Distribution of Mistletoes in a Patchy Habitat

DISTRIBUTION OF MISTLETOES IN A PATCHY HABITAT

Sonja Joy Vermeulen B.A. (Cantab) M.Sc. (Zimbabwe)

A thesis submitted for the degree of Doctor of Philosophy of the University of London and for the Diploma of Imperial College

NERC Centre for Population Biology Imperial College of Science, Technology and Medicine Silwood Park, Ascot, Berkshire, UK

January 1999 Abstract

Distributions of three species of tropical African mistletoes, Erianthemum dregei (Eckl. & Zeyh.) Tieghem, Erianthemum virescens (N.E. Br.) Wiens & Polh. and Agelanthus subulatus (Engl.) Polh. & Wiens (Loranthaceae), were assessed at multiple scales in patchy miombo woodland at a 3 x 4 km study site in Zimbabwe. Among woodland clumps, likelihood of occupancy increased with clump size for all species, varied with habitat type for E. virescens and decreased with clump isolation for E. dregei. Among host trees, likelihood of occupancy increased with host size, varied among host species and, for E. dregei and E. virescens, did not vary with local host density, but was reduced on the most isolated hosts. For all three species the mean number of mistletoes per host increased linearly with host basal girth rather than with canopy volume. Mistletoes were spatially aggregated within host canopies but infected hosts were not spatially aggregated at distances up to 20 m. Establishment experiments showed that establishment success contributed to the observed differences in infection with host species and host size, but not to spatial aggregation of mistletoes above the scale of single branches. Establishment success on branches already supporting an adult mistletoe was strongly reduced. Observations of avian dispersers suggested that aggregation of mistletoes within hosts and the lower likelihood of infection of isolated hosts of E. dregei were due to patterns of seed dispersal. The findings of the study generally supported the theory that decreasing patch occupancy with distance from sources of propagules depends on decreasing dispersal probability, while variation in occupancy with patch size and quality depends on differences in within-patch demographic rates. Acknowledgments

My first debt is to my inspiring supervisor, Professor John Lawton, and my two advisors, Professor Mick Crawley and Dr Roger Polhill, for sharing so much of their time, knowledge and enthusiasm with me throughout the past three years.

This study was carried out under the tenure of a Beit Fellowship. I am grateful to the Beit Trust for the financial support which made my time at Imperial College possible.

In Zimbabwe practical assistance came from all comers. The World Wide Fund for Nature Zimbabwe Programme Office granted me an Honorary Fellowship and gave me access to a four wheel drive vehicle, field equipment and GIS software. Vehicles were also loaned in times of crisis by Stephanie Rodgers, Mark Hyde, Ricky Vermeulen and Ana Scoto, and for an extended period by Jan and Rae Vermeulen. The Department of Surveying at the University of Zimbabwe gave me full use of their GPS receiver, base station and software. The National Herbarium allowed access to their collections of Loranthaceae. Maureen Silva-Jones of the Tree Society of Zimbabwe put me in contact with Gordon Estates and several other possible study sites.

For invaluable assistance in the field I thank Gideon March, who worked with me throughout, Stephanie Rodgers and Time Mtema.

Several people made expedient contributions to my data analyses. David Coomes wrote a spatial analysis programme especially for me. Solomon Bhunu and Mike Rosenbaum introduced me to PFINDER and IDRISI software respectively.

For useful discussion on various details of this study I thank Bob Drummond, Catherine Dzerefos, Peter Frost, Hlka Hanski, Don Kirkup, Jake Overton, Dan Racey, Mark Rees, Lindsay Turnbull, Teresa Vermeulen and Sue Worsley. I thank everybody at Silwood Park for creating the conducive material and intellectual environment in which this study was undertaken, especially my lab-mates over the years: Jill Birch, Daniela Brunner, Enrique Chaneton, Andy Gonzalez, Paul Hopkinson, Pablo Inchausti, Norma OHea, Owen Petchey, Diane Srivastava and Matt Walker.

Stephanie Rodgers kindly drew the figures in Chapter Two.

Finally I thank Trevor and May Gordon, and the entire Gordon family, for giving me the freedom of their farm to conduct my fieldwork, even when it entailed infecting a large number of trees with parasites, and for their boundless generosity and hospitality. Trevor is an expert amateur botanist and a Director of the National Botanic Gardens. Our mutual interests soon developed into a profound friendship. Sadly, May died in April 1998, aged 94. Here I wish to pay tribute to these two extraordinary people. Table of Contents

Chapter One; Introduction 13 1.1. Overview 13 1.2. Distributions of plants over space and over habitat space 14 1.3. The metapopulation approach 17 1.4. Mistletoes in patchy habitat: a framework 24 1.4.1. Aim and approach 24 1.4.2. General assumptions 26 1.4.3. Study species 30 1.5. Structure of the thesis 31

Chapter Two: Study organisms and study site 34 2.1. Study organisms 34 2.1.1. An introduction to mistletoes 34 2.1.2. Species descriptions 36 2.1.3. Host ranges 39 2.2. Study site 41

Chapter Three: Distribution of mistletoes among woodland clumps 44 3.1. Introduction 44 3.2. Methods 48 3.3. Results 50 3.3.1. Patterns of habitat and habitat occupancy 50 3.3.2. Effects of area, habitat type and distance 56 3.3.3. Tests of the sampling hypothesis 61 3.3.4. Evidence of local extinction 61 3.4. Discussion 63

Chapter Four: Distribution of mistletoes among and within trees 67 4.1. Introduction 67 4.2. Methods 71 4.2.1. Erianthemum dregei and Erianthemum virescens 71 4.2.2. Agelanthus subulatus 73 4.2.3. Analysis 73 4.3. Results 75 4.3.1. Distribution of host trees 77 4.3.2. Distribution of mistletoes among hosts 77 4.3.3. Effects of host size, host species and location 78 4.3.4. Effects of host density 89 4.3.5. Spatial aggregation among infected hosts 93 4.3.6. Spatial aggregation within hosts 103 4.4. Discussion 104 4.4.1. Effects of host size and species 104 4.4.2. Effects of distance from seed source 107 4.4.3. Effects of habitat type 109 4.4.4. Conclusions 110 Chapter Five: Establishment and adult survival 112 5.1. Introduction 112 5.2. Methods 116 5.2.1. Establishment experiments 116 5.2.2. Survey of dead mistletoes and scars 118 5.2.3. Annual recruitment and mortality 118 5.3. Results 119 5.3.1. Establishment experiments 119 5.3.2. Survey of dead mistletoes and scars 130 5.3.3. Annual recruitment and mortality 133 5.4. Discussion 135

Chapter Six: Dispersal 142 6.1. Introduction 142 6.2. Methods 144 6.3. Results 145 6.4. Discussion 149

Chapter Seven: Synthesis and discussion 154 7.1. Patch size, extinction, isolation and colonisation 154 7.2. Aggregation of mistletoes 156 7.3. Linking the branch, tree and clump scales 160 7.4. Interspecific differences 162 7.5. Termite mounds as nutrient hotspots 165 7.6. Effects of habitat fragmentation 167 7.7. Future work 170

References 172 List of tables

Table 1.1. Summary of distinctions between within-patch and between-patch processes 26

Table 2.1. Phenology of flowering and fruiting of the three mistletoe species Erianthemum dregei, Erianthemum virescens md Agelanthus subulatus 39

Table 3.1. Logistic regression analysis for presence or absence of Erianthemum dregei in all 80 woodland clumps containing hosts, using the following factors: natural log of area in m^ and habitat type 58

Table 3.2. Regression coefficients of significant factors associated with presence or absence of Erianthemum dregei in all 80 woodland clumps containing hosts 58

Table 3.3. Logistic regression analysis for presence or absence of Erianthemum virescens in all 224 woodland clumps containing hosts, using the following factors: natural log of area in m^ and habitat type 58

Table 3.4. Regression coefficients of significant factors associated with presence or absence of Erianthemum virescens in all 224 woodland clumps containing hosts..59

Table 3.5. Logistic regression analysis for presence or absence of Erianthemum dregei in 66 woodland clumps for which independent distance measures were taken, using the following factors: natural log of area in m^, distance from nearest occupied clump in m and distance from nearest large occupied clump in m 59

Table 3.6. Regression coefficients of significant factors associated with presence or absence of Erianthemum dregei in 66 woodland clumps with independent distance measures 60

Table 3.7. Logistic regression analysis for presence or absence of Erianthemum virescens in 199 woodland clumps for which independent distance measures were taken, using the following factors: natural log of area in m^), habitat type, distance from nearest occupied clump in m and distance from nearest large occupied clump in m 60

Table 3.8. Logistic regression analysis for presence or absence of Agelanthus subulatus in all 16 woodland clumps containing hosts, using the following factors: natural log of area in m^, distance from nearest occupied clump in m and distance from nearest large occupied clump in m 60

Table 3.9. Regression coefficients of significant factors associated with presence or absence of Agelanthus subulatus in all 16 woodland clumps containing hosts 61

Table 4.1. Mean density of hosts of Erianthemum dregei and Erianthemum virescens per 50 X 50 m plot by habitat type and by clump size 76 Table 4.2. G-test of goodness of fit to the negative binomial of the distributions of Erianthemum dregei (all hosts and hosts in large woodland clumps combined with isolated hosts), Erianthemum virescens and Agelanthus subulatus among hosts, showing mean number of mistletoes per host, variance around the mean, aggregation factor and number of hosts in sample 78

Table 4.3. Numbers of hosts and infected hosts of Erianthemum dregei in plots in medium and small woodland clumps 79

Table 4.4. Logistic regression analysis for presence or absence of Erianthemum dregei on host trees, using the following factors: host species, location and natural log of basal girth of host 80

Table 4.5. Regression coefficients of significant factors associated with presence or absence of Erianthemum dregei on host trees 81

Table 4.6. Regression analysis with Poisson errors for number of individuals of Erianthemum dregei on host trees, using the following factors; host species, location and natural log of basal girth of host 82

Table 4.7. Regression coefficients of significant factors associated with numbers of Erianthemum dregei on host trees 82

Table 4.8. Logistic regression analysis for presence or absence of Erianthemum virescens on host trees, using the following factors: host species, location and natural log of basal girth of host 85

Table 4.9. Regression coefficients of significant factors associated with presence or absence of Erianthemum virescens on host trees 85

Table 4.10. Regression analysis with Poisson errors for number of individuals of Erianthemum virescens on host trees, using the following factors: host species, location and natural log of basal girth of host 86

Table 4.11. Regression coefficients of significant factors associated with numbers of Erianthemum virescens on host trees 86

Table 4.12. Logistic regression analysis for presence or absence of Agelanthus subulatus on host trees, using the following factors: location and natural log of basal girth of host 87

Table 4.13. Regression coefficients of significant factors associated with presence or absence of Agelanthus subulatus on host trees 87

Table 4.14. Regression analysis with Poisson errors for number of individuals of Agelanthus subulatus on host trees, using the following factors: location and natural log of basal girth of host 88 Table 4.15. Regression coefficients of significant factors associated with numbers of Agelanthus subulatus on host trees 88

Table 4.16. Regression analysis for density of occupied hosts of Erianthemum dregei versus host density and the square of host density in 21 randomly located 50 x 50 m plots 90

Table 4.17. Regression analysis for density of occupied hosts of Erianthemum dregei versus host density and the square of host density in 30 random and contiguous 50 X 50 m plots 90

Table 4.18. Regression analysis for density of occupied hosts of Erianthemum virescens in 28 randomly chosen 50 x 50 m plots, using the following factors: host density, the square of host density and habitat type 92

Table 4.19. Aggregation factors for hosts of Erianthemum dregei compared to all trees and of occupied hosts compared to all hosts in three 100 x 100 m plots in large woodland clumps at radii of 5, 10, 15 and 20 m from focal trees 97

Table 4.20. Aggregation factors for larger hosts of Erianthemum dregei, those large enough to have more than mean 15 % chance of infection, compared to all hosts and of occupied larger hosts compared to all larger hosts in Large 2 at radii of 5, 10, 15 and 20 m from focal trees 97

Table 4.21. Aggregation factors for hosts of Erianthemum virescens compared to all trees and of occupied hosts compared to all hosts in nine 50 x 50 m plots covering small woodland clumps, at radii of 5, 10, 15 and 20 m from focal trees 101

Table 4.22. Aggregation factors for occupied hosts of Agelanthus subulatus compared to all hosts in a 1600 x 1600 m area at radii of 10, 15 and 20 m from focal trees.... 102

Table 4.23. Goodness of fit tests for observed and expected frequencies of number of 20° sectors separating individual mistletoes on hosts supporting two individuals of Erianthemum dregei or Erianthemum virescens 104

Table 4.24. Goodness of fit tests for observed and expected frequencies of maximum number of 20° sectors separating two individual mistletoes on hosts supporting three individuals of Erianthemum dregei or Erianthemum virescens 104

Table 5.1. Logistic regression analysis for survival of experimentally planted Erianthemum dregei to three weeks and one year, using the following factors: species, natural log of girth and prior infection status of target tree 123

Table 5.2. Logistic regression analysis for survival of experimentally planted Erianthemum virescens to three weeks and one year, using the following factors: species, natural log of girth and prior infection status of target tree 123

Table 5.3. Logistic regression analysis of effect of branch position on survival of Erianthemum dregei to one year, controlling for tree identity 124 Table 5.4. Logistic regression analysis of effect of branch position on survival of Erianthemum virescens to one year, controlling for tree identity 124

Table 5.5. Wilcoxon signed rank V statistics for establishment success of Erianthemum dregei and Erianthemum virescens on matched pairs of naturally infected and uninfected branches at successive time periods 125

Table 5.6. Logistic regression analysis for survival of experimentally planted Erianthemum dregei to three weeks, six weeks and six months, using the following factors: species, natural log of girth and location (isolated or non-isolated) of target tree 127

Table 5.8. Logistic regression analysis of effects of source host species and target host species on survival of Erianthemum dregei to six months, controlling for effect of infection or non-infection of branches 129

Table 5.9. Aggregation factors for ever occupied hosts of Erianthemum dregei compared to all hosts in three 100 x 100 m plots in large woodland clumps at radii of 5, 10, 15 and 20 m from focal trees 131

Table 5.10. Aggregation factors for ever occupied hosts of Erianthemum virescens compared to all hosts in nine 50 x 50 m plots covering small woodland clumps, at radii of 5, 10, 15 and 20 m from focal trees 131

Table 5.11. Goodness of fit tests for observed and expected frequencies of number of 20° sectors separating individual mistletoes on hosts supporting two individuals (both live and dead) of Erianthemum dregei or Erianthemum virescens 132

Table 5.12. Goodness of fit tests for observed and expected frequencies of maximum number of 20° sectors separating two individual mistletoes on hosts supporting three individuals (both live and dead) of Erianthemum dregei or Erianthemum virescens 132

Table 5.13. Recruitment of Erianthemum dregei on individual hosts in 21 randomly chosen plots and all isolated hosts in two years 134

Table 5.14. Mortality of Erianthemum dregei on individual hosts in 21 randomly chosen plots and all isolated hosts in two years 134

Table 5.15. Recruitment of Erianthemum virescens on individual hosts in 21 randomly chosen plots and all isolated hosts in two years 135 Table 5.16. Mortality of Erianthemum virescens on individual hosts in 21 randomly chosen plots and all isolated hosts in two years 135

Table 6.1. Waiting times until the arrival of the first bird to remove one or more seeds from visible mistletoe fruits of Erianthemum dregei and Erianthemum virescens, on isolated hosts and hosts in large woodland clumps 146

Table 6.2. Numbers of visits and numbers of seeds consumed by birds feeding on mistletoes 147

Table 6.3. Contingency table showing number of seeds of Erianthemum dregei taken by all starlings and barbets divided between isolated hosts and hosts in large woodland clumps and between occasions where the bird remained in the host tree for less than or more than two minutes after feeding 148

Table 6.4. Contingency table showing number of seeds of Erianthemum virescens taken by all starlings and barbets divided between isolated hosts and hosts in large woodland clumps and between occasions where the bird remained in the host tree for less than or more than two minutes after feeding 148

Table 7.1. Summary of contrasts between Erianthemum dregei, Erianthemum virescens mdAgelanthus subulatus at the study site 164

10 List of Figures

Figure 1.1. Flow chart showing some mechanisms through which patch size, quality and isolation affect likelihood of patch occupancy, showing three pathways by which patch size may influence the rate of extinction (1,2 and 3) 28

Figure 2.1. Erianthemum virescens in fruit 37

Figure 2.2. Agelanthus subulatus in flower 38

Figure 3.1. Map of 2x2 km study site showing woodland clumps of habitat types miombo woodland, terminalia woodland, termite mound remnants, termite mounds on dambos and rocky outcrops on dambos 52

Figure 3.2. Map of 2x2 km study site showing woodland clumps occupied by Erianthemum dregei, vacant but suitable clumps, where unoccupied hosts were present, and unsuitable clumps, where hosts were absent 53

Figure 3.3. Map of 2 x 2 km study site showing woodland clumps occupied by Erianthemum virescens, vacant but suitable clumps and unsuitable clumps 54

Figure 3.4. Map of 2x2 km study site showing woodland clumps occupied by Agelanthus subulatus, vacant but suitable clumps and unsuitable clumps 55

Figure 3.5. Incidence function with clump area for Erianthemum dregei 56

Figure 3.6. Incidence function with clump area for Erianthemum virescens 57

Figure 3.7. Incidence function with clump area for Agelanthus subulatus 57

Figure 3.8. Map of 2 x 2 km study site showing woodland clumps in which extinction of Erianthemum virescens has occurred 62

Figure 4.1. Variation in occupancy by Erianthemum dregei with host basal girth and host species in large woodland clumps and among isolated hosts, showing unoccupied Julbernardia globiflora, unoccupied Brachystegia spiciformis, occupied J. globiflora and occupied B. spiciformis 80

Figure 4.2. Variation in occupancy by Erianthemum virescens with host basal girth and host species in woodland clumps and among isolated hosts, showing unoccupied hosts of most species, unoccupied hosts of Acacia gerrardii and Grewia monticola, occupied hosts of most species and occupied hosts of A. gerrardii and G. monticola 84

Figure 4.3. Variation in occupancy hy Agelanthus subulatus with host girth, showing unoccupied and occupied Pterocarpus angolensis 88

11 Figure 4.4. Density of hosts infected by Erianthemum dregei as a function of total host density in 21 randomly located 50 x 50 m plots, showing the fitted line y = 0.1084 X 90

Figure 4.5. Density of hosts infected by Erianthemum dregei as a function of total host density in 30 random and contiguous 50 x 50 m plots, showing the fitted line y = 0.235 X - 0.000938 91

Figure 4.6. Density of hosts infected by Erianthemum virescens as a function of total host density in 28 randomly located 50 x 50 m plots, showing plots in miombo and terminalia woodland, termite mounds and rocky outcrops, showing the fitted line y = 0.358 X 92

Figure 4.7. Maps of occupied and vacant hosts of Erianthemum dregei in three 100 X 100 m plots 94

Figure 4.8. Maps of occupied and vacant hosts of Erianthemum virescens in four small woodland clumps on termite mounds 98

Figure 4.9. Map of occupied and vacant hosts of Erianthemum virescens in a 100 X 100 m plot 100

Figure 4.10. Map of occupied and vacant hosts of Agelanthus subulatus in a 1600 X 1600 m area 103

Figure 5.1. Survival of experimentally planted Erianthemum dregei on hosts Julbernardia globiflora and Brachystegia spiciformis and on non-hosts Lannea discolor and Erythrina abyssinica 121

Figure 5.2. Survival of experimentally planted Erianthemum virescens on hosts Lannea discolor and Erythrina abyssinica and on non-hosts Julbernardia globiflora and Brachystegia spiciformis 122

Figure 5.3. Survival of experimentally planted Erianthemum dregei on uninfected branches and distally from the trunk on naturally infected branches of hosts Julbemardia globiflora and Brachystegia spiciformis 125

Figure 5.4. Survival of experimentally planted Erianthemum virescens on uninfected branches and distally from the trunk on naturally infected branches of hosts Lannea discolor and Erythrina abyssinica 126

Figure 7.1. Hypothesised dispersal function for mistletoe seeds with distance from the parent plant 157

Figure 7.2. Schematic representation of regional habitat distributions for mistletoes at the study site 169

12 Chapter One

Chapter One: Introduction

1.1. Overview

The habitats of all species are patchy at one or more scales. Spatial heterogeneity is particularly distinct where there are discrete habitat patches within an inhospitable matrix. Insular habitats like these are ubiquitous. They include oceanic islands, canopy gaps, rock pools, faeces, tree holes, and various living organisms, either animals, such as individual hosts of parasites and parasitoids, or parts of plants, such as individual leaves, flowers or roots. Insular habitats are becoming even more common as human disturbance causes loss and fragmentation of natural terrestrial environments (Saunders et al. 1991; Morris 1995). For resident species, the effects of insular habitat structure on population dynamics and regional distribution will depend on the scale of patch distribution relative to the distance and frequency of movement among patches. At one extreme, populations in individual patches may be independent of each other, and at the other extreme there may be complete mixing, so that over many patches there is effectively one population. However, in the intermediate case, where populations in individual patches are sufficiently separate that demographic events are asynchronous, and yet sufficiently connected that migration among patches occurs periodically, the overall population dynamics will depend on the interplay of local (within-patch) and regional (between-patch) processes.

The conceptual basis of contemporary investigations into the distribution of organisms in insular habitats is the metapopulation approach, which is outlined below (Section 1.3). Empirical studies on occupancy of insular habitats by plants have lagged behind those on animals and existing theory has been developed primarily for animals (Husband and Barrett 1996), even though a metapopulation approach has been considered imperative to the understanding of plant population dynamics (Silvertown 1991), and has proved useful in the small number of studies where it has been applied (Kadmon and Shmida 1990; Ouborg 1993; Cipollini et al. 1994; Overton 1994; Quintana-Ascencio and Menges 1995).

13 Chapter One

One of the major problems in investigating the metapopulation dynamics of plants is that there may be temporal dispersal, via the seed bank, in addition to spatial dispersal. A bridge between studies on plants and animals can be provided by research on plants without seed banks. Epiphytic parasitic plants, commonly known as mistletoes, possess this feature. Furthermore, since mistletoes grow only on trees, and usually only on a subset of the tree species present, their habitats can be identified precisely. Models of regional occupancy, for example incidence functions, require identification of all occupied and vacant habitat, and therefore a clear distinction between habitat and non-habitat (Hanski 1992). This has been a major challenge to field studies (Lawton and Woodroffe 1991; Thomas et al. 1992; Sjorgren Gulve

1994), in particular to those on plants (Paine 1988; Quintana-Ascencio and Menges 1995).

My study assesses the distributions of three tropical African mistletoe species, Erianthemum dregei (Eckl. & Zeyh.) Tieghem, Erianthemum virescens (N.E. Br.) Wiens & Polh. and Agelanthus subulatus (Engl.) Polh. & Wiens (Loranthaceae), in patchy habitat at several scales at a study site in Zimbabwe. The central aim of the study is to investigate how the structure of the habitat, which for insular habitats can be specified in terms of the density and arrangement of habitat patches of different kinds, influences the distributions of the resident organisms. I use a framework provided by the metapopulation approach to disentangle the complex set of interacting environmental and intrinsic factors which determine plant distributions at multiple spatial scales. The remainder of this chapter develops this framework and sets out the structure of the thesis.

1.2. Distributions of plants over space and over habitat space

If habitat is patchily distributed with respect to space, then it follows that the distributions of organisms within that habitat must also be patchy with respect to space (I use the word "patchy" to denote any distribution that is not universal). This is the most fundamental explanation of why any chosen species does not occur everywhere. A less prosaic supposition is that the distribution of the chosen species may further be patchily distributed within its habitat, with respect to habitat space.

14 Chapter One

How would this patchiness arise? Any observed distribution will be determined by the past and present spatial pattern of the species' life history processes and on the interaction of those processes with the past and present spatial pattern of its habitat. This sounds obvious, but as Tilman et al. (1997) note, substantial attention has been given to the influence of spatial variation in environmental conditions, in other words variation in habitat quality, on species distributions, but it is not always acknowledged that spatial heterogeneity in life history processes will result in patchy distributions even in a completely homogenous environments.

Patchy distributions can have many different patterns, which may be usefully classified into three types: random, regular or aggregated. In regular distributions, two randomly chosen individuals are less likely to occur in the same sampling unit than expected from a random distribution. This type of pattern is sometimes called repulsive or uniform. Conversely, in aggregated distributions, two randomly chosen individuals are more likely to occur in the same sampling unit than expected from a random distribution. Aggregated distributions are also called contagious or clumped. Of course the null expectation for any chosen species within any domain of habitat is that the observed distribution will be random. However, random spatial distribution patterns of species with respect to space and with respect to habitat are probably unusual in nature (Diggle 1983; Greig-Smith 1983; Tilman et al. 1997). This is because a random distribution over habitat space can only arise in the rare event that all contributory life history processes and their interactions with habitat structure are random, or where not random, exactly compensatory.

The aspects of life history which contribute to the spatial distributions of plants are numerous, as reviewed for example by Hutchings (1986). In this study I divide them for convenience into three; dispersal, establishment and adult survival. These processes are generally sequential within a single generation, so that the pattern of dispersal (which is superimposed on the pattern of habitat) is modified by the pattern of establishment which in turn is modified by the pattern of adult survival. A non- clonal plant has one dispersal event per lifetime, and therefore only one opportunity of moving from one place to another. All other life history processes occur at a single location. If each germination site is regarded as a single patch, then dispersal is a

15 Chapter One between-patch process and establishment and adult survival are both within-patch processes.

Distributions of organisms are necessarily spatial, simply because each organism occupies space. However, we can usefully distinguish between self-organised spatial patterns and patterns where the spatial component is coincidental with some other variable among the patches. Consider the distribution of organisms among patches in an insular habitat. If we find that they are not randomly distributed, there may be a correlation between the presence of the organism in the patch and some characteristic of the patch. For example, a species of parasite may be more likely to be found on a female host than a male host. We might also test whether parasitised hosts are spatially aggregated. If they are, it may be that this aggregation is associated with aggregation of hosts with that characteristic, say because female hosts tend to group together. On the other hand, spatial aggregation of parasitised hosts may also occur where female hosts are randomly distributed over space. This pattern may arise as a result of an undetected environmental commonality among adjacent hosts, or may be self-organised, determined by a spatial pattern in some aspect of the life history of the parasite which is not host-specific, for example the pattern of dispersal.

Spatial patterns in species distributions cannot be described without explicit reference to scale. A general finding is that patterns and their causes vary with scale (Wiens et al. 1987; Powell 1989; Ives et al. 1993). Therefore a multi-scale approach is advisable (Levin 1992; May 1993). It may be useful to define scale arbitrarily (Turner et al. 1989), but more often organism-defined scaling, that is a definition of scale appropriate to the biology of the organism in question, is advocated (Wiens 1989; Lord and Norton 1990; Collins and Glenn 1997). An organism-defined scale is frequently specified in terms of the habitat of the organism (Hails and Crawley 1992; Ives et al. 1993; Snodgrass and Meffe 1998). Habitat heterogeneity may be continuous over a range of scales (Palmer 1988), but often a hierarchy of scales is clearly apparent and provides the most useful framework (Kotliar and Wiens 1990). Applying the patch terminology that is appropriate to insular habitats, in a nested hierarchy the entire habitat space (comprising all patches) at one scale is subsumed into a single patch at the next hierarchical level.

