listed research priority was understanding orchid population sizes, distributions and trends. This includes research on species distribution modelling and the impacts of climatic change, which has not been a major focus of research to date. Monitoring populations and their habitats is another priority and requires field surveys and long-term habitat assessments (Kull et al. 2008, Liu et al. 2010a). The ecology and life history of orchids is complex and an important priority for conservation research, with specific associations between many orchid species and specific mycorrhizae, pollinators, seed dispersal (Swarts and Dixon 2009a, Reiter et al. 2018).
Understanding key threats to orchids and identifying practical solutions to eliminate or mitigate threats is a high priority for orchid conservation. For instance, many orchids are affected by habitat loss from development, agriculture, roads, forestry, grazing, fire and illegal collection,
93 but there are other less common threats that need further investigation, including the impact of small population sizes, loss of pollinators and climate change (Wraith and Pickering 2018,
Wraith and Pickering 2019). The least important research priority for orchids on the IUCN Red
List was taxonomy, and research on harvest and trade management plans. Although illegal collecting and harvesting is a known threat, orchids still suffer from black market trade including for collecting and products such as Salep and traditional medicines (Ghorbani et al.
2014, Hinsley et al. 2017a, Hinsley et al. 2017b). With all orchids listed on the Convention on
International Trade in Endangered Species (CITES) list, there are strict limits on orchid trade across countries, however, within many countries trade remains an issue (Hinsley et al. 2017a,
Hinsley et al. 2017b, Gale et al 2019, Lawson et al. 2019).
Conservation priorities
With rapidly changing environments and limited conservation funding, it is important to focus conservation efforts on key priorities in targeted areas. Our study highlighted geographic patterns for these priorities and in some cases, priorities were broad based, such as species management which applied to many orchids around the world. This includes ex-situ conservation, further developing genome resource banks and continuing work on propagation techniques. Protection and management of orchid habitat is another priority particularly for orchids threatened by biological resource use (illegal collection, harvesting and logging), development and agriculture globally which would also have a positive flow on effects for the entire ecosystems (Wan et al. 2014). However, large scale conservation efforts involve a great deal of effort and planning including by governments and is currently not well addressed in key areas for orchids, such as Madagascar (Cribb and Hermans 2007, Harper et al. 2007).
Education and awareness are major priorities for orchid conservation including communication, especially for orchids threatened by human intrusion and disturbance including tourism and recreation (Swarts and Dixon 2009b, Wraith and Pickering 2017). This is important as much of on ground conservation is conducted and driven by community groups and societies both in terms of labour and funding (Light 2003). Increased awareness and education can be achieved
94 by engaging local community groups and schools in conservation and propagation techniques
(Dixon and Phillips 2007). In many cases effective conservation measures can include simple actions such as signage to inform tourists how to minimise their impacts in protected areas, but also rely on researchers to better communicate their results with the general public (Wraith and
Pickering 2017).
Law and policy was not seen as a high priority for orchid conservation based on the Red List data, but education and awareness were often listed. Due to the exploitation of orchids worldwide it is important that orchid collectors and societies are aware of the importance of adhering to CITES regulations when exchanging orchid material (Hinsley et al. 2017a, Hinsley et al. 2017b, Fay 2018, Gale et al 2019). However, even with strict regulations, the illegal collection and trade of orchids remains prevalent across the globe (Wraith and Pickering 2018,
Lawson et al. 2019). The effectiveness of the current CITES regulations and other protocols require both revision and stricter implementation to successful reduce the illegal orchid trade
(Lawson et al. 2019). Orchids in Cypripedilinae had the largest number of threatened species with law and policy a priority, which was not surprising as Paphiopedilum orchids have a long history of illegal collecting (Thomas 2006, Ballantyne and Pickering 2012, Wraith and
Pickering 2017). Interestingly law and policy were not listed as a priority for orchids in
Madagascar, which has the largest number of threatened species. Livelihood, economic and other incentives were listed as the lowest priority for orchid conservation, except for orchids in
East Asia including in China, Vietnam and India. This was also a priority for certain orchid tribes including Cypripedilinae and Cypripedilineae and those orchids threatened by pollution.
Gaps in research and conservation
Based on our review of the current scope of research into orchid conservation and the priorities on IUCN Red List, there are some important gaps. This includes the need for more research on understanding and monitoring populations, trends and distributions for threatened species including assessing the impacts of climate change so we can better focus on ground conservation (Figure 6). Due the vast diversity of orchids with most species relying on highly
95 specific and complex interactions with other biota, future research could further focus on the ecology of threatened orchids including their interactions with fungi, pollinators, habitats and threats. We increasingly know about threats to orchids on a broad scale but understanding finer scale threats to specific species and how to mitigate them requires more research including links between species ecology and spatial distribution modelling (Figure 6). For example, mapping fine scale distributions of threats could highlight appropriate areas for translocation and/or relocation of specific species. Three major gaps in conservation were highlighted by our study
(Figure 6). The first is protection and management of orchid species which can involve physical efforts such as caging populations or developing management plans in collaboration with local governments and land managers. The second involves protecting threatened orchid habitats and third is education, awareness and communication (Figure 6).
Monitoring populations, trends & distributions
Research Ecology
Threats and mitigation Gaps in orchid conservation Protection and managenment of species
Protection and Conservation management of priorities orchid habitat
Education, awareness & communication
Figure 6. A conceptual diagram highlighting gaps between research in orchid conservation and the research priorities for orchids on the IUCN Red List.
