NOVEL PREDATORS AND NAÏVE PREY: HOW INTRODUCED MAMMALS SHAPE BEHAVIOURS AND POPULATIONS OF NEW ZEALAND LIZARDS JOANNE MARIE HOARE 2006 Novel predators and naïve prey: how introduced mammals shape behaviours and populations of New Zealand lizards Joanne Marie Hoare A thesis submitted to Victoria University of Wellington in fulfilment of the requirement for the degree of Doctor of Philosophy in Ecology and Biodiversity Victoria University of Wellington Te Whare W ānanga o te Ūpoko o te Ika a M āui 2006 for Olive and friends i Abstract Biotas that evolved in isolation from mammalian predators are susceptible to degradation due to recent human-mediated introductions of mammals. However, behavioural, morphological and life historical adaptations of prey to novel mammalian predators can allow prey to persist in mammal-invaded areas. Lizards in New Zealand are an ideal group for exploring the effects of invasive mammals on vertebrate prey because: (1) the ca. 80 endemic species evolved without mammals as a major influence for 80 my, (2) mammalian introductions during the past 2000 y have differentially affected lizard species, and (3) some species coexist with mammals on the mainland as well as occurring on mammal-free offshore islands. I tested three hypotheses: (1) lizard populations that have persisted on New Zealand’s mainland are no longer declining in the presence of introduced mammalian predators, (2) introduced mammals induce behavioural shifts in native lizards, and (3) lizard behavioural patterns and chemosensory predator detection abilities vary according to exposure to introduced mammals. Trends in capture rates of five sympatric native lizard populations over a 23 year (1984-2006) period demonstrate that not all lizard populations that have persisted thus far on New Zealand’s mainland have stabilised in numbers. Large, nocturnal and terrestrial species remain highly vulnerable at mainland sites. Introduced kiore, Rattus exulans , induce behavioural changes in Duvaucel’s geckos, Hoplodactylus duvaucelii . A radio telemetric study demonstrated that geckos start reverting to natural use of habitats within six months of kiore eradication. Activity patterns of common geckos, H. maculatus , and common skinks, Oligosoma nigriplantare polychroma , in laboratory trials are also correlated with their exposure to mammalian predators. Lizard activity (time spent moving) increases relative to freeze behaviour with greater exposure to ii mammals. However, specific antipredator behaviours are not elicited by chemical cues of either native (tuatara, Sphenodon spp) or introduced (ship rat, R. rattus ) predators. Lizard populations may persist by changing their behaviours in the presence of invasive mammals. However, the continued declines of particularly vulnerable mainland lizard taxa suggest that mammal-induced behavioural shifts may only slow population declines rather than enabling long-term survival. Eradicating pest mammals from offshore islands has proven effective at restoring both populations and behaviours of native lizards, but lizard populations on the mainland also deserve conservation priority. Research directed at understanding the synergistic effects of invasive species that are causing continued lizard population declines and mammal-proof fencing to protect the most vulnerable mainland populations from extinction are both urgently required. iii Acknowledgements My PhD has been an incredible journey, made possible by the support of so many people. Help has come in all shapes and sizes, from throwing a borrowed generator off a tiny boat onto an island of rock in 3 m swells, to sharing copious quantities of chocolate during long nights crawling about in pursuit of geckos. I would like to especially thank my supervisors, Charles Daugherty and Nicky Nelson, for their enthusiasm for the project and unwavering belief that I was up to the task. Rick Shine is responsible for the initial brain-wave that sent me scrambling to find tuatara poo, and Shirley Pledger helped me to untangle the resulting statistical nightmares. Charlie’s Angels (the herpetological variety) have been fabulous friends! Thanks so much to Kelly Hare, Sue Keall, Jen Moore, Hilary Miller, Kim Miller, Kristina Ramstad, Jeanine Refsnider, Libby Liggins, Steph Godfrey and the token male, David Chapple, for the rock-climbing, the gossip and the ‘coffees’. My support network of family, friends and fellow trampers were brilliant throughout. Thanks especially to my mum for the final 48 hour proof reading ‘party’. I am particularly grateful to Edwin Hermann, for creating ‘AnimalSpy’, to Grant Timlin for lending an emergency generator, to James Russell for catching rats, and to James Allen and Shane Harnett for daring boat drop-offs to, and rescues