16 Chapter One

1.3. The metapopulation approach

The term metapopulation was first used in the sense derived from Levins (1969) to describe a "population of populations" and is now used broadly to describe any set of local populations linked by dispersal (Hanski and Gilpin 1991). The essential feature of the metapopulation approach is that regional habitat is perceived as insular in nature, comprising discrete patches, each of which may be occupied or vacant at any time depending on the balance between the rates of two key processes, colonisation and extinction. The now diverse family of models that constitute the metapopulation approach can all be traced back to Levins'original mathematical formulation (Levins 1969), in which the rate of change in the proportion of patches that are occupied is equal to the rate at which patches are colonised minus the rate at which patches go extinct: dP/dt = mP(l-P) - eP (Equation 1.1) where P is the proportion of habitat patches occupied, m the colonisation parameter (colonisation rate per patch) and e the extinction parameter (extinction rate per patch).

The Levins model is a direct analogue of simple models of population growth such as the logistic model. Its usefulness as a conceptual tool becomes apparent through direct comparison with the logistic model, which is usually expressed as:

dN/dt =rN(l- N/K) (Equation 1.2)

where N is population size, r is the intrinsic rate of increase and K is the population size at equilibrium, or carrying capacity. The key difference is that N, a measure of population size in the logistic model, is replaced in the Levins model by a measure of occupied habitat (P in Equation 1.1). Thus the Levins model is not a population model per se, but a model of habitat occupancy. Usually occupancy is expressed as the occupied proportion of the total number of patches, but the model can equally well be used to describe the number of patches that are occupied, as Levins did in his original formulation (Levins 1969). Next, birth and death, which additively determine r in the logistic model, are partitioned and replaced by colonisation and extinction

17 Chapter One respectively in the Levins model. Finally, the term K is missing in the Levins model. Density-dependence at the patch level is implicit in the Levins model; all patches are either vacant or at K.

Altogether, the Levins model relies on several important assumptions: 1. The total number of patches is large and constant over time. 2. All vacant patches may potentially become occupied and all occupied patches may potentially become vacant. 3. Vacant patches become occupied by colonisation events and occupied patches become vacant by extinction events. 4. Extinction events are not synchronised among patches. 5. Colonisation and extinction parameters are constant over time. 6. All patches are equal in terms of likelihood of colonisation and extinction. 7. All occupied patches have an effectively equal population size.

Clearly the Levins model is an extreme abstraction of the real world. In particular, the sixth assumption can never be fulfilled by a real system, simply because in order for all patches to have an equal chance of colonisation, they must all be equally connected to all other patches. The Levins model is parametric like the logistic model, treating all patches as equally likely to interact with all others; it acknowledges the importance of space but is not spatially explicit. The seventh assumption allows the simplification of ignoring within-patch dynamics and treating all patches as being in a simple binary state of either vacant or occupied, which requires that a vacant patch reaches maximum population size immediately upon colonisation. A real system will only approximate to this assumption if local population dynamics are much faster than regional dynamics (Hanski 1991).

There has been considerable debate over the general applicability of the metapopulation approach, particularly the Levins model, because of its strict assumptions (Harrison 1991; Doak and Mills 1994; Hastings and Harrison 1994). The current consensus is that as long as these assumptions are examined explicitly, a metapopulation approach can be illuminating for a wide variety of systems (Husband and Barrett 1996; Harrison and Taylor 1997). In general, the approach is applicable where two criteria are fulfilled. First, habitat must be readily distinguishable from

18 Chapter One non-habitat, even when it is vacant, and exist as a large number of patches within a matrix of non-habitat. Second, regional patch occupancy must be dynamic, determined by the balance of colonisation and extinction, so that even at equilibrium colonisation and extinction events can be observed.

Bearing in mind its particular limiting assumptions, the Levins model offers substantial insight into the nature of regional patch occupancy. Equation 1.1 has a single non-trivial equilibrium at P = i - e/m. We can draw several interesting predictions from this solution. Firstly, a proportion of patches will always remain occupied unless there is no extinction whatsoever. We can always expect to find vacant patches in a metapopulation; if extinctions do not occur the regional population is a "patchy population" without metapopulation structure (Harrison 1991). The second prediction is that the metapopulation will only persist \im> e. Thus for a given extinction rate, there is a threshold colonisation rate below which the metapopulation will not persist. Likewise for a given colonisation rate there is an upper threshold for the extinction rate.

An important feature of the Levins model is that the colonisation rate is a quadratic function, dependent on both the number of patches which can supply colonists and the number of empty patches, while the extinction rate is linear. A variation on the Levins model uncouples the colonisation rate from the proportion of patches already occupied (Hanski and Gilpin 1991): dP/dt = m(l-P) - eP (Equation 1.3)

This represents a mainland-island system, or a system in which there is a constant propagule rain (Harper 1977; Gotelli 1991). The patch structures of real metapopulations fall anywhere in the continuum between the original Levins model, where all patches have equal probabilities of colonisation and extinction, and the mainland-island structure, where there is one large patch that has a negligible chance of extinction and supplies a steady rate of migrants to surrounding small patches (Hanski and Gilpin 1991; Harrison 1991). The intermediate case in which there are a few large and many small populations is referred to as a source-sink metapopulation (Harrison 1991).

19 Chapter One

A further modification of the Levins model is the introduction of the rescue effect (Brown and Kodric-Brown 1977), by which occupied patches have lower risk of extinction at high P because immigration from surrounding patches is more likely (Hanski 1982): dP/dt = mP( 1-P) - eP( 1-P) (Equation 1.4)

Versions of the model including the rescue effect are applicable to many real systems and are particularly mathematically tractable (Hanski 1997a, 1997b). To complete the set of variations on the Levins model, both constant propagule rain and the rescue effect can be incorporated (Gotelli 1991): dP/dt = m( 1-P) - eP(l-P) (Equation 1.5)

These three models have different equilibria from the Levins model. Equations 1.3 and 1.5 have single stable equilibria at m/m+e and m/e respectively. Equation 1.4 does not have a stable equilibrium: if m > e then P goes to 1 (towards a patchy population sensu Harrison 1991) and if m < e then P goes to 0 (Hanski 1982).

I have drawn attention to these variations on the Levins model to illustrate that they can give rise to very different predictions of the equilibrium value of P for identical values of m and e (Gotelli 1991). However, in all systems, with or without the rescue effect and constant propagule rain, both the equilibrium and dynamic values of P depend on the balance of m and e. What then are the factors which determine the values of the colonisation and extinction parameters?

To answer this question, the metapopulation approach turns to the theory of island biogeography (MacArthur and Wilson 1967), which was developed to explain species numbers on oceanic islands. The theory predicts that any island will have an equilibrium number of species at which there is a balance between the rate of colonisation, which decreases with distance of the island from the continental mainland, and the rate of extinction, which decreases with increasing island area. The analogous prediction for single species that larger, less isolated islands or habitat patches are more likely to be occupied than smaller, more isolated habitat patches has

20 Chapter One been confirmed for many taxa, including various vertebrates (Peltonen and Hanski 1991; Sjorgren Gulve 1994; Aberg et al. 1995), invertebrates (Harrison et al. 1988; Schoener 1991; Thomas et al. 1992; Hanski et al. 1995a) and flowering plants (Bond et al. 1988; Ouborg 1993; Quintana-Ascencio and Menges 1995). There is also considerable evidence that these results are due to higher extinction rates in small patches (Harrison et al. 1988; Peltonen and Hanski 1991; Verboom et al. 1991) and lower colonisation rates of more isolated patches (Thomas et al. 1992; Ouborg 1993; Nieminen 1996).

This evidence from field studies and the theory of island biogeography contradict the standard assumption of metapopulation theory that the colonisation and extinction parameters are constant over the entire network of patches. Clearly, in real systems, patches differ sufficiently enough that their chances of going extinct or of being colonised vary. The modem metapopulation approach has incorporated the possibility of differences among patches through application of incidence functions (Diamond and Marshall 1977), which describe how the probability of occupancy of individual patches in a network varies with any continuous explanatory variable, such as patch area, number of other species present or frequency of disturbance. The metapopulation approach follows the theory of island biogeography and the empirical evidence in regarding patch size as the major determinant of the chance of extinction and patch isolation as the major determinant of the chance of colonisation (Hanski 1994, 1997b). Both the metapopulation incidence function approach and the theory of island biogeography predicate the increase in risk of extinction with decreasing patch size on the assumption that population size varies directly with patch size, and smaller populations have a higher risk of extinction due to demographic stochasticity (MacArthur and Wilson 1967; Hanski 1994). It is also possible that greater environmental stochasticity can cause smaller patches to have a higher risk of extinction (Bond et al. 1988; Harrison 1991).

A description of patches in terms of area and isolation still assumes homogeneity among patches in other attributes. In real systems patches may differ in habitat quality. Variation in quality will not affect their chances of receiving a propagule, that is their chance of colonisation, but will affect the population density within the patch and hence their chance of extinction. The usual way of modelling this is to

21 Chapter One include patch quality in any measurement of patch size, modifying area into "effective area" (Harrison et al. 1988; Verboom et al. 1991; Hanski 1994). In effect, the general concept of patch size includes connotations of both area and quality. The concept of patch isolation also depends on two aspects: the density of patches over the entire domain of habitat and the degree to which the patches are aggregated (Greig-Smith 1983; Doak et al. 1992).

By linking m and e to patch size and patch isolation, the metapopulation approach directly relates habitat occupancy to habitat structure. We can then make predictions as to how changes in habitat structure will affect occupancy. For example, consider the changes in habitat structure in an environment where human activity has caused fragmentation. Patch density is reduced, mean patch isolation increases, mean m decreases and the proportion of patches occupied, P, decreases. The more aggregated the remaining patches, the less mean m is reduced and the less P is reduced. Mean patch area is also reduced and therefore mean e increases and P decreases. The decrease in regional occupancy can lead alternatively to a new stable equilibrium, unstable dynamics or regional extinction, depending on the functions of the colonisation and extinction rates (Equations 1.1, 1.3, 1.4 and 1.5; Gotelli 1991;

Hanski and Gilpin 1991) and on local dynamics (Hanski 1985; Hanski et al. 1995b), but in all cases P decreases. The relationship between habitat structure and occupancy means that straightforward qualitative predictions can be made, without recourse to complex modelling, about how comparable networks of patches at different localities, the same network at different times, or the same network containing comparable species, will differ in the proportion of habitat that is occupied (Peltonen and Hanski 1991; Hanski et al. 1995a; Quintana-Ascencio and Menges 1996; Nieminen and Hanski 1998; Pfister 1998).

Of course, a more sophisticated approach is possible and often desirable. Most natural metapopulations do not conform neatly to the Levins model and its simple variations outlined here. Later metapopulation models have sought to relax the Levins model's stringent assumptions and incorporate realistic features such as local dynamics (Hastings and Wolin 1989; Hastings 1991; Gyllenberg and Hanski 1992; Gyllenberg et al. 1997), spatial arrangement of patches (Fahrig and Paloheimo 1988; Perry and Gonzalez-Andujar 1993; Hanski and Thomas 1994), predator-prey

22 Chapter One dynamics (Nee 1994; Hassell and Wilson 1997), coexistence of competitors (Hanski 1983; Tilman et al. 1994; Lehman and Tilman 1997) and correlation in conditions among patches (Harrison and Quinn 1989; Smith and Gilpin 1997). The modified models are usually complex and reliant on simulations, but they provide estimates of population parameters which compare well with field data, and make useful novel predictions (Hanski et al. 1995a and b; Kareiva and Wennergren 1995; Hanski and Simberloff 1997).

In summary, we have seen that metapopulation models are a class of mathematical models used to make predictions about the distribution of organisms in habitats which can be characterised as consisting of discrete patches. It is worth making a note here about terminology, for while the word "metapopulation" is not inaccurate, it is somewhat misleading as a description of the full range of systems to which the Levins model and its derivatives can be applied. Firstly, as I have already noted, they are models of habitat occupancy rather than pure population models. Furthermore, while the prefix "meta" implies a system of local populations, the Levins model can be applied equally well to systems in which only one individual is able to dwell in each patch. In fact it is these systems which most closely fit the assumption of the model that colonised patches move immediately to saturated population size. Finally, the metapopulation approach can be used to describe systems in which the proportion of patches that are occupied does not depend on actual metapopulation processes, that is processes whose rates are determined by regional occupancy. A simple variation on the Levins model gives the mainland-island model (Equation 1.3), which is the single- species version of the theory of island biogeography. In this model both colonisation and extinction rates are independent of regional occupancy. The metapopulation approach can be applied to a wide spectrum of insular habitats, which makes it a powerful framework for the real world, where composite metapopulations of adjacent, interacting systems of different types and also hierarchically nested metapopulations are no doubt common (Harrison and Taylor 1997).

23 Chapter One

1.4. Mistletoes in patchy habitat: a framework

1.4.1. Aim and approach

Mistletoes are parasitic plants which occupy habitat that is patchy over several scales. In this study I consider three species of tropical African mistletoes, Erianthemum dregei, Erianthemum virescens and Agelanthus subulatus (Loranthaceae), which share the same life habit and mode of dispersal, at a study site of approximately 4 km by 3 km, which is described in detail in Chapter Two. My broad aim is to answer the following two questions for each of the species at multiple spatial scales: 1. What is the pattern of distribution of the species over habitat space? 2. What evidence is there that the structure of the habitat has influenced the pattern of distribution of the species over habitat space? In this section I draw together the premises developed in Sections 1.2 and 1.3 to create a framework for tackling these questions.

At and below the scale of the entire study site, the habitat of the mistletoes is arranged in a distinct hierarchy of scales, each of which is relevant to their biology, or organism-defined. An individual mistletoe grows at a single position on a branch of a tree. Branches are grouped into trees and trees are grouped into clumps of woodland. The woodland clumps are distributed over the study site according to the pattern of clearance for agriculture on the uplands and the pattern of scattered outcrops on the intervening dambos (low-lying seasonally waterlogged grasslands). For brevity I label these scales the branch scale, the tree scale and the clump scale. At each of these scales the habitat of the mistletoes is insular, comprising a large number of discrete habitat patches in a matrix of non-habitat. I take an individual patch to mean an individual branch, tree or woodland clump at each of the respective scales. The three scales form a nested hierarchy, in that the entire domain of habitat becomes a single patch at progressively broader levels (see Section 1.2), although it is also possible to consider the distribution of mistletoes among patches at the finer scales over the domain of the broader scales, for example among trees over the entire study site.

24 Chapter One

The insular structure of the mistletoes'habitat at all scales suggests that a metapopulation approach is applicable. The power of the metapopulation approach as a framework for answering the two broad questions outlined above lies in these three simplifying binary distinctions: habitat patches versus non-habitat, vacant patches versus occupied patches and within-patch processes versus between-patch processes. The first two of these distinctions allow assessment of the distribution of organisms over their habitat space, which has different implications to their distribution over absolute space or over an undefined space (as in the logistic model). The distinction between within-patch and between-patch processes is the crux of the framework I propose here, as it connects habitat structure to patch occupancy, and leads to simple qualitative hypotheses about the nature of that connection.

Plants are sedentary, and during the lifetime of an individual non-clonal plant there is a maximum of one between-patch process, a single dispersal event. Dispersal can otherwise occur within the patch, as long as the defined scale of the patch is larger than the space occupied by a single individual plant. Within-patch dispersal is possible at each of the branch, tree and clump scales. Post-dispersal plant life history processes, essentially establishment and adult survival (following the scheme of Section 1.2), occur exclusively within the patch. In the metapopulation approach, the only between-patch process is colonisation and the only within-patch process is extinction (except where there is a rescue effect and colonisation and extinction are confounded at high regional occupancy, which can be discounted in this system where rates of population growth are intrinsically low). Tallying the concepts of colonisation and extinction with plant life history processes, the one process that determines the rate of colonisation is between-patch dispersal, while within-patch dispersal, establishment and adult survival contribute to within-patch population size and hence to the rate of extinction.

The metapopulation approach further asserts that colonisation and extinction are each primarily dependent on different aspects of habitat structure (Section 1.3). The rate of colonisation, and therefore the rate of between-patch processes, depends chiefly on patch isolation, which in turn depends on the density and aggregation of patches over the domain of habitat space. The rate of extinction by contrast depends chiefly on patch size, which can be expressed as an amalgam of patch area and patch quality.

25 Chapter One

The suite of distinctions between within-patch and between-patch processes are summarised in Table 1.1. Throughout this study I use this framework to link observed species distributions, life history processes and habitat structure.

Table 1.1. Summary of distinctions between within-patch and between-patch processes.

Factor Within-patch Between-patch

Metapopulation process extinction (e) colonisation (m)

Life history processes within-patch dispersal between-patch dispersal establishment adult survival

Key habitat attribute patch size patch isolation determining rate of (area and quality) (density and aggregation) metapopulation process

Now we have a framework that links the scales at which habitat patchiness can be recognised and provides hypotheses of how the structure of the habitat, expressed as the area, quality and isolation of patches, will affect habitat occupancy. The approach in this study will be to test these hypotheses and the assumptions on which they rest as far as possible at each of the three defined scales. I shall deal with the specific predictions and assumptions in the relevant chapters, but deal with some general issues in the remainder of this chapter.

1.4.2. General assumptions

A preliminary concern is whether an approach based on metapopulation principles is in fact appropriate for the chosen study system, and vice versa whether the system provides a good test of hypotheses about the effects of patch structure on occupancy. There are two basic requirements for application of the metapopulation approach; first that habitat is distinguishable from non-habitat and exists as a large number of patches in a matrix of non-habitat and second that patch occupancy is determined by a balance of ongoing colonisation and extinction events (Section 1.3). Since mistletoes grow only on trees, and usually a particular subset of the tree species present at any one site, they have easily recognisable habitat, even when it is vacant. This trait is unusual

26 Chapter One among plants and is the reason that I chose mistletoes as a study system. At all three of the scales chosen for study here, the habitat of the mistletoes does comprise a large number of patches separated by non-habitat, fulfilling the first requirement. The second requirement, that colonisation and extinction result in a dynamic pattern of occupancy, needs to be tested in the field, through checking for evidence of colonisation and extinction events in patches at the various scales.

As well as assuming the fundamental requirements of the metapopulation approach, the framework summarised in Table 1.1 assumes exclusive causal relationships between patch size and rate of extinction and between patch isolation and rate of colonisation. Although this distinction, illustrated in Figure 1.1, will not always hold in real systems, it is the underlying assumption of the theory of island biogeography, adopted by metapopulation theory (MacArthur and Wilson 1967; Hanski 1994), and provides a tractable working model. A major focus of this study will be to assess as far as possible whether observed variation in patch occupancy with patch size or patch isolation are due to the processes of dispersal, establishment or adult survival. Of course, in natural systems, these population dynamics will depend on a complex suite of interacting intrinsic and environmental factors, with possible negative or positive density-dependence, such as Allee effects (e.g. Kuussaari et al. 1998). Models of patch colonisation and extinction are numerous (Hansson 1991; Foley 1997), but have underlying principles in common, which I discuss in the remainder of this section.

The model of within-patch dynamics implicit in the theory of island biogeography and the Levins model is that post-colonisation within-patch population growth is rapid (compared to the rate of between-patch dispersal), until a maximum population density is reached which is maintained by density-dependence. Thus the mean population density is constant for all patch sizes and the regional population is randomly distributed among patches of all sizes. The risk of extinction will decrease with population size, but not patch size per se, at a rate depending on the relative contributions of demographic and environmental stochasticity (Pimm et al. 1988; Harrison 1991). This pathway is shown by arrow 1 in Figure 1.1.

27 Chapter One

PATCH PATCH PATCH DISTANCE QUALITY SIZE

BETWEEN- WITHIN- PATCH PATCH PROCESSES PROCESSES

POPULATIO SIZE

OLONISATION EXTINCTIO

OCCUPANCY

28 Chapter One

Two Other pathways are possible, which are not included in the theory of island biogeography but are frequently cited in discussions of the species-area relationship and the effects of habitat fragmentation (Connor and McCoy 1979; Harrison and Fahrig 1995; Andren 1996; Bender et al. 1998). The first is that patch size may affect the rate of within-patch population dynamics (arrow 2), for example because small patches experience greater environmental stochasticity due to edge effects or greater risk of disturbance (Saunders et al. 1991; Fahrig and Merriam 1994). This pathway will result in varying population density with patch size. Secondly, patch size may have a direct effect on the risk of extinction due to environmental catastrophe (arrow 3), independent of population size. I draw attention to this because at the tree scale, where individual trees are treated as habitat patches, there is patch turnover. Deaths of occupied host trees entail extinction of mistletoe populations. The chance of host death, which is thought not to be related to mistletoe load in most systems (Reid et al. 1995), will have a stochastic element but will increase with increasing host size/age.

Turning to patch isolation, the qualitative relationship between distance from sources of propagules and chance of arrival (colonisation) is not contentious, but quantification can be difficult. Functions of the probability of seed dispersal with distance will tend to reach a peak at some distance from the parent plant and then follow a leptokurtic decline (Willson 1992), but the best mathematical descriptions of these curves can vary considerably among systems (Portnoy and Willson 1993; Willson 1993). The distribution of habitat patch sizes will affect patterns of dispersal. Colonisation rates will be independent of regional patch occupancy if the system approximates to a mainland-island model (Equation 1.3). This may be true of my system at the clump scale but not at the tree or branch scales, where all patches are similar and the Levins model (Equation 1.1) is perhaps more apt. However the difference between the Levins model and the mainland-island model is immaterial to the slope of increase of equilibrial P with m at constant e, as the respective equilibria of 1 - elm and mim+e show. Finally, unlike patch size, patch isolation has no obvious unit of measurement. Isolation of individual patches may be measured most simply as distance from a single nearest neighbour, but this will not always be the most

29 Chapter One biologically relevant measure (Hanski 1997b). Among groups of patches, patch isolation varies inversely with density, and is reduced if patches are aggregated.

1.4.3. Study species

The inclusion of three co-occurring species of mistletoes provides some potentially interesting contrasts among differing habitat characteristics and perhaps also rates of population processes. The chosen mistletoes are all in the same family (Loranthaceae) and have an identical life habit and similar guilds of pollinators, dispersers and predators (Polhill and Wiens 1998). However their host ranges are very different. The three species, A. subulatus, E. dregei and E. virescens are respectively monophagous, narrowly polyphagous (four hosts) and broadly polyphagous (at least 35 hosts). Their respective host ranges are also entirely exclusive. Hence the same landscape provides different habitat structures at all scales for the three sympatric species of mistletoe. In the absence of life history differences, the regional habitat occupancy of the three species at all scales should rank according to the abundance of their respective habitats, because the colonisation parameter m increases with patch density.

As noted earlier, the mistletoe system was chosen because the habitats of mistletoes can be recognised in the absence of the parasites; precise mapping of occupied and unoccupied hosts is possible in the field. Mistletoes also have several other advantages as a system for studying the effects of habitat structure on plant distributions. They do not undergo seed dormancy (Lamont 1983) and thus do not have seed banks. This means that habitat patches can become occupied only via colonisation, and not via recruitment from the seed bank, which is a complication for the application of a metapopulation approach to most seed-bearing plants (Husband and Barrett 1996). A complication in applying the metapopulation approach to animals can arise if patches become vacant through mass dispersal rather than only through extinction (Lawton and Woodroffe 1991; Hill et al. 1996). Clearly this does not apply to mistletoes or any other non-clonal plants as they are sedentary. A further advantage of mistletoes as a system for this type of study are that both established plants and seeds are macroscopic and occur in small enough numbers to be counted with relative ease. Lastly, when adult individuals die they leave behind scars on the

30 Chapter One host, which can be used as indicators of previous extinction events. The major disadvantage of the system is that the large scales of time and space over which mistletoe populations vary cannot be investigated fully in short-term studies and preclude many forms of experimental manipulation.

1.5. Structure of the thesis

Within the constraints of time and logistics, it was not feasible to assess occupancy and the processes of dispersal, establishment and adult survival at the full range of patch sizes and degrees of isolation at three scales for three species. Therefore I undertake a broad examination of patterns of occupancy at the clump and tree scales, with reference to the branch scale as an adjunct to the tree scale. In the appraisal of contributory life history processes, I concentrate on comparison between patches of maximum contrast, that is between hosts in large woodland clumps, which effectively comprise continuous woodland, and isolated hosts, which are located singly or in very small groups. These isolated hosts represent a convergence between the clump and tree scales. At the clump scale they are the smallest patches, and frequently the most isolated, while at the tree scale they comprise patches of similar size to those in continuous woodland, but at the extreme of isolation.

This chapter has established a framework for investigating the distribution of plants in habitat that is patchy at multiple scales, using three species of tropical mistletoe in fragmented woodland as a study system. Chapter Two is a further introductory chapter, which describes the study site and the biology of mistletoes, particularly the three study species, in detail.

Chapter Three examines patch occupancy at the clump scale, in a network of woodland clumps covering a 2 x 2 km square. The 304 clumps are a mixture of naturally occurring wooded outcrops and remnants of woodland surviving after clearance for agriculture in the late 1950s. Thus the woodland clumps vary in history and tree species composition as well as in size and isolation. For the three species E. dregei, E. virescens and A. subulatus I assess variation in likelihood of occupancy with clump area, quality and isolation. In the null model, where individual mistletoes

31 Chapter One are randomly distributed with respect to patch size so that population density is constant in clumps of all sizes, the chance of a clump being occupied will increase with patch size simply because a larger proportion of the total regional habitat is sampled. I look for deviation from this model. The effective areas of clumps are modified by habitat quality, which I take at this scale as the proportion of trees in the clump that are suitable hosts for the particular species of mistletoe. The proportions of hosts vary among patches of five different ecological habitat types so that habitat type is effectively equivalent to patch quality. I measure the final patch characteristic, isolation, as single distances from the nearest presently occupied and the nearest long- term occupied woodland clump.

Chapter Four examines the distribution of mistletoes among and within trees in plots scattered throughout the 3 x 4 km study site. Thus it stresses the tree scale, but also provides tests of hypotheses at the broader clump scale and at the narrower branch scale. The concept of a habitat patch at the tree scale is very different from the clump scale, because the patches are themselves living organisms, which grow, age and die. As at the clump scale, I assess variation in likelihood of patch occupancy with size, quality and isolation. Size of individual trees as habitat patches is most appropriately measured in terms of canopy volume or total branch length available to mistletoes. Host size and age vary together and their respective effects on occupancy by mistletoes is still a subject of some contention; here I refer simply to variation with size/age. I use estimates of host volume to test the null model that mean mistletoe density is constant with patch size, and therefore that patch size per se has no effect on rates of within-patch population processes. Patch quality is compared among host species for the two polyphagous mistletoes and patch isolation is investigated via three different routes: simulation analysis of spatial aggregation of occupied hosts, regression analysis of variation in occupancy with local host density and comparison of presence and numbers of mistletoes on hosts in woodland clumps of different sizes and on isolated hosts. Finally, I also test whether mistletoes are spatially aggregated at a finer scale, within the canopies of their hosts.

Chapters Five and Six seek to identify the life history processes that cause the patterns of mistletoe distribution described in Chapter Four. Chapter Five deals with establishment and adult survival, by means of a series of establishment experiments

32 Chapter One and censuses of scars on hosts from dead mistletoes, natural recruitment and natural mortality. In general establishment rates will be more important than rates of adult mortality in determining observed patterns of adult plant distributions. The establishment experiments measure establishment success of E. dregei and E. virescens on branches of varying host species (quality), size, location (isolated versus non-isolated hosts) and position in the canopy. They also compare establishment on naturally infected and uninfected branches to test for possible density-dependence at this stage in the mistletoes' life history. Chapter Six turns to dispersal, asking whether observed spatial patterns of mistletoe aggregation may indeed be due to variation in the chance of dispersal. I compare the frequency of visits by mistletoe-feeding birds to isolated and non-isolated hosts and estimate the proportion of within-host and between-host dispersal. Chapters Five and Six both concentrate on E. dregei and E. virescens, since A. subulatus fruited outside my annual field season.

