THE EFFECTS OF HABITAT FRAGMENTATION ON THE DEMOGRAPHY AND POPULATION GENETIC STRUCTURE OF UROMYS CAUDIMACULATUS. Craig Streatfeild BSc. (Hons) School of Natural Resource Sciences, Queensland University of Technology Brisbane, Queensland, Australia This dissertation is submitted in fulfilment of requirements for the degree of Doctor of Philosophy 2009 The Giant white-tailed rat, Uromys caudimaculatus (top; photo courtesy Chris Chafer). View of the Atherton Tablelands showing the highly fragmented nature of the remaining rainforest (bottom). ii ABSTRACT Habitat fragmentation can have an impact on a wide variety of biological processes including abundance, life history strategies, mating system, inbreeding and genetic diversity levels of individual species. Although fragmented populations have received much attention, ecological and genetic responses of species to fragmentation have still not been fully resolved. The current study investigated the ecological factors that may influence the demographic and genetic structure of the giant white-tailed rat (Uromys caudimaculatus) within fragmented tropical rainforests. It is the first study to examine relationships between food resources, vegetation attributes and Uromys demography in a quantitative manner. Giant white-tailed rat densities were strongly correlated with specific suites of food resources rather than forest structure or other factors linked to fragmentation (i.e. fragment size). Several demographic parameters including the density of resident adults and juvenile recruitment showed similar patterns. Although data were limited, high quality food resources appear to initiate breeding in female Uromys. Where data were sufficient, influx of juveniles was significantly related to the density of high quality food resources that had fallen in the previous three months. Thus, availability of high quality food resources appear to be more important than either vegetation structure or fragment size in influencing giant white- tailed rat demography. These results support the suggestion that a species’ response to fragmentation can be related to their specific habitat requirements and can vary in response to local ecological conditions. In contrast to demographic data, genetic data revealed a significant negative effect of habitat fragmentation on genetic diversity and effective population size in U. caudimaculatus. All three fragments showed lower levels of allelic richness, number of private alleles and expected heterozygosity compared with the unfragmented continuous rainforest site. Populations at all sites were significantly differentiated, suggesting restricted among population gene flow. The combined effects of reduced genetic diversity, lower effective population size and restricted gene flow suggest that long-term viability of small fragmented populations may be at risk, unless effective management is employed in the future. iii A diverse range of genetic reproductive behaviours and sex-biased dispersal patterns were evident within U. caudimaculatus populations. Genetic paternity analyses revealed that the major mating system in U. caudimaculatus appeared to be polygyny at sites P1, P3 and C1. Evidence of genetic monogamy, however, was also found in the three fragmented sites, and was the dominant mating system in the remaining low density, small fragment (P2). High variability in reproductive skew and reproductive success was also found but was less pronounced when only resident Uromys were considered. Male body condition predicted which males sired offspring, however, neither body condition nor heterozygosity levels were accurate predictors of the number of offspring assigned to individual males or females. Genetic spatial autocorrelation analyses provided evidence for increased philopatry among females at site P1, but increased philopatry among males at site P3. This suggests that male-biased dispersal occurs at site P1 and female-biased dispersal at site P3, implying that in addition to mating systems, Uromys may also be able to adjust their dispersal behaviour to suit local ecological conditions. This study highlights the importance of examining the mechanisms that underlie population-level responses to habitat fragmentation using a combined ecological and genetic approach. The ecological data suggested that habitat quality (i.e. high quality food resources) rather than habitat quantity (i.e. fragment size) was relatively more important in influencing giant white-tailed rat demographics, at least for the populations studied here . Conversely, genetic data showed strong evidence that Uromys populations were affected adversely by habitat fragmentation and that management of isolated populations may be required for long-term viability of populations within isolated rainforest fragments. KEYWORDS: fragmentation, Uromys caudimaculatus, demography, microsatellite, genetic differentiation, assignment tests, genetic diversity, bottlenecks, effective population size, genetic autocorrelation, sex-biased dispersal, mating system. iv TABLE OF CONTENTS Abstract……………………………………………………………………………………….i Table of Contents…………………………………………………………………………..iii List of Figures…………………………………………………………………………......viii List of Tables……………………………………………………………………...