from, islands. Leigh Bull, Tony Whitaker and the ‘Hatchet’ crew provided excellent constructive criticism of manuscripts, Dianne Brunton and the Ecology and Conservation group at Massey Albany hosted me during the rainbow skink work, Lois and Colin Burrows provided excellent hospitality and Greg Kerr sent miles of cotton. I have had the pleasure of working with a whole bunch of fantastic people in the field. Thanks so much to Marleen Baling, Jason Christensen, Jennie Francke, Bruce Galloway, Jen Germano, Rod Hobson, Cameron Jack, Michael Killick, Kerri Lukis, Peter Martin, Rhys Mills, Jo Peace, Richard Romijn, Cielle Stephens and Chris iv Wedding. A number of Department of Conservation (DoC) staff and iwi members have gone out of their way to support my work; thanks to Lynn Adams, Rob Chappell, Emma Craig, Joe Davis, Al Fastier, Pete Gaze, Peter Johnston, Jason Roxburgh and Dave Towns. My work was supported by Ng āti Koata, Te Ātiawa, Ng āti Toa and Ng āti Hei and approved by the DoC (permits TAK 0304c, BRO 0401, LIZ 0409, WE/102/RES, AK- 15608-FAU and WK-15607-RES) and the Victoria University of Wellington Animal Ethics Committee (permits 2003R16 and 2003R20). My research was funded primarily by the Foundation for Research, Science & Technology (Top Achiever Doctoral Scholarship). I also thank Victoria University of Wellington, the Society for Research on Amphibians and Reptiles in New Zealand, the Australian Environmental Protection Agency and the Allan Wilson Centre for Molecular Ecology and Evolution for funding. I am grateful to the donors of the Shirtcliffe Fellowship, Helen Stewart Royle Scholarship, Masterton Trust Lands Trust Tertiary Grant and the Freemasons’ University Scholarship. Table of contents Abstract…………………………………………………………………………………………………..i Acknowledgements……………………………………………………………………………………….iii CHAPTER 1. New Zealand lizards as a model to address the influence of novel predators on evolutionarily naïve prey 1.1 Evolution in isolation from mammalian predation pressure…………………… 1 1.2 The impacts of invasive species on natives: current knowledge and limitations…………………………………………………………………………………………………….3 1.3 New Zealand lizards as a model system in which to test non-lethal effects of novel predators………………………………………………………………. 4 1.4 Thesis structure…………………………………………………………………………5 ……………… CHAPTER 2. Long-term monitoring of a lizard guild reveals imminent extinction of the last mainland population of Cyclodina whitakeri 2.1 Abstract………………………………………………………………………………………………9 ………………. 2.2 Introduction……………………………………………………………………………………10 ….. 2.3 Methods……………………………………………………………………………………………….13 2.3.1 Study site and species……………………………………………………………………………..13 2.3.2 Lizard trapping………………………………………………………………………16 ….. 2.3.3 Weather data………………………………………………………………………………18 ………………….. 2.3.4 Habitat sampling…………………………………………………………….18 2.3.5 Mammal trapping and stomach content analyses………………………………..19 2.3.6 Statistical analyses…………………………………………………………….20 2.4 Results……………………………………………………………………………….21 2.5 Discussion…………………………………………………………………………………………27 . 2.5.1 Synergistic effects of habitat changes and introduced predators on mainland lizard populations………………………………………………………28 2.5.2 Conservation management of herpetofauna at disturbed sites…………………30 CHAPTER 3. Spatial avoidance enables the large, nocturnal gecko Hoplodactylus duvaucelii to persist with invasive kiore, Rattus exulans 3.1 Abstract……………………………………………………………………………..34 3.2 Introduction……………………………………………………………………………………35 ….. 3.3 Methods……………………………………………………………………………………………….38 3.3.1 Study species……………………………………………………………………………38 . 3.3.2 Study sites…………………………………………………………………………….39 3.3.3 Capture and radio tracking of Duvaucel's geckos…………………………………………………………………………….41 3.3.4 Capture and spool-and-line tracking of kiore…………………………………43 3.3.5 Data collection and analyses…………………………………………………44 3.4 Results………………………………………………………………………………..49 CHAPTER 3. continued 3.5 Discussion…………………………………………………………………………………………55 ………………. 3.5.1 The influence of introduced rodents on recruitment patterns………………56 3.5.2 Behavioural responses to introduced predators……………………………………………………57 3.5.3 Habitat use shifts driven by introduced predators………………………………………………….58 3.5.4 Management implications………………………………………………………………………………………..60 CHAPTER 4. Chemical discrimination of food, conspecifics and predators by apparently visually-orientated diurnal geckos, Naultinus manukanus 4.1 Abstract………………………………………………………………………………………….61 4.2 Introduction……………………………………………………………………………………62 ….. 4.3 Methods……………………………………………………………………………………………….65 4.3.1 Study animals……………………………………………………………………………65 . 4.3.2 Experimental procedure…………………………………………………………………………….66 4.3.3 Statistical analyses…………………………………………………………………………….69 4.4 Results………………………………………………………………………………..71