Chapter Seven synthesises the findings of the preceding chapters, linking the branch, tree and woodland clump scales and the patterns of occupancy to the patterns of dispersal, establishment and adult survival. I finish the chapter by commenting on some overall observations of the study and drawing out interesting unanswered questions.

33 Chapter Two

Chapter Two: Study organisms and study site

2.1. Study organisms

2.1.1. An introduction to mistletoes

The term mistletoe is used to describe members of the angiosperm families Viscaceae and Loranthaceae, which are all obligate hemiparasites of trees and shrubs, and are usually epiphytic. Mistletoes are completely or partially self-sufficient for the products of photosynthesis (Moore 1994), but rely on the host plant for water and other nutrients, via a bridge of living tissue, known as the haustorium, which connects the xylem or phloem of the parasite indirectly to the equivalent tissue of the host (Kuijt 1969). The Viscaceae are widespread geographically, incorporate 400 species in seven genera, and include the only species of mistletoe that occurs in Britain, Viscum album. The Loranthaceae are largely confined to the tropics, but are a bigger and more diverse family, with 900 species in 65 genera (Barlow 1983).

Most mistletoes reproduce sexually only (Kuijt 1969). In the Loranthaceae, the vectors of both pollen and seeds are generally birds (Calder 1983). African Loranthaceae show very little variety in type of fruit or mode of dispersal, but great diversity in floral structure and specialised mechanisms of pollination (Polhill 1989; Kirkup 1998). Most African Loranthaceae are pollinated by sunbirds (Nectariniidae). The mistletoes typically have an explosive mechanism by which the flower opens and releases pollen when probed by a sunbird seeking nectar (Feehan 1985). Almost all Loranthaceae have bisexual flowers and among the few species with unisexual flowers dioecy is unknown (Kuijt 1969). Many species self-pollinate and some can produce fruit in the absence of pollinators (Docters van Leeuwen 1954). Ovules are absent in mistletoes and therefore the embryo and its surrounding tissue is not technically a seed, and the fruit is a pseudoberry rather than a true berry. These anatomical features do not affect the role of the fruit in dispersal and the term "seed" is considered convenient (Kuijt 1969; Willson 1992). Each fruit contains one seed. Bird-dispersed mistletoe fruits have three distinct layers in the pericarp: a sticky viscous layer surrounding the embryo, enclosed by a thin

34 Chapter Two brightly coloured skin (together making up the seed) and an outer fleshy epicarp (Kuijt 1969).

In general frugivorous birds seek to eat not the epicarp of mistletoe fruits but the viscous material, or viscin, which lies within the seed. There are several ways in which birds of different species handle mistletoe fruits: pecking the viscin without removing the seed, removing the seed and then wiping it from the beak after swallowing as much of the viscin as possible, or swallowing the whole seed and later regurgitating or defecating it (Liddy 1983). The stickiness of the viscin means that even birds which regurgitate or defecate mistletoe seeds must wipe them from their bodies onto their perch (Godschalk 1983; Reid 1989). After seeds have been deposited, usually in groups corresponding to single feeding sessions (Davidar 1983; Sargent 1995), the viscin dries and glues them in place (Kuijt 1969). In Africa, mistletoe fmits are eaten by many frugivorous species of bird, though the tinker barbets are thought to be the most important dispersers in savanna ecosystems (Dowsett-Lemaire 1982; Godschalk 1983, 1985).

The process of germination in mistletoes is triggered by excision of the fruit from the adult plant, a phenomenon unknown in any other group of plants. Thus, unless environmental conditions are adverse, there is no period of dormancy and seeds germinate soon after being deposited on a host branch (Lamont 1983). Establishment of the haustorium starts when the radicle produces a holdfast, or haustorial disc, with an airtight connection to the bark of the host. The haustorial disc pulls open the dead layers of bark from the host and exposes living cells. Penetration of the host tissues is then by both mechanical and chemical means (Knutson 1983).

Owing to the dirth of long-term studies, there is little quantitative information about the lifespans of mistletoes. In a population survey of Phoradendron juniperinum, using anatomical and morphological indices of age, Dawson et al. (1990) estimated the oldest mistletoes to be 19 years old. There was a sharp decline in the number of mistletoes over the age of 10 years and the authors suggested that the maximum size of individual parasites is limited by their physiology: when the cost of maintaining old, inefficient photosynthetic or xylary tissue exceeds the gain of carbon or water, an individual dies.

35 Chapter Two

Mistletoes rarely cause death of the trees or shrubs which they parasitise (Knutson 1983; Reid and Lange 1988), but they commonly cause the death of infected branches, especially distal to the mistletoe (Knutson 1983; Sargent 1995; Tennakoon and Pate 1996). They may also have more general negative effects on their hosts, reducing growth (Reid et al. 1994) or reproduction (Silva and Martinez del Rio 1996). In the coniferous plantations of western North America mistletoes cause greater losses in yields than any other disease (Hawksworth 1983).

2.1.2. Species descriptions

Thirty-five species of Loranthaceae, as well as several species of Viscaceae, occur in Zimbabwe (Polhill and Wiens 1998). This study concentrates on three of the loranthaceous species: Erianthemum dregei (Eckl. & Zeyh.) Tieghem, Erianthemum virescens (N.E. Br.) Wiens & Polh. mdAgelanthus subulatus (Engl.) Polh. & Wiens. All three of these mistletoes are superficially similar in appearance. They grow to a maximum of 1-2 m in height and are densely branched, resembling pendulous bushes. They have simple leaves that reach a maximum size of about 6 cm in E. virescens, 10 cm in E. dregei and 12 cm in A. subulatus (Polhill and Wiens 1998). Adult individuals are clearly distinct and do not have closely spaced haustoria as is common in other mistletoes, particularly the Viscaceae. Nor was epiparasitism of one mistletoe on another observed at the my study site in Darwendale, although A. subulatus is known to be occasionally epiparasitic elsewhere (Polhill and Wiens 1998).

E. dregei, E. virescens and A. subulatus all have explosively opening flowers which are pollinated by sunbirds (Kirkup 1998). It is probable that all three species are able to pollinate successfully among flowers on the same plant and hence to have the capacity to develop local populations following the dispersal of only one individual (D. Kirkup, personal communication). The fruits of E. dregei and E. virescens are very similar in size and stmcture, but differ in colour. At the Darwendale site, both were 1-1.5 cm in length, including the epicarp, with a seed of 0.7-1.2 cm in length. In E. dregei, the epicarp, which is on display to potential dispersers, is red and the seed is orange. In E. virescens, the epicarp is turquoise and encloses a red seed. E. virescens is illustrated in Figure 2.1 and A. subulatus in Figure 2.2.

36 Chapter Two

a. fruiting twig x 0.5

b. detached leaf and fruit x 1

d. detached dead flower x 1 c. detached mut x 1

Figure 2.1. Erianthemum virescens in fruit

37 Chapter Two

Figure 2.2. Agelanthus subulatus in flower xl

38 Chapter Two

At the Darwendale site I observed that all three species were deciduous to some degree, E. virescens the most, losing all its leaves by the end of the dry season (September), and E. dregei the least. The three species also differed in the phenology of their flowering and fruiting, without any overlap (Table 2.1). Among individuals of E. dregei, flowering and fruiting were highly synchronised, but this was less the case for E. virescens. Since all field work was done between September and April of sequential years, the fruiting of A. subulatus was not closely observed.

Table 2.1. Phenology of flowering (f) and fruiting (F) of the three mistletoe species Erianthemum dregei, Erianthemum virescens and Agelanthus subulatus.

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec E. dregei ffffffff FFFF E. virescens A. subulatus ffffffffffffffffffff ffff

2.1.3. Host ranges

The host ranges of mistletoes vary from very broad to species-specific (Norton and Carpenter 1998). The size and identity of a mistletoe species' host range can vary over space, over scales of 100 to 1000 km (Thomson and Mahall 1983; Monteiro et al. 1992). Due to the paucity of collections, the host ranges of most African Loranthaceae are not well known, but it is clear that the three species studied here have different host ranges in different geographical locations (Polhill and Wiens 1998). Thus a necessary component of this study was to ascertain the host ranges of the three species at the study site. All observed host species were identified and recorded over a period of three years. Names of trees follow Coates Pal grave (1986).

Erianthemum dregei was found to parasitise four closely related legumes, the two dominant miombo species and two congeners; Brachystegia boehmii Brachystegia glaucescens Brachystegia spiciformis (dominant) Julbemardia globiflora (dominant)

39 Chapter Two

Erianthemum virescens was found to have a wide host range. Thirty-five species of trees were identified as hosts to E. virescens and this a probably a subset of the total host range of this mistletoe. Despite its wide host range, including many legumes, E. virescens was found not to share any of the host species of E. dregei. Effectively the full set of potential host species is partitioned between the two Erianthemum species, although of course it is not possible to say whether this is by chance or through competitive exclusion over evolutionary time. Only a small number of the common tree species were not infected by either Erianthemum, notably Terminalia sericea and Burkea africana. This is the complete list of tree species found infected by E. virescens: Acacia amythethophylla Acacia gerrardii Acacia goetzei Acacia karroo Acacia nigrescens Azanza garckeana Cassia abbreviata Combretum apiculatum Combretum collinum Combretum hereroense Combretum molle Dalbergia melanoxylon Dalbergia nitidula Dichrostachys cinerea Dombeya rotundifolia Erythrina abyssinica Erythrina latissima Euclea divinorum Eicus sur Elacourtia indica Grewia flavescens Grewia monticola Jacaranda mimosifolia Lannea discolor Ochna schweinfurthiana Peltophorum africanum Pseudolachnostylis maprouneifolia Rhoicissus revoilii Rhus longipes Securinega virosa Senna singueana Vangueria infausta Vangueria randii Vitex payos Ziziphus mucronata

40 Chapter Two

Agelanthus subulatus occurred on only one species of tree, Pterocarpus angolensis, which was never found to be infected by Erianthemum spp. It seems hkely that at this study site A. subulatus is specific to one host species, since it was not found on the congeneric Pterocarpus rotundifolius, which was frequently encountered at the site.

The collections of the National Herbarium in Harare, Zimbabwe, suggest that the host ranges recorded for E. dregei and E. virescens in this study are similar to elsewhere in Southern Africa. Specimens of E. virescens at the Herbarium come from a wide variety of hosts including many exotics. E. dregei specimens have all been collected from Brachystegia spp. and Julbernardia spp. except for one from an exotic acacia. However, in South Africa E. dregei is found on many tree species, including Dichrostachys cinerea (Dzerefos 1995), which was never a host at this site.

Specimens of A. subulatus at the Herbarium show that the species is not universally confined to Pterocarpus angolensis. Elsewhere it has been collected commonly from P. angolensis, but also from P. rotundifolius, Burkea africana, Brachystegia spiciformis and Albizia antunesiana.

2.2. Study Site

The study was carried out at Gordon Estates, Darwendale, Zimbabwe. The site was chosen because the natural vegetation was cleared during one discrete period into a mosaic pattern typical of large-scale farming areas in Zimbabwe, and throughout the world. For the purposes of this study, an area uniform in soils and topology, bounded by a game fence, was chosen as a broad site. Occupancy by mistletoes of individual trees singly and in plots was measured throughout this area, which extends approximately 4x3 km. Mapping of woodland clumps was done within a 2 x 2 km square area inside the broad site (see Chapter Three for maps). The 2x2 km area was typical of the broader site and indeed the surrounding landscape beyond the confines of the study site.

The site is tropical, lying at 17°S and 30°E, at an altitude of 1420 m. The mean annual

rainfall is 818 mm, with a range from 312 mm to 1305 mm (from records for past

41 Chapter Two

50 years, collected at the site on behalf of the Zimbabwe Government Meteorological Office). Rainfall is highly seasonal, concentrated in the summer months from November to April. The rainfall in the three years of field work was slightly above average, with 1055 mm in 1995-1996, 964 mm in 1996-1997 and 847 mm in 1997-1998. The 1997-1998 season included the wettest January ever recorded at the site, with 353 mm falling in a single month.

Soils at the site are uniform granitic sands (J. Everitt, unpublished farm report) supporting a natural vegetation cover of open miombo woodland. Miombo woodland is a widespread vegetation type in central Africa, and is defined as being dominated by trees of the genera Brachystegia, Julbernardia and Isoberlinia (White 1983), which are all legumes (Caesalpinioideae). At the Darwendale site the most common species is Julbernardia globiflora. There are also some pockets of terminalia woodland, where the miombo dominants are replaced by Terminalia sericea. Altogether 128 indigenous and naturalised species of tree (woody plants which grow to over 1.5 m in height) are known to occur in the study area (T. Gordon, personal communication). The understorey is a mixture of shrubs and grasses, particularly of the genus Hyparrhenia.

Before 1950, when the farm was acquired by its present owner, the study site was used for subsistence agriculture which required small areas of woodland to be cleared for homesteads and for fields on a rotational basis. The 1953 aerial photograph of the site shows that woodland cover was continuous. During the 1950s the study site was cleared extensively to allow large-scale cultivation. Since 1961 no further clearance has been done. Thus the present fragments of miombo woodland have been in place for 37 years. They have been fairly well preserved from human disturbance because the owner does not allow wood-cutting, and this policy is enforced by the presence of the game fence. Interspersed with the fields and remnants of woodland are dambos (low-lying seasonally waterlogged grasslands). Small woodland clumps occur naturally on the dambos where there are termite mounds or rocky outcrops. These clumps provide an interesting contrast with the remnants of miombo woodland for two reasons, firstly because their fragmented spatial pattern pre-dates the 1950s clearance, probably by many centuries, and secondly because they differ in tree species composition.

42 Chapter Two

The study site is currently used for the cultivation of tobacco, which is grown in rotation, with one crop year followed by two years of fallow, during which fields are planted with grass. Cattle are grazed here during the rainy season and the area is also a sanctuary for several small captive populations of game, mainly indigenous large herbivores such as giraffes, zebras and various types of buck. These are not kept for any commercial purpose.

The field work for this study was carried out over the period of three consecutive rainy seasons in 1995-1996, 1996-1997 and 1997-1998.

43 Chapter Three

Chapter Three: Distribution of mistletoes among woodland clumps

3.1. Introduction

Clearance of natural vegetation for agriculture inevitably causes loss of habitat for indigenous species. Usually clearance is spatially discontinuous, so that the remaining habitat is fragmented as well as diminished in total area. Thus the process of fragmentation has altogether three consequences for regional habitat structure: loss of habitat, lower mean habitat patch size and higher mean distance among patches. It is well established that for many taxa of animals and some plants in fragmented habitats or naturally patchy habitats the probability of occupancy, or incidence function (Hanski 1997b), is positively related to patch size (e.g. Peltonen and Hanski 1991; Verboom et al. 1991; Thomas et al. 1992; Ouborg 1993; Quintana-Ascencio and Menges 1995) and negatively related to patch isolation (e.g. Harrison et al. 1988; Kadmon and Shmida 1990; Thomas et al. 1992; Ouborg 1993; Aberg et al. 1995).

The most parsimonious explanation for the typical positive incidence function with patch area is that populations in individual patches are samples of the pre- fragmentation population. Likelihood of including individuals of the initial population will increase with the size of the sample taken (the "sampling hypothesis" of Connor and McCoy 1979). According to this hypothesis, only habitat loss has any effect on patch occupancy and neither patch size per se nor patch isolation have any additional effects. The sampling hypothesis will apply generally to fragmented habitats immediately after a fragmentation event, but with time the characteristics of the individual patches may become determinants of patch occupancy, giving rise to incidence functions based on biological processes rather than features of sampling.

Explanations of incidence functions that invoke biological processes fall into two groups. First, smaller patches may be more prone to edge effects, microclimatic changes and disturbance (Bond et al. 1988; Saunders et al. 1991). Higher environmental stochasticity in small patches will result in higher rates of extinction.

44 Chapter Three

Fragmentation influences incidence functions via patch size but not via patch isolation. Second, metapopulation theory and the theory of island biogeography, which view colonisation and extinction as the major determinants of patch occupancy, contend that the probability of local demographic extinction decreases with increasing population size, and hence with increasing patch size (MacArthur and Wilson 1967; Hanski 1991). Note that this basic model does not suggest any effect of patch size above that implied by the sampling hypothesis. However, although metapopulation theory classically emphasizes demographic stochasticity, recent metapopulation models have also included environmental stochasticity (Gyllenberg et al. 1997).

Metapopulation theory and the theory of island biogeography also address the effects of patch isolation. More isolated patches are less likely to be encountered by dispersing individuals and are thus less likely to be colonised, leading in turn to a lower chance of occupancy (Ebenhard 1991). Decrease in the probability of patch occupancy with increasing isolation has been confirmed for many taxa at a variety of sites (see references above). Where individual patches are equally likely to be sources of colonists, as in the classic Levins metapopulation model (see Chapter One), then distance of a patch from the nearest occupied patches is expected to be a determinant of probability of occupancy in that patch. Where a small number of large, permanently occupied patches supply the bulk of colonists, as in the source-sink model, then distance from these large patches is more important (Harrison 1991; Eriksson 1996).

Intrinsic variation in habitat quality among patches may also influence rates of extinction or colonisation and therefore occupancy (Harrison et al. 1988; Paine 1988; Lawton and Woodroffe 1991). For example, patches with a particular feature could be more attractive to dispersing individuals or their animal vector, and therefore receive a higher number of colonists. Importantly, patch quality can vary with patch size. Larger patches are likely to incorporate a wider variety of habitat than small patches, which may account for their increased chance of occupancy by particular species (Connor and McCoy 1979; Brown 1984). Furthermore, remnant patches of habitat in cleared agricultural landscapes are unlikely to be random samples of the initial habitat, as certain vegetation types will tend to be cleared preferentially (Saunders et al. 1991).

45 Chapter Three

The relative roles of sampling, environmental change and metapopulation dynamics in determining patch occupancy in fragmented habitats can only be distinguished experimentally (Connor and McCoy 1979). However, most real, large-scale networks of patches are not amenable to manipulation. Nonetheless a survey, even at a single point in time, can indicate whether fragmentation has caused any effect on occupancy additional to the simple sampling effect, and point to the processes determining regional occupancy (Hanski 1992). The distinctive prediction of metapopulation theory is that increasing patch isolation will cause a reduction in likelihood of occupancy above that explained by patch size (Hanski 1991, 1997b). The environmental change hypothesis predicts that population density will be reduced in smaller patches. The usual way of measuring this effect is to compare population densities in patches of different size (Andren 1994; Bender et al. 1998), but it is possible to reject the sampling hypothesis in its strict form even in the absence of population density data, as I show below.

The sampling hypothesis predicts that if individuals are randomly dispersed over the sample space, then the probability of finding at least one individual in a sample will increase with the area sampled according to the binomial expansion:

P = \ - {\ - Po) (Equation 3.1)

where P is probability of occupancy of a sample of area A and Pg is probability of occupancy of a sample of area Ao (usually the minimum sampling area). This decelerating curve can be usefully linearised as In (P/l-P). The slope of this line against In (Area) is always negligibly lower than one for the sampling hypothesis with random distribution. For a patchy habitat, a slope of more than one indicates that either individuals are regularly distributed or that the occupancy rate of patches increases faster with size than predicted by patch area alone. Thus under regular distribution of individuals the environmental change hypothesis would predict a slope of more than one. Obversely, a slope of less than one indicates an aggregated distribution of individuals or a slower increase in patch occupancy with area than predicted by area alone.

46 Chapter Three

This chapter examines the occupancy by three species of mistletoe, Erianthemum dregei, E. virescens and Agelanthus subulatus, of woodland clumps in the 2 x 2 km study site. The present clumps of woodland are of two origins. On the uplands are remnants of continuous miombo or terminalia woodland which was cleared in the 1950s, while on the intervening dambos are naturally occurring scattered clumps of trees on termite mounds and rocky outcrops (see Chapter Two). Therefore mistletoe populations in clumps of miombo or terminalia woodland were initially samples of the pre-clearance population, but those on the dambos must have arisen from colonisation events. Since the regional arrangement of woodland clumps on the uplands has been in place for less than 50 years, these clumps may not have reached a post-fragmentation equilibrium (Hanski 1997a), and may not yet display the consequences of insular habitat structure. It is likely then that the clumps on dambos will show greater decrease in likelihood of occupancy with isolation than those on the uplands.

As well as history, the woodland clumps of the uplands and dambos vary in tree species composition and hence in density of hosts for the three mistletoe species. In other words, woodland clumps vary in the quality of the habitat which they offer each species, where quality modifies patch area into effective area (see Section 1.3). According to the sampling hypothesis (Equation 3.1), if host density and aggregation in a given type of habitat (e.g. miombo woodland) are constant with area, then the likelihood of occupancy will increase at the same rate with patch area for all habitat types, but be lower or higher at a given area depending on host density in that habitat type. A difference in the rate of increase in probability of occupancy with area would suggest that some aspect of patch quality, for example host density or host aggregation, or perhaps some other factor such as microclimate or attractiveness to frugivorous birds, changes with patch area. The same argument applies to comparisons among the three species. The species whose hosts occur in the largest proportion of woodland clumps is expected to have the highest regional occupancy, because relative isolation of patches with suitable habitat is lowest and thus colonisation events are most likely, but the rate of increase in chance of occupancy with area will be the same for all three species, regardless of the density of their hosts or frequency of infection of individual hosts.

47 Chapter Three

The aims of this chapter are to ascertain whether there is any evidence of metapopulation processes at the clump scale and to test several specific predictions which are suggested by the framework developed in Chapter One and by the structure of the landscape at the study site: 1. Likelihood of patch occupancy by mistletoes will decrease with patch isolation, and the effects of patch isolation will be more pronounced on dambos, where the patch structure has been in place for a long period, than on uplands, where the patch structure is of recent origin relative to the lifespans of mistletoes and their hosts. 2. Regional occupancy of woodland clumps by the three species of mistletoes will rank in order of the regional abundance of their hosts, but the rate of increase in occupancy with area will be constant for all three species. 3. For any one species of mistletoe, occupancy of individual clumps will be proportional to host density (effective area). Thus clumps of habitat types with high host density will have greater likelihood of occupancy than clumps of the same size of habitat types with low host density, but the rate of increase in occupancy with area will be constant for all habitat types.

3.2. Methods

All woodland clumps in a 2 x 2 km square area of the study site were identified on a 1:50 000 1995 aerial photograph. Adjacent woodland clumps were regarded as distinct if they were separated by a distance of at least 25 m devoid of woody plants over 1.5 m in height, except in the case of strips of trees between cultivated fields, where cut-off points were chosen where roads ran through the strips. These distinctions were verified in the field. A total of 305 clumps of woodland were identified, ranging in size from single isolated trees to tens of hectares. All were searched by two observers for mistletoes of the three species E. dregei, E. virescens and A. subulatus. The areas of the woodland clumps were calculated by the GIS package LDRISI for Windows from the scanned aerial photograph. Distances between clumps were measured directly from the photograph to an accuracy of 5 m.

48 Chapter Three

Habitat quality was described in terms of simple observational classes. Clumps were classified into five habitat types: 1. miombo woodland (numerically dominated by Brachystegia spiciformis and Julbernardia globiflora) 2. terminalia woodland (dominated by Terminalia sericea) 3. remnant termite mound from cleared woodland 4. termite mound on dambo 5. rocky outcrop on dambo Clumps of habitat the first three types are remnants created by clearance in the 1950s, while clumps on dambos occur naturally and, as the 1953 aerial photograph shows, were in existence prior to the period of clearance and presumably for a long time previously. However, termite mounds on uplands (type 3) and those on dambos (type 4) are indistinguishable in terms of tree species composition. Note that large clumps of miombo and terminalia woodland (types 1 and 2) can also contain termite mounds within them which are equivalent to type 3.

Logistic regression analysis of the association of occupancy with area, isolation and habitat type of individual woodland clumps was carried out using the statistical package GLIM Version 3.77 (Royal Statistical Society, London). Using this technique of generalised linear modelling, the total deviance and degrees of freedom for the full data set were calculated first, and then the deviance and degrees of freedom for the maximal model, which included all factors (explanatory variables and their interactions). Next each second order interactive factor was taken out of the maximal model in turn and only those whose removal caused a significant decrease in the explained deviance were retained. The first order factors were then similarly removed in turn from a model containing all first order factors and significant second order factors.

In logistic regression, which uses a binomial error structure, the reduction in deviance caused by the removal of each term approximates to a (chi-square) value (Crawley 1993). Here values that corresponded to probability levels of more than 0.05 were regarded as insignificant. Significant categorical factors (habitat type) were examined for differences among categories and collapsed wherever the collapsed categorisation

49 Chapter Three did not lead to a significant decrease in explained deviance compared to the uncollapsed categorisation. In this way, final models including only significant terms was obtained. Note that with binomial errors the sum of the partitioned deviance is not equal to the total deviance.

In the initial analysis habitat type was set at five levels for E. virescens according to the classification given above, but only four levels for E. dregei because of the paucity of clumps on termite mounds (types 3 and 4) containing hosts. The effect of habitat type was not analysed for A. subulatus because of the small number of woodland clumps in which its hosts occurred. The derived equations relating the likelihood of infection to the areas of woodland clumps were used to identify the group of largest patches which were most likely to be occupied for each species. These were, arbitrarily, all patches with more than 90 % chance of being occupied for E. virescens, and all patches with more than 75 % chance of being occupied for E. dregei and A. subulatus.

All clumps too close to the edge of the study area for the distance to the closest occupied clump or closest occupied large clump were excluded from analyses including distance. Furthermore, in a small number of cases neighbouring clumps were each other's closest occupied clump and thus recorded identical, non- independent measures of distance. Therefore all analyses including distance were carried out twice, dropping the first of each such pair of clumps (randomly selected) in the first instance and then the second. The two sets of data gave indistinguishable results and only the first is presented.

3.3. Results

3.3.1. Patterns of habitat and habitat occupancy

Mapping of the 2 x 2 km study area (Figure 3.1) showed that the uplands, on which terminalia woodland, miombo woodland and termite mound remnants (blue, green and yellow respectively) occurred, were interspersed with four dambos, where small scattered woodland clumps on termite mounds and rocky outcrops (red and purple

50 Chapter Three respectively) were located. On the uplands, terminalia woodland was confined to one corner of the site. Patch size was to some extent coincident with habitat type, since all of the largest clumps were miombo woodland while termite mounds and rocky outcrops supported only small clumps of woodland.

Hosts of E. dregei occurred in a high proportion of clumps of miombo woodland (its two most common hosts, Julbernardia globiflora and Brachystegia spiciformis, being the dominants of miombo woodland) and to a lesser extent in terminalia woodland, on rocky outcrops. Only nine out of 91 termite mounds supported hosts of E. dregei. Hosts of E. virescens, which has at least 35 host species at the site, were widespread, occurring frequently in clumps of all habitat types. There were clear differences in the density of hosts of E. virescens between miombo and terminalia woodland (low) and termite mounds (high). Rocky outcrops were intermediate. The rarest species, A. subulatus, has only one host species at the site. Individuals of this species, Pterocarpus angolensis, were confined mainly to miombo woodland.

Of the total 305 clumps of woodland that were distinguished at the site, 80 (26 %) contained one or more individuals of the four host species of E. dregei, 224 (73 %) contained hosts of E. virescens and 16 (5 %) contained hosts of A. subulatus. This result confirmed that E. virescens has the most regionally abundant habitat, followed by E. dregei then A. subulatus. The largest woodland clumps, which were all miombo woodland, included hosts of all three mistletoes. For all three species, clumps containing hosts were not always occupied. E. dregei occupied 24 out of 80, or 30 %, of all suitable clumps (Figure 3.2). E. virescens and A. subulatus were both more widely distributed among suitable clumps than E. dregei. E. virescens occupied 138 out of 224 possible clumps (62 %), scattered widely throughout the uplands and dambos (Figure 3.3). A. subulatus occurred at a very high frequency, occupying 13 out of 16 possible clumps (81 %) in spite of the regional rarity of clumps containing hosts (Figure 3.4).

