RAINFOREST REGENERATION IN FRAGMENTED FOREST LANDSCAPES Gail Louise Stride Doctor of Philosophy University of York Biology September 2018 Abstract Rainforests are severely threatened by agricultural expansion, frequently resulting in the fragmentation of formerly extensive tracts of continuous forest. The immediate and longer-term effects of fragmentation on tree regeneration, and on alpha- and beta-diversity, remain poorly understood. Forest area and isolation can drive changes in diversity, and may be key considerations for conserving forest biodiversity in human-modified landscapes. I studied trees, saplings, and seedlings (pre- and post- fragmentation recruits), in 14 forest fragments and 5 continuous forest sites in Sabah, Malaysian Borneo. Local alpha-diversity of seedlings was significantly lower in fragments than in undisturbed continuous forest, and lowest in the smallest fragments, potentially signalling an extinction debt. However, saplings showed no declines in alpha-diversity, suggesting that density dependent mortality and/or year- to-year variation in recruitment may compensate for reductions in seedling richness: low seedling diversity may not necessarily translate into low sapling diversity. Nonetheless, 57-64% of genera in small fragments occurred only as adult trees, with no seedlings present, indicating a recruitment failure of some genera. This contributed to greater distinctiveness (increased beta-diversity) of seedling communities in small fragments, which were diverging from trees in the same fragment, and from seedlings in other fragments. Divergence, which has not yet been observed in mature trees, may continue as seedling cohorts mature, causing fragment communities to follow different trajectories of change. Regeneration of 25 functionally-important dipterocarp species was reduced in fragments by almost half (comparing four fragments and four continuous forest sites), but some dipterocarps were still recruiting seedlings effectively in fragments. Collectively, the research shows that there may be some taxonomic impoverishment within fragments (reduced plot-scale alpha-diversity; possible losses from entire fragments), but that continued recruitment in fragments is resulting in increasingly divergent plant communities (increased beta-diversity). Hence, forest fragments continue to make a valuable contribution to landscape-scale diversity and warrant future protection. 2 Contents Abstract 2 List of tables 6 List of figures 7 Acknowledgements 9 Author’s declaration 10 CHAPTER 1 – General introduction 11 1.1 Why are tropical forests so diverse? 13 1.2 Threats to tropical diversity and the impact of habitat fragmentation 19 Habitat fragmentation and its impacts on trees 19 1.3 Biodiversity hotspots and threats to Southeast Asian rainforests 23 Changing climatic cues on Borneo 24 Lowland dipterocarp forest in Southeast Asia 26 1.4 The importance of dipterocarps in Southeast Asian rainforests 27 1.5 Study location and site selection 33 1.6 Thesis aims and rationale 33 Chapter 2 – Contrasting patterns of local richness of seedlings, saplings and trees 34 may have implications for regeneration in rainforest remnants Chapter 3 – Divergent tree seedling communities indicate different trajectories 34 of change among rainforest remnants Chapter 4 – Forest fragmentation alters recruitment of tropical trees: a study of 35 dipterocarps on Borneo CHAPTER 2 – Contrasting patterns of local richness of seedlings, saplings and trees 36 may have implications for regeneration in rainforest remnants 2.1 Abstract 37 2.2 Introduction 38 2.3 Methods 40 Study region and sites 40 Floristic surveys 40 Site and plot characteristics 42 Data analyses 44 2.4 Results 45 3 Variation in plant genus richness among study sites 47 Effects of site characteristics on plant richness 47 2.5 Discussion 49 No effects of fragmentation on tree genus richness 50 Reduced local genus richness of seedlings in fragments 50 Long-term viability of fragments and conflicting results from saplings 50 2.6 Conclusions 51 2.7 Author contributions and acknowledgements 52 CHAPTER 3 – Divergent tree seedling communities indicate different trajectories of 53 change among rainforest remnants 3.1 Abstract 54 3.2 Introduction 55 3.3 Methods 57 Study sites 57 Floristic surveys of tree and seedling communities 58 Measuring site area and isolation 59 Data analyses 60 Computing distinctiveness and divergence of communities 60 Divergence and distinctiveness in relation to site area and isolation 60 Variation in divergence and distinctiveness due to recruitment failure 60 3.4 Results 61 Variation in divergence and distinctiveness, and the role of site area and isolation 61 Role of recruitment failure 65 3.5 Discussion 66 Fragmentation is increasing the distinctiveness of seedling communities among 67 sites Fragmentation is increasing the divergence of communities within sites 68 The landscape perspective 69 3.6 Author contributions and acknowledgements 70 CHAPTER 4 – Forest fragmentation alters recruitment of tropical trees: a study of 71 dipterocarps on Borneo 4.1 Abstract 72 4.2 Introduction 73 4 4.3 