96 Limitations
Important limitations to our knowledge about threats and priorities needs to be considered.
There are limitations when using academic literature to facilitate analyses due to social, economic and perceptions such as favoured taxa and biomes which can cause biases in spatial and temporal patterns (Pickering et al. 2018). In this study we used data from a range of sources including the IUCN Red List which have limitations. As the IUCN Red List relies on data submitted by countries, there are important gaps. Data can often be over simplified, for example orchids listed in China have every conservation priority listed for each species and although it is possible that each species requires all priorities, this seems unlikely. Other limitations come from missing or outdated data. For instance, countries such as Australia have few orchids on the
IUCN Red List, but many orchids listed as threatened on the national list (Wraith and Pickering
2018). It is important that countries accurately contribute to global listings such as the IUCN
Red List and that the data is updated frequently as this will not only contribute to accurate assessments of global patterns of threats and threatened species but help to focus research and management priorities more broadly. Here we also used global species occurrence records from the Global Biodiversity Information Facility (GBIF) which is an important resource for assessing global patterns in biodiversity and threats, but like many such resources has limitations. For example, these types of crowd sourced databases often include inaccuracies in records such as missing or vague coordinates, low resolution location data, misidentified species and sampling bias (Hortal et al. 2007, Meyer 2016). These biases were reduced through an initial assessment of records and by visually assessing and removing points that were determined to be suspect.
As biodiversity is facing increasing diversity and severity of threats, most obviously from climate change, securing resources and funding for specific groups or species is both even more important, but also, increasingly difficult. Although we highlighted where orchid conservation and research efforts should focus, it not realistic to assume that these can and will be achieved in a timely manner. Each of these priorities requires funding, governmental cooperation,
97 community action and engagement and time, which for many species is quickly running out.
Global collaboration and communication are crucial to conservation success particularly for orchids which include some of the most complex and rarest species on the planet.
Conclusions
Orchid conservation research has focused on taxonomy in the past and more recently on genetic diversity, mycorrhizal symbionts and propagation techniques, all of which are vital for successful orchid conservation. However, orchid conservation research should increasingly focus on population monitoring, species distribution and climate change impacts and adaptation, better understanding orchid ecology including habitat requirements and threat mitigation. Also, on ground orchid conservation should increasingly focus on protection and management of individual species as well as habitats, contributing to the survival of orchids and their communities. As orchid conservation often relies on the generosity of local governments, land managers, orchid societies and conservation action groups, education, awareness and communication between researchers and these communities remains critical.
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104 Chapter 6. Discussion and Conclusion
6.1 Introduction
Orchids are the most diverse group of flowering plants, yet due to the accumulative effects of diverse anthropogenic activities, many have been driven to extinction and even more are at risk (Dixon and Phillips 2007, Swarts and Dixon 2009a, Wraith and
Pickering 2017, Fay 2018, Wraith and Pickering 2018, Wraith and Pickering 2019). In order to ensure their future, it is important to understand what is threatening them, what drives these threats and how we can prioritise conservation efforts to enhance effectiveness. (Wraith and Pickering 2017, Kearney et al. 2018, Wraith and Pickering
2018, Wraith and Pickering 2019). In my thesis these questions were addressed including identifying important threats to orchids at a global and continental level, identifying novel methods for spatially analysing the distribution of threats as well as presenting recommendations for conservation and research priorities.
The results of the thesis highlight that the most severe and common threats to orchids globally are illegal collecting and harvesting, habitat modification, human intrusion and disturbance, agriculture and tourism and recreation. Many of these threats are linked and co-occur as threat syndromes, which will be discussed in more detail in the following sections. The thesis identified how the risk of extinction for many orchids is exacerbated by tourism and recreation when trampling and collecting damages orchids in the wild, including in protected areas. Due to the severity of threats to orchids it is vital to understand where species are threatened, and by what. Therefore, the distribution of major threats to orchids were mapped globally and in Australia to highlight geographic patterns in individual threats and threat syndromes. The broader implications of the spatial analyses are discussed in detail in the following sections.
105 Having established the scale and extent of threats to orchids globally and in Australia, it was important to prioritise future conservation and research. This was done by analysing published academic literature to identify what is known and key gaps, as well as by conducting a detailed assessment of conservation priorities at a global scale using data from the IUCN Red List. The remainder of this Chapter therefore discusses in more detail the implications of the research from Chapters 2-5, in relation to the broad thesis aims (which are re-stated as subtitles 6.2-6.6). The final section summarises the key contributions of the thesis to orchid conservation, implications for conservation and management, how the methods used in the thesis could be applied to other threatened taxa, limitations of the current research, and future research directions.
6.2 Aim 1: What are the major threats to orchids globally?
A global analysis of threats to orchids using data from the IUCN Red List highlighted a series of key threatening processes (Chapter 2, Wraith and Pickering 2018). The results highlighted that threats to orchids are numerous, occur in patterns across the globe and act as threat syndromes. Many of the threats are similar to those for other plants on the
IUCN Red list, however the frequency with which orchids are affected differs to other plants (Figure 6.1). Orchids were most commonly and severely impacted by biological resource use including the illegal collection of wild orchids (Wraith and Pickering 2017,
Wraith and Pickering 2019, IUCN 2019). Illegal collecting also threatens many other plants, but it was not the most common threat across all plants on the Red List, with housing and urban areas the most common threat currently listed (Figure 6.1). Orchids were also threatened by logging, development for housing and urban areas and small holder farming practices, as are many other plants on the Red List (Wraith and
Pickering 2018). However, orchids were more likely to be affected by human intrusion and disturbance, and roads and railroads than other plants on the Red List (Figure 6.1).