51 Chapter Three

Figure 3.1. Map of 2 x 2 km study site showing woodland clumps of habitat types miombo woodland (green), terminalia woodland (blue), termite mound remnants (yellow), termite mounds on dambos (red) and rocky outcrops on dambos (purple).

52 Chapter Three

Figure 3.2. Map of 2 x 2 km study site showing woodland clumps occupied by Erianthemum dregei (dark blue), vacant but suitable clumps (light blue), where unoccupied hosts were present, and unsuitable clumps (grey), where hosts were absent.

53 Chapter Three

Figure 3.3. Map of 2 x 2 km study site showing woodland clumps occupied by Erianthemum virescens (dark blue), vacant but suitable clumps (light blue) and unsuitable clumps (grey).

54 Chapter Three

Figure 3.4. Map of 2 x 2 km study site showing woodland clumps occupied by Agelanthus subulatus (dark blue), vacant but suitable clumps (light blue) and unsuitable clumps (grey).

55 Chapter Three

3.3.2. Effects of area, habitat type and distance

Logistic regression showed that whether or not a woodland clump was occupied by mistletoes was positively related to the area of the clump for all three species, accounting for 50 % of the total variation in occupancy for A. subulatus, but only 21 % for E. dregei and 13 % for E. virescens. Incidence functions showing probability of occupancy with area suggested differences among the three species. For E. dregei, clumps of less than 150 m^ (In = 5) were never occupied, and probability of occupancy increased slowly with clump area at smaller clump sizes (Figure 3.5). For E. virescens there was a faster increase in probability of occupancy at smaller clump sizes, while at larger clump sizes the incidence function reached a plateau at less than P = 1 (Figure 3.6; though it was clear from Figure 3.3 that at maximum clump sizes all clumps were occupied). The third species A. subulatus was found only in larger woodland clumps and showed a steep rise in likelihood of occupancy with area (Figure 3.7). However, in the logistic regression, where the increase of probability of occupancy is modelled as an S-shaped curve symmetrical about the P = 0.5 value, there were no differences in the rate of change of probability of occupancy with area among the three species (%^ = 2.07, df = 2, p > 0.05, n = 320).

1 09 0.8 0.7 - 0.6 P 0.5 0,4 0.3 0.2

0.1 0 <5 5 6 7 8 9 >9 (n=5) (n=19) (n=17) (n=18) (n=8) (n=5) (n=8)

In (area in m^)

Figure 3.5. Incidence function (probability of occupancy, P) with clump area for Erianthemum dregei.

56 Chapter Three

1 0.9 0.8 0.7 0.6 P 0.5 0.4 0.3 - 0.2 0.1

0 - 0M 4 5 6 7 8 >8 (n=9) (n=30) (n=55) (n=75) (n=30) (n=10) (n=13)

In (area in m^)

Figure 3.6. Incidence function (probability of occupancy, P) with clump area for Erianthemum virescens.

0.9 0.8 0.7

0.6 - f05 0.4 - 0.3

0.2 - 0.1 0 6-7 >9 (n=6) (n=4) (n=6)

In (area in m^)

Figure 3.7. Incidence function (probability of occupancy, P) with clump area fox Agelanthus subulatus.

Analysis for E. dregei alone showed that while clump area was significantly associated with likelihood of occupancy, there were no differences among habitat types (Table 3.1), and the final statistical model included only area (Table 3.2). For E. virescens habitat type did have an effect (Table 3.3). The five initial habitat types collapsed into three statistically distinguishable categories. In order of increasing probability of occupancy, the two woodland types (miombo and terminalia) formed one group, rocky outcrops a second group and the two termite mound types a third

57 Chapter Three

(Table 3.4). There was no interaction between habitat type and area of the woodland clumps (Table 3.3).

Factor Deviance df P r^

In A 21.64 1 <0.001 0.214 H 254 3 NS H.ln A 3J8 3 NS

Model 21.64 1 0.214

Residual 7^25 78

Total 100.89 79

Table 3.2. Regression coefficients of significant factors associated with presence or absence of Erianthemum dregei in all 80 woodland clumps containing hosts. The model has the form In (P/l-P) = Constant + In A where P likelihood of occupancy and A is clump area in m^.

Factor Regression coefficient s.e.

Constant -5.77 1.34 In A 0.676 0.175

Table 3.3. Logistic regression analysis for presence or absence of Erianthemum virescens in all 224 woodland clumps containing hosts, using the following factors; natural log of area in m^ (In A) and habitat type (H).

Factor Deviance df P r'

In A 3830 1 <0.001 0128 H 21.20 2 <0.001 0.071 H.ln A 4.48 2 NS

Model 51.02 3 0.171

Residual 76

Total 298.35 79

58 Chapter Three

Table 3.4. Regression coefficients of significant factors associated with presence or absence of Erianthemum virescens in all 224 woodland clumps containing hosts. Habitat type HI is miombo and terminalia woodland, H2 rocky outcrops on dambos and H3 termite mounds. The model has the form In (P/l-P) = Constant + In A where P is likelihood of occupancy and A is clump area in m^. The given constant is for HI and those for H2 and H3 and their associated standard errors are differences from HI rather than absolute values.

Factor Regression coefficient s.e.

Constant -5.33 1.09 H2 0.781 0348 H3 1.79 0.428 In A 0.797 0.151

Distance to the nearest occupied clump was found to have a small but significant association with likelihood of occupancy for E. dregei (Table 3.5; Table 3.6). The distance to the nearest clump large enough to be practically certain of permanent occupancy was also tested, and found to have no effect. Occupancy was not related to distance from occupied clumps for E. virescens (Table 3.7). Distance also had no effect on occupancy of clumps by A. subulatus (Table 3.8) and the final model included area alone (Table 3.9). However, for all three species, the largest clumps were close to other clumps, which may have affected the analysis. The maximum isolation distances were fairly low: 215 m for E. dregei, 150 m for E. virescens and 260 m for A. subulatus.

Table 3.5. Logistic regression analysis for presence or absence of Erianthemum dregei in 66 woodland clumps for which independent distance measures were taken, using the following factors: natural log of area in m^ (In A), distance from nearest occupied clump in m (DO) and distance from nearest large occupied clump in m (DL, replacing DO in model).

Factor Deviance df P r%

In A 5.95 1 <0.05 0.079 DO 4.08 1 <0.05 0.054 DL 020 1 NS DO.ln A 036 1 NS DL.ln A 1.01 1 NS

Model 13.28 2 0.176

Residual 64

Total 75.31 66

59 Chapter Three

Table 3.6. Regression coefficients of significant factors associated with presence or absence of Erianthemum dregei in 66 woodland clumps with independent distance measures. The model has the form In (P/l-P) = Constant + In A + DO where P is likelihood of occupancy, A is clump area in m^ and DO is distance from nearest occupied clump in m.

Factor Regression coefficient s.e.

Constant -4.04 1.77 In A 0^42 0.232 DO -0.0106 0.00580

Table 3.7. Logistic regression analysis for presence or absence of Erianthemum virescens in 199 woodland clumps for which independent distance measures were taken, using the following factors: natural log of area in m^ (In A), habitat type (H), distance from nearest occupied clump in m (DO) and distance from nearest large occupied clump in m (DL, replacing DO in model).

Factor Deviance df P r^

In A 4&20 1 <0.001 0.160 H 2440 2 <0.001 0.094 DO 0.50 1 NS DL 0.20 1 NS H.ln A 2.91 2 NS DO.In A 1.00 1 NS DL.ln A 048 1 NS EDO 3.71 2 NS H.DL 3.89 2 NS

Model 5&39 3 0.209

Residual 21329 195

Total 269.68 198

Table 3.8. Logistic regression analysis for presence or absence of Agelanthus subulatus in all 16 woodland clumps containing hosts, using the following factors: natural log of area in m^ (In A), distance from nearest occupied clump in m (DO) and distance from nearest large occupied clump in m (DL, replacing DO in model).

Factor Deviance df P r^

In A 7.67 1 <0.01 0.497 DO 0.03 1 NS DL &23 1 NS DO.ln A 0.03 1 NS DL.ln A 032 1 NS

Model 7.67 1 0.497

Residual 7.77 14

Total 15.44 15

60 Chapter Three

Table 3.9. Regression coefficients of significant factors associated with presence or absence of Agelanthus subulatus in all 16 woodland clumps containing hosts. The model has the form In (P/l-P) = Constant + In A where P is likelihood of occupancy and A is clump area in m^.

Factor Regression coefficient s.e.

Constant -12.8 9.70 In A 1.93 1.45

3.3.3. Tests of the sampling hypothesis

The slopes of In (P/l-P) with In (Area) differed significantly from the value of one predicted for the sampling hypothesis with random distribution in the case of E. dregei (Table 3.2; t = 1.85, df = 79, p <0.05, Student's t-test) but not E. virescens (Table 3.4; t = 1.34, df = 223, p >0.05). The slope for A. subulatus had a high standard error because of the small number of samples and did not differ from one (Table 3.9; t = 0.64, df= 15, p >0.05).

3.3.4. Evidence for local extinction

Several woodland clumps were not currently occupied by mistletoes but showed evidence of previous infection, in the form of dead mistletoes attached to branches, or scars from previous haustorial attachments. Two clumps showed evidence of extinction of E. dregei (2 % of all clumps containing hosts), 14 ofE. virescens (6 %) and none of A. subulatus. No differences were found for E. virescens in patch area between currently occupied woodland clumps and clumps where there was evidence of extinction (%^ = 0.89, df = 1, p > 0.05, n = 151). The largest clump where extinction was recorded was 2528 m^ (In = 7.84), well over the median clump size of 524 m^ for clumps containing hosts of E. virescens. Clumps where extinction of E. virescens had occurred were scattered throughout the study site and thus did not suggest any evidence of spatial correlation among extinction events (Figure 3.8).

61 Chapter Three

Figure 3.8. Map of 2 x 2 km study site showing woodland clumps in which extinction of Erianthemum virescens has occurred (orange).

62 Chapter Three

3.4. Discussion

The probabihty of occupancy of woodland clumps by mistletoes increased with clump area, as expected. However, for two of the three species, E. virescens and A. subulatus, there was no evidence to reject the hypothesis that the increase with area was due purely to a sampling effect. For E. dregei, occupancy showed a small but significant increase with decreasing patch isolation in addition to the variation in area (Table 3.5), which implies that the regional distribution of this species cannot be explained by the sampling hypothesis alone, and that a metapopulation process, specifically dispersal between patches, is a determinant of regional distribution. Interestingly, occupancy was related to distance from the nearest occupied habitat patch, but not to the nearest large (permanently occupied) patch, which suggests a stepping-stone dispersal process (Gilpin 1980) and provision of colonists from many or all patches rather than long-distance dispersal events from an effective mainland (Harrison 1991; Eriksson 1996).

Despite there being no statistically detectable effect of isolation on the distribution of E. virescens, this species showed alternative evidence of a dynamic pattern of regional occupancy over time, or a metapopulation structure in the broad sense of the term (Harrison 1997). Hosts of E. virescens were found in clumps throughout the study site, both on uplands and on dambos (Figure 3.3). Therefore, while populations in clumps on the uplands may be derived from a continuous pre-clearance population, those on the dambos must have arisen through colonisation events and cannot be samples of a former population. There was evidence that extinction events as well as colonisation events have occurred (Figure 3.8) in clumps on uplands and on dambos, and that these were not spatially correlated. There was however no evidence that probability of colonisation decreased with patch isolation or that probability of extinction decreased with patch size.

Since E. virescens was the only species that occurred frequently on both uplands and dambos, it was the only species for which a comparison could be made between the effects of isolation in a long-established patch network and a more recent patch network, but no effect of patch isolation in either system was found. The finding that only E. dregei showed a relationship between patch isolation and occupancy was

63 Chapter Three surprising. E. virescens on dambos would be expected to show the strongest relationship if the effect of patch isolation increased with longevity of regional patch structure. Alternatively, A. subulatus, which had the fewest number of woodland clumps containing hosts, would be expected to show the strongest relationship if the relative degree of patch isolation was most important.

Hosts of E. virescens occurred in a higher proportion of clumps than hosts of E. dregei, and as predicted E. virescens had a higher frequency of regional occupancy than the congeneric E. dregei. However, A. subulatus, which was expected to have the lowest level of patch occupancy because of the small proportion of clumps in which its hosts were found, had a higher frequency of occupancy than either Erianthemum species. Therefore this species must have a higher rate of colonisation per patch than predicted from the density of its hosts, or a lower rate of extinction per patch. Possibly these differences act at the scale of individual hosts, leading to a higher frequency of infection per host and thus to a higher frequency of patch occupancy at the broader clump scale.

Although the slopes of In (PH-P) against In (Area) did not differ among the three species, the fitted model for E. dregei on its own (Table 3.2) had a slope lower than the value of one predicted for the sampling hypothesis with random distribution. There are three possible explanations for this: that hosts are aggregated, that mistletoes are aggregated more than hosts, or that small clumps are disproportionately favourable as habitat for E. dregei. The plotted incidence function for E. dregei (Figure 3.5) showed that there was a shallow rate of increase in likelihood of occupancy over a wide range of patch sizes at the smaller end of the spectrum. The most likely explanation is that hosts of E. dregei are aggregated at a broad scale, so that even in woodland clumps of 3000 m^ (In = 8) there may be very few hosts and the likelihood of occupancy is correspondingly low. This would explain the slope of less than one for In (P/l-P) against In (Area). Only in clumps of several hectares, which were with one exception miombo woodland (Figure 3.1), do hosts occur at sufficient densities for the probability of occupancy to rise rapidly with area.

By contrast, the incidence function for E. virescens (Figure 3.6) showed a relatively faster increase at smaller clump areas and slower increase at larger clump areas,

64 Chapter Three which is most hkely explained by the expected higher densities of its hosts in the habitat types that comprise the majority of small clumps (termite mounds and rocky outcrops) than in terminaha or miombo woodland. Logistic regression analysis showed that the incidence functions for E. virescens varied among habitat types (Table 3.3), with clumps of the same area most likely to be occupied if located on termite mounds, then rocky outcrops on dambos, then miombo or terminalia woodland (Table 3.4). The pattern of statistical aggregation (miombo + terminalia; termite mounds on uplands + termite mounds on dambos) and the order of ranking support the supposition that these differences are explained by the proportion of hosts in each type. Alternatively they might be explained by differences in infection frequencies of individual hosts in the three categories.

The fact that remnant termite mounds on uplands was statistically lumped with termite mounds on dambos rather than with other remnants on uplands also suggests that there are no broad differences between the two interspersed systems of uplands and dambos. For E. virescens, either the regional occupancy on the uplands has already reached a post-fragmentation equilibrium (Hanski 1997a), or, more likely, occupancy of woodland in the uplands was never higher than on the dambos. It is feasible that the general density of hosts of E. virescens in miombo and terminalia woodland is so low that the interior termite mounds act as individual habitat patches in much the same way as those on dambos. For E. dregei, by contrast, which occurs mainly in the tracts of miombo woodland which have been extensively cleared, one effect of clearance seems to be a decline in occupancy of isolated clumps.

Considering that this woodland was cleared less than fifty years ago, habitat fragmentation appears to have had a rapid effect on the distribution of E. dregei, considering that its generation time is probably in the order of ten to twenty years (Dawson et al. 1990; Polhill and Wiens 1998).

Summarising the outcomes of the three predictions made at the beginning of the chapter, several surprising results were obtained. First, likelihood of patch occupancy only decreased with patch isolation for one of the three species, E. dregei. The effects of patch isolation were therefore most pronounced where E. dregei occurred, which was on the uplands, contrary to the prediction that effects would be more pronounced on the dambos. Second, regional occupancy did not rank with regional abundance of

65 Chapter Three hosts of the three species. The species with the regionally rarest host, A. subulatus, showed the highest occupancy. The rates of increase in probability of occupancy with patch area were however statistically identical, as predicted. Third, the occupancy of clumps did appear to be proportional to relative host density for one species, E. virescens, though not E. dregei. As predicted, the rate of increase in the likelihood of occupancy was the same for all habitat types.

The results of this chapter have led to the hypothesis that many of the differences in the distribution among woodland clumps among the three study species and among habitat types may be due to differences in host densities within the clumps, or to differences in the frequency of infection among individual hosts. Also, the finding that one species, E. dregei, showed a reduced occupancy in small isolated clumps, in spite of the relatively short time since clearance and the small range of isolation distances, suggests that comparisons between hosts in these and in larger clumps merits further attention. Chapter Four goes on to assess the distribution of mistletoes among trees within woodland clumps of different sizes and types.

66 Chapter Four

Chapter Four: Distribution of mistletoes among and within trees

4.1. Introduction

Mistletoes usually infect only a subset of the total number of woody species at any site (Norton and Carpenter 1998; Polhill and Wiens 1998). At the Darwendale site, for example, the three mistletoes Erianthemum dregei, Erianthemum virescens and Agelanthus subulatus have distinct and exclusive host ranges. Thus their habitat is structured as a network of discrete patches, in this case individual host trees, in a matrix of non-habitat. Clearly mistletoes will not be randomly distributed with respect to woodland if they cannot infect all trees. Furthermore, it has been found that even within the set of trees that are hosts (i.e. with respect to habitat space), distributions of mistletoes tend not to be random. All available studies report aggregated distributions of mistletoes among hosts (Hoffmann et al. 1986; Donohue 1995; Martinez del Rio et al. 1995; Norton et al. 1997a), conforming where tested to the negative binomial distribution (Thomson and Mahall 1983; Reid and Lange 1988; Monteiro et al. 1992; Overton 1994), which is not surprising, since distributions of parasites among their hosts are typically described by the negative binomial (Crofton 1971).

Chapter One introduced the argument developed from metapopulation theory that in a habitat comprising discrete patches, the structure of the habitat will affect its pattern of occupancy by resident organisms. Specifically, the likelihood that individual patches are occupied will increase with patch size, due to decreasing chance of extinction, and decrease with patch isolation, due to decreasing chance of colonisation. There is substantial evidence from the literature that the aggregated distribution of mistletoes among hosts is indeed associated with characteristics of individual host trees.

67 Chapter Four

Considering patch size first, volume is more appropriate than area as a measure of size when patches are the canopies of trees. Previous studies have found invariably that the likelihood that individual hosts are occupied by mistletoes increases with correlates of canopy volume, such as girth or height (Thomson and Mahall 1983; Hoffmann et al. 1986; Reid and Lange 1988; Reich et al. 1991; Overton 1994; Donohue 1995; Martinez del Rio et al. 1995; Norton et al. 1997a), and that the number of mistletoes on a host also increases with host size (Reid and Lange 1988; Overton 1994; Donohue 1995). Metapopulation theory assumes that the size of a population within a patch is directly proportional to patch size. The simple volume- occupancy relationship is complicated for mistletoes by the fact that trees grow with age. Various authors have argued that the volume-occupancy relationship is due to the length of time over which mistletoes have accrued (Overton 1994), physiological or architectural changes in the host with age (Reid and Lange 1988; Norton et al. 1997a) or volume per se (Martinez del Rio et al. 1995), but the supporting evidence is inconclusive. Unfortunately, without very long term studies it is impossible to distinguish the effects of host age and size on mistletoe accumulation. The fact that trees age has a further implication for regional patch structure, since the eventual death of hosts results in patch turnover. Assuming that trees that die are replaced, the death of hosts does not affect the regional density of patches, but does provide an additional mechanism by which patches can become extinct.

Where a species of mistletoe has more than one host species at a site, the various host species often differ in frequency of infection (Thomson and Mahall 1983; Hoffmann et al. 1986; Reid and Lange 1988; Monteiro et al. 1992; Martinez del Rio et al. 1995). In the terminology of Chapter One, these host species vary in the quality of habitat which they provide for the mistletoe species. The general metapopulation approach assumes that within-patch dynamics are so much more rapid than between-patch dynamics that any differences in rates of within-patch processes among patches of different quality are irrelevant to overall habitat occupancy. The critical effect of quality is on the maximum population size that the patch can support, so that quality modifies patch size into effective patch size (Hanski 1994). This approach provides the simplest prediction of differences in occupancy among various host species. Alternatively, the quality of habitat provided by various host species may influence

68 Chapter Four the rates of within-patch population processes of the mistletoes, such as establishment and adult mortality, which will also lead to differences in levels of host occupancy and may also lead to differences in the rate of increase in the number of mistletoes with host size.

Little is known about how occupancy of host trees by mistletoes varies with isolation. The primary prediction arising from metapopulation theory is that the proportion of patches that are occupied will increase with increasing patch density because of an increase in the colonisation rate, so that individual hosts in subsites with higher host density should have a greater likelihood of infection by mistletoes. While this prediction holds true regardless of whether dispersing propagules come from a single source (mainland-island model) or from all occupied patches (Levins model), at the tree scale the regional system is expected to correspond more closely to the Levins model, since host trees comprise a large number of small and similar patches. This leads to a second prediction that because dispersal in the Levins model is localised, likelihood of occupancy of hosts will depend on their distance from other occupied hosts. Therefore occupied hosts will be spatially aggregated. However, as discussed in Chapter One, spatial aggregation of occupied patches is not always due to localised between-patch dispersal, but may also arise where hosts with particular characteristics which affect occupancy, such as species or size, are aggregated in space.

Only three studies relevant to the effect of host isolation on occupancy by bird- dispersed mistletoes are available in the literature, of which two found spatial aggregation of infected hosts (Elias 1987; Donohue 1995) and one did not (Overton 1996). Both Elias (1987) and Donohue (1995) found that aggregation of mistletoes within quadrats (measuring 10 x 10 m and 50 x 30 m respectively) was associated with aggregation of large individuals of their preferred hosts. Elias did not find any pattern of mistletoe distribution independent of host characteristics, but Donohue (1995) found that aggregation of occupied hosts within quadrats occurred above that explained simply by host distributions. Infected hosts were more likely to have an infected neighbour than predicted by chance, but this aggregation was highly localised, occurring between pairs of adjacent trees but not over any greater extent. In an equivalent study, Overton (1996) surprisingly found no aggregation whatsoever

69 Chapter Four among infected hosts at two sites where hosts were randomly distributed, in spite of locahsed dispersal of mistletoe seeds.

As well as testing predictions about the effects of the size, species and isolation of individual host trees on mistletoe distributions, investigation of the distribution of mistletoes among trees can also be used to test hypotheses at higher and lower spatial scales, at the clump scale and at the branch scale. Chapter Three put forward the prediction that in habitats which are fragmented over broad scales, the density of resident species may be lower in smaller remnant patches than in larger ones, if the process of fragmentation has led to non-random patterns of dispersal or mortality. It is possible to test this by comparing the occupancy of individual host trees in woodland clumps of various sizes. At the scale below the level of individual trees, single hosts themselves comprise patch networks of individual branches, referred to as the branch scale in Chapter One. Assuming that all branches of the same size within a tree are equally susceptible to infection by mistletoes and evenly spaced, any spatial aggregation of mistletoes among branches is expected to be due to effects of dispersal rather than aggregation of similar patches. Although it is well established that mistletoes tend to be markedly aggregated at the scale of individual trees (see references above), spatial aggregation of mistletoes within those hosts has not been examined in previous studies.

This chapter examines the distribution of the three mistletoe species E. dregei, E. virescens and A. subulatus among their hosts, treating individual host trees as discrete habitat patches, with the aim of testing the following predictions which arise from the metapopulation approach via the framework outlined in Chapter One: 1. Likelihood of occupancy of hosts will increase with increasing host volume. 2. Host species will modify effective patch volume, so that higher quality host species will have a higher likelihood of occupancy at a given volume, but the rate of increase of likelihood of infection will increase with host volume at an equal rate for all host species. 3. The density of mistletoes on individual hosts will be constant among occupied hosts and therefore the number of mistletoes per host will increase directly with host volume.

70 Chapter Four

4. The likelihood of occupancy will increase with host density and therefore a greater proportion of hosts will be infected at localities with higher host density. 5. Following from the previous prediction, isolated hosts will be less likely to be infected than hosts in woodland clumps. 6. Occupied hosts will show aggregation due to localised dispersal over and above any pattern due to the distribution of hosts of similar size or species. 7. Applying the same argument at the branch scale, occupied branches within a tree will be spatially aggregated because of localised dispersal.

I test these predictions for hosts of E. dregei and E. virescens in randomly selected plots with different host densities and located in different sized woodland clumps throughout the study site, but also with a complete sample of all of the most isolated patches at this scale, which are host trees that occur singly, or in very small groups, isolated by open space from other clumps of woodland. For A. subulatus, a complete sample of hosts over a broad area is used rather than hosts in plots, because of the relative rarity of its single host species.

4.2. Methods

4.2.1. Erianthemum dregei and Erianthemum virescens

Pairs of random coordinates of longitude and latitude were located on a 1:50 000 aerial photograph of the study site throughout the entire area within the game fence. Points that did not fall on a clump of woodland were rejected. Selected points were located on the ground and checked for the presence of hosts of either E. dregei or E. virescens. Square plots of 50 x 50 m (a quarter of a hectare) were marked out from all points with one or more hosts of either species, on random compass bearings, except in smaller woodland clumps where the bearing was chosen along the longest axis of the clump, to include as many of the trees as possible.

71 Chapter Four

Twenty-one plots were chosen in this way. I classified them a priori according to whether they fell on large woodland clumps, where the woodland extended beyond the boundary of the plot in all directions, on medium clumps, which extended less than 50 m along one axis, or on small clumps, which extended less than 50 m in all directions. Size of the woodland clumps coincided to some extent with habitat type (see Chapter Three). Five plots fell on large woodland clumps (four miombo, one terminalia), eight on medium clumps (four miombo, two terminalia and two rocky outcrops) and eight on small clumps (two miombo, two rocky outcrops and four termite mounds). The random sample of 21 plots did not include sufficient numbers of E. virescens hosts, so an additional seven small woodland clumps on termite mounds were randomly chosen from the clumps surveyed in Chapter Three. Three of the five plots in large woodland clumps were later quadrupled in size to one hectare. This was chiefly for purposes of spatial analysis, although the full data sets were also used in regression analysis for E. dregei.

In addition to the basic survey, complete surveys of the most isolated hosts of the two Erianthemum species were made. All woodland clumps in the survey of Chapter Three which contained three or fewer hosts of E. virescens and less than ten other trees were selected. For E. dregei, the same process yielded a small number of samples, so all woodland clumps in the broader study area within the game fence with three or fewer hosts and less than ten other trees were identified from the 1:50 000 aerial photograph and on the ground. I will refer to the trees measured in this way as isolated hosts or isolated trees.

In the marked plots the relative positions of all trees (woody plants over 1.5 m in height) were measured, correct to 0.5 m, using a tape measure and compass. The species and basal girth (approximately 30 cm above ground) were recorded for all trees in plots and for all isolated hosts. Every tree was searched systematically for mistletoes by two observers. All individuals were identified to species and their approximate two-dimensional location in the canopy in terms of compass bearing and distance from the trunk of the host tree were noted.

72 Chapter Four

4.2.2. Agelanthus subulatus

Since Agelanthus subulatus and its host Pterocarpus angolensis were relatively rare, it was possible to record all host and mistletoe individuals over an area of approximately 1600 X 1600 m within the study site. The UTM coordinates (eastings and northings) of all individuals of P. angolensis in this area were mapped using a Trimble Pathfinder GPS receiver and corrected to an accuracy of 0.5 m by Trimble software using simultaneous GPS recordings from the permanent base station at the Surveying Department of the University of Zimbabwe. The basal girths and numbers of live mistletoes were recorded for all the individuals of P. angolensis.

