Assessing extinction risk in anemonefishes Maarten De Brauwer Supervisors: Dr. Jean-Paul Hobbs Prof. Euan Harvey This thesis is submitted in partial fulfilment of the requirements for a Bachelor of Science (Honours) SCIE4501-450 4 FNAS Research Thesis Faculty of Natural and Agricultural Sciences The University of Western Australia Submitted May 2014 Formatted in the style of the journal Conservation Biology Abstract Anemonefishes are coral reef icons and an important contributor to coral reef tourism and the marine ornamental trade. All 28 species have an obligate symbiotic relationship with sea anemones, which makes them vulnerable to habitat destruction. Many anemonefish species are also vulnerable due to their low abundance and/or small geographic ranges, while impacts such as climate change and over-harvesting have caused local extinctions. Despite these vulnerabilities and threats, extinction risk has not been assessed for the majority of anemonefish species. Using a global database, this study assessed the extinction risk of all 28 species of anemonefish according to criteria B1, B2, C and D of The International Union for Conservation of Nature (IUCN) Red List. This study found that 100% of species under criterion B2 and 36% of species under criterion D2 face elevated risk of extinction and satisfy criteria for being listed in IUCN threatened categories. A restricted area of occupancy (criterion B2) was the most important driver for listing species as threatened. Endemic species are most at risk, eight of which could potentially be listed as Critically Endangered. These results highlight the vulnerabilities of habitat specialists and the urgent need to formally assess the extinction risk of anemonefishes. Formal placement on the IUCN Red List is likely to lead to the development of suitable protective measures to guarantee the persistence of this coral reef icon. Furthermore, listed anemonefishes could serve as a flagship or model group for other, less studied, habitat specialists. Key Words anemonefishes, Amphiprion, Premnas, extinction risk, endemic species, IUCN, habitat specialists, coral reefs 2 Table of contents Research thesis Acknowledgements ...................................................................................................... 4 Introduction .................................................................................................................. 5 Methods ........................................................................................................................ 7 Results ........................................................................................................................ 13 Discussion .................................................................................................................. 18 References .................................................................................................................. 22 3 Acknowledgments Writing a research thesis is impossible to do on your own. Therefore, I would like to thank the following people without whom this thesis would never have been submitted. First and foremost, I would like to thank Eva “Boss” McClure. Without her invitation to do fieldwork I would never have returned to university study in the first place. Eva and Derek Sun were the ones who convinced me that studying in Australia was possible. Thank you. Further, I would like to express my gratitude to my supervisors Dr Jean-Paul Hobbs and Prof Euan Harvey. JP, thank you for offering me this fantastic project and for sharing your ideas. Your support, great feedback, and advice made a world of difference. I am looking forward to working with you in the future. Also, thank you Euan for giving me the chance to pursue my dream of becoming a real marine biologist and for getting me in touch with JP. I would like to thank the numerous people and organisations who contributed their data to this thesis: Michael Berumen, Ashley Frisch, Nick Graham, Alison Green, Andrew Halford, Alec Hughes, Jean-Paul Hobbs, Michael Kulbicki, Sangeeta Manghubhai, Tim McClanahan, Jennifer McIlwain, Maya Srinavasan, Shaun Wilson, the Western Australia Department of Parks and Wildlife, the Khaled bin Sultan Living Oceans Foundation and Reef Life Survey. This year would never have been possible without the financial support of my parents. I owe them a huge amount of gratitude. Thank you, I promise I will come back to Belgium one day. Melanie Trapon was always there for me with moral support, feedback and thought-provoking insights in the world of academia. For interesting, prolonged lunchtime sessions that sparked my imagination and provided an outlet for frustration, thank you Emily, Kelly, Katie and James. Lastly, I’d like to thank the people in the