106 Unlike some other threatened plants, orchids are also severely impacted by tourism and recreation, including the development of tourism infrastructure (Wraith and Pickering
2017).
Orchids
All plants
Figure 6.1. The most common threats for orchids globally (Top) and all plants (Bottom) on the IUCN Red List (2019) and where the same threats occur for both groups of plants, they are given the same colour coding. T & R = tourism and recreation.
107 Tourism and recreation is increasing exponentially at a global scale, and as a result is increasingly threatening biodiversity (Newsome et al. 2012, Monz et al. 2013, Rankin et al. 2015), but what was not clear was its impact on orchids (Ballantyne and Pickering
2012). A detailed analysis of IUCN Red List data for orchids highlighted the scale of tourism and recreation as a threat including illegal collecting of wild orchids (Chapter 3,
Wraith and Pickering 2017). This research demonstrated how tourism and recreation is increasingly recognised as a major threat to orchids, exponentially increasing since 2012 and is now listed as threatening 40% of Red Listed orchids (Chapter 3, Wraith and
Pickering 2017). This included 98 orchid species threatened by the construction of tourism and recreation facilities, 90 species impacted by disturbance such as trampling, and 78 species that were the target of illegal collecting within protected areas (Figure
6.2).
Figure 6.2. Schematic overview of the percentage of threatened orchids on the IUCN
Red List impacted by tourism and recreation threats based on data from Wraith and
Pickering (2017).
108 With the impacts of tourism and recreation increasingly recognised as threatening many plants including orchids (Pickering and Hill 2007, Ballantyne and Pickering 2012,
Newsome et al. 2012, Ballantyne and Pickering 2013, Rankin et al. 2015), the severity of the threat for orchids was analysed in more detail in the thesis. As a result, this research demonstrated that the impacts of tourism and recreation on many orchids are ongoing, causing very rapid declines to populations, affecting the majority of populations of some orchids and causing severe impacts (Chapter 3, Wraith and
Pickering 2017). As with the results for the global analysis, tourism and recreation is also a major threat to orchids in Australia including the impacts of trampling and development (Ballantyne and Pickering 2012, Ballantyne and Pickering 2013, Wraith and Pickering 2017, Wraith and Pickering 2019). Illegal collection was thought to be a declining threat to orchids in Australia, but it is still listed as a major threat in Australia as it is for orchids globally.
As tourism and recreation is a major threat to orchids globally, more research is required on its impacts as well as more frequently on-ground monitoring and it needs to be more often addressed in conservation and management plans (Chapter 3, Wraith and
Pickering 2017). This particularly applies in protected areas with high diversity of terrestrial orchids that are also popular for nature based tourism. In these situations a range of methods can be used to try to minimise impacts from nature based tourism.
These include minimising disturbance during the construction of facilities, and relocating or diverting trails and similar types of infrasturure to areas away from the orchids. Similarly, the use of raised boardwalks or similar structures can reduce damage to orchids from trampling (Hill and Pickering 2006, Monz et al. 2013). Limiting infrastructure such as resorts, carparks and facilities is important to reduce land clearing impacts, particularly in threatened species’ habitat both in and outside protected areas
109 (Ballantyne and Pickering 2012). Increased signage within protected areas could also be used to raise awareness of threats to orchids and other plants, including encouraging tourists to stay on designated tracks and to not pick orchids and other plants.
To explore threats to orchids in more detail, a continental scale analysis for Australian orchids was conducted (Chapter 4, Wraith and Pickering 2019). This Chapter determined that orchids in Australia are impacted by similar threats to globally listed species, including the impacts of invasive species, habitat modification and grazing.
However, this research determined that orchids in Australia were commonly and severely impacted by changes to, or inappropriate, fire regimes. This was more often a threat in Australia than for orchids globally (Figure 6.3) (Chapter 4, Wraith and
Pickering 2019). Fire is often an important ecological process in many Australian ecosystems, with some orchids such as the genera Pyrorchis, benefiting from fire
(Tiong and Cootes 2015). The increasing frequency and severity of fires in Australia, however, is threatening many orchids (Duncan et al. 2005, Coates and Duncan 2009,
Brown et al. 2016). These can be natural or stochastic fire events, as well as planned management burns to reduce the overall risk of fires, particularly in close proximity to human dwellings (Duncan et al. 2005, Bradstock 2010, New et al. 2010). The study of fire and its impacts on orchids remains limited, though research has demonstrated that fires during periods when Australian orchids are dormant does less damage than when the orchids are flowering (Reiter and Pollard 2013, Jasinge et al. 2018). Unfortunately, the frequency, severity and spread of fires in Australia has increased dramatically with climate change and will continue to do so with dramatic effects on biodiversity (Pitman et al. 2007, Williams et al. 2009, Dowdy 2018, Clarke et al. 2019), increasingly threatening orchids with extinction, particularly terrestrial species in forests, woodlands and grasslands.