4.2.3. Analysis

The variance to mean ratios of numbers of mistletoes per host were calculated to test whether mistletoes of each species were randomly distributed among all hosts. The numbers per host were also fitted to a negative binomial distribution. The maximum likelihood value of the aggregation factor (k) of the expected negative binomial distribution for each of the three species was estimated with a GLIM macro (Royal Statistical Society, London).

Regression analysis of mistletoe presence and the numbers of mistletoes per host was carried out using the statistical package GLIM version 3.77, using models with binomial and Poisson errors respectively. Deviance and degrees of freedom were calculated successively for the full data set, then the maximal model including all factors (all explanatory variables and their interactions) and then progressive models which excluded each factor in turn, to derive final models including only significant factors (P < 0.05), as described in Chapter Three. The models of numbers of mistletoes per tree using Poisson errors were scaled so that the residual deviance approximately equalled the residual degrees of freedom.

The categorical factors included in the regression analysis were host species and location. Two of the four host species of E. dregei occurred in the plots: Brachystegia spiciformis and Julbernardia globiflora and these were distinguished in the analyses.

73 Chapter Four

Of the total 35 recorded host species of E. virescens (see Chapter Two), 29 occurred in the plots. For the initial analyses, all host species of E. virescens with 20 or more recorded individuals, namely Acacia gerrardii (63), Cassia abbreviata (36), Combretum molle (54), Erythrina abyssinica (23), Euclea divinorum (20), Grewia flavescens (27), Grewia monticola (77), Lannea discolor (206), Senna singueana (44) and Ziziphus mucronata (35) were treated separately while the remaining 19 host species (103 individuals) were lumped.

Each 50 X 50 m plot was initially treated as a separate location. The locations were nested for analysis into large, medium and small woodland clumps, as described above (Section 4.2.1), and labelled Large 1 to 5, Medium 1 to 8 and Small 1 to 15. All isolated trees were lumped as one further location. The three one hectare plots in large woodland clumps each contained four 50 x 50 m locations in terms of the analyses, although they were adjacent. These were labelled Large 2.1 to 2.4, 3.1 to 3.4 and 4.1 to 4.4. For E. dregei all of these were entered into the analysis, but for E. virescens, which had fewer hosts in large woodland clumps, only the randomly chosen 50 x 50 m plots were used, giving a total of five locations in large woodland clumps (Large 1 to 5). Excluding plots where hosts of the respective Erianthemum species did not occur, there were 26 initial locations each for E. dregei (fourteen large, seven medium, four small, one isolated) and E. virescens (five large, eight medium, twelve small, one isolated). For A. subulatus the analysis was simpler, with only one host species and two locations, either larger woodland clumps (corresponding to large or medium woodland clumps) or isolated trees.

Spatial aggregation of infected hosts relative to uninfected hosts and hosts relative to all trees was assessed using a specifically designed programme written in the language C. The data were taken from three plots of 100 x 100 m in large woodland clumps for E. dregei (Large 2, 3 and 4) from all plots in small woodland clumps with more than 10 hosts for E. virescens, and from the whole data set excluding the six most isolated trees for A. subulatus. For each species and plot in turn, the programme randomly shuffled the labels infected and uninfected among the full set of actual coordinates of trees in a Monte Carlo process of 500 simulations. For each simulation the number of infected hosts within radii of 5, 10, 15 and 20 m of every infected host

74 Chapter Four were counted and summed. The ratio of the observed (actual) sum of infected hosts around infected hosts to the median value of the 500 runs was taken as the aggregation index A, where for random distributions A = 1, for aggregated distributions A > 1 and for regular distributions A < 1. The 95 % upper and lower confidence limits of A were calculated from the 500 runs. Any effect of reduced sampling area at plot edges was nullified because it applied equally to the observation and all simulations. The programme was used in an identical manner to test the spatial aggregation of hosts relative to all trees.

Two-dimensional spatial aggregation of mistletoes within individual trees was tested for all trees supporting either two or three individuals of E. dregei or E. virescens. For each tree the total circular area of the canopy was divided into eighteen sectors of 20° each and the sector in which each mistletoe occurred was recorded. Expected distributions of the distances between the two mistletoes for hosts with two individuals, and the furthest distance between two mistletoes for hosts with three individuals, were calculated by full enumeration of the ways in which two or three mistletoes can be allocated among 18 sectors with 0-9 sectors of separation. The expected distributions were compared to the observed distributions using a G-test for goodness of fit. There were insufficient numbers of hosts with more than three mistletoes and of hosts of A. subulatus to test spatial aggregation.

4.3. Results

4.3.1. Distribution of host trees

The hosts of both E. dregei and E. virescens were highly aggregated among the 21 randomly selected plots (variance:mean ratio = 53.7 and 9.94 respectively). Including the additional seven randomly chosen plots on termite mounds showed how the distributions of the hosts of the two species were related to habitat type. Hosts of E. dregei were present in all five plots in miombo woodland, in two out of three plots in terminalia woodland but in only one out of eleven plots on termite mounds. Hosts of E. virescens occurred in plots of all habitat types but at higher densities in plots on

75 Chapter Four termite mounds (Table 4.1). The differences in density of hosts of E. virescens among the three grouped habitat types miombo + terminalia woodland, rocky outcrops and termite mounds were significant (F = 4.08, df = 2 and 25, p < 0.05), with termite mounds higher than woodland (t = 4.46, df = 23, p < 0.001) or rocky outcrops (t = 2.11, df = 14, p < 0.05). Note that the differences in host densities among these habitat types would be even more pronounced if expressed per unit area of woodland clump rather than per quarter hectare, because the small clumps (rocky outcrops and termite mounds) did not cover the full extent of the 50 x 50 m plots. Note also that on the same system of measurement, isolated hosts of both species occurred at densities of 1-3 hosts per quarter hectare.

Since large woodland clumps were generally miombo or terminalia woodland (Chapter Three) and small clumps were generally on termite mounds, the densities of hosts of the two mistletoes by clump size mirrored the differences among habitat types (Table 4.1). Variance in the density of hosts of E. dregei was high among plots in large woodland clumps. An additional finding was that termite mounds were uncommon in miombo and terminalia woodland. Only one termite mound was located in the total 3.5 ha surveyed in large woodland clumps.

Table 4.1. Mean density of hosts of Erianthemum dregei and Erianthemum virescens per 50 x 50 m plot by habitat type and by clump size.

Plot category Erianthemum dregei Erianthemum virescens n

Mean s.e. Mean s.e. Miombo 34^ 13.1 7jW 1.84 10 Terminalia 333 1.67 3.67 &882 3 Rocky outcrops 12.5 7.15 11.3 4^7 4 Termite mounds 0.273 &273 25.8 3.76 11 Large clump 56.4 23.1 9.80 2.31 5 Medium clump 12^ 3.60 &88 2j2 8 Small clump 1.80 19.3 3.97 15

Of the four hosts of E. dregei, only two, Julbernardia globiflora and Brachystegia spiciformis, were encountered in the 50 x 50 m plots. J. globiflora was more common than B. spiciformis, comprising 78.1 % of all recorded hosts of E. dregei (n = 429) in the 21 randomly selected plots, and 31.7 % of all trees (n = 1055) in these plots, making it the most common species of tree at the study site. However, the distribution

76 Chapter Four of the two host species was not random among the plots and nor were the size distributions. For example, comparing the three plots in large woodland clumps that were expanded to one hectare, Large 4 entirely lacked B. spiciformis, while Large 3 had more B. spiciformis than J. globiflora. The frequency distributions of host girths were skewed towards smaller trees in Large 2 and larger trees in Large 3, while Large 4 was intermediate (see Figure 4.1 in the following section, Section 4.3.2). Most of the more common hosts of E. virescens were found in both miombo woodland and on termite mounds, with the exception of Acacia gerrardii, Grewiaflavescens and G. monticola, which were confined to termite mounds.

4.3.2. Distribution of mistletoes among hosts

Overall 15 % of hosts of E. dregei (n = 993) and 25 % of hosts of E. virescens (n = 688) were infected. The rarest species, A. subulatus, infected a higher proportion of its hosts, 54 % (n = 82). Individual mistletoes were not randomly distributed among their hosts. The variance to mean ratios of number of mistletoes per host were 3.98, 8.86 and 5.39 for & dregei, E. virescens and A. subulatus respectively. The distributions of E. virescens and A. subulatus conformed to negative binomial distributions and had low values of the aggregation factor k, which correspond to highly aggregated distributions. The distribution of E. dregei among the full set of hosts did not fit the negative binomial, but if hosts in small and medium clumps were excluded, the distribution of mistletoes among hosts conformed to the negative binomial distribution (Table 4.2). The maximum numbers of mistletoes on one host were 13 for E. dregei and 47 for E. virescens. In the separate sample used for A. subulatus, the maximum recorded number of mistletoes on one host was 16, but in one of the plots sampled for E. dregei and E. virescens (Medium 2) an individual Pterocarpus angolensis tree supported 51 individuals of A. subulatus.

77 Chapter Four

Table 4.2. G-test of goodness of fit to the negative binomial of the distributions of Erianthemum dregei (all hosts and hosts in large woodland clumps combined with isolated hosts), Erianthemum virescens and Agelanthus subulatus among hosts, showing mean number of mistletoes per host, variance around the mean, aggregation factor (k) and number of hosts in sample (n).

Species Mean Variance G df P k n

E. dregei 0339 1.35 9.93 3 <0.05 - 993 E. dregei 0324 L22 5.51 2 >0.05 0.139 867 (large + isolated) E. virescens 0.822 7.28 247 4 >0.05 0.156 688 A. subulatus 2.02 10.9 242 1 >0.05 0460 82

4.3.3. Effects of host size, host species and location

Regression analysis for each of the three species showed that the non-random distributions of mistletoes among hosts were associated with host characteristics, with interesting differences among the three species. Here I report the regression analysis for presence/absence of mistletoes on hosts and the number of mistletoes per host, in detail for each species in turn. Although the distribution of mistletoes among hosts generally fitted the negative binomial distribution, scaled Poisson models provided a better fit to the data than negative binomial models in the analyses of numbers of mistletoes per host.

Erianthemum dregei

In the initial analysis for E. dregei, the 13 plots in medium and small woodland clumps showed no consistency, in that location was a significant factor but standard errors of the differences among the plots were too large to separate the plots into groups, and for this reason they were excluded from the overall analysis. They included 126 hosts, only 13 % of the total measured, and were characterised by small numbers of hosts and a binomial distribution between infected and uninfected plots (Table 4.3).

78 Chapter Four

Table 4.3. Numbers of hosts and infected hosts of Erianthemum dregei in plots in medium and small woodland clumps.

Plot Brachystegia spiciformis Julbernardia globiflora

Number Number infected Number Number infected Medium 1 4 2 7 3 Medium 2 5 4 8 0 Medium 3 8 2 1 0 Medium 4 1 0 20 0 Medium 5 10 0 23 0 Medium 6 8 2 2 0 Medium 8 3 0 2 0 Small 3 10 2 0 0 Small 4 3 1 4 1 Small 5 0 0 7 2

Among the 772 hosts in large woodland clumps and the 95 isolated hosts, likelihood of host occupancy increased with host basal girth (Table 4.4; Table 4.5). One host species, B. spiciformis, was more likely to be infected than the other, J. globiflora. There was no interaction between species and girth, showing that the likelihood of occupancy increased at the same rate with girth for both species.

Location was also a significant factor (Table 4.4). Isolated hosts were less frequently infected than hosts in large woodland clumps (Table 4.5). There was a high degree of conformity among the fourteen 50 x 50 m plots in large woodland clumps. Only one plot, Large 4.4 (n = 56 hosts), differed significantly from the other 13 plots. All hosts in this plot were J. globiflora. Their frequency of infection was equal to the overall infection frequency of B. spiciformis (Table 4.5). However, all hosts in the other three plots included in Large 4 were also J. globiflora and these were not infected at this higher frequency. Among all locations there was no interaction between location and species or location and girth (Table 4.4). The lack of difference by location was surprising considering the spatial contrasts in size and species distributions (Figure 4.1).

79 Chapter Four

0^5 1 06^ & & as- I 8 a4 &(U5 4=! ^ 014 13 ().05 4 R H II — I"" I <20 30 50 70 90 no >120 <20 30 50 70 90 110 :>120 girth class (cm) girth class (cm)

a. Large 2 b. Large 3

a2Si ^ &2 4 R !

5? 0.15 &CU5

0.1 cd 13 0.05 4 n 1 _a. <20 30 50 70 90 no <30 30 50 70 90 110 =>120 girth class (cm) girth class (cm)

c. Large 4 d. Isolated hosts

Figure 4.1. Variation in occupancy by Erianthemum dregei with host basal girth and host species in large woodland clumps and among isolated hosts, showing unoccupied Julbernardia globiflora (clear), unoccupied Brachystegia spiciformis (dots), occupied J. globiflora (forward slashes) and occupied B. spiciformis (back slashes).

Table 4.4. Logistic regression analysis for presence or absence of Erianthemum dregei on host trees, using the following factors: host species (SP), location (L) and natural log of basal girth of host (In G).

Factor Deviance df P r-

SP 2&16 1 <0.001 0.027 L 37.12 2 <0.001 0.049 InG 4128 1 <0.001 0.055 SP.ln G &26 1 NS L.ln G 0.66 2 NS SP.L 0 56 2 NS

Model 114.67 4 0.153

Residual 635.26 862

Total 749.93 866

80 Chapter Four

Table 4.5. Regression coefficients of significant factors associated with presence or absence of Erianthemum dregei on host trees. Host species SPl is Brachystegia spiciformis and SP2 is Julbernardia globiflora. Location LI denotes all hosts in large woodland clumps excluding those in Large 4.4, L2 denotes hosts in Large 4.4 and L3 denotes isolated hosts. The model has the form In (P/l-P) = Constant + In G where P is likelihood of occupancy and G is basal girth of the host in cm. The given constant is for SPl at LI and those for SP2, L2 and L3 and their associated standard errors are differences from SPl at LI rather than absolute values.

Factor Regression coefficient s.e.

Constant -6.60 1.06 SP2 -1.16 0.252 L2 1.07 0328 L3 -1.85 0.441 InG 1.43 0.236

In the regression analysis for numbers of individuals of E. dregei per host, the explanatory variables explained a higher proportion of the variance than explained in the presence/absence analysis. Number of mistletoes per host increased with host basal girth and was higher for B. spiciformis than for J. globiflora, but without differences in the rate of increase with girth between the two host species (Table 4.6; Table 4.7). The slope of the rate of increase in numbers of mistletoes with the natural log of girth did not significantly different from a value of one (t = 1.07, p > 0.05, Student's t-test). Once again there was no interaction between species and girth. However, by contrast to the presence/absence analysis, isolated hosts did not differ significantly from hosts in large woodland clumps (Table 4.7).

Since this analysis included all hosts, both infected and uninfected, it was expected that infected isolated hosts had higher numbers of mistletoes per tree than infected hosts in large woodland clumps. However, analysis of occupied hosts only showed no significant differences by location in a model including species and girth (%^ = 9.76, df = 12, p > 0.05, n = 133). The statistical discrepancy was probably due to the small number of infected isolated hosts of E. dregei. The mean number of E. dregei per occupied host was 2.11 (s.e. = 0.187, n = 126) in large woodland clumps and 1.86 (s.e. = 0.340, n = 7) for isolated hosts.

The numbers of mistletoes per host, where both infected and uninfected hosts were included, were consistent for most of the plots in large woodland clumps, but differed in Large 2.3, 2.4 (n = 208 hosts) and 4.1 (n = 55 hosts). Large 2.3 and Large 2.4,

81 Chapter Four which were contiguous, also showed a steeper slope of increase in number of mistletoes with girth, while Large 4.1 had a slope that was not significantly different from zero (Table 4.7). The interaction between girth and location meant that girth could not be removed from the model independently of location and therefore that the deviance explained by girth and by the interaction between girth and location could not be partitioned (Table 4.6).

Table 4.6. Regression analysis with Poisson errors for number of individuals of Erianthemum dregei on host trees, using the following factors; host species (SP), location (L) and natural log of basal girth of host (In G).

Factor Deviance df P r^

SP 83.47 1 <0.001 0X#8 L 30j^ 2 <0.001 0.025 SP.ln G 0.04 1 NS L.lnG 162.47 3 <0.001 0.132 SP.L 2 NS

Model 449.57 6 0.366

Residual 77&43 860

Total 1228.00 866

Table 4.7. Regression coefficients of significant factors associated with numbers of Erianthemum dregei on host trees. Host species SPl is Brachystegia spiciformis and SP2 is Julbernardia globiflora. Location LI denotes all isolated hosts and all hosts in woodland clumps excluding those in Large 2.3, 2.4 and 4.1, L2 denotes hosts in Large 2.3 and 2.4 and L3 denotes hosts in Large 4.1. The model has the form In N = Constant + In G where N is number of mistletoes and G is basal girth of the host in cm. The given constant is for SPl at LI and those for SP2, L2 and L3 and their associated standard errors are differences from SPl at LI rather than absolute values. Separate coefficients of In G are given for LI, L2 and L3.

Factor Regression coefficient s.e.

Constant -5.24 0.672 SP2 -1.35 0.153 L2 -7.60 1.69 L3 7jG 3J3 Ll.lnG 1.15 0.140 L2.1n G 3.00 0.350 L3.1n G -0.672 0.945

82 Chapter Four

Erianthemum virescens

For E. virescens, all of the initial 21 randomly selected plots in large, medium and small woodland clumps were included in the analysis, along with the seven additional randomly selected plots on termite mounds. The nine extra plots adjacent to the random plots in large woodland clumps (Large 2, 3 and 4) were not included.

Likelihood of occupancy increased with host basal girth (Table 4.8; Table 4.9). The initial analysis included 11 categories of host species, referring to ten species recording 20 or more individuals and one group for all other species. Most host species were identical in terms of frequency of infection. Only Acacia gerrardii and Grewia monticola differed, exhibiting a steeper increase in likelihood of infection with girth than all other species, including the congeneric Grewia flavescens (Table 4.9).

Isolated hosts did not differ in frequency of infection from hosts in large or medium woodland clumps (Table 4.9), and there were no differences among plots for large or medium woodland clumps. Hosts in small woodland clumps, almost all on termite mounds (Section 4.3.1) were more likely to be occupied by E. virescens than hosts in other locations. There was no interaction between location and species and location and girth. Eleven out of twelve of the plots containing hosts of E. virescens and covering small woodland clumps, or 285 out of 290 hosts, were on termite mounds. Hosts in Small 2 and Small 13 (both termite mounds) showed a higher frequency of infection than hosts in other plots in small woodland clumps (Table 4.9). Host species and location were confounded as 23 out of 24 hosts in Small 2 and 24 out of 27 hosts in Small 13 were A. gerrardii and 75 % of all recorded A. gerrardii were in these two plots. The differences among the various locations are illustrated in Figure 4.2.

To test the possibility that the difference in likelihood of occupancy between small woodland clumps and isolated host was an effect of habitat type, the logistic regression analysis was repeated using only hosts on termite mounds. In a model containing host species, girth and location at three factor levels (small clumps excluding Small 2+13, Small 2+13, isolated hosts), there was a significant lower

83 Chapter Four

chance of occupancy by E. virescens of isolated hosts on termite mounds compared to hosts in small woodland clumps on termite mounds (t = 2.05, df = 268, p < 0.05, Student's t-test).

0^1 0.2

^015 ^CU5 4 a- ^ (U cS 0.1 I I Q) ^ CW5 4 XL XL n <20 30 50 70 90 no >LW <20 30 50 70 90 HO >120 girth class (cm) girth class (cm)

a. Large and medium clumps b. Small clumps excluding 2 + 13

0.3 ^a25 o 0.15 ^ a2 ^ CU5 ^ 01 3 am- 0 m M <20 30 50 70 90 110 :>120 <20 30 50 70 90 110 >120 girth class (cm) gii1h class (cm)

c. Small 2 and Small 13 d. Isolated hosts

Figure 4.2. Variation in occupancy by Erianthemum virescens with host basal girth and host species in woodland clumps and among isolated hosts, showing unoccupied hosts of most species (clear), unoccupied hosts of Acacia gerrardii and Grewia monticola (dots), occupied hosts of most species (forward slashes) and occupied hosts of^. gerrardii and G. monticola (back slashes').

84 Chapter Four

Table 4.8. Logistic regression analysis for presence or absence of Erianthemum virescens on host trees, using the following factors: host species (SP), location (L) and natural log of basal girth of host (In G).

Factor Deviance df P r'

SP 2&46 1 <0.001 0.031 L 38.61 2 <0.001 0X#8 SP.ln G 53.66 1 <0.001 0.080 L.lnG 2.61 2 NS SP.L 0.07 2 NS

Model 8205 5 0J^6

Residual 587.97 539

Total 670.02 544

Table 4.9. Regression coefficients of significant factors associated with presence or absence of Erianthemum virescens on host trees. Host species SPl denotes all hosts species other than SP2 and SP2 denotes Acacia gerrardii and Grewia monticola. Location LI denotes all isolated hosts and hosts in large and medium woodland clumps, L2 denotes all hosts in small woodland clumps other than Small 2 and Small 13 and L3 denotes hosts in Small 2 and Small 13. The model has the form In (P/l-P) - Constant + In G where P is likelihood of occupancy and G is basal girth of the host in cm. The given constant is for SPl at LI and those for SP2, L2 and L3 and their associated standard errors are differences from SPl at LI rather than absolute values. Separate coefficients of In G are given for SPl and SP2.

Factor Regression coefficient s.e.

Constant -3.86 0.782 SP2 -8.60 2.10 L2 0j#2 0.232 L3 1.77 0U#8 SPl.lnG &587 0.182 SP2.1n G 2jW 0.508

As was the case for E. dregei, a greater proportion of the total deviance was explained in the regression analysis of number of individuals of E. virescens per host than in the presence/absence analysis (Table 4.10). Number of mistletoes per host increased with host basal girth, at a greater rate for A. gerrardii and G. monticola than for other host species (Table 4.11). Two other host species, Erythrina abyssinica and Grewia flavescens, had higher mean numbers of mistletoes per individual tree, but did not exhibit any increase in number with increasing basal girth. The slope for all species excluding A. gerrardii, G. monticola, E. abyssinica and G. flavescens did not differ significantly from a value of one (t = 0.08, p > 0.05, Student's t-test).

85 Chapter Four

Table 4.10. Regression analysis with Poisson errors (scale factor = 2.2) for number of individuals of Erianthemum virescens on host trees, using the following factors: host species (SP), location (L) and natural log of basal girth of host (In G).

Factor Deviance df P r'

SP 47^8 3 <0.001 0.057 L 80.65 2 <0.001 0.096 SP.ln G 125.37 3 <0.001 0.150 L.lnG 0.99 2 NS SP.L 4.11 6 NS

Model 290.27 8 0.348

Residual 544.03 536

Total 834.30 544

Table 4.11. Regression coefficients of significant factors associated with numbers of Erianthemum virescens on host trees. Host species SPl denotes all hosts species other than SP2 to SP4, SP2 denotes Acacia gerrardii and Grewia monticola, SP3 denotes Erythrina abyssinica and SP4 denotes Grewia flavescens. Location LI denotes all isolated hosts and hosts in large and medium woodland clumps and L2 denotes all hosts in small woodland clumps. The model has the form In N = Constant + In G where N is number of mistletoes and G is basal girth of the host in cm. The given constant is for SPl at LI and those for SP2, SP3, SP4 and L2 and their associated standard errors are differences from SPl at LI rather than absolute values. Separate coefficients of In G are given for SPl, SP2, SP3 and SP4.

Factor Regression coefficient s.e.

Constant -5.37 &584 SP2 -3.51 1.11 SP3 825 1.56 SP4 4.19 1.32 L2 1.37 0.157 SPl.In G 1.01 CU28 SP2.1n G 1.93 0.220 SP3.1n G -0.278 0.279 SP4.1n G 0.171 0.343

Hosts of E. virescens in small woodland clumps, on termite mounds, had a greater mean number of mistletoes than isolated hosts or hosts in large or medium woodland clumps. Hosts in Small 2 and Small 13 (A. gerrardii), which were more likely to be infected than hosts in other small woodland clumps (Table 4.9), did not differ in mean number of mistletoes (Table 4.11), suggesting that they supported smaller numbers of mistletoes per infected host. Further analysis of infected hosts of E. virescens only showed that this was not the case. Infected individuals of A. gerrardii supported similar numbers of E. virescens to all other host species excluding E. abyssinica, G. flavescens and G. monticola in a model including girth and location (t = 0.61,

86 Chapter Four p > 0.05, n = 166, Student's t-test). The mean number of E. virescens per infected individual of A. gerrardii was 2.90 (s.e. = 0.502, n = 20) compared to 2.96 (s.e. = 0.352, n = 94) for the group of other hosts.

Agelanthus subulatus

Hosts of the third mistletoe species, A. subulatus, also showed an increase in likelihood of occupancy with basal girth (Figure 4.3). There was no difference in frequency of infection between more and less isolated hosts (Table 4.12; Table 4.13). Mean number of mistletoes also increased with girth, but unlike the two Erianthemum species, regression analysis of number of mistletoes per host did not explain a greater proportion of the deviance than explained in the presence/absence analysis (Table 4.14; Table 4.15). the slope of number of mistletoes versus the natural log of girth did not differ significantly from a value of one (t = 0.53, p > 0.05, Student's t-test).

Table 4.12. Logistic regression analysis for presence or absence of Agelanthus subulatus on host trees, using the following factors; location (L) and natural log of basal girth of host (In G).

Factor Deviance df P r?

L 1.44 1 NS InG 19.66 1 <0.05 0.174 L.lnG 0.04 1 NS

Model 19.66 1 0.174

Residual 93^8 80

Total 113.24 81

Table 4.13. Regression coefficients of significant factors associated with presence or absence of Agelanthus subulatus on host trees. The model has the form In (P/l-P) = Constant + In G where P is likelihood of occupancy and G is basal girth of the host in cm.

Factor Regression coefficient s.e.

Constant -12.3 3.36 InG 2^0 0.725

87 Chapter Four

Table 4.14. Regression analysis with Poisson errors (scale factor = 3.2) for number of individuals of Agelanthus subulatus on host trees, using the following factors: location (L) and natural log of basal girth of host (In G).

Factor Deviance df P r'

L 332 1 NS InG 14.46 1 <0.001 0.140 L.ln G 3.05 1 NS

Model 14.46 1 0.140

Residual 88.57 80

Total 103.03 81

Table 4.15. Regression coefficients of significant factors associated with numbers of Agelanthus subulatus on host trees. The model has the form In N = Constant + In G where N is number of mistletoes and G is basal girth of the host in cm.

Factor Regression coefficient s.e.

Constant ^^3 1.48 InG 1.16 0.301

0.16

0.14

0.12 I

a 0.1 i I ^ 0.08 I . ipS 0.06 H 0.04 I

0.02 0 -T T ! 11I Ill <20 30 50 70 90 110 130 150 170 190 >200 girth class (cm)

Figure 4.3. Variation in occupancy hy Agelanthus subulatus with host girth, showing unoccupied (clear) and occupied (shaded) Pterocarpus angolensis.

88 Chapter Four

4.3.4. Effects of host density

The 50 X 50 m plots in large, medium and small woodland clumps included a wide range of densities of hosts of E. dregei and E. virescens. The lack of variation among plots in the regression analysis for presence/absence of mistletoes (Table 4.4; Table 4.8) suggested that host density had little or no effect on occupancy, which was confirmed by further analysis.

