Seed Dispersal and Frugivory: Ecological Consequences for Tree Populations and Bird Communities Von der Fakultät für Mathematik, Informatik und Naturwissenschaften - Fachbereich 1 - der Rheinisch - Westfälischen Technischen Hochschule Aachen zur Erlangung des akademischen Grades eines Doktors der Naturwissenschaften genehmigte Dissertation vorgelegt von Diplom-Biologin Bärbel Bleher aus Urach, jetzt Bad Urach Berichter: Universitätsprofessor Dr. rer. nat. Ingolf Schuphan Universitätsprofessor Dr. rer. nat. Hermann Wagner Tag der mündlichen Prüfung: 13. September 2000 If I know a song of Africa, of the giraffe and the African new moon lying on her back, of the plows in the fields and the sweaty faces of the coffee pickers, does Africa know a song of me? Will the air over the plain quiver with a color that I have had on, or the children invent a game in which my name is, or the full moon throw a shadow over the gravel of the drive that was like me, or will the eagles of the Ngong Hills look out for me? T. Blixen dedicated to my parents CONTENTS 1. GENERAL INTRODUCTION 1 1.2 SEED DISPERSAL BY ANIMALS AND CONSEQUENCES FOR PLANTS 1 1.2 FRUIT AVAILABILITY AND CONSEQUENCES FOR FRUGIVOROUS ANIMALS 2 1.3 RELEVANCE FOR CONSERVATION 3 1.4 AIMS OF THESIS 4 2. SEED DISPERSAL BY BIRDS IN A SOUTH AFRICAN AND A MALAGASY COMMIPHORA SPECIES 7 2.1 INTRODUCTION 7 2.2 THE TREES 8 2.3 STUDY SITES 9 2.4 METHODS 10 2.4.1 FRUGIVORE DIVERSITY 10 2.4.2 TREE OBSERVATIONS 10 2.4.3 FRUIT TRAPS 10 2.5 RESULTS 11 2.6 DISCUSSION 16 2.7 SUMMARY 19 3. CONSEQUENCES OF FRUGIVORE DIVERSITY FOR SEED DISPERSAL, SEEDLING ESTABLISHMENT AND THE SPATIAL PATTERN OF SEEDLINGS AND TREES 21 3.1 INTRODUCTION 21 3.2 STUDY SITES AND SPECIES 22 3.2.1 STUDY SITES 22 3.2.2 STUDY SPECIES 23 3.3 METHODS 24 3.3.1 SEED DISPERSAL 24 3.3.1.1 Fruit traps 24 3.3.1.2 Tree observations 25 3.3.2 SEEDLING ESTABLISHMENT, DISPERSAL BENEFIT AND SEEDLING DISTRIBUTION 25 3.3.2.1 Seedling establishment 25 3.3.2.2 Benefit of seed dispersal 26 3.3.2.3 Seedling distribution 27 3.3.3 SPATIAL DISTRIBUTION OF TREES 28 3.3.3.1 Field data 28 3.3.3.2 Computer simulation 28 3.4 RESULTS 29 3.4.1 SEED DISPERSAL 29 3.4.2 SEEDLING ESTABLISHMENT, DISPERSAL BENEFIT AND SEEDLING DISTRIBUTION 32 3.4.2.1 Seedling establishment 32 3.4.2.2 Benefit of seed dispersal 33 3.4.2.3 Seedling distribution 33 3.4.3 SPATIAL DISTRIBUTION OF TREES 35 3.4.3.1 Field data 35 3.4.3.2 Computer simulation 36 3.5 DISCUSSION 37 3.6 SUMMARY 41 4. SEED DISPERSAL, BREEDING SYSTEM, TREE DENSITY AND THE SPATIAL PATTERN OF TREES 43 4.1 INTRODUCTION 43 4.2 METHODS 44 4.2.1 SIMULATION MODEL 44 4.2.1.1 Tree populations 44 4.2.1.2 Simulation parameters 45 4.2.1.3 Running the simulation 46 4.2.2 DETECTING SPATIAL PATTERNS 46 4.2.3 STATISTICAL ANALYSIS 47 4.3 RESULTS 47 4.3.1 FACTORS INFLUENCING SPATIAL PATTERNS 47 4.3.2 SEED DISPERSAL AND SPATIAL PATTERNS 49 4.3.3 BREEDING SYSTEM AND SPATIAL PATTERNS 50 4.3.4 TREE DENSITY AND SPATIAL PATTERNS 51 4.3.5 START POPULATION AND SPATIAL PATTERNS 51 4.3.6 COMBINED EFFECTS OF DISPERSAL DISTANCE AND TREE DENSITY 52 4.4 DISCUSSION 53 4.5 SUMMARY 56 5. FRUIT AVAILABILITY AND KEYSTONE PLANT SPECIES FOR FRUGIVORES IN A DRY FOREST IN KWAZULU - NATAL, SOUTH AFRICA 59 5.1 INTRODUCTION 59 5.2 STUDY SITE 60 5.2.1 LOCATION 60 5.2.2 CLIMATE 61 5.2.3 VEGETATION 62 5.2.4 FRUGIVORE COMMUNITY 63 5.3 METHODS 63 5.3.1 FRUIT AVAILABILITY AND ABUNDANCE 63 5.3.2 FRUIT UTILIZATION BY THE FRUGIVORE COMMUNITY 64 5.4 RESULTS 64 5.4.1 FRUIT AVAILABILITY AND ABUNDANCE 64 5.4.2 FRUIT UTILIZATION BY THE FRUGIVORE COMMUNITY 67 5.4.2.1 Frugivore community 67 5.4.2.2 Plants used by frugivores 70 5.5 DISCUSSION 73 5.5.1 FRUIT AVAILABILITY 73 5.5.2 FRUGIVORE COMMUNITY 74 5.5.3 RESOURCE UTILIZATION AND KEYSTONE SPECIES 75 5.6 SUMMARY 77 6. GENERAL CONCLUSIONS 79 7. REFERENCES 83 8. APPENDIX 96 9. ACKNOWLEDGEMENTS 103 10. CURRICULUM VITAE 105 1. GENERAL INTRODUCTION . 1. General Introduction Mutualistic plant-animal interactions exist in a wide variety with one of the most important being seed dispersal or the transport of seeds away from a parent plant by animals (Howe & Westley 1988). Not only plants depend on animals for the dispersal of their seeds, animals, too, rely on plants for fruit as a food resource. Seed dispersal by animals and frugivory have reached their pinnacle in tropical forests, where a percentage of up to 90% of tree and shrub species produce fleshy fruits adapted to animal dispersal and eaten by a large number of vertebrates (Frankie et al. 1974, Foster 1982a, Howe & Smallwood 1982, Howe 1986). Howe & Westley (1988, p.105) state that "one of the exciting challenges of modern ecology is to acquire an understanding of the means by which plants and animals exploit each other to their mutualistic benefit". For this understanding both facets of the mutualistic interaction between animals providing seed dispersal and plants providing fruits as a food resource have to be examined and its consequences for their mutualistic partners determined. 