110 Changes in fire regimes is just one of the impacts of climate change, and climate change is now considered to be the single most important threat to ecosystems globally (Díaz et al. 2019, Scheffers and Pecl 2019). International and Australian lists of threatened plants including orchids are not fully reflective of the scale of climate change as a threatening process. In Australia it was only listed as a threat for 21 species of orchids and 85 orchids on the IUCN Red List (Chapter 4, Wraith and Pickering 2019). The impacts of climate change on orchids, are not restricted to those from fire, although this link needs to be studied further (Dowdy 2018). Changes in other processes with a warmer and often drier climate will also affect orchids. For example, climate change has already resulted in the loss of orchids in many regions across the globe (Liu et al. 2010,
Seaton et al. 2010, Vogt-Schilb et al. 2015). These areas include Central America, where increased temperatures altered fire regimes in the mountain rainforest in the
Montebello region of Mexico, which has already caused extinction of 22 endemic orchids. Changes in annual precipitation from 1997-2004 have also caused a severe decline in the epiphytic orchid Aspasia principissa in Panama (Zotz and Schmidt 2006,
Seaton et al. 2010). Populations of European orchids have also declined, with northwards range shifts occurring due to climate change, increasingly limiting terrestrial species to more northern latitudes (Pfeifer et al. 2010, Molnár et al. 2012, Vogt-Schilb et al. 2015). Climate change is also causing changes in key symbiotic associations including between orchids and mycorrhiza and orchid pollinators (Fay 2018). Although climate change is recognised as a major threat to biodiversity within the scientific community, some governments and communities remain sceptical that it is occurring, that it is caused by humans or that it will have much effect (Engels et al. 2013, Ecklund et al. 2017). Unfortunatly this, along with other factors, has restricted the effectiveness of many global strategies attempting to limit climate change to 1.5-2 degrees of
111 warming (Smith et al. 2018).
Orchids in Australia
All IUCN Red Listed orchids
Figure 6.3. The most commonly listed threats to orchids in Australia (Top) and globally
(Bottom) based on data from the Australian Government, and the IUCN Red List (2019) with the same threats in the two datasets colour coordinated.
112 To appropriately address major threats, it important to understand what is associated with and often driving them (Pimm et al. 2014). This was addressed in Chapter 4 by using generalised linear models to assess the relationship between a wide range of variables known to affect orchids. The results showed the percentage of native vegetation cover was a key driving factor for species threatened by habitat modification, grazing and weeds, with reduced vegetation cover in a region increasing the risk of extinction for orchids from these threats (Chapter 4, Wraith and Pickering 2019).
Interestingly, this study showed that species within protected areas were more likely to be impacted by changes in fire regimes and by tourism and recreation, which should be a focus for future research and management. Orchids more likely to occur in protected areas were less likely to be affected by habitat modification. These results provide useful information for future conservation and management plans. However, to successfully mitigate major threats to orchids and other plants at a global and continental scale, it is important to understand where the threats occur, which is discussed next.
6.3 Aim 2: Where are threats to orchids occurring and which habitats are most at risk?
The previous section discussed the major threats to orchids at a global and continental scale, however this thesis also examined spatial patterns in the distribution of threats as well as identifying at risk habitats. Over half of all threatened orchids had limited distributions, with many species naturally restricted to single countries (endemics). In
Chapter 2 it was shown that country endemics were more likely to be threatened by energy production and mining, natural systems modification and biological resource use than orchids with broader distributions (Chapter 2, Wraith and Pickering 2018). Spatial analyses also demonstrated that threats to orchids varied among regions with the largest
113 number of threatened orchids on the IUCN Red List in Africa, Asia and South America
(Chapter 2, Wraith and Pickering 2018).
The most commonly listed threat to orchids globally was illegal collecting which was particularly important for orchids in South and South East Asia (Chapters 2, 3, Wraith and Pickering 2017, Wraith and Pickering 2018). Orchid trade is an important industry in places such as south China, where 1.2 million orchids are sold annually, many illegally collected from the wild (Gale et al. 2019). Orchids in forests are most at risk from illegal collecting, and there are important areas of forest in China containing many rare orchids (Liu et al. 2010). The prevalence of illegal collecting is exacerbated in
China due to limited laws protecting wild orchids (Gale et al. 2019). Orchids in East
Asia are also threatened by climate change and pollution; however, these threats were not listed for orchids in many other areas. Orchids in Asia were also affected by other threatening processes including human intrusion and disturbance and development including from tourism and recreation, however, agriculture was not as commonly listed as a threat as it was for orchids in other regions (Chapter 2).
The analysis of IUCN Red List data highlighted the importance of conserving orchids in
Madagascar, as orchids from this country accounted for nearly 50% of those on the Red
List and ~10% of all orchids in Madagascar are threatened (Chapter 2, Wraith and
Pickering 2018). Orchids in Madagascar are severely impacted by land clearing for agricultural practices, tourism infrastructure and logging, reflecting the increasing rate at which these land uses are changing ecosystems in Madagascar. In contrast to some other countries, few orchids in Madagascar were listed as threatened by human intrusion and disturbance (Chapter 2, Cribb et al. 2003, Harper et al. 2007, Brummitt et al. 2015,
Wraith and Pickering 2018).
114 As demonstrated in this thesis, data from the IUCN Red List is useful when assessing threatened species and taxonomic patterns in threats (Hoffmann et al. 2008, Brummitt et al. 2015). However, there are numerous limitations associated with the IUCN Red List data (Chapters 2, 3 and 4, Possingham et al. 2002, Rodrigues et al. 2006). The most important limitation is missing data. For orchids, there are numerous species on the Red
List with incomplete data and, where there was data, for some it did not fully reflect rapid changes in threats such as climate change (Chapters 2 and 3). There are also large gaps in data for particular countries, with only ~5 orchid species from Australia on the
IUCN Red List, out of approximately 184 nationally threatened species of orchids
(Chapter 4, Australian Government 2016, Wraith and Pickering 2019, IUCN 2019). To ensure accurate and comprehensive data is available on global red lists, it is important to have representation and contributions from all regions as new data or information emerges and to also prioritise research in regions that have limited data and resources
(Schatz 2009).