Erianthemum dregei

For E. dregei, when only the randomly selected plots were included, the density of occupied hosts increased linearly with the overall density of hosts, meaning that the proportion of hosts that were occupied was constant over all densities (Table 4.16; Figure 4.4). The fitted intercept was not significantly different from zero (F = 2.18, df = 1 and 19, p > 0.05). Inclusion of the additional contiguous plots in Large 2, 3 and 4 produced a significantly decelerating curve (Table 4.17), but the two plots with highest density were adjacent in Large 2 (Figure 4.5). Once again the fitted intercept was not significantly different from zero (F = 0.76, df = 1 and 28, p > 0.05).

Neither the linear nor the polynomial model was satisfactorily robust, because the variance increased with the mean, but they provided a better spread of residuals than alternative maximum likelihood models. Although a Michaelis-Menten model would give an asymptotic curve more appropriate to the data than the quadratic curve that ultimately decelerates (Figure 4.5), the large number of zero values in the data meant that the quadratic model was superior overall.

89 Chapter Four

Table 4.16. Regression analysis for density of occupied hosts of Erianthemum dregei versus host density (D) and the square of host density (D^) in 21 randomly located 50 x 50 m plots.

Factor Deviance df F P r'

D 183.06 1 11,56 <0.001 0.578 D^ 1.44 1 0.20 NS

Residual 133.51 19

Total 316.57 20

20 40 60 80 100 120 140 160 density of hosts per plot

Figure 4.4. Density of hosts infected by Erianthemum dregei as a function of total host density in 21 randomly located 50 x 50 m plots, showing the fitted line y = 0.1084x.

Table 4.17. Regression analysis for density of occupied hosts of Erianthemum dregei versus host density (D) and the square of host density (D^) in 30 random and contiguous 50 x 50 m plots.

Factor Deviance df F P r?

D 435.39 1 35.11 <0.001 0.556 D^ 9&55 1 9^2 <0.001 0.115

Residual 256.76 27

Total 782.70 29

90 Chapter Four

20 40 60 80 100 120 140 160 180 200 density of hosts per plot

Figure 4.5. Density of hosts infected by Erianthemum dregei as a function of total host density in 30 random and contiguous 50 x 50 m plots, showing the fitted line y = 0.235 x - 0.000938 x^. Contiguous plots are marked by shaded squares (Large 2), open squares (Large 3) and triangles (Large 4).

Erianthemum virescens

For E. virescens, the proportion of hosts infected did not change with host density in a sample including all randomly chosen plots and further randomly chosen plots in small woodland clumps, and there was a close fit between density of hosts and density of occupied hosts over all densities (Table 4.18; Figure 4.6). Adding the factor habitat type, the slopes of the three grouped habitat types were not different (Table 4.18), but the intercepts for miombo and terminalia woodland differed from termite mounds (difference = 3.67, s.e. = 1.19, n = 25, t = 3.08, p < 0.01, Student's t-test) although neither differed from the intermediate value for rocky outcrops on dambos. The intercept for the single fitted line for all habitat types did not differ from zero (F = 2.24, df = 1 and 26, p > 0.05), but among the separate fitted lines for habitat type, that for termite mounds was significantly higher than zero (t = 1.85, df = 10, p < 0.05) and that for miombo and terminalia woodland significantly lower (t = 2.91, df = 11, p < 0.01).

91 Chapter Four

The habitat type miombo and terminalia woodland corresponded closely to large and medium clumps while termite mounds corresponded closely to small woodland clumps. Using clump size rather than habitat type in the analysis gave a similar result to that using habitat types with indistinguishable slopes, but a difference in intercepts between miombo and terminalia woodland and termite mounds (difference = 3.34, s.e. = 1.19, n = 17, t = 3.12, p < 0.01, Student's t-test), though no differences of either large or small from medium woodland clumps.

Table 4.18. Regression analysis for density of occupied hosts of Erianthemum virescens in 28 randomly chosen 50 x 50 m plots, using the following factors: host density (D), the square of host density (D^) and habitat type (H).

Factor Deviance df F P r'

D ##30 1 124.98 <0.001 0.597 4.45 1 0.51 NS H 41.16 2 10.39 <0.001 0.050 H.D 5^5 2 1.36 NS

Residual 293.40 24

Total 27

20 30 40 density of hosts per plot

Figure 4.6, Density of hosts infected by Erianthemum virescens as a function of total host density in 28 randomly located 50 x 50 m plots, showing plots in miombo and terminalia woodland (squares), termite mounds (triangles) and rocky outcrops (diamonds), showing the fitted line y = 0.358 x.

92 Chapter Four

4.3.5. Spatial aggregation among infected hosts

Erianthemum dregei

The Monte Carlo simulation test showed that hosts of E. dregei in the 100 x 100 m plots were not aggregated compared to all trees, except at the smallest scale of 5 m from focal trees in one plot. Large 2 (Table 4.19). This result was obtained despite the wide variation in the structure of the woody vegetation in these three plots (Section 4.3.1; Figure 4.1), for example the much higher density of trees in Large 2. Maps of infected and uninfected hosts of E. dregei illustrated the differences in host density among the three plots and also suggested that infected hosts were not spatially aggregated (Figure 4.7). The simulation test confirmed this result for scales of 5, 10, 15 and 20 m from focal trees, because in no case did the aggregation factor A exceed unity for occupied hosts compared to all hosts (Table 4.19).

However, in Large 2, occupied hosts had a significantly regular distribution compared to all hosts at radii of 5 m, with A < 1. This was the same scale at which hosts were aggregated, in a plot where trees tended to be small, which suggested that the regularity of occupied hosts could be associated with regular spacing of larger hosts, which were more likely to be occupied. Using the derived regression equations (Table 4.5) to calculate the girths of the two hosts B. spiciformis and J. globiflora above which there was a greater than mean 15 % likelihood of occupancy, the simulation test showed that these larger hosts were significantly regular compared to all hosts, but within the group of larger hosts, occupied hosts were distributed randomly (Table 4.20).

93 Chapter Four

100 o r- —o-o -0 • • • ' <>• • > $ • o o ^ • 90 • A • > o o • Oo o o • • o o o > > o 80 o < •o o o o • A • o 70 • o ^ < • o > o o <> > o 60 • o <> o o ^ •< o o < o < o < 0 o O <0 o ^ 00 j. o 40 A ^ o o o % ^ o o 6 • • o oo % ^ • o :? o x> o • o ^ f /\ 30 L o<> o o o o < 0 CO A ^ o o • o ^ o 1 ' • O :: « o w O A 20 • o ^ 0 • > h 0 •o

/\ 10 o '

Figure 4.7.a. Large 2

94 Chapter Four

100 r o o o 4 90 o • •

80 • Y > o A 70 • • • •

< • 60 • o • < • 50 • o 40 • • 30 • x o • O

20 •

< > • • • • 10 •

• 0 0 10 20 30 40 50 60 70 80 90 100

Figure 4.7.b. Large 3

95 Chapter Four

100 • ) i o o • o o o • 0 <• o $ oO 90 - o ^ 0)0 • > o c • o • o 4 A 4> 80 o • A • • < • o < > <> o < > > 70 o • o ^ > • o • • o > • o o o 60 o ' o < o 1 < > o • • ^ < o < • 00 ^ 50 T O ' o • o ^ < o • o O c o o 'o o > 40 - A o • o r ^ o 4 o ' • ^ o< < A o 30 O V o o o o o 20

~~Figure 4.7. Maps of occupied (shaded) and vacant hosts of Erianthemum dregei in three 100 x 100 m plots. Axes indicate distance in metres.~~

~~96 Chapter Four~~

Table 4.19. Aggregation factors (A) for hosts of Erianthemum dregei compared to all trees and of occupied hosts compared to all hosts in three 100 x 100 m plots in large woodland clumps at radii of 5, 10, 15 and 20 m from focal trees. The lower 95 % confidence interval is given for values of A > 1 and the upper 95 % confidence interval is given for values of A < 1.

~~Large 2 Large 3 Large 4~~

A 95% P A 95 % P A 95 % P C. L C. L CI. Hosts versus all trees 5 m 1.14 0.07 <0.01 0^7 0.57 NS 048 0.06 NS 10 m 1.00 0.04 NS 1.11 0.31 NS 1.02 0.06 NS 15 m 049 0.05 NS 1.06 0^4 NS 1.03 0.05 NS 20 m 046 0.04 NS 046 0.27 NS 1.01 0.05 NS Occupied hosts versus all hosts 5 m 0J8 0J3 <0.01 1J3 0^7 NS 0^6 1.14 NS 10 m 1J2 039 NS 1.25 0.50 NS 1^2 0.47 NS 15 m 042 oja NS 0^3 0^0 NS 048 033 NS 20 m 1.13 0.31 NS 1.10 032 NS 048 0^8 NS Counts n (trees) 614 303 328 n (hosts) 417 49 236 n (occ. 50 24 43 hosts)

Table 4.20. Aggregation factors (A) for larger hosts of Erianthemum dregei, those large enough to have more than mean 15 % chance of infection (Brachystegia spiciformis > 32 cm and Julbernardia globiflora > 67 cm basal girth), compared to all hosts and of occupied larger hosts compared to all larger hosts in Large 2 at radii of 5, 10, 15 and 20 m from focal trees. The lower 95 % confidence interval is given for values of A > 1 and the upper 95 % confidence interval is given for values of A < 1.

~~A 95%Cj. P~~

Larger hosts versus all hosts 5 m 0^8 0^8 <0.05 10 m 0.71 0.19 <0.01 15 m 0.71 0.17 <0.01 20 m 0.75 0.15 <0.01 Occupied larger hosts versus all large hosts 5 m 1.00 0.50 NS 10 m 1.00 0.36 NS 15 m 0^9 0.32 NS 20 m 1.12 0.35 NS Counts n (hosts) 417 n (larger hosts) 82 n (occ. larger hosts) 26

~~97 Chapter Four~~

~~Erianthemum virescens~~

Maps of infected and uninfected hosts of E. virescens in small woodland clumps did not indicate spatial aggregation of infected hosts in clumps of varying size and host density (Figure 4.8). In seven out of nine cases there was no evidence of spatial aggregation or regularity of hosts compared to all trees or of occupied hosts compared to all hosts (Table 4.21). The two exceptions were Small 12, where occupied hosts had a significantly regular distribution compared to all hosts at radii of 15 m, and Small 13, where the 27 hosts were aggregated compared to all 31 trees at radii of 5, 10 and 15 m, but occupied hosts were randomly distributed among all hosts. Small 2 comprised host species only. In large woodland clumps, the rate of infection of hosts was very low, as seen for example in Large 4 (Figure 4.9).

~~35 0^ o o • 40 30~~

~~o 25~~

~~o 15 • o 0 o 10 CO o • o~~

~~0 10 15 20 25 30 35 40 0 5~~

~~Figure 4,8.a. Small 12~~

~~98 Chapter Four~~

~~< > 35~~

~~30 •~~

~~• 20 o~~

~~15 •~~

~~• o • 10 o • o o~~

•

~~10 15 20 25 30 35 b. Small 13~~

~~25 » o .r~~

~~20 • o o~~

~~< 15 • 0~~

~~o (,o <>• o •~~

~~0 0 5 10 15 20 25 c. Small 14~~

~~Figure 4.8. Maps of occupied (shaded) and vacant hosts of Erianthemum virescens in three small woodland clumps on termite mounds. Axes indicate distance in metres.~~

~~99 Chapter Four~~

~~100 o O <>~~

~~80 o o o~~

~~70 •~~

~~60 9 < •~~

~~> • A 50 o > o •~~

~~40 o o o 30 o o o > o 20 O~~

~~< o o 10 o~~

~~> o~~

~~0 10 20 30 40 50 60 70 80 90 100~~

~~Figure 4.9. Map of occupied (shaded) and vacant hosts of Erianthemum virescens in a 100 x 100 m plot (Large 4). Axes indicate distance in metres.~~

~~100 Chapter Four~~

Table 4.21. Aggregation factors (A) for hosts of Erianthemum virescens compared to all trees and of occupied hosts compared to all hosts in nine 50 x 50 m plots covering small woodland clumps, at radii of 5, 10, 15 and 20 m from focal trees. The lower 95 % confidence interval is given for values of A > 1 and the upper 95 % confidence interval is given for values of A < 1. Dashes mark insufficient numbers of trees for calculations.

~~Small 2 Small 6 Small 7~~

A 95 % P A 95% P A 95 % P C. I. C.I. C. I. Hosts versus all trees 5 m 1.00 0.00 NS 0.97 0.20 NS 048 0.17 NS 10 m 1.00 0.00 NS 049 CU8 NS 0.90 0.12 NS 15 m .1.00 0.00 NS 1.01 0.12 NS 0.90 0.12 NS 20 m 1.00 0.00 NS 1.01 0^8 NS 049 0.01 NS Occupied hosts versus all hosts 5 m 0^3 0.60 NS 0^6 2.14 NS 0^8 NS 10 m 0^9 0.24 NS 0^3 0.44 NS 043 0.15 NS 15 m 048 0.11 NS 0.80 0^9 NS 1.03 0.17 NS 20 m 1.00 0.02 NS 0^6 0.28 NS 1.00 0.02 NS Counts n (trees) 25 60 40 n (hosts) 25 43 21 n (occ. 12 13 11 hosts)

~~Small 9 Small 10 Small 12~~

A 95% P A 95% p A 95 % P C.I. C. I. C. I. Hosts versus all trees 5 m 1.05 0.08 NS 046 0.14 NS 1.33 006 NS 10 m 0.97 0.06 NS 046 0.13 NS 1.03 0.19 NS 15 m 048 0.05 NS 048 0.07 NS 043 0.11 NS 20 m 1.00 0.01 NS 1.01 0.02 NS 046 0^8 NS Occupied hosts versus all hosts

5 m 1.67 0.67 NS ------10 m 1.32 0.34 NS - - - 0.80 0.53 NS 15 m 1.05 0.18 NS 1.00 0.00 NS 0.56 0.44 <0.05 20 m 0.99 0.05 NS 1.00 0.00 NS 042 0.58 NS Counts n (trees) 31 20 44 n (hosts) 29 17 27 n (occ. 13 5 7 hosts)

~~101 Chapter Four~~

~~Table 4.21 continued~~

~~Small 13 Small 14 Small 15~~

A 95 % P A 95% P A 95% P C. I. C. I. C. I. Hosts versus all trees 5 m 0.22 <0.05 1.06 0.12 NS 1.02 0.11 NS 10 m 1.18 0.12 <0.05 1.03 0.08 NS 1.02 0.03 NS 15 m 1.13 0.10 <0.05 1.00 0.03 NS 1.00 0.00 NS 20 m 1.07 0.08 NS 1.00 0.01 NS 1.00 0.00 NS Occupied hosts versus all hosts 5 m 043 0.57 NS 1.03 0.41 NS 1.16 0^8 NS 10 m 0.76 0.54 NS 049 037 NS 1.01 0.04 NS 15 m 0^6 cwo NS 049 0.16 NS 1.00 0.00 NS 20 m 0^6 0^8 NS 1.01 0.02 NS 1.00 0.00 NS Counts n (trees) 31 52 40 n (hosts) 27 46 34 n (occ. 10 16 18 hosts)

~~Agelanthus subulatus~~

Visual examination of the complete map of occupied and unoccupied hosts of A. subulatus over a 1600 x 1600 m area also did not identify spatial aggregation of occupied hosts at any scale although hosts were clearly aggregated with respect to space at larger scales (Figure 4.10). The simulation test showed that infected hosts were not aggregated relative to all hosts at radii of 10, 15 or 20 m (Table 4.22).

Table 4.22. Aggregation factors (A) for occupied hosts of Agelanthus subulatus compared to all hosts in a 1600 X 1600 m area at radii of 10, 15 and 20 m from focal trees. The lower 95 % confidence interval is given.

~~A 95%CJ. P~~

~~10 m 1.44 0.57 NS 15 m 1.16 0.35 NS 20 m 1.12 0.34 NS~~

~~n (hosts) 72 n (occupied hosts) 36~~

~~102 Chapter Four~~

~~8035500 8036000 8036500 8037000 8037500 243500~~

~~• 244000 * ^~~

~~244500 1~~

~~• 245000 o~~

•

~~• 245500~~

~~Figure 4.10. Map of occupied (shaded) and vacant hosts of Agelanthus subulatus in a 1600 x 1600 m area. Axes indicate UTM coordinates (northings and eastings) in metres.~~

~~4.3.6. Spatial aggregation within hosts~~

Data were too sparse to test for within-tree aggregation of A. subulatus. For both E. dregei and E. virescens, there was significant spatial aggregation of mistletoes within canopies of trees supporting either two or three individual mistletoes (Table 4.23; Table 4.24). Mistletoes on hosts supporting larger numbers of individuals also appeared to be aggregated, but there were not enough cases to apply the goodness of fit test. A further observation which was not quantified was that although individual mistletoes were aggregated within the canopy, they were seldom near each other on the same branch.

~~103 Chapter Four~~

Number of Erianthemum dregei Erianthemum virescens sectors Observed Expected G Observed Expected G frequency frequency frequency frequency 0 6 1.6 33^8 7 2.2 47.78 1 5 3.1 (P<0.001) 9 4.3 (P<0.001) 2-3 7 6.2 10 8.7 4-6 5 9.3 6 13.0 7-9 5 7.8 7 1&8

Number of Erianthemum dregei Erianthemum virescens sectors Observed Expected G Observed Expected G frequency frequency frequency frequency 0-3 5 1.6 16.69 6 2.6 31.43 4-6 4 4.0 (P<0.001) 11 6.5 (P<0.001) 7-9 5 8.4 6 13.9

~~4.4. Discussion~~

~~4.4.1. Effects of host size and species~~

Mistletoes of all three species, E. dregei, E. virescens and A. subulatus, were highly aggregated within certain hosts. As predicted and as found in many previous studies (see references in Section 4.1), this aggregation was to some extent associated with the quality (species) and size (volume and age) of host trees. The negative constants in the models of mistletoe presence/absence and of numbers of mistletoes (Tables 4.5, 4.7, 4.9, 4.11, 4.13 and 4.15) indicated that there are threshold minimum sizes for infection among hosts. The two hosts of E. dregei differed as predicted by a simple metapopulation model, in that the host Brachystegia spiciformis was more likely to be infected, but the rate of increase of chance of infection with increasing basal girth was the same for both host species. This similarity between the two hosts is perhaps not surprising since Brachystegia and Julbernardia are closely related genera.

~~104 Chapter Four~~

However, for E. virescens, there was also consistency among the many host species, in spite of their diversity. The only two host species which showed a major difference from the others were Acacia gerrardii and Grewia monticola, which were two of the three host species of E. virescens that were found only on termite mounds (Section 4.3.1). The model for A. gerrardii and G. monticola predicted a much more rapid increase in numbers of mistletoes with girth than predicted for other host species (Table 4.11), but within the range of girths of 20 - 80 cm, in which most individuals of these two host species fell (Figure 4.2), the model for A. gerrardii and G. monticola and that for other species predict very similar numbers of mistletoes per host. Two other host species, Grewia flavescens and Erythrina abyssinica, were not more likely to be infected than other hosts, but had higher mean numbers of E. virescens and showed no increase in the number of mistletoes with girth (Table 4.11). G. flavescens was the only climber among the hosts of E. virescens. Basal girth is probably not a good indicator of the canopy volume or age of individuals of this species. For E. abyssinica the results were skewed by one individual supporting 47 mistletoes.

I predicted that the number of mistletoes per tree would increase with canopy volume, or even at a greater rate than canopy volume, allowing for the additional effect of accumulation of mistletoes with host age. According to the rules of scaling, volume increases with length to the power of three. Since most tree canopies in miombo woodland are not spherical but tend to be flattened, a sensible estimate is that canopy volume will increase with basal girth to a power between two and three. Regression analyses of destructive sampling of the two dominant miombo species in Zimbabwe, B. spiciformis and J. globiflora, the chief hosts of E. dregei at this study site, confirms this expectation (P. Frost, unpublished data, n = 51, r^ = 0.75 - 0.96):

~~length of current growth of twigs a biomass of current growth a basal girth~~

If mistletoe abundance scales simply with available branch length or canopy volume, we might therefore expect numbers of mistletoes to increase as basal girth Contrary to expectation, the number of mistletoes per host increased linearly with girth for all three species, giving coefficients of 1.15, 1.01 and 1.16 for In (number of mistletoes) with In (basal girth) in the cases of E. dregei, E. virescens and A. subulatus

~~105 Chapter Four~~

respectively, for most host species at most localities (Tables 4.7, 4.11 and 4.15). These slopes did not differ from a value of one, but did differ from a value of 2.17 for E. dregei (t = 7.29, p < 0.001, Student's t-test), E. virescens (t = 9.06, p < 0.001) and A. subulatus (t = 3.36, p < 0.001). Thus numbers of mistletoes increased with girth rather than with volume, so that larger trees had lower densities of mistletoes per unit canopy volume than smaller trees.

A general increase in mean numbers of mistletoes with host size/age can be ascribed to any of three general and non-exclusive explanations: accumulation, changes in dispersal probability or changes in survival probability within the host. Overton (1994) argued that within-host dispersal is far more likely than between-host dispersal and thus an already occupied host is far more likely to gain further mistletoes than an unoccupied host, which leads to accumulation of mistletoes in particular hosts over time and explains the general volume-occupancy relationship. Alternatively, there may be changes in the host with size/age. Dispersal probability may increase with size because larger hosts provide a larger target for birds; even if birds perch randomly they are more likely to land on a larger tree (Hoffmann et al. 1986; Martinez del Rio et al. 1995). The likelihood of successful establishment or of adult survival may also increase with host size/age, because of physiological or architectural changes in the host (Reid and Lange 1988; Norton et al. 1997a).

This study described a slightly more complex pattern which has not been given attention previously, in that while numbers of mistletoes increased with host size/age, mistletoe density within the canopy decreased. Therefore the possible explanations must account for limitation of growth of mistletoe populations within hosts with host size/age. Following on from Overton's accumulation hypothesis, the most likely explanation is that the rates of dispersal and establishment of mistletoes are constrained by something other than habitat volume, and accrual with time does not keep pace with increases in host volume. Alternative explanations are that dispersal probability per unit volume actually decreases with host size because birds prefer not to perch in larger trees, which is very unlikely, or that probability of establishment or adult survival diminishes with host age/size (older and larger trees are less susceptible to mistletoes). A further possible explanation is that the presence of established

106 Chapter Four mistletoes in a host limits further infection; there is density-dependence not in terms of numbers per unit host volume, but simply in terms of numbers per host. Chapter Five presents establishment experiments that test for the effects of host size and density-dependence in establishment success, testing the last two of these hypotheses, and Chapter Seven discusses the alternatives in light of these experiments.

~~4.4.2. Effects of distance from seed source~~

Mistletoes showed different patterns of spatial aggregation at different scales. Adult mistletoes were seldom found near to each other on the same branch. At a slightly broader scale, they were aggregated within the host canopy (Tables 4.23 and 4.24). However, at a broader scale again, there was no evidence of spatial aggregation of infected hosts (Tables 19, 21 and 22). Finally, at the broadest scale investigated, isolated hosts of E. dregei were less likely to be infected than non-isolated hosts (Table 4.5), but there were no differences for E. virescens or A. subulatus (Tables 4.9 and 4.13). Only one of these scales, aggregation among infected hosts, has been studied previously (Elias 1987; Donohue 1995; Overton 1996), finding similar results to those at this study site, with very little or no spatial aggregation of infected hosts independent of aggregation of hosts with characteristics conducive to infection (see Section 4.1).

One prediction arising from metapopulation theory is that localised dispersal will lead to aggregation of established plants at all scales relevant to the vector of dispersal, unless there is an overriding spatial pattern affecting the rate of within-patch processes, most importantly establishment, but also or alternatively post-establishment mortality. By the same logic, wherever aggregation of mistletoes occurs independently of aggregation of habitat with particular characteristics conducive to infection, it must be due to dispersal. Therefore I anticipate that the aggregation of mistletoes within hosts and the difference between likelihood of infection of isolated and non-isolated hosts is due to dispersal and not to establishment or adult survival. I also predict that differences in either establishment success or adult survival explain the lack of aggregation of mistletoes on branches with fruiting mistletoes (which are expected to have maximum likelihood of receiving dispersed seeds) and the lack of

107 Chapter Four aggregation among infected hosts. These options are considered in the following two chapters. Chapter Five considers establishment and adult survival rates among and within hosts to support or refute the various predictions that patterns among or within hosts are due to within-patch processes. Chapter Six compares dispersal probability of isolated and non-isolated hosts and estimates the degree and scale of localised dispersal.

Since metapopulation theory predicts that the frequency of occupancy will increase with decreasing patch isolation, and hence with increasing patch density, an accelerating slope of the number of hosts infected with number of hosts in a 50 x 50 m plot was expected. No such pattern was found (Tables 4.16 and 4.18; Figures 4.4 and 4.6). If anything, hosts of E. dregei showed signs of decreasing likelihood of infection at high density (Table 4.17; Figure 4.5). A decrease in the frequency of infection with host density suggests limitation by the density of dispersers (frugivorous birds). Perhaps a trade-off between decreasing patch isolation and increasing ratio of hosts to dispersers explains the lack of change in the proportion of hosts that are infected with increasing host density. Another contributory factor is the fact that mean host size decreased with increasing host density, as is illustrated by the size distributions for hosts of E. dregei in the three hectare plots in large woodland clumps (Figure 4.1), creating another trade-off between one factor that promotes occupancy and one that limits occupancy. The only known previous study which considered the relationship between host density and density of infected hosts found higher levels of infection where hosts were less dense, a counter-intuitive finding that was apparently due to the prevalence of larger hosts in less dense stands (Donohue 1995).

It was also surprising that the relationship between density of infected hosts and density of all hosts showed so little variance for E. virescens (Figure 4.6), far less than for E. dregei (Figure 4.5). The species with the greater availability of hosts, in this case E. dregei, has the more fine-grained habitat and therefore would be expected to show less variation in occupancy among plots. The cause of the very high degree of consistency among plots for E. virescens is unknown. Although E. dregei showed higher variance (Figure 4.5), which may be due to the pronounced aggregation of its hosts even in large woodland clumps (Table 4.1), there was nonetheless remarkable

108 Chapter Four consistency in likelihood of occupancy among plots. Where differences did occur, they did not distinguish the same plots in the two analyses of presence/absence of mistletoes (Table 4.5) and numbers of mistletoes (Table 4.7). There was no obvious pattern to the plots which differed from the majority, except that they always occurred in Large 2 or Large 4; these two plots had the highest densities and lowest mean size of hosts of E. dregei among the five plot locations in large woodland clumps. The surprisingly high slope of number of mistletoes with girth in Large 2.3 and 2.4 (Table 4.7) is probably due to the under-representation of larger hosts at this locality (Figure 4.1).

~~4.4.3. Effects of habitat type~~

Chapter Three found that the likelihood of occupancy by E. virescens varied among woodland clumps of different habitat types and suggested that the differences might be due simply to differences in host density, or that there might additionally be differences in the density of mistletoes per host and hence per unit area. The results of this chapter confirmed that termite mounds did have higher densities of hosts of E. virescens than plots in miombo or terminalia woodland (Table 4.1). Furthermore, hosts on termite mounds were more likely to be occupied by E. virescens than hosts in woodland and supported more mistletoes per host (Tables 4.9 and 4.11). The intermediate habitat type, rocky outcrops, was intermediate in host density, but was not sampled sufficiently to assess density of mistletoes per host.

Although there was no difference for E. virescens between the frequency of occupancy of isolated hosts and those in large woodland clumps, there was a difference between isolated hosts and those on termite mounds. To test whether this was solely an effect of habitat type, the comparison was confined to isolated hosts and small woodland clumps on termite mounds only. Isolated hosts on termite mounds were less likely to be occupied than hosts in small woodland clumps on termite mounds, which showed that there was an effect of isolation independent of the effect of habitat type.