……......xi List of Appendices………………………………………………………………………...xiii Acknowledgements……………………………………………………………………….xiv Statement of Original Authorship…………………………………………………….....xvi 1. General Introduction _____________________________________- 1 - 1.1 Habitat fragmentation_______________________________________ - 1 - 1.2 Genetic consequences of fragmentation ________________________ - 5 - 1.3 The model system _________________________________________ - 7 - 1.4 The highly fragmented landscape of the Atherton Tableland ________ - 8 - 1.4.1 Significance of the study region ___________________________________- 8 - 1.5 Study species_____________________________________________ - 9 - 1.6 The aims and objectives of the present study ___________________ - 11 - 2. Assessment of the model system _________________________- 15 - 2.1 Introduction _____________________________________________ - 15 - 2.2 Methods ________________________________________________ - 16 - 2.2.1 Study sites __________________________________________________- 16 - 2.2.2 Vegetation structure and floristic diversity __________________________- 20 - 2.2.3 Food resources diversity and density ______________________________- 22 - 2.2.4 Mammal trapping _____________________________________________- 26 - 2.2.5 Data analysis ________________________________________________- 28 - 2.2.5.1. Vegetation structure _______________________________________- 28 - 2.2.5.2. Floristic diversity __________________________________________- 28 - 2.2.5.3. Food resource diversity_____________________________________- 29 - 2.2.5.4. ‘Trappability’ of U. caudimaculatus and small mammal diversity _____- 30 - v 2.3 Results _________________________________________________ - 30 - 2.3.1 Vegetation structure and floristic diversity __________________________ - 30 - 2.3.2 Food resource diversity ________________________________________ - 32 - 2.3.3 Mammal trapping intensity and trappability _________________________ - 34 - 2.3.4 Small mammal species richness _________________________________ - 36 - 2.4 Discussion ______________________________________________ - 37 - 3. Uromys caudimaculatus demography within fragmented habitats: effects of habitat quantity versus quality. _____________________ - 41 - 3.1 Introduction _____________________________________________ - 41 - 3.2 Methods ________________________________________________ - 43 - 3.2.1 Mammal trapping_____________________________________________ - 43 - 3.2.2 Food resource density _________________________________________ - 44 - 3.2.3 Vegetation structure __________________________________________ - 44 - 3.2.4 Demographic variables ________________________________________ - 44 - 3.2.5 Data analysis ________________________________________________ - 45 - 3.2.5.1. Food resources and vegetation structure_______________________ - 45 - 3.2.5.2. Demographic variables ____________________________________ - 46 - 3.2.5.3. Demography, vegetation structure and food resources ____________ - 46 - 3.3 Results _________________________________________________ - 47 - 3.3.1 Vegetation structure and food resources___________________________ - 47 - 3.3.2 Giant white-tailed rat demographic parameters______________________ - 50 - 3.3.2.1. Sex ratios _______________________________________________ - 55 - 3.3.2.2. Persistence _____________________________________________ - 57 - 3.3.3 Uromys demography, vegetation structure and food resource density ____ - 57 - 3.3.3.1. Timing of reproduction _____________________________________ - 60 - 3.4 Discussion ______________________________________________ - 61 - 3.4.1 Temporal variation in food resource production _____________________ - 61 - 3.4.2 U. caudimaculatus demographic parameters _______________________ - 63 - 3.4.3 Food resources ______________________________________________ - 66 - vi 3.4.4 Competition, predation, vegetation structure, dispersal and den sites _____- 69 - 3.5 Conclusion ______________________________________________ - 72 - 4. Effects of habitat fragmentation on genetic diversity and population genetic structure in a rainforest rodent, Uromys caudimaculatus._- 73 - 4.1 Introduction _____________________________________________ - 73 - 4.2 Methods ________________________________________________ - 76 - 4.2.1 Sample collection