As Australia has high orchid diversity, many of which are threatened but poorly represented on the IUCN Red List, it was important to analyse what threatens them and where they are threatened (Chapter 4). This study demonstrated a novel technique for mapping hotspots of threats as well as potentially suitable habitat for translocations
(Chapter 4, Wraith and Pickering 2019). Through the utilisation of citizen science data from the Atlas of Living Australia, key areas and habitats in need of immediate conservation efforts were identified. For example, the temperate forests in the state of
Victoria have the highest number of threatened orchids (Chapter 4, Duncan et al. 2005,
Backhouse 2007, Wraith and Pickering 2019), due in part to the impacts on terrestrial orchids of large-scale land clearing (Duncan et al. 2005). Other orchid hotspots include the South West Floristic Region of Western Australia and east Tasmania, both of which
115 have experienced changes in fire regimes (Phillips et al. 2007, Swarts and Dixon 2009a,
Phillips et al. 2011). Other interesting patterns emerged such as how illegal collecting was a major issue for orchids in the World Heritage Wet Tropics area of North
Queensland. These findings highlighted that even within a single country there are important geographical differences in threatening processes within a single taxonomic group.
The methods used to assess the geographic pattern of threats provide important insights for conservation biology and threatened species management and can be applied to other threatened taxa. For example, this method could be used on a finer scale, where there are more accurate species occurrence records and combined with distribution models to identify suitable habitat for species relocations, translocations and prioritising new conservation areas. However, some limitations need to be recognised, including the scale and accuracy of species occurrence records (McPherson et al. 2006, Meyer 2016).
For example, threatened species records are often deliberately kept vague or altered to protect species from illegal collection and therefore additional data, including field surveys, are required for more accurate spatial analysis of species and threat distributions.
The previous sections discussed key threats to orchids at a global and continental scale including the benefits and limitations of the methods used to assess the distribution of threats. The next section addresses how these threats impact different orchid life forms and genera.
6.4 Aim 3: What is the impact of threats on orchid life forms and genera?
Orchids are unique plants due to their complex biology. They occupy a range of habitats even within the same region, with some species that grow on the ground obtaining
116 nutrients from the soil via mychorhizae (terrestrial species), while others require host trees (epiphytes) or rocks (lithphytes) for growth and derive nutrients from moisture in the air and debris as well as mychorhizae (Jones 2006). Due to the variety of life forms within the family it is impotant to understand how threats are impacting each of them.
At a global level (Chapter 2), threats to orchids differed depending if the species was terrestrial, epiphytic or lithophytic (Wraith and Pickering 2018). Most orchids on the
IUCN Red List are terrestrial and are commonly threatened by biological resource use including illegal collecting and logging practices. Terrestrial orchids are also heavily impacted by agriculture and human intrusion and disturbance (Chapter 2, Wraith and
Pickering 2018).
Tourism and recreation was also a common threat for terrestrial orchids (Chapter 3).
There are a range of reasons for this, including that terrestrial orchids are more likely to be damaged by trampling from tourism activies such as hiking, mountain bike riding, 4- wheel driving and horse riding than epiphytic species (Light and MacConaill 2007,
Ballantyne and Pickering 2012). Some terrestrial orchids also have prominent and easily acessible flowers, and may be damaged by people collecting flowers which affects the reproductive success of populations. In contrast, some terrestrial species when not in flower are harder to see, and so tourists may be unaware they are trampling them (Light and MacConaill 2007, Ballantyne and Pickering 2012). Epiphytic orchids were more likely to be threatened by illegal collecting, as many epiphytes can be propagated from wild collected plants, with many of the orchids sold on the black market in China epiphytic species (Flores-Palacios and Valencia-Diaz 2007, Mondragón 2009, Phelps and Webb 2015, Hinsley et al. 2017). Research suggests that epiphytes do not recover well from illegal collecting but the extent of the impacts requires further research
(Flores-Palacios and Valencia-Diaz 2007, Liu et al. 2014).
117 Epiphytic orchids were also proportionally more likely to be threatened by agriculture than terrestrial species, which is likely due to the impact of clearing host trees, particularly for orchids limited to forests (Gradstein 2008, Parra‐Tabla et al. 2011,
Adhikari et al. 2012). Lithophytic orchids are less common in general, and therefore there were fewer of them on the IUCN Red List. The ones that were listed were more most commonly threatened by biological resource use, human intrusion and disturbance and natural system modifications (Chapter 2, Wraith and Pickering 2018).
Certain genera of orchids were associated with particular threats as seen in Chapters 2, 3 and 4. The two most commonly threatened orchid genera on the IUCN Red List are
Paphiopedilum and Cypripedium commonly known as slipper orchids with over 200 species threatened (Chapter 2, Wraith and Pickering 2018, IUCN 2019). Slipper orchids are collected in many parts of the world as they are charismatic and diverse. Collecting has caused declines in populations of some of the species, and some are close to extinction such as Paphiopedilum canhii and Paphiopedilum vietnamense (Teoh 2019).
As a result of their attractiveness for collectors all Pahpiopedilum species are on the
CITES Appendix 1, which lists the most threatened taxa globally and prohibits any commercial trade. However, as discussed previously, these regulations are not entirey successful (Gale et al. 2019, Lawson et al. 2019, Teoh 2019).