~~The interesting contrasts firstly between termite mounds and miombo or terminalia woodland and secondly between woodland clumps on termite mounds and isolated~~

109 Chapter Four hosts on termite mounds could be caused by either higher rates of dispersal to individual hosts or higher rates of within-host establishment and/or adult survival. These were not investigated further in this study. Instead I concentrated on the contrast between isolated hosts of both E. dregei and E. virescens and non-isolated hosts in large woodland clumps. However, in the final chapter, Chapter Seven, I speculate further on the characteristics of termite mounds which might lead to the observed high densities of E. virescens.

The distributions of hosts in different habitat types (Table 4.1) also supported the hypothesis raised in Chapter Three that the deviation of the variation in occupancy with clump size from the sampling hypothesis for E. dregei could be due to host aggregation at scales up to 3000 m^. Hosts of E. dregei were highly aggregated in 50 X 50 m plots (2500 m^) even in miombo woodland. This was unexpected, as the hosts of E. dregei, namely B. spiciformis and /. globiflora, are the dominants of miombo woodland. However densities of the two species were not consistent among miombo subsites, and groves of non-host species such as Monotes glaber and Parinari curatellifolia were common.

~~4.4.4. Conclusions~~

In summary, four of the seven predictions made at the beginning of the chapter were upheld and three refuted: 1. As predicted, likelihood of occupancy of hosts increased with increasing host volume. 2. Frequency of occupancy varied to some extent among host species, and tended to vary in the way predicted by a simple metapopulation framework, with a constant rate of increase of likelihood of infection with host volume for all host species. 3. Contrary to prediction, the number of mistletoes per unit volume was not constant with increasing host size, but instead decreased with size, intriguingly showing a linear dependence on basal girth for all three species of mistletoe on their exclusive host sets. 4. Also contrary to prediction, there was also no variation in local density of infected hosts with overall local host density.

~~110 Chapter Four~~

5. At the extremes of density, comparing isolated hosts to those in woodland clumps, hosts of both E. dregei and E. virescens were less frequently infected if isolated than in large woodland clumps or in clumps on termite mounds, respectively, though there was no difference for A. subulatus. 6. At a narrower scale, the degree of isolation from infected hosts had no influence on likelihood of infection, since spatial aggregation of occupied hosts within woodland clumps was not apparent for any of the three species of mistletoe. This finding was contrary to prediction. 7. Mistletoes of both E. dregei and E. virescens were spatially aggregated within the canopies of their hosts.

The theoretical framework for this study developed in Chapter One hypothesised that differences in likelihood of patch occupancy with patch size or quality are due to differences in the rates of within-patch processes, possibly establishment, adult survival or patch extinction rates, and that the differences with patch isolation are due to differences in the rates of between-patch processes, specifically between-patch dispersal. Chapter Five considers rates of establishment and adult survival, to assess whether rates of within-patch processes provide possible explanations of differences with host size and quality and whether they can be excluded as explanations of differences with host isolation. Chapter Six considers whether dispersal rates might lead to the observed occupancy levels of isolated and non-isolated hosts of E. dregei and E. virescens, and to the aggregation of mistletoes of these two species within hosts.

~~Ill Chapter Five~~

~~Chapter Five: Establishment and adult survival~~

~~5.1. Introduction~~

Chapter Four identified several patterns of mistletoe distribution with respect to habitat: 1. Mistletoes were highly aggregated in particular individual host trees. 2. Likelihood of occupancy increased with host size/age. 3. Likelihood of occupancy varied with host species. 4. Mistletoe density decreased with host size/age. 5. Mistletoes were spatially aggregated within the canopies of infected hosts, but were seldom observed close together on the same branch. 6. Occupied hosts were not spatially aggregated. 7. Isolated hosts of Erianthemum dregei were less likely to be occupied than hosts in large woodland clumps.

There are two broad types of explanation to account for the observed patterns: either they are due to variation in likelihood of dispersal (between-patch dynamics) or they are due to variation in post-dispersal persistence (within-patch dynamics). As discussed in Chapter One (Section 1.4), persistence within the patch depends on a number of factors, including rates of establishment, adult mortality and host mortality. The hypothesis outlined in Chapter One was that patterns of mistletoe distribution with respect to patch distance from sources of seeds are determined by between-patch dynamics, that is by dispersal, and that patterns with respect to patch size and quality are determined by within-patch dynamics. The aim of this chapter is to investigate whether within-patch dynamics can be eliminated as explanations of non-random patterns with host isolation (points 5 and 7 above) and supported as explanations of non-random patterns with host size and species (points 2, 3 and 4), and further to assess whether the surprising lack of aggregation of occupied hosts (point 6) might be explained by within-patch dynamics.

~~112 Chapter Five~~

Observed post-dispersal distributional patterns of adult plants are determined primarily by patterns of establishment and modified by patterns of post-establishment mortality (Hutchings 1986). Thus the primary focus of this chapter is relative establishment success, investigated via a series of establishment experiments testing the dependence of establishment on various host characteristics. The three mistletoe species at the study site, Erianthemum dregei, E. virescens and Agelanthus subulatus, each have one fruiting period per year, which is a characteristic shared by many Loranthaceae of Africa (Polhill and Wiens 1998) and elsewhere (Reid et al. 1995). Since A. subulatus fruited outside my annual field season, this species could not be included in the establishment experiments, but for E. dregei and E. virescens the full set of experiments were conducted. Most of the experiments were without known precedent in the literature.

The two species of Erianthemum had clearly defined and non-overlapping host ranges at the Darwendale study site (Chapter Two). Therefore a preliminary test of their distribution among the full set of tree species was to determine whether the mistletoes could establish on host species on which adult plants had not been recorded. Even within the set of host species, more and less frequently infected host species were recorded. For E. dregei, the host B. spiciformis was infected more frequently than J. globiflora and supported higher numbers of mistletoes. The possibility that this pattern was determined by relative establishment success on the two host species was tested. The difference between the two host species could otherwise be due to the existence of two host races of E. dregei, one of which infects B. spiciformis and the other J. globiflora, leading to two effectively separate sympatric populations. The existence of host races and geographical races of other species of mistletoes has been demonstrated experimentally (May 1971; Clay et al. 1985; Overton 1993).

One suggested explanation for the increase in likelihood per host of occupancy and number of mistletoes with host size is an increase in susceptibility to mistletoes with host size/age. Alternatively the opposite argument, that susceptibility decreases with host size/age, can be invoked to explain the lower densities of mistletoes in larger hosts (Section 4.4.1). Although the establishment experiments were not specifically designed to measure for the effects of host size on establishment success, the basal

113 Chapter Five girths of all experimental trees were measured and a post facto test was possible. The size of the branch on which mistletoe seeds germinate also affects establishment. Two experimental studies have found optimal host branch diameters for mistletoe establishment of 10 - 14 mm (Sargent 1995) and 7-20 mm (Yan and Reid 1995). This interesting finding shows that the entire branch length in a host canopy is not available for infection, but only young branches. In this study I controlled branch diameter in all experiments within the range of 10 - 15 mm.

While it is hypothesised that the variation in occupancy with host size and species might be due to variation in establishment success, the observed patterns of spatial aggregation of mistletoes independent of habitat aggregation are not expected to be due to differences in establishment success. Therefore establishment experiments tested the effects of position in the canopy at the smaller scale of observed aggregation, and differences between isolated and non-isolated hosts at the broader scale. Where spatial aggregation was absent, at the intermediate scale, among occupied hosts within woodland clumps, the pattern may be explained by immunity of uninfected trees to mistletoes. This was tested by a comparison of establishment success on unoccupied hosts and hosts already occupied by one or more mistletoes.

Davidar (1993) noted that naturally occurring mistletoes at different life stages, from seeds through to adults, were successively less spatially aggregated, suggesting density-dependent establishment. Subsequently, two studies have experimentally compared establishment success of mistletoe seeds planted singly and in groups, one finding no effect (Sargent 1995) and one reporting increased survival of seeds planted singly, but without statistical analysis (Larson 1991). At the Darwendale study site, the casual observation that adult mistletoes were not found close together on the same branch suggested that establishment might be density-dependent in this system. I set up a different test to that of Sargent and Larson, by planting seeds on branches distal to established adult mistletoes. Tests of density-dependence at broader scales, within neighbouring branches and whole trees, were provided by the comparisons of establishment success by position in the canopy and by prior infection status of the host as a whole.

~~114 Chapter Five~~

Variation in post-establishment survival can modify observed distributional patterns of adult mistletoes. The haustorium which connects a mistletoe to its host generally forms a large swelling (Kuijt 1969; Calvin and Wilson 1998). Mistletoes that die may remain in situ or fall off, leaving a scar, sometimes referred to as a woodrose, on the host in the place of the haustorium. Scars may persist for long periods of time before being lost by branch abscission. The presence of dead mistletoes and scars allowed some assessment of mortality of E. dregei and E. virescens, but with limitations, since the number of scars on a host depends both on the mortality rate of mistletoes old enough to leave scars and on the rate of loss of scars through branch abscission. The two rates may vary differently with host size/age, species and between more and less isolated trees. Among host species there is a further complication that haustorial anatomy is known to vary (Dzerefos 1995; Calvin and Wilson 1998). The assumption that rates of scar loss are consistent within the canopies of individual hosts and within 50 X 50 m plots is more robust, and therefore I used a survey of dead mistletoes and scars to test whether all presently and previously occupied hosts were distributed randomly with respect to all hosts, as was found for presently occupied hosts alone (Section 4.3.5), and whether dead mistletoes showed similar patterns of aggregation within hosts to live mistletoes (Section 4.3.6).

To gain an overall estimate of prevailing rates of recruitment and adult mortality of mistletoes at the site, and of colonisation and extinction rates among hosts, the randomly chosen plots set up for the survey of Chapter Four (Section 4.2.1) were revisited in two successive years for repeat censuses. If host trees do act as individual habitat patches forming a metapopulation in the general sense, then rates of recruitment within hosts are will be faster than colonisation of previously unoccupied hosts, and extinctions of within-host populations will occur periodically (Hanski and Gilpin 1991).

~~115 Chapter Five~~

~~5.2. Methods~~

~~5.2.1. Establishment experiments~~

Establishment experiments were set up in the 1996-1997 and 1997-1998 seasons, during the December fruiting period of E. dregei and the January fruiting period of E. virescens. In all cases the same protocol was followed. Seeds were collected from a large number of individuals, thoroughly mixed and planted out within 8 hours of collection. The outer fleshy pericarp and inner pigmented coat were removed by hand immediately prior to planting. Discoloured or misshapen fruits were discarded. The seed, or more correctly the embryo in its layer of viscin, was then pressed onto the upper side of the branch. Seeds were always planted in groups of ten, spaced along the branch at intervals of approximately 3 cm. Only branches of 1.0 - 1.5 cm in diameter were used. All branches in this size range and within reach by stepladder (0 - 3 m above ground) were identified and the requisite number of branches for each experiment was chosen randomly from this sample. Experimentally infected branches were numbered using unobtrusive peach-coloured paint, and the positions of the first and the last seed on each branch were marked. The basal girths of experimental trees were recorded and the approximate two-dimensional positions in the canopy of naturally occurring and experimentally planted mistletoes were noted.

Survival of seedlings was recorded first at one week and then at successive periods up to one year. At each assessment, every seed was scored as missing, dead, live without leaves or live with leaves. They were considered to have germinated once the green embryo had extended out through the layer of viscin, and to be alive as long as they remained green.

The establishment experiments in year one and year two were designed to test for the effects on establishment of E. dregei and E. virescens of prior infection status of the host (year one and year two), prior infection status of the branch (year two), host location (year two), host girth (year one and year two), host species (year one and year two) and species of host from which seeds were collected (year two). In year one

~~116 Chapter Five seeds of E. dregei and E. virescens were planted on each others' hosts as well as on their true hosts. The detailed designs of the experiments are described below.~~

In year one 40 target trees were selected, ten each of the species Julhernardia globiflora, Brachystegia spiciformis (hosts of E. dregei), Lannea discolor and Erythrina abyssinica (hosts ofE. virescens), scattered in the largest woodland clumps. For each species, five trees were already infected by mistletoes and the other five showed no evidence of past or present infection. Four uninfected branches were chosen randomly on each tree. Three branches of each of the twenty E. dregei hosts and one branch of each of the twenty hosts of E. virescens were planted with E. dregei. The remaining branches, one on every E. dregei host and three on every E. virescens host, were later planted with E. virescens. Ten seeds were planted on each of the four branches on each of the forty trees, giving a total of 800 E. dregei and 800 E. virescens.

In year two a total of 1560 seeds were planted on 95 target trees in four different experimental designs. In design one, 10 trees each of /. globiflora and B. spiciformis that were already infected by E. dregei were selected in the largest woodland clumps. Seeds of E. dregei were placed on one branch per tree that was already infected, with the first seed within 50 cm of and distal to the established mistletoe, and on one randomly chosen uninfected branch, giving a total of 400 seeds on 20 trees. In design two, ten uninfected trees of each of J. globiflora and B. spiciformis in the largest woodland clumps and ten isolated trees of each of the two host species were selected. Seeds of E. dregei were planted on one branch per tree, giving a total of 400 seeds on 40 trees. All E. dregei seeds that were planted out in designs one and two were sorted prior to planting by the host from which they were collected (/. globiflora or B. spiciformis) and on each branch five seeds from each source host species were placed in random order.

In design three, eight infected trees each of L. discolor and E. abyssinica were selected in the largest woodland clumps plus eight isolated infected isolated trees of each species. Seeds of E. virescens were planted on one infected and one uninfected branch of each tree as for design two, giving a total of 640 seeds on 32 trees. Finally, in

117 Chapter Five design four, three pairs of neighbouring trees of Grewia monticola on termite mounds were identified in which one neighbour was infected by a large number of mistletoes and the other uninfected, although their canopies were interlocking. Seeds of E. virescens were planted on two randomly chosen uninfected branches of each tree, giving a total of 120 seeds on six trees.

The paired uninfected and infected branches within trees (year two design two and design four) were compared by a Wilcoxon signed rank test. All other comparisons were done by logistic regression using GLIM Version 3.77 (Royal Statistical Society, London), where the reduction in deviance due to the removal of a factor from the full model approximates to a value (see Sections 3.2 and 4.2.3).

~~5.2.2. Survey of dead mistletoes and scars~~

Dead mistletoes and scars were counted, and their approximate two-dimensional positions in the canopy recorded, for all trees surveyed in the thirty 50 x 50 m plots and all isolated hosts described in Section 4.2.1. To ascertain whether the full set of all presently and previously occupied hosts were randomly distributed among all hosts, maps of hosts within plots were tested for randomness using the Monte Carlo simulation technique developed in Chapter Four (Section 4.2.3), for E. dregei and E. virescens only. Likewise, to ascertain whether dead mistletoes were aggregated within host canopies, a goodness of fit test was used to compare observed two- dimensional spatial distributions to the distributions expected by random, for all hosts supporting two or three individuals of E. dregei or E. virescens (see Section 4.2.3).

~~5.2.3. Annual recruitment and mortality~~

The 21 randomly selected 50 x 50 m plots and all isolated hosts described in Section 4.2.1 were revisited in two seasons succeeding the initial survey (1996-1997 and 1997-1998). All recruitment and deaths of E. dregei and E. virescens were recorded. Previously unrecorded young mistletoes were counted among the recruitment cohort if their seed was no longer visible and a haustorial swelling had developed.

~~118 Chapter Five~~

~~Germinating seeds and very young seedlings were not included. Deaths of both infected and uninfected hosts were also noted.~~

~~5.3. Results~~

~~5.3.1. Establishment experiments~~

~~Germination and development~~

The seeds of both E. dregei and E. virescens began to germinate within 24 hours of being placed on branches. Germination rates were high for both species in both years. In year one 92.8 % ofE. dregei and 93.5 % of E. virescens had germinated after one week and in year two the rates were 100 % and 93.8 %. No further germination occurred after this time. Germination rates did not differ among treatments. All live seedlings had produced a saucer-shaped holdfast against the branch by one week, irrespective of the species or prior infection status of the tree. Seedlings penetrated the bark of trees rapidly. When seedlings that died between one week and three weeks were removed from the branch, the bark underneath was always cracked. Host reactions were visible as exudate around the seedlings.

E. dregei developed faster than E. virescens. By three weeks, 15.8 % of seedlings of E. dregei in year one on true hosts and 52.2 % in year two had produced a pair of leaves. For E. virescens, no seedlings had produced leaves by three weeks in either year, but 62.8 % in year two had leaves by six weeks (not measured in year one). Overall, establishment was more successful in year two than in year one for both species. E. dregei had a higher germination rate in year two, equal survivorship to three weeks (63.5 % in both years), then much higher survivorship to six weeks in year two (44.3 % compared to 10.2 % on true hosts in year one). E. virescens showed a higher survivorship to three weeks in year two than in year one on true hosts (66.9 % versus 41.3 %).

~~119 Chapter Five~~

For E. virescens there was also a considerable difference between the two years in the proportion of mistletoes that disappeared from experimental branches. After three weeks 18.4 % were missing in year one but only 2.7 % in year two. For E. dregei the equivalent figures were 7.1 % in year one and 7.3 % in year two. Disappearance of seeds appeared to be predominantly due to predation rather than dislodging, for three reasons. First, no further disappearance occurred after three weeks (the proportions of seeds missing were identical after six months or a year). Second, loss of seeds was aggregated among branches (variance:mean ratio = 4.88 in year one, 4.05 in year two, for both species combined), suggesting localised foraging by predators. Third, the viscin dried and set the seeds in place so firmly that heavy rainstorms were never observed to dislodge seeds, even when they were freshly planted.

In some cases death of the mistletoe seedlings was accompanied by death of the twig on which they had been planted. This happened for two out of the 80 experimental branches on which seeds of E. dregei were planted in year one, on two individuals of the host species J. globiflora. In year two, in the experiment comparing establishment on already infected branches and paired uninfected branches on the same tree for E. dregei (design two), four experimental branches died, and they were all previously infected. Only the portion of the branch distal to the already established mistletoe died. Two of these were B. spiciformis and two J. globiflora. One other experimental branch died in year two, also a branch of /. globiflora experimentally infected with E. dregei (design three). Unfortunately these sample sizes were too small for statistical analyses, and it may or may not be significant that only host branches of E. dregei died and none of E. virescens.

~~Year one: development on non-hosts~~

~~Seeds of E. dregei and E. virescens germinated equally well on each other's host species as on their own host species (%^ = 0.09, df = 1, p > 0.05 for E. dregei\~~

- 1.22, df = 1, p > 0.05 for E. virescens-, n = one branch per tree on 40 trees for each species). However, after three weeks there was already a significant reduction in survival of seedlings of E. dregei on its non-hosts L. discolor and E. abyssinica

~~120 Chapter Five~~

(X^ = 9.59, df = 1, p < 0.01, n = 40) and by six weeks there were few survivors on the two non-host species (Figure 5.1). There were no differences between the two non- hosts in the performance of E. dregei, measured at three weeks = 0.47, df = 1, p > 0.05, n = 20). Most of the seedlings of E. dregei on L. discolor and E. abyssinica did not produce leaves. The exceptions were on one individual of L. discolor, where several seedlings of E. dregei developed a pair of leaves by three weeks and survived to six weeks. However, by this stage the infected branch was producing a copious gelatinous exudate around the seedlings with plumules and after seven weeks these seedlings had disappeared entirely.

~~Seedlings of E. virescens on its non-hosts J. globiflora and B. spiciformis were~~

~~measured only at one week, three weeks and one year (Figure 5.2). The survival on~~

~~non-hosts was not significantly lower at three weeks = 3.08, df = 1, p > 0.05,~~

~~n = 40) but after one year there were no survivors on non-hosts (x^ = 47.15, df = 1,~~

~~p < 0.001, n = 40). There were no differences between the two non-host species in~~

~~the performance of E. virescens, measured at three weeks (%^ = 2.06, df = 1, p > 0.05,~~

~~n = 20).~~

~~- 180~~

~~- 140~~

~~- 100~~

~~weeks~~

Figure 5.1. Survival of experimentally planted Erianthemum dregei on hosts Julbernardia globiflora and Brachystegia spiciformis (solid line, scale on left-hand axis) and on non-hosts Lannea discolor and Erythrina abyssinica (dashed line, scale on right-hand axis).

~~121 Chapter Five~~

~~weeks~~

Figure 5.2. Survival of experimentally planted Erianthemum virescens on hosts Lannea discolor and Erythrina abyssinica (solid line, scale on left-hand axis) and on non-hosts Julbernardia globiflora and Brachystegia spiciformis (dashed line, scale on right-hand axis).

~~Year one: effect of branch, host species, girth and prior infection status of natural hosts~~

Logistic regression treating each seed as a separate data point showed that there were significant differences in the number of mistletoes surviving to one year among branches nested within hosts for both E. dregei = 59.03, df = 40, p < 0.05, n = 600) and E. virescens = 77.48, df = 40, p < 0.001, n = 600). Further analyses were done comparing the number of survivors per tree, ignoring the differences among branches. For E. dregei, there were no effects of host species, host girth or prior infection status of the host on the number of mistletoes surviving to three weeks or one year (Table 5.1). For E. virescens, there were similarly no effects of host species, girth or prior infection status on survival to one year, but at three weeks there was a difference in the slope with girth between the two hosts (Table 5.2). For E. abyssinica the slope did not differ from zero (slope = -0.299, s.e. = 0.278, t = 1.08, n = 20, p > 0.05, Student's t-test) but/or L. discolor it was significantly negative (slope = -1.81, s.e. = 0.484, t = 3.74, n = 20, p < 0.01, Student's t-test).

~~122 Chapter Five~~

Table 5.1. Logistic regression analysis for survival of experimentally planted Erianthemum dregei to three weeks and one year, using the following factors: species (SP) (Julbernardia globiflora or Brachystegia spiciformis), natural log of girth (In G) and prior infection status (I) of target tree (n = 20 trees each planted with 30 seeds).

~~Factor Deviance df P~~

~~Three weeks SP 1.08 1 NS InG 0.91 1 NS I 0.11 1 NS SP.I 2.77 1 NS SP.ln G 0.01 1 NS LlnG 1 NS~~

~~Residual 2945 13~~

~~Total 40.94 19 One year SP 0.01 1 NS InG 1.66 1 NS I 0.04 1 NS SP.I 1.52 1 NS SP.ln G 339 1 NS LlnG 0.04 1 NS~~

~~Residual 3&02 13~~

~~Total 3&93 19~~

Table 5.2. Logistic regression analysis for survival of experimentally planted Erianthemum virescens to three weeks and one year, using the following factors: species (SP) {Lannea discolor or Erythrina abyssinica), natural log of girth (In G) and prior infection status (I) of target tree (n = 20 trees each planted with 30 seeds).

~~Factor Deviance df P~~

~~Three weeks SP 1.56 1 NS I 0.97 1 NS SP.I &20 1 NS SP.ln G 5.98 1 <0.05 I.lnG 0.73 1 NS~~

~~Residual 99.37 14~~

~~Total 117.59 19 One year SP 1.51 1 NS InG 1 NS I 2.60 1 NS SP.I 3^2 1 NS SP.ln G 3.55 1 NS LlnG 1.90 1 NS~~

~~Residual 31.06 13~~

~~Total 48.68 19~~

~~123 Chapter Five~~

~~Year one: effect of position in canopy~~

The proportion of seeds establishing was compared for branches within three 20° sectors of established mistletoes and those more than three 20° sectors from established mistletoes for all occupied hosts of E. dregei and E. virescens. There were no differences in performance near or far from established mistletoes (Table 5.3; Table 5.4).

Table 5.3. Logistic regression analysis of effect of branch position (P) (within or beyond three 20° sectors of an established mistletoe) on survival of Erianthemum dregei to one year, controlling for tree identity (T) (n = 300 seeds on 10 trees).

~~Factor Deviance df P~~

~~P 180 1 NS T 11.33 9 NS P.T 9.00 7 NS~~

~~Residual 12.00 12~~

~~Total 3120 29~~

Table 5.4. Logistic regression analysis of effect of branch position (P) (within or beyond three 20° sectors of an established mistletoe) on survival of Erianthemum virescens to one year, controlling for tree identity (T) (n = 300 seeds on 10 trees).

~~Factor Deviance df P~~

~~P 0.16 1 NS T 17.35 9 <0.05 P.T 8.64 7 NS~~

~~Residual 2&17 12~~

~~Total 54 29~~

~~Year two: effect of prior infection status of branch~~

Combining data from the two hosts of each species of mistletoe, presence of a established adult mistletoe on the branch between the trunk and the experimental seeds considerably reduced the proportion of seedlings that survived to six weeks and beyond for both E. dregei (Figure 5.3) and E. virescens (Figure 5.4). The Wilcoxon signed rank test showed that for both species the difference between treatments was

124 Chapter Five not significant at three weeks, but were significant at six weeks, three months and six months (Table 5.5; n = 20 pairs of branches for E. dregei and 32 pairs of branches for E. virescens). For both species the maximum increase in the difference between treatments occurred between three weeks and six weeks.

~~Erianthemum dregei Erianthemum virescens~~

~~V P V P 3 weeks 77.5 NS 189 NS 6 weeks 25.5 <0.01 123.5 <0.01 3 months 16.5 <0.001 82 <0.001 6 months 16 <0.001 49.5 <0.001~~

~~3 100~~

~~weeks~~

Figure 5.3. Survival of experimentally planted Erianthemum dregei on uninfected branches (solid line) and distally from the trunk on naturally infected branches (dashed line) of hosts Julbernardia globiflora and Brachystegia spiciformis.

~~125 Chapter Five~~

~~300~~

~~250 \\\ \\ \\ 200 v\ x\ f \ \ \ \ I \ \ 150 \ V \ — \ \ 100~~

~~10 15 20 25 weeks~~

Figure 5.4. Survival of experimentally planted Erianthemum virescens on uninfected branches (solid line) and distally from the trunk on naturally infected branches (dashed line) of hosts Lannea discolor and Erythrina abyssinica.

~~Year two: effect of host species, girth and location~~

For E. dregei, there were no effects of host girth or location (isolated versus non- isolated) on survival of mistletoes to six months or any shorter time period, but host species had a significant effect from six weeks onwards, with seedlings on B. spiciformis performing better than those on J. globiflora (Table 5.6). At this stage there were 104 survivors on B. spiciformis and 80 on J. globiflora, and by six months these had decreased to 79 on B. spiciformis and 52 on J. globiflora. For E. virescens, there were no differences between the host species L. discolor and E. abyssinica in survival of mistletoes to six months or any shorter interval, but both species exhibited a negative effect of host girth, with worse survival on larger hosts. This was apparent for both isolated and non-isolated hosts from six weeks onwards, but only for non- isolated hosts at three weeks (Table 5.7).

~~126 Chapter Five~~

Table 5.6. Logistic regression analysis for survival of experimentally planted Erianthemum dregei to three weeks, six weeks and six months, using the following factors: species (SP) (Julbernardia globiflora or Brachystegia spiciformis), natural log of girth (In G) and location (L) (isolated or non- isolated) of target tree (n = 40 trees each planted with 10 seeds).