Marine Ecology lab for being a warm and welcoming group of people. I would particularly like to thank Todd Bond, who introduced me to GIS. All the world is a laboratory to the inquiring mind ~ Martin H. Fischer Word Count 6352 4 Introduction Coral reefs provide habitat for thousands of species, supporting more than one third of the world’s known marine biodiversity (Knowlton et al. 2010). Millions of people depend on a wide range of coral reef species for food, tourism and trade (Costanza et al. 1997; UNEP 2004). However, increasing anthropogenic impacts are threatening the future of coral reefs. Currently 20% of coral reefs have been destroyed and another 50% are at risk of collapse (Wilkinson 2006). Habitat degradation and loss leads to a reduction in the abundance of species that rely on coral reefs. The challenge is to identify the types of species that are most susceptible to these impacts, so that management strategies can be devised to mitigate the threat. The species most vulnerable to extinction tend to be those with low abundances and small geographic ranges (Gaston 1998). Furthermore, ecological specialists are likely to be impacted more severely than generalists (McKinney 1997; Koh et al. 2004; Munday 2004). Positive associations between low abundance, small range size and specialisation mean that endemic species face a much higher risk of extinction (“triple jeopardy”: Munday (2004)). On coral reefs, species that have obligate relationships with specific habitats, such as gorgonians (Reijnen et al. 2010), sponges (Wulff 2006) and corals (Munday et al. 1997) are likely to be most at risk from habitat degradation and loss (Munday 2004). Ultimately, the disappearance of specific microhabitats inevitably leads to the disappearance of their obligate symbionts (Dulvy et al. 2003; Travis 2003; Jones et al. 2004; Munday 2004). Therefore, there is a need to identify habitat specialists that have small range sizes and low abundances because these are the species most at risk of extinction. Anemonefishes are the best known habitat specialists on coral reefs. They are famous for their symbiotic relationship with anemones, and are among the most popular attractions for snorkel and dive tourism (Coghlan & Prideaux 2012) and the most traded species in the global marine ornamental trade (Wabnitz et al. 2003). All 28 anemonefish species live in an obligate symbiotic relationship with up to 10 species of host anemone (Fautin & Allen 1992; Allen et al. 2008; Allen et al. 2010). Anemonefishes are found in shallow reefs environments throughout the tropical and subtropical regions of the Indo-Pacific and Red Sea. Many anemonefishes are endemic to isolated parts of the world (Fautin & Allen 1992), and if these species also have low abundance, then this will greatly increase their risk of extinction. 5 Despite their popularity, little research has been done on the abundance of anemonefishes or the threats they face (Shuman et al. 2005; Jones et al. 2008; Hill & Scott 2012). At a local scale, collection of anemones and anemonefishes for the marine ornamental trade has caused significant declines in populations as well as local extinctions (Sin et al. 1994; Hattori 2002; Shuman et al. 2005). Host anemones usually have very low abundances on coral reefs (Richardson et al. 1997; Chadwick & Arvedlund 2005; De Brauwer et al. Appendix 2) and are susceptible to temperature induced bleaching (Jones et al. 2008; Hill & Scott 2012; Hobbs et al. 2013), which can cause mass mortality of anemones and local extinctions of anemonefish (Hattori 2002). Rising sea temperatures associated with climate change are predicted to lead to an increase in the severity and frequency of bleaching events (Hoegh-Guldberg 1999). This represents a serious global threat to the future of anemones and anemonefishes (Hobbs et al. 2013). Determining which anemonefish species are most at risk of extinction (Hutchings 2001; Dulvy et al. 2004) is important for developing protective measures to ensure their conservation (Bellwood et al. 2004). The International Union for Conservation of Nature (IUCN) provides a valuable framework to objectively assess the extinction risk of species through the use of the Red List of Endangered Species (Rodrigues et al. 2006). The goals of the Red List are: 1) identify and document species most in need of conservation attention; and 2), provide a global index of the state of degeneration of biodiversity (Mace et al. 2008; IUCN 2014). A species’ risk of extinction is assessed using Red List criteria (e.g. geographic range size and abundance) and assigned to one of nine different categories, implying different probabilities of extinction (Fig. 1). Species considered to be endangered with extinction are placed in one of three “threatened”