Materials and methods 75 Study sites 75 Locating dipterocarp trees and assessing recruitment 77 Data analyses 79 4.4 Results 81 4.5 Discussion 85 Seedling occurrence 85 Seedling abundance 86 Confounding effects 87 Species traits (wood density and flower size) 87 4.6 Conclusions 89 4.7 Declarations 89 CHAPTER 5 – General discussion 90 5.1 Summary of thesis findings 91 Chapter 2 – Contrasting patterns of local richness of seedlings, saplings and trees 92 may have implications for regeneration in rainforest remnants Chapter 3 – Divergent tree seedling communities indicate different trajectories 93 of change among rainforest remnants Chapter 4 – Forest fragmentation alters recruitment of tropical trees: a study of 94 dipterocarps on Borneo 5.2 What is the importance of small fragments for conservation? 95 5.3 Why is recruitment so unpredictable? 99 5.4 Do fragmentation impacts depend on biogeographic region? 101 5.5 Conservation of fragmented tropical landscapes and future research needs 104 5.6 Conclusions 107 List of Appendices 109 Appendix 1 – Supporting information for Chapter 2 110 Appendix 2 – Supporting information for Chapter 3 135 Appendix 3 – Supporting information for Chapter 4 137 References 149 5 List of Tables Table 1.1 – Summary information for study sites. 32 Table 2.1 – Summary information for study sites. 43 Table 2.2 – Top ranked generalised linear mixed models of factors affecting tree, 49 sapling and seedling richness in 93 plots nested within 19 sites. Table 3.1 – General linear model metrics for tree distinctiveness, seedling 65 distinctiveness, and tree-seedling divergence. Table 3.2 – Beta regression model metrics relating to the proportions of genera 65 occurring in each site that were present as both trees and seedlings, trees only, or seedlings only. Table 4.1 – Dipterocarp species included in the study. 78 Table 4.2 – Top ranked generalised linear mixed models of factors affecting dipterocarp 84 seedling occurrence and abundance-when-present. 6 List of Figures Figure 1.1 – Hypotheses for the latitudinal diversity gradient. 14 Figure 1.2 – Photos: a forest fragment surrounded by oil palm plantations; looking out 18 over an oil palm plantation to a distant fragment of forest; palm fruits; structural simplification of environment inside an oil palm plantation relative to native forest. Figure 1.3 – Map of the four Southeast Asian biodiversity hotspots and forest cover on 24 Borneo. Figure 1.4 – Photos: lowland dipterocarp rainforest in the Danum Valley Conservation 26 Area; roads into the forest create edges, but can be useful for moving about; a dipterocarp demonstrating why it’s so appealing to loggers. Figure 1.5 – Map of study area location on Borneo. 30 Figure 2.1 – Map of study area location on Borneo and diagram of sampling design. 41 Figure 2.2 – Overall frequency distribution of sapling and tree stem sizes in forest 45 fragments, logged forest, and primary forest sites. Figure 2.3 – Effect of fragmentation on genus richness of trees, saplings, and seedlings, 46 in primary, logged, and fragmented forest sites. Figure 2.4 – Effect of site characteristics on tree, sapling, and seedling genus richness. 48 Figure 3.1 – Map of study area location on Borneo and diagram of sampling design. 58 Figure 3.2 – Divergence and distinctiveness of tree and seedling communities at sites in 62 relation to site area and isolation. Figure 3.3 – Chao-Sørensen dissimilarity between pairs of sites, and observed genus 64 richness constructed using sample-based rarefaction curves, for sites grouped by area and isolation. Figure 3.4 - The proportion of genera occurring in each site shown as the percentage of 66 genera present as trees and seedlings, trees only, or seedlings only. Figure 4.1 – Map of study area location on Borneo and diagram of sampling design. 76 Figure 4.2 – Histogram showing the number of conspecific seedlings recruited per tree 80 in continuous forest and forest fragments, and examples of variation in species’ seedling recruitment success in each forest type. 7 Figure 4.3 – Species’ sensitivity to fragmentation with respect to seedling occurrence 82 and seedling abundance-when-present. Figure 4.4 – Results of averaged seedling occurrence and seedling abundance-when- 83 present models based on the full dataset and the data subset containing only 14 species found in both forest types. Figure 5.1. Photo of Vatica dulitensis (Dipterocarpaceae) seedlings in logged forest. 91 8 Acknowledgements I have a huge number of people to thank for their support, help, and advice over the course of my PhD. I am extremely grateful to Prof. Jane Hill and Prof. Chris Thomas for their guidance and input, for keeping me on track and focussed on what was important, and for having a great sense of humour. Thanks also go to my other supervisors – Drs Jenny Hodgson, Mike Senior, and Colin McClean for their valuable insights and comments, and to my Training Advisory Panel members Dr Jon Pitchford and Prof. Sue Hartley for their input and enjoyable discussions. Thanks also go to the Natural Environment Research Council and Proforest for providing funding for the project.