~~Factor Deviance df P~~

~~Three weeks SP 0.03 1 NS InG 0.04 1 NS L 1 NS SP.L 0.47 1 NS SP.ln G 0.24 1 NS L.lnG 331 1 NS~~

~~Residual 96.14 33~~

~~Total 101.92 39 Six weeks SP 534 1 InG 0.42 1 NS L 0.31 1 NS SP.L 2.71 1 NS SP.ln G 228 1 NS L.lnG 0.62 1 NS~~

~~Residual 93.61 33~~

~~Total 106.55 39 Six months SP 1 <0.01 InG 0.17 1 NS L 0.75 1 NS SP.L 2.85 1 NS SP.ln G 0.95 1 NS L.lnG 0.05 1 NS~~

~~Residual 103.02 33~~

~~Total 125.22 39~~

~~127 Chapter Five~~

Table 5.7. Logistic regression analysis for survival of experimentally planted Erianthemum virescens to three weeks, six weeks and six months, using the following factors: species (SP) (Lannea discolor or Erythrina abyssinica), natural log of girth (In G) and location (L) (isolated or non-isolated) of target tree (n = 32 infected branches and 32 uninfected branches each planted with 10 seeds).

~~Factor Infected branches Uninfected branches~~

~~Deviance df P Deviance df P Three weeks SP 2.00 1 NS 1.45 1 NS InG 0.76 1 NS - - - L 0.87 1 NS OjW 1 NS SP.L 1.11 1 NS 3j6 1 NS SP.ln G &43 1 NS 0.01 1 <0.05 L.lnG &09 1 NS 4.91 1 NS~~

~~Residual 35.91 25 53.28 25~~

~~Total 40.97 31 47.71 31 Six weeks SP &73 1 NS 1.21 1 NS InG &35 1 NS 8.93 1 <0.01 L 0.02 1 NS 3J^ 1 NS SP.L 0.04 1 NS 0.01 1 NS SP.ln G 0.10 1 NS &23 1 NS L.ln G 0.04 1 NS 0.02 1 NS~~

~~Residual 74.64 25 49.63 25~~

~~Total 75.97 31 63.57 31 Six months SP 0J8 1 NS 2J2 1 NS InG OjJ 1 NS 6.74 1 <0.01 L 0.12 1 NS 0.01 1 NS SP.L 1.36 1 NS 0.02 1 NS SP.ln G 1 NS 0.77 1 NS L.lnG 0^3 1 NS 1.07 1 NS~~

~~Residual 59.04 25 49.61 25~~

~~Total 63^3 31 5&91 31~~

~~Year two: effect of prior infection status of host Grewia monticola~~

This small experiment showed that the uninfected individuals of G. monticola which had canopies interlocked with trees of the same species that were naturally highly infested with E. virescens, were not immune to infection. At six months 15 out of 60 seedlings (25.0 %) survived on the uninfected trees, distributed among all three individuals, and 13 out of 60 (21.7 %) survived on their infected neighbours.

~~128 Chapter Five~~

~~Year two: effect of position on branch and seed source~~

All E. dregei planted in year two (designs one and two) were included in a test for the effect of position on the branch, ranked from position one, which was most proximal to the trunk on uninfected branches and most proximal to the trunk and the established mistletoe on infected branches, to position ten which was most distal. Position had no effect on survival of mistletoes to six months on infected or uninfected branches (X^ = 10.40, df = 9, p > 0.05 for interaction term; = 6.20, df = 9, p > 0.05 for position term; n = 800). Similarly, for E. virescens there was no effect of position (%^ = 8.78, df = 9, p > 0.05 for interaction term; = 6.13, df = 9, p > 0.05 for position term; n = 640).

Survival of E. dregei was also tested for the effect of the species of host from which seeds were collected. There were no differences in performance of seeds collected from J. globiflora and those collected from B. spiciformis on target trees of either host species (Table 5.8). All seeds were more likely to establish on B. spiciformis.

Table 5.8. Logistic regression analysis of effects of source host species (S) {Julbernardia globiflora or Brachystegia spiciformis) and target host species (T) on survival of Erianthemum dregei to six months, controlling for effect of infection or non-infection (I) of branches (n = 800 seeds on 60 trees).

~~Factor Deviance df P~~

~~S 0.80 1 NS T 4.50 1 <0.05 S.T 0.80 1 NS~~

~~Residual 972.90 795~~

~~Total 977.40 799~~

~~129 Chapter Five~~

~~5.3.2. Survey of dead mistletoes and scars~~

~~General patterns~~

A large number of hosts of both E. dregei and E. virescens showed signs of previous infection by mistletoes in the form of scars, but were not currently occupied: 68 out of 228 hosts of E. dregei (30.1 %) and 36 out of 209 hosts of E. virescens (17.2 %) which had ever been occupied now had scars but no live mistletoes. Due to the loss of scars from hosts these figures are if anything underestimates of the overall extinction rate of within-host populations. It is probable that almost all scars were of the two Erianthmum species on their respective hosts since other species of mistletoes were hardly ever encountered on these hosts.

The largest number of scars on a host without live mistletoes was 47 on one isolated individual of G. monticola, a host of E. virescens. Although all those mistletoes were not necessarily alive simultaneously, this is nevertheless an indication that extinction is possible even for the upper range of within-host population sizes, and without the death of the host. In fact no deaths of occupied or unoccupied hosts were recorded during the two seasons when the 21 randomly chosen plots were resurveyed. For E. dregei, the largest number of scars on a host without current infection was 10, and the largest number overall was 11, on a host with 13 live mistletoes.

~~Spatial distribution among hosts~~

The inclusion of hosts showing evidence of previous infection in the test for randomness of spatial distribution of occupied hosts compared to all hosts did not show any aggregation of ever infected hosts of E. dregei in three one hectare plots (Table 5.9), nor of ever infected hosts of E. virescens in nine quarter hectare plots (Table 5.10). Thus there was no evidence that the present lack of spatial aggregation among occupied hosts (Section 4.3.5) has been preceded by a spatially aggregated pattern in the recent past. Presently and previously occupied hosts of E. dregei were significantly regular at all scales in Large 2 (Table 5.9).

~~130 Chapter Five~~

Table 5.9. Aggregation factors (A) for ever occupied hosts of Erianthemum dregei compared to all hosts in three 100 x 100 m plots in large woodland clumps at radii of 5, 10, 15 and 20 m from focal trees. The lower 95 % confidence interval is given for values of A > 1 and the upper 95 % confidence interval is given for values of A < 1.

~~Large 2 Large 3 Large 4~~

A 95% P A 95% P A 95 % p C. I. C. I. C. I. Ever occupied hosts versus all hosts 5 m 0^3 0^2 <0.01 1.25 0.42 NS 1.00 0.31 NS 10 m 0.64 0.19 <0.01 1.00 035 NS 1.09 0^5 NS 15 m 0.63 0.16 <0.01 1.07 0J5 NS 1.10 0.21 NS 20 m 0.69 0.14 <0.01 1.08 032 NS 1.15 0^0 NS Counts n (hosts) 417 49 236 n (occ. 75 27 69 hosts)

Table 5.10. Aggregation factors (A) for ever occupied hosts of Erianthemum virescens compared to all hosts in nine 50 x 50 m plots covering small woodland clumps, at radii of 5, 10, 15 and 20 m from focal trees. The lower 95 % confidence interval is given for values of A > 1 and the upper 95 % confidence interval is given for values of A < 1.

~~Small 2 Small 6 Small 7~~

A 95% P A 95 % P A 95 % P C. I. C. I. C. I. Ever occupied hosts versus all hosts 5 m 0^3 0.60 NS 1.06 0.41 NS 0.95 0.25 NS 10 m 042 0.25 NS 1.09 oua NS 044 0.16 NS 15 m 048 0.09 NS 1.06 0^3 NS 1.00 0.14 NS 20 m 1.02 0.02 NS 1.05 0.17 NS 1.00 0.02 NS Counts n (hosts) 25 43 21 n (occ. 12 20 12 hosts) Small 9 Small 10 Small 12

A 95% P A 95% P A 95 % P C. I. C. I. CI. Ever occupied hosts versus all hosts 5 m 1.67 0.73 NS 2.00 1.33 NS 033 0^8 NS 10 m 132 038 NS 1.50 0^8 NS 0.63 0^7 NS 15 m 1.05 0.17 NS L15 0.15 NS 0.75 038 NS 20 m 049 0.07 NS 1.00 0.07 NS 1.00 0.26 NS Counts n (hosts) 29 17 27 n (occ. 13 6 8 hosts)

~~131 Chapter Five~~

~~Table 5.10 continued~~

~~Small 13 Small 14 Small 15~~

A 95 % P A 95% P A 95% P C. I. C. I. C. I. Ever occupied hosts versus all hosts 5 m 043 0.57 NS 1.26 0.59 NS 1.13 0.23 NS 10 m 0.81 049 NS 1.03 0.16 NS 1.01 0.04 NS 15 m 0^9 038 NS 1.04 0.07 NS 1.00 0.01 NS 20 m 0^6 0^4 NS 1.00 0.03 NS 1.00 0.00 NS Counts n (hosts) 27 46 34 n (occ. 10 26 18 hosts)

~~Spatial distribution within hosts~~

Dead mistletoes and scars showed similar patterns of aggregation within host canopies as live mistletoes. In analyses for dead and live mistletoes combined, there was significant spatial aggregation of mistletoes within canopies of trees supporting either two or three individual mistletoes for both E. dregei and E. virescens (Tables 5.11 and 5.12).

Number of Erianthemum dregei Erianthemum virescens sectors Observed Expected G Observed Expected G frequency frequency frequency frequency 0 7 1.9 41.94 5 1.9 3&22 1 7 3.9 (P<0.001) 7 3.9 (P<0.001) 2-3 7 7.8 7 7.8 4-6 7 11.7 10 11.7 7-9 7 11.7 6 11.7

Number of Erianthemum dregei Erianthemum virescens sectors Observed Expected G Observed Expected G frequency frequency frequency frequency 0-3 7 3.1 33^9 6 3.3 18.70 4-6 12 7.7 (P<0.001) 10 8.2 (P<0.001) 7-9 8 16.2 13 17.5

~~132 Chapter Five~~

~~5.3.3. Annual recruitment and mortality~~

Recruitment and mortality of both species, E. dregei and E. virescens, were recorded in the 21 marked plots in both years (Tables 5.13 to 5.16). The recorded numbers of recruitments are more likely to be underestimates than overestimates because false negatives are likely but false positives extremely unlikely in searches for young mistletoes. The recorded numbers of deaths are likely to be accurate without false positives or negatives.

The observed recruitment events translated into recruitment rates for E. dregei of 3.0 % in year one and 3.6 % in year two. Mortality rates were slightly higher; 4.1 % in year one and 6.6 % in year two (n = 169 in year one and 167 in year two). For E. virescens, levels of recruitment and mortality were in the same range. Recruitment rates were 1.7 % in year one and 8.0 % in year two, while mortality rates were 3.9 % in year one and 4.6 % in year two (n = 179 in year one and 175 in year two). The numbers of recorded recruitment events and deaths were too small for any detailed statistical analysis for either species. The data did not indicate any outstanding differences by host species, basal girth or location (Tables 5.13 to 5.16), except that in year two a high proportion of both deaths and recruitment of E. virescens occurred in one plot, Small 2. For both species, more than one death or more than one recruitment event were frequently recorded on a single host.

Extinctions of within-host populations were recorded for both E. dregei and E. virescens, where the population was reduced to zero by one or more deaths within a single host. None of these extinctions were due to the death of the host tree. No deaths of occupied or unoccupied hosts of either Erianthemum species were recorded. Like extinctions, colonisation events were recorded for both species. For E. dregei and E. virescens respectively, combining both years, 50.0 % (n = 12) and 23.5 % (n = 17) recruitment events occurred on previously uninfected hosts. The extinction and colonisation events translated into low annual rates of extinction and colonisation among all hosts. For E. dregei, the colonisation rate per host was 0.5 % in year one and 0.7 % in year two, while the extinction rate was 0.5 % in year one and 0 % in year

~~133 Chapter Five two (n = 419). For E. virescens, the colonisation rate was 0.4 % in year one and 1.3 % in year two, while the extinction rate was 0 % in year one and 0.4 % in year two (n = 231).~~

~~Table 5.13. Recruitment of Erianthemum dregei on individual hosts in 21 randomly chosen plots and all isolated hosts in 1996-1997 (year one) and 1997-1998 (year two).~~

Number of new Prior number of Host species Host basal girth Location individuals individuals (cm) 1996-1997 1 0 B. spiciformis 123 Medium 1 1 4 B. spiciformis 137 Medium 2 1 1 J. globiflora 101 Large 1 1 2 J. globiflora 55 Large 2 1 0 B. spiciformis 73 Large 3 1997-1998 1 0 J. globiflora 83 Medium 1 1 1 B. spiciformis 98 Medium 1 1 0 B. spiciformis 207 Medium 2 1 0 J. globiflora 58 Medium 2 1 2 B. spiciformis B. 108 Large 1 1 3 spiciformis 127 Large 2

~~Table 5.14. Mortality of Erianthemum dregei on individual hosts in 21 randomly chosen plots and all isolated hosts in 1996-1997 (year one) and 1997-1998 (year two).~~

Number died Prior number of Host species Host basal girth Location individuals (cm) 1996-1997 1 1 J. globiflora 48 Medium 1 1 4 B. spiciformis 137 Medium 2 1 1 B. spiciformis 213 Medium 2 1 7 B. spiciformis 108 Large 1 1 3 J. globiflora 46 Large 2 2 12 B. spiciformis 112 Large 3 1997-1998 3 5 B. spiciformis 74 Medium 2 2 3 J. globiflora 75 Large 1 1 2 J. globiflora 101 Large 1 3 7 B. spiciformis 108 Large 1 1 2 B. spiciformis 132 Large 3 1 10 B. spiciformis 111 Large 3

~~134 Chapter Five~~

~~Table 5.15. Recruitment of Erianthemum virescens on individual hosts in 21 randomly chosen plots and all isolated hosts in 1996-1997 (year one) and 1997-1998 (year two).~~

Number of new Prior number of Host species Host basal girth Location individuals individuals (cm) 1996-1997 1 0 L. discolor 44 Large 2 1 22 C. apiculatum 164 Small 5 1 10 E. abyssinica 140 Isolated 1997-1998 1 3 L. discolor 69 Medium 4 1 1 D. cinerea 55 Medium 6 1 0 D. cinerea 36 Medium 6 1 4 A. gerrardii 100 Small 2 2 1 A. gerrardii 38 Small 2 2 9 A. gerrardii 57 Small 2 1 1 A. gerrardii 38 Small 2 1 0 A. gerrardii 39 Small 2 1 4 G. monticola 45 Small 2 1 0 G. monticola 26 Small 2 2 1 G. flavescens 101 Small 6

~~Table 5.16. Mortality of Erianthemum virescens on individual hosts in 21 randomly chosen plots and all isolated hosts in 1996-1997 (year one) and 1997-1998 (year two).~~

Number died Prior number of Host species Host basal girth Location individuals (cm) 1996-1997 1 3 D. cinerea 47 Medium 6 2 3 C. mo lie 57 Small 3 2 2 C. mo lie 53 Small 3 2 5 E. abyssinica 103 Isolated 1997-1998 1 6 A. gerrardii 100 Small 2 1 11 A. gerrardii 57 Small 2 1 3 A. gerrardii 27 Small 2 2 6 A. gerrardii 76 Small 2 2 7 C. molle 98 Small 6 1 1 G. monticola 21 Small 7

~~5.4. Discussion~~

Two predictions were made at the beginning of the chapter: that differences in likelihood of occupancy with host size or species may or may not be related to rates of within-host establishment or adult survival and that differences in host occupancy with host isolation or branch isolation from seed sources are not related to differences in rates of within-host establishment or adult survival. These general predictions were upheld by the results, and further insights into the patterns of within-host population processes of E. dregei and E. virescens were gained.

~~135 Chapter Five~~

At the Darwendale study site, E. dregei and E. virescens were never found either dead or aUve on each other's host species (Chapter Two). An establishment experiment found that seedlings did not survive for more than seven weeks on non-host trees, that is hosts of the other Erianthemum species (Figures 5.1 and 5.2). Host reactions in the form of exudate around seedlings were seen on hosts and non-hosts, but were most copious on one non-host branch (L. discolor) where E. dregei seedlings had reached the stage of producing a pair of leaves. Hoffmann et al. (1986) found a similar result, where Tristerix tetrandrus (Loranthaceae) germinated equally well on hosts and non-hosts, but died within a few weeks on non-hosts. Histological examination showed that seedlings on non-hosts failed to penetrate past the cortex of the branch on which they were planted.

Even within the set of natural hosts, there was evidence that differences in establishment success could give rise to the observed reduced likelihood of occupancy and mean number of E. dregei per host on /. globiflora relative to B. spiciformis, since in one of the two years establishment was significantly better on B. spiciformis (Tables 5.1 and 5.6). One hypothesis was that the difference in occupancy between the two host species might be related to separate host races of E. dregei, but an establishment experiment showed that E. dregei at this site does not have host races (Table 5.8). For E. virescens, establishment did not differ on the two hosts L. discolor and E. abyssinica (Tables 5.2 and 5.7), which was not surprising as they were not found to have different likelihoods of occupancy (Table 4.7) and apparent differences in mean numbers of mistletoes were due only to one exceptional host individual (Table 4.9). Unfortunately differences in establishment on the host species that did unequivocally support more E. virescens, namely A. gerrardii and G. monticola, were not tested, as they were absent from large woodland clumps. Previous studies have shown that differences in frequency of occupancy among host species are associated with differences in establishment success in some cases (Hoffmann et al. 1986), but must be due to differences in post-establishment survival in others (Yan and Reid 1995).

~~136 Chapter Five~~

The estabhshment experiments also gave the unexpected result that establishment success was significantly reduced on larger hosts of E. virescens (Tables 5.2 and 5.7), which may be one mechanism by which mistletoe density is lower in the canopies of larger hosts than those of smaller hosts (see Chapter Four). An explanation for this result might be that the seeds were always experimentally planted 0 - 3 m above ground. In larger trees this represents a smaller proportion of the total canopy, and therefore gradients from the upper part of the canopy to the lower part, for example in shade or nutrient allocation, would be more pronounced than in small trees. It would be interesting to compare the vertical distribution of adult mistletoes in large and small hosts and to examine seedling establishment experimentally at different heights in the canopy.

Where spatial aggregation of adult mistletoes occurred in the absence of aggregation of host characteristics, within host canopies and also between isolated hosts of E. dregei and those in large woodland clumps (Sections 4.3.3 and 4.3.5), the non-random patterns were not apparently due to differences in establishment success (Table 5.3 to 5.7). The spatial aggregation of mistletoes in canopies did not appear to be due to differential adult survival either, since dead mistletoes of E. dregei and E. virescens were as highly aggregated in the canopy (Tables 5.11 and 5.12) as live mistletoes (Tables 4.23 and 4.24). At the intermediate scale, among hosts within plots, a surprising lack of spatial aggregation of occupied hosts occurred (Section 4.3.4). One possible explanation is that unoccupied hosts were not susceptible to mistletoes. Again, this was not the case, as establishment was equally successful on unoccupied and occupied hosts of both E. dregei and E. virescens (Tables 5.1 and 5.2 and small experiment on host G. monticola). The data also showed that previously occupied hosts combined with currently occupied hosts were not spatially aggregated (Tables 5.9 and 5.10). The lack of spatial aggregation of infected hosts remains a mystery; the most feasible explanations, taking into account all the data obtained, are discussed in Chapter Seven.

The proximity of other mistletoes could hypothetically have a negative or positive effect on survival of establishing mistletoes of the same species. A positive effect would indicate spatial variation in the suitability of the habitat, as hypothesised above.

~~137 Chapter Five~~

and a negative effect would indicate density-dependent mortality. At the scale of entire host trees, and also at a smaller scale, comparing among sectors of the canopy, neither positive nor negative effects of naturally occurring mistletoes were found (Tables 5.1 to 5.4). However, at the smallest scale, where seeds were experimentally planted on branches that already supported an adult mistletoe within 50 cm of the first seed and between the seeds and the host trunk, a strong decrease in establishment was observed on already occupied branches for both E. dregei and E. virescens (Figures 5.3 and 5.4). This would explain the casual observation that adult mistletoes were seldom encountered close together on the same branch and would also contribute to the pattern of relatively lower densities of mistletoes in larger host canopies.

Mine is the first known study of the effect of adult mistletoe plants on establishment success of young mistletoes. It would be interesting to investigate whether such powerful density-dependent establishment is a general feature of Loranthaceae and Viscaceae. At the tree scale, a previous study has found the same result found here, that prior infection status of the experimental tree had no influence on establishment success of mistletoes (Overton 1994). Another study, however, found that establishment was less successful on already infected hosts (Hoffmann et al. 1986). Intriguingly, this experiment was carried out not on trees but on shrubs, with a total stem girth at breast height of less than 0.5 m. Perhaps the small size of the shrubs meant that the presence of an established mistletoe affected the entire host plant, while for the much larger trees, such as those in this study, the effects of established mistletoes are relatively localised within the canopy.

This leads on to speculation about the physiological mechanisms controlling establishment success. Clearly there is little interaction between the host and the mistletoe at the stage of mistletoe seed germination. In the establishment experiments germination was equally successful everywhere, as has also been found by others (Clay et al. 1985; Murphy et al. 1993; Yan and Reid 1995). The trigger for germination in mistletoes is rupture of the pigmented skin around the layer of viscin (Lamont 1983) and seeds will germinate successfully on any surface (personal observations; Yan and Reid 1995). All observed differences in performance at the Darwendale site, between hosts and non-hosts, hosts of different species, larger and

~~138 Chapter Five~~

smaller hosts and infected and uninfected branches, became significant at three to six weeks. Although seedlings penetrated the outer bark quickly, since the host bark was cracked under seedlings which died shortly after one week, perhaps the crucial period at which nutrients are required from the host is at three to six weeks for E. dregei and E. virescens. This is also the time at which leaves first appear on the seedlings. Effects of nutrient uptake would certainly explain why density-dependent suppression of establishment was very localised within the canopy of experimental trees, while, as noted, Hoffmann et al.(1986) working on a shrub species found that the entire host was affected.

Of course the differences among treatments are not necessarily explained by differences in nutrient uptake. For example, the degree of shading, which has been found to be an important determinant of establishment success of Tapinanthus bangwensis (Loranthaceae) (Room 1973), could explain the differences between larger and smaller hosts and further why non-isolated (more shaded) hosts of E. virescens showed the effects of size earlier than isolated hosts in year two (Table 5.7). The negative effect of an established mistletoe on the experimental branch could be explained by direct interference rather than by competition for nutrients from the host. I tested for the effect of position on the branch on both naturally infected and uninfected branches since a nutrient gradient might be expected to most strongly affect seeds most distal from the host trunk. May (1971) found reduced establishment success for mistletoe seeds nearest the ends of experimental branches. In this study, I did not find an equivalent result, even on branches supporting an adult mistletoe (Table 5.8), but the seeds were only about 3 cm apart, giving a total distance of 27 cm for 10 seeds.

Differences among treatments were more pronounced in the second year of establishment experiments, when overall establishment success was higher. The reasons for the improved establishment success could be many, and include higher predation in the first year in the case of E. virescens. Studies on demography of mistletoe populations have sometimes found J-shaped curves with a predominance of small mistletoes (Reid and Lange 1988; Norton et al. 1997a), but also bell-shaped curves (Dawson et al. 1990; Reid et al. 1995), which were interpreted as suggesting

~~139 Chapter Five~~

that years of high recruitment were infrequent. Peaks in the size distribution were in one case correlated with years of high precipitation (Dawson et al. 1990). Natural levels of recruitment at the Darwendale study site were consistent over the two years, ranging from 3 to 8 % for the two species of Erianthemum (Section 5.3.3). Of course recruitment is not limited only by establishment success, but also by fruiting intensity and density of dispersers, which can likewise differ among years (Reid et al. 1995).

Recruitment was approximately balanced by mortality in the natural populations of E. dregei and E. virescens during the two years. Although this superficially indicates populations at equilibrium, the populations may be driven by episodic peaks of recruitment or mortality. Like recruitment, adult mortality can vary substantially over time, for example increasing dramatically in years of drought (Reid and Lange 1988). There was also an indication of differences by location at the Darwendale site, with a high proportion of recruitment and mortality recorded in a single plot in year two (Tables 5.15 and 5.16). This finding was surprising in light of the very low variance among plots in the proportion of hosts which are occupied by E. virescens (Figure 4.6), which would suggest a high level of spatial conformity in demographic events.

The overall mortality rates of E. dregei and E. virescens of 3.9 to 6.6 % suggest lifespans in the order of 20 years, which agrees with data from two morphological aging studies, suggesting lifespans of 10 to >20 years for three species (Loranthaceae) in one study (Norton et al. 1997b) and a maximum of > 20 years for Phoradendron juniperinum (Viscaceae) in the other (Dawson et al. 1990). Unfortunately the data in this study were too few to assess associations between natural mortality and host characteristics, nor to test for density-dependence. Nonetheless it was clear that large numbers of deaths could occur on one host, with either the continuation of the population or extinction (Section 5.3.2). One of the conditions for a Levins model metapopulation (see Section 1.3) is that even the largest within-patch populations must be at risk of extinction (Harrison 1991), which seems possible for populations of E. dregei and E. virescens at the tree scale. A large proportion of hosts of both species of Erianthemum showed evidence of extinction of former mistletoe populations (Section 5.3.2), showing that extinctions as well as colonisations are common events

~~140 Chapter Five among host trees. Both extinction and colonisation occurred in the marked plots (Section 5.3.3).~~

Another condition for the Levins metapopulation, and for metapopulations in the broad sense, is that dispersal within the patch is more common than between-patch dispersal (Hanski and Simberloff 1997). Overall natural recruitment rates of 50.0 % within-host for E. dregei and 76.5 % within-host for E. virescens suggest that this condition may indeed be fulfilled for populations at the tree scale for the two species. This chapter has shown that establishment rates do not explain the high degree of aggregation of mistletoes within hosts. Chapter Six considers whether dispersal can explain the concentration of recruitment within already infected hosts, and hence the general patterns of aggregation.

~~141 Chapter Six~~

~~Chapter Six: Dispersal~~

~~6.1. Introduction~~

One of the possible explanations for a non-random spatial distribution of plants is that the pattern of dispersal is not random. The hypothesis used in this study is that non- random patterns with respect to distance from potential seed sources (fruiting plants) are due to non-random dispersal. Chapter Four identified two patterns of aggregation with distance. First, mistletoes were spatially aggregated within the canopies of hosts, and distributed among hosts according to a negative binomial distribution, with high numbers of mistletoes in particular hosts and none in others. Second, isolated hosts of Erianthemum dregei were less likely to be occupied than non-isolated hosts in large woodland clumps. This pattern did not hold true for E. virescens or Agelanthus subulatus. The aim of this chapter is to investigate whether there is any evidence of non-random dispersal of mistletoe seeds, within and between host trees, and comparing isolated and non-isolated hosts. As in Chapter Five, the field work was carried out only in the fruiting seasons of E. dregei and E. virescens, and A. subulatus had to be excluded because it fruits in the dry season, outside the period of field work.

Most species of mistletoes of both families, Viscaceae and Loranthaceae, are dispersed by birds (Kuijt 1969; Reid et al. 1995). Mistletoe fruits contain a single seed. Birds seek to eat the viscous layer of the seed rather than the fleshy epicarp of the fruit (see Chapter Two for a full explanation of the parts of the fruit). There are three main methods by which frugivorous birds handle mistletoe seeds after removing them from their epicarps. Some species swallow entire seeds and later defecate them, sometimes needing to wipe the resultant viscous faeces from their bodies. Others swallow the seeds but regurgitate them shortly afterwards and wipe them from their beaks. The third method tends to be used by more opportunistic feeders, which do not swallow seeds but simply peck at the viscous layer, sometimes with the seeds held between their feet (Reid 1991). Most studies have found that several species of birds at one locality eat the seeds of a particular mistletoe species, but one bird species is most effective as a disperser (Liddy 1983; Reid 1989; Murphy et al. 1993; Larson