1.2 Seed dispersal by animals and consequences for plants The important role that animals, and especially birds, play in the seed dispersal of tropical plants is well documented (e.g. Howe & Estabrook 1977, Howe & Vande Kerckhove 1981, Howe 1986). In general, three hypotheses have been proposed to explain the benefit of seed dispersal for the plants (Howe & Smallwood 1982). The escape hypothesis assumes that seeds and seedlings might escape from disporportionate mortality near the parent due to pathogens, predators or seedling competition. The colonization hypothesis is applied when seed dispersal might allow the parent plants to establish their offspring in vacant sites. The directed dispersal hypothesis assumes that dispersing agents transport seeds to special microsites critical for germination and establishment. Many studies have been conducted to evaluate these hypotheses, however, although several have supported the first one, results remain controversial and hypotheses are not mutually exlusive (for a review see Clark & Clark 1984). 1 1. GENERAL INTRODUCTION . Whatever hypothesis might be applied, in general, the seed shadow or the spatial distribution of seeds around the parent plant shows a peak under and close to the parent tree and a steady decline away (Willson 1992). Fruit-eating animals might alter the shape of the seed shadow and consequently exert varying influence on plants depending on their behavior: animals may drop seeds under the parent plant during fruit handling, destroy them or disperse them from the vicinity of the parent plant. Only in the latter case do they benefit the plant as various studies have shown that survival of seeds and seedlings is higher further away from the parent plant (Janzen 1970, Connell 1971, Augspurger 1983, 1984, Howe et al. 1985). Consequently, seed dispersal is though to affect seedling establishment and the spatial pattern of seedlings and saplings (Fleming & Heithaus 1981, Howe 1986). Differential seedling distribution might be a critical determinant of offspring survival and influence density, spatial patterning and composition of plant communities in general (Fleming & Heithaus 1981, Coates-Estrada & Estrada 1986, Howe 1986). Fruit-eating animals therefore might have a significant influence on the population dynamics of tropical forest communities, however, studies linking animal-mediated seed dispersal and seedling distribution with the spatial pattern and dynamics of plant populations are rare (but see Fleming & Heithaus 1981). 1.2 Fruit availability and consequences for frugivorous animals Complementing the diversity of fruits suitable for consumption by animals is an equivalent diversity of frugivores, i.e. fruit-eating birds and mammals that depend mainly on fleshy fruit. In tropical forests, frugivorous animals are the dominant group of vertebrates. The challenge of frugivores is to find, eat and subsist partly or entirely on fruits that are mostly deficient in protein, but rich in carbohydrates or lipids (Howe & Westley 1988). Fruit availability is one crucial factor influencing the frugivore community (Howe & Estabrook 1977, Thompson & Willson 1979). It appears to be highly variable also in the tropics and marked by periods of scarcity and abundance (Terborgh 1986a). Most phenological studies report seasonality with fruit being more limiting in some seasons than in others for most tropical ecosystems (e.g. Frankie et al. 1974, Foster 1982a). Consequently, frugivorous animals are facing seasonal irregularities in their food resources. Plants providing 2 1. GENERAL INTRODUCTION . fruits during periods of low general fruit production play an important role in maintaining entire frugivore communities (Howe 1977). These so-called "keystone resources" have been identified for several forests with figs being of importance (Leighton & Leighton 1983, Terborgh 1986a) as well as a variety of lipid-rich arillate species (Leighton & Leighton 1983, Gautier-Hion & Michaloud 1989). To make the keystone species concept more applicable for conservation, it was recently defined as "a species whose impacts on its community or ecosystem are large, and much larger than would be expected from its abundance" (Power & Mills 1995). Consequently, rather uncommon or rare species might be keystones as compared to abundant dominants. Phenological studies assessing fruit availability and identifying keystone species exist for various tropical forests in the Neotropics and South-East Asia, however, only a few are known for the African continent and none for Southern Africa.