The previous sections have discussed the most common threats to orchids, spatial patterns in threatening processes including habitats, life forms and genera that are particularly at risk. It is also impotant to know how these threats interact with each other, as well as other factors, to fully utilise this information and mitigate threats more successfully. This will be discussed in the following section.
118 6.5 Aim 4: Are orchids impacted by threat syndromes?
Understanding the complex nature of threatening processes is critical in correctly managing and developing conservation strategies, as it is unlikely species can be conserved by the removal of single threats (Burgman et al. 2007, Swarts and Dixon
2009a, Kearney et al. 2018). Chapters 2, 3 and 4 demonstrated how orchids experience threats as syndromes. Chapter 2 identified four key threat syndromes threatening orchids globally, with the first affecting endemic terrestrial orchids in forest habitats
(Figure 6.4). This was particularly evident for orchid species used for medicinal purposes in South East Asia such as many Paphiopedilum and Cypripedium (Chapter 2,
Wraith and Pickering 2018, Gale et al. 2019). By understanding threats to terrestrial orchids that are also endemic we can focus on measures to restrict their collection, including better monitoring adherence to the CITES agreement within known hotspots
(Lawson et al. 2019). Other strategies to reduce illegal orchid collecting include creating and monitoring conservation reserves, legal propagation of desirable orchids to help satisfy demand, and educating collectors and the wider community to increase support for orchid conservation (Subedi et al. 2013, Liu et al. 2014, Wraith and Pickering 2018).
The second major threat syndrome included climate change and pollution. Although climate change is increasing and is potentially the major threat to biodiversity globally
(Thomas et. 2004, Malcom et al. 2006, Wake and Vredenburg 2008, Seaton et al. 2010,
Urban 2015, Bitencourt et al. 2016), the impact on orchids is still emerging and currently it is only commonly listed as a threat to orchids in East Asia (Figure 6.4). In this and other regions, suitable habitat for some orchids is limited to small areas at higher altitudes and with climatic warming these are further restricted. As a result, orchids, particularly epiphytes, are having to shift to higher elevations and the total area of habitat will be smaller (Liu et al. 2010). Pollution is exacerbating the impacts of
119 climate change in some regions (Ramanathan and Feng 2009, Serengil et al. 2011) further limiting the availability of suitable habitats, particularly in niche areas. Far more research is required to fully understand the impacts of climate change on orchids at a global and local scale (Seaton et al. 2010, Fay 2018). Large scale threats such as land clearing, trampling and fragmentation also commonly co-occurred with climate change and pollution. Consequently, these threats require large scale conservation and management solutions such as identifying and protecting natural areas of high orchid conservation value as well as utilising global collaborations with governments, non- government agencies, landholders and the general public (Kark et al. 2009, Mazor et al.
2013, Kark et al. 2015). Although large scale conservation efforts are difficult to accomplish due to issues with funding and labour intensity, they remain important, and increasingly so in a changing climate.
Other threat syndromes identified for orchids were more localised. For example, for epiphytic orchids in Madagascar, habitat loss from agricultural land clearing is a major threat (Figure 6.4). Similarly, land clearing for agriculture is affecting terrestrial orchids in South and South East Asia (Liu et al. 2015, Fay 2018, Wraith and Pickering 2018).
Understanding these interactions, particularly in regions with many threatened orchids such as Madagascar, is important and can have direct conservation implications. For example, orchids within these categories should become a priority for conservation efforts (Fay 2018, Wraith and Pickering 2018).
120 Threat syndrome Threat syndrome Threat syndrome Threat syndrome 1 2 3 4
Terrestrial Climate Epiphytic Terrestrial orchids change orchids orchids
South & Forest habitat Pollution Madagascar South East Asia
Illegal Agricultural Shifting collecting land clearing agriculture
East Asia
Country endemics
Figure 6.4. Four major threat syndromes affecting orchids on the IUCN Red List using data from Wraith and Pickering (2018).
Threatened orchids in Australia are most commonly and severely impacted by changes in or inappropriate fire regimes, invasive species, habitat modification, grazing, tourism and recreation and illegal collection (Chapter 4, Wraith and Pickering 2019). As with threatened orchids globally, some of these threats co-occur as threat syndromes, particularly for orchids in temperate forests (Chapter 2 and 3, Brummitt et al. 2015,
Wraith and Pickering 2017, Wraith and Pickering 2018). Understanding how these and other threats are distributed across the continent is particularly important when identifying key areas for conservation including areas for translocation and further
121 research (Evans et al. 2011). Other key conservation and research priorities are discussed in the following section.
6.6 Aim 5: What are the key priorities for orchid conservation and research?
The analysis of data from the IUCN Red List in conjunction with a bibliometric analysis determined trends in orchid conservation research and where research and conservation efforts should be focused in the future (Chapter 5). Orchid conservation is an inherently difficult task due to the complex nature of individual species including species-specific symbionts such as mycorrhizae and pollinators and often highly limited habitat requirements (Swarts and Dixon 2009a, Fay 2018, Gale et al. 2018). The results of the bibliometric analysis showed that orchid conservation research in the last 10 years focused on genetics and taxonomy, mycorrhizal associations, propagation and pollination. These topics, although vital for conservation, often focus on single species, in single regions resulting in important gaps in knowledge about factors at broader scales and across higher taxa groupings within orchids (Swarts and Dixon 2009a, Fay et al. 2015, Fay 2016, Shefferson et al. 2019, Wraith et al. In press).
