Impact of Alien Slugs on Native Plant Seedlings in a Diverse Mesic Forest, O‘Ahu, Hawai‘I, and a Study of Slug Food Plant Preferences
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IMPACT OF ALIEN SLUGS ON NATIVE PLANT SEEDLINGS IN A DIVERSE MESIC FOREST, O‘AHU, HAWAI‘I, AND A STUDY OF SLUG FOOD PLANT PREFERENCES A THESIS SUBITTED TO THE GRADUATE DIVISION OF THE UNIVERSITY OF HAWAI‘I IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE IN BOTANICAL SCIENCES (BOTANY-ECOLOGY, EVOLUTION, AND CONSERVATION BIOLOGY) MAY 2006 By Stephanie M. Joe Thesis Committee: Curtis C. Daehler, Chairperson Donald R. Drake David C. Duffy Robert H. Cowie We certify that we have read this thesis and that, in our opinion, it is satisfactory in scope and quality as a thesis for degree of Master of Science in Botanical Sciences (Botany-Ecology, Evolution, and Conservation Biology) THESIS COMMITTEE Chairperson ACKNOWLEDGEMENTS Funding for this study was received from the Ecology, Evolution and Conservation Biology Research Grant, the Beatrice Krauss Fellowship in Botany and the Sigma Xi Grants in Aid of Research. My committee has been absolutely vital throughout. I am grateful to my advisor Curtis C. Daehler for his enthusiasm and diligence, Robert H. Cowie for sound advice and thorough editing, Donald R. Drake for encouraging me to study slugs rather than worms and David C. Duffy for sticking by me through the whole ordeal. Additionally, I thank the U.S. Army Garrison Natural Resource Staff, without whom this project would never have succeeded. They grew the plants, provided materials and staff and helped collect data. In particular, I am grateful to Naomi Arcand, Seth Cato, Vincent Costello, Hoala Fraiola, Victor Göbel, Julia Gustine, Kapua Kawelo, Matthew Keir, David K. Palumbo, Leanne Obra, Jobriath Rohrer, Dominic Souza, Robert Romualdo, William Weaver and Lauren Weisenberger for their help. Students, researchers and staff from the University of Hawai‘i helped out as well. I would like to thank Kyle K. Koza, Victor Cizankas, Will Haines, Mitsuko Yorkston, Charles Chimera and Karen Brimacombe. Above all, I thank my husband, Paul D. Krushelnycky. iii ABSTRACT Introduced species have the potential to cause serious ecological disruption, particularly on oceanic islands. When introduced species invade natural areas, endemic species may be threatened, especially when the invasive species represent guilds or functional groups that were previously lacking. Hawai‘i has no native slugs, but over a dozen species are now established. Slugs are important seedling predators in their native habitats, and in introduced habitats they can cause major shifts in the abundance some plant species. In order to better investigate slug impacts on native plants in Hawai‘i, I carried out research which 1. identified differences in the acceptability of five native plant species to five alien slug species 2. assessed the effect of slug herbivory on the growth and survival of three native and two alien plant species, and 3. measured changes in seedling regeneration due to slug herbivory. Results from feeding assays indicated a significant difference in palatability among plant species, but no statistical difference in overall feeding preference among slug species. Urera kaalae (Urticaceae) was found to be significantly more palatable than the other four plant species and, thus, is predicted to be more vulnerable to slug herbivory in the field. I tracked the fate of planted seedlings and natural germinants from the seed bank in both slug-excluded and slug-accessible plots in diverse mesic forest in the iv Wai‘anae Mountains on the island of O‘ahu. Among seedlings that survived to the end of the experiment, there was no significant difference between slug- herbivory treatments in growth index measurements. There was little germination from the seed bank, with no statistical difference in total number of seedlings between treatments. However, two of the three native species, Schidea obovata (Caryophyllaceae) and Cyanea superba (Campanulaceae) had significant reductions in survival of 49% and 53%, respectively, in the slug-exposed treatment. Survival of two invasive species, Clidemia hirta (Meslastomataceae) and Psidium cattleianum (Myrtaceae) was not significantly affected by slugs. This study demonstrates that slugs may pose a serious threat to native plant species by reducing their survival and thereby facilitate the success of certain invasive species. v TABLE OF CONTENTS Acknowledgements . iii Abstract . iv List of Tables . viii List of Figures . viii Chapter 1: Literature review and discussion of hypotheses . 1 Introduction . 1 Study organisms . 2 Impacts of slug herbivory . 3 Slugs in Hawai‘i . 5 Hypotheses . 7 Chapter 2: Palatability of native plant species to alien slug species . 16 Introduction . 16 Materials and methods . 18 Study organisms . 18 Feeding trial protocol . 21 Statistical Analysis . 24 Results . 24 Discussion . 25 Chapter 3: Impact of alien slugs on native plant seedlings . 37 Introduction . 37 Materials and methods . 40 Field site . 40 Study species . 42 Seedling preparation . 43 Experimental design . 44 Slug monitoring . 47 Statistical analysis . 47 Results . 49 Plant growth . 49 Herbivory damage . 49 vi Seedling survival . 50 Seed bank regeneration . 51 Slug monitoring . 51 Discussion . 51 Appendix A: Change in plant size index over time . 63 Appendix B: Change in leaf number over time . 68 Appendix C: Change in herbivore damage over time . 73 Literature cited . 78 vii LIST OF TABLES Table Page 1.1 Gastropod families containing slugs . 9 1.2 List of slugs found within the state of Hawai‘i . 10 1.3 List of native species threatened by alien slugs . 11 2.1 Mean acceptability indices (AI) for 25 slug-plant species pairs . 30 2.2 ANOVA using AI scores from 25 slug-plant species pairs . 31 2.3 Secondary plant compounds repellent to slugs . 31 3.1 Seedling height (mm) by species on day 0 of the study . 55 3.2 Two-way ANOVA of seedling survival by herbivory treatment . 55 3.3 Number of germinants from seed bank by herbivory treatment . 55 LIST OF FIGURES Figure Page 2.1 Slug collection sites on the Island of O‘ahu . 32 2.2 Percent of slugs engaged in feeding . 33 2.3 Mean AI scores for each plant species (all slug species) . 34 2.4 Distribution of AI scores . 35 2.5 Boxplot showing weight distribution of slug species . 36 3.1 Location of Kahanahāiki Management Unit . 56 3.2 Plant growth in slug-exposed vs. slug-excluded plots . 57 3.3 Leaf change in slug-exposed vs. slug-excluded plots . 58 3.4 Herbivory damage in slug-exposed vs. slug-excluded plots . 59 3.5 Survival in slug-exposed vs. slug-excluded plots . 60 3.6 Survival over time by plant species . 61 3.7 Slug counts at refugia over time . 62 viii CHAPTER 1 LITERATURE REVIEW AND DISCUSSION OF HYPOTHESES INTRODUCTION The deliberate and accidental introduction of alien species into new habitats where they establish and spread is a significant component of human-caused global change (Vitousek et al. 1997). Through predation on and competition with native species, introduced species accelerate extinction rates and reduce global biodiversity (Gurevitch and Padilla 2004). For instance, approximately 42% of the species on the U.S. Threatened and Endangered species lists are at risk primarily because of the activities of introduced species (Pimentel et al. 2004). In other regions of the world, introduced species seriously threaten up to 80% of native endangered species (Armstrong 1995). The endangerment and loss of native species is particularly acute on oceanic islands, which have unusually high rates of endemism (Kaneshiro 1988). In the Hawaiian Islands, where a considerable portion of intact native ecosystems are under State and Federal protection (Cuddihy and Stone 1990), invasive species are now the primary threat to the persistence of the native flora and fauna (Loope 1992). For native Hawaiian plants, competition from invasive plants and herbivory by invasive animals are two of the most important forces responsible for declining populations (Bruegmann et al. 2002). 1 Herbivory is central to the organization of biotic communities (Marquis 1992; Janzen 1970). By influencing plant species composition, it also has indirect effects on most other species in a community. While vertebrate herbivores are frequently the focus of studies regarding plant community dynamics (Kotanen 1995; Stone 1985), the impacts of invertebrates are important as well. Among invertebrate herbivores, terrestrial molluscs, such as slugs and snails, are some of the most important grazers of temperate grassland species (del-Val and Crawley 2004; Hitchmough 2003). Because these animals are known to target seedlings (Hanley et al. 1995), they can have profound consequences for native plant recruitment and therefore adult species composition (Hanley et al. 2002; Hanley et al. 1996). They may also play an important role in the success or failure of rare plant restoration efforts. Study organisms Slugs are a polyphyletic group of terrestrial gastropods descended from snails. The absence of a shell gives them their distinctive form, which arose by way of convergent evolution in multiple snail lineages (Runham and Hunter 1970). As a result of this evolutionary history, there exists a continuum of gastropod forms in terms of shell reduction, with snails at one end, slugs at the other, and various intermediate forms, sometimes referred to as “semi-slugs”, in between. Thus, the number of gastropod species considered to be slugs is not definitive. To avoid confusion, my use of the term is limited to those families considered to be slugs by South (1992) (Table 1.1). 2 The repeated evolution of the slug form in several gastropod lineages is a testament to its utility, particularly in calcium-poor, wet environments, such as those found on many volcanic islands. Both slugs and snails are hermaphroditic and many species can self-fertilize (Jordaens et al. 2000) as well as tolerate a wide range of temperatures (Rollo and Shibata 1990). These traits make slugs excellent colonizers and potential invaders when introduced into new areas. Slugs will feed on a variety of foods including carrion, animal feces, lichens, a variety of small animals and other slugs (South 1992).