Understanding trends in conservation research is important, including identifying gaps in knowledge for individual species and large taxonomic groups, such as orchids (Dixon and Phillips 2007, Fay et al. 2015, Fay 2016). Identifying these gaps can lead to the implementation of novel conservation methods, funding can be appropriately allocated, and important conservation research can continue (Halpern et al. 2006). The results of this Chapter will help with shaping orchid conservation priorities and include key recommendations. Based on the analyses in this Chapter orchid conservation research should increasingly focus on understanding and monitoring populations, trends and species distributions including assessing the impacts of climate change (Figure 6.5).
122 Climate change is devastating biodiversity globally (Wake and Vredenburg 2008, Liu et al. 2010, Urban 2015), but as highlighted in this thesis research on impacts of climate change on orchids and the scale of the threat is still limited and needs to be prioritised
(Simmons et al. 2018).
Research should continue to focus on the ecology of threatened orchids including their interactions with fungi, pollinators, habitats and threats. Due the vast diversity of orchids, with many species relying on highly specific and complex interactions with other biota, understanding their ecology is vital, but will often need to be done species by species (Dixon and Phillips 2007, Swarts and Dixon 2009a, Fay et al. 2015, Fay
2016, Shefferson et al. 2019). Another focus should be assessing finer scale threats to individual species and how to mitigate them, including research assessing species ecology in combination with spatial distribution modelling. This thesis provides novel and useful information on large scale threats to orchids on a global and continental scale. However, to apply practical mitigation strategies, patterns in threats need to also be understood at a more local level (Wraith and Pickering 2019).
This Chapter also determined that future conservation efforts should focus on protection and management of orchid species in-situ (Figure 6.5) (Gale et al. 2018). This requires collaboration from researchers, community members and governments with long term funding and labour both for research and management (Selwood et al. 2019). Small scale practical solutions which have shown positive outcomes include: (1) caging populations to reduce the impact of native and invasive grazing pressures; (2) propagation of species within botanic gardens and research facilities followed by translocations; (3) reduction in trampling damage via raising boardwalks, diverging trails and education programs to raise awareness; and (4) propagating wild orchids to reduce demand for collecting from the wild, among others (Reiter et al. 2016, Bickerton
123 2018). Mapping threat distributions, as presented in Chapter 4, offers a cost effective and efficient method for identifying where threat syndromes are occurring and could also be used in conjunction with on-ground surveys.
This Chapter also highlighted protecting threatened orchid habitats as a major priority at a global scale and as such will require international collaboration between researchers and conservationists (Balmford et al. 2005). Research suggests that creating specific orchid reserves would be an effective approach for orchid conservation in southern
China, and such an approach may be beneficial in other areas with high orchid diversity, such as Madagascar (Zhang et al. 2015). The methods for mapping threat distributions
(Chapter 4) could be used to help identify and prioritise areas and habitats most at risk from major threats and syndromes (Wraith and Pickering 2019). Education, awareness and communication remains fundamental for orchid conservation and remains a key priority. This includes engaging with local communities, schools and governments
(Dixon and Phillips 2007, Swarts and Dixon 2009b, Liu et al. 2015, Gale et al. 2018).
For example, in countries such as Australia, native orchid societies contribute to orchid conservation by dedicating time, funding and expertise to help conserve threatened orchid species and should be informed when new research emerges and consulted when new conservation efforts are being planned (Gale et al. 2018). Educating businesses that specialise in orchid horticulture including those with ornamental or medicinal value should also be a priority. There has been success in reducing the collection of wild orchids in China through propagating desirable species (Liu et al. 2014). This method also supports local economies and could be applied in other areas (Liu et al. 2014).
Education and awareness should also extend to tourists in protected areas, including avoiding trampling orchids and not collecting plants (Ballantyne and Pickering 2012,
Ballantyne and Pickering 2013, Rankin et al. 2015).
124 Monitoring populations, trends & distributions
Research priorities Ecology
Threats and mitigation Gaps in orchid conservation Protection and managenment of species
Protection and Conservation management of priorities orchid habitat
Education, awareness & communication
Figure 6.5. Schematic overview of the gaps in orchid conservation research and priorities based on the data on the IUCN Red List adapted from Wraith et al. (In press).
6.7 Contribution to conservation, limitations and future directions
Orchid conservation is an inherently difficult task due to the rare, complex and elusive nature of threatened orchids, the intractability of some threats, a lack of resources and government action to both address some threats and to protect specific habitats (Dixon and Phillips 2007, Swarts and Dixon 2009a, Liu et al. 2010, Seaton et al. 2010, Fay
2018, Wraith and Pickering 2019). The results of this thesis provide a novel way to assess threats to orchids at a global and continental scale and highlight where orchid conservation and research need to focus in the future. Specifically, this thesis has determined:
125 1. Globally orchids are most commonly threatened by illegal collection and
harvesting, habitat loss from agricultural practices and development and human
intrusion and disturbance.
2. Tourism and recreation is an increasing and major threat to orchids including
illegal collecting in protected areas, trampling from recreation activities and the
development of tourism infrastructure.
3. Orchids in Australia are most severely impacted by changes in or inappropriate
fire regimes, weeds, grazing, habitat modification, tourism and recreation and
illegal collecting.
4. A reduction in native vegetation is the most common driver for the number of
threatened orchids in Australia and is also the main cause of threats from habitat
modification, grazing and weeds. Orchids with an increased presence in
protected areas are often impacted by fire regimes and tourism and recreation,
but less likely to suffer from habitat modification.
5. Threats to orchids often co-occur and act as threat syndromes.
6. Mapping the distribution of threats to orchids and other taxa is an important way
to identify areas at risk from threat syndromes and to identify suitable habitat for
orchids.
7. Orchids in temperate forests are most at risk from major threats.
8. Orchids in the genera Paphiopedilum and Cypripedium are more at risk from
major threats than other genera, especially from illegal collecting.
9. Orchid conservation research is a large and important field. It has focused
heavily on taxonomy, molecular biology and fungal associates and research on
conservation is growing exponentially.
126 10. Future research on orchid conservation should focus on monitoring population
trends and distributions, threats and threat mitigation including the impact of
climate change and ecology.
11. Orchid conservation should focus on global priorities including the protection
and management of orchid habitats and species as well as education, awareness
and communication from researchers to governments, community members and
orchid societies.
This thesis has provided a useful method for assessing the distribution of threatening processes for orchids. Globally this method could be adapted and re-applied to a range of spatial scales and taxa. This could include an assessment of the known threats for the species or group including the severity of the threats, an interpolation analysis to identify the geographical distribution of these threats. Following this method can highlight at risk areas or habitats for the target species and help develop key conservation priorities either at a local or large scale to ensure other working conservation groups target similar issues (Figure 6.6).
127 Identify threats, severity & distributions
Effiecient & cost effective threatened species conservation
Determine Identify threat conservation syndromes priorities
Figure 6.6. A schematic overview of the key aspects to consider when developing a conservation or management plan for threatened species.
To use this method (Figure 6.6), there needs to be adequate data on threatened species both at a local and global scale. For example, the continental scale analysis presented in
Chapter 4 relied on data about threatened orchids from the Australian Government combined with occurrence records from the Atlas of Living Australia (Australian
Government 2016). In the absence of such data, extensive research and on-ground surveys would be necessary before spatial patterns in threats could be identified.
Therefore, it is important that government agencies work with researchers and community groups to maintain accurate and comprehensive listings of threatened species and that the data is available to researchers (Balmford et al. 2005, Bottrill et al.
2011, Liu et al. 2015). It also cannot be assumed that any threat listed for a species pertains to the whole of its distribution as the analysis is dependent on the data available and therefore threat distributions may be over or underestimated. As such threat
128 syndrome mapping should be treated with caution and ground truthing is often necessary. There is also the potential for cross-jurisdictional overlaps or oversights in listing threats depending on how and who assessed. This can potentially lead to variability in threats based on different perceptions which should be acknowledged and considered in future research.
Although globally threatened species databases such as the IUCN Red List are useful, including here for the global assessments, there are still numerous limitations with such lists, and, as such, the use of these types of lists should be treated with some caution
(Possingham et al. 2002, Dorey and Walker 2018). For example, there is often an underrepresentation, or significant lag, in listing threatened species for some regions and groups of organisms, which was apparent for orchids (Rodrigues et al. 2006).
Inadequate data in threatened species lists is often due to the combined effects of limited funding, a lack of government cooperation or priorities in listing, and a lack of research on species status and threats (Schatz 2009). Australia is a prime example highlighting issues with missing Red List data, particularly for orchids. There were only five
Australian species of orchids on the Red List even though there are 184 orchids species listed as threatened with available data by the Australian Government (Rankin et al.
2015; Australian Government 2016, Wraith and Pickering 2017, Wraith and Pickering
2018, Wraith and Pickering 2019). There are also limitations for species that are listed on the IUCN Red List. For example, many orchid species on the Red List are missing data on threats and conservation priorities. This limitation needs to be considered when using the data for research. More comprehensive, accurate and current information on threats to species including in the Red List is important, not only for research, but also for conservation. This will require consistent and long-term collaboration between
129 governments, agencies and researchers for each region and will enhance our understanding of global patterns in biodiversity and extinction risks at a global scale.
6.8 Conclusions
This thesis examined threats to orchids at a global and continental scale, analysed the effect of interactions between threats which result in threat syndromes, spatially analysed where threats to orchids are occurring and which habitats are most at risk, investigated the impact of threats on orchid life forms and genera, and analysed trends and gaps in orchid conservation and research to assess key priorities for future conservation. Importantly, the results of these studies have highlighted that orchids are impacted by a wide range of anthropogenic activities including illegal collecting, tourism and recreation, habitat loss, fire regimes and invasive species which commonly co-occur as threat syndromes. The results also highlight that the severity and extent of the threat from climate change is not reflected in current listing documents for most orchids, and future research is needed on impacts including on orchids and other biota.
Spatially assessing threats to orchids and other threatened species is a novel and useful method for highlighting areas and habitats at risk of threats and threat syndromes and provides important information for conservationists to assist them in better management. The results of this thesis also highlight the need for other research such as monitoring orchid populations including trends and distributions, climate change, ecology, threats and threat mitigation, protection and management of species and their habitats and overall increasing education and awareness.
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142 Appendices
Appendix 1 Griffith University policy on the inclusion of papers within the thesis.
Accessed November 2019 https://intranet.secure.griffith.edu.au/research/griffith- graduate-research-school/preparing-your-thesis/inclusion-of-papers-within-the-thesis.
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146 Appendix 2 Chapter 2 supplementary material (appendix 1) for the paper Wraith, J. and
C. Pickering (2018). Quantifying anthropogenic threats to orchids using the IUCN Red
List. Ambio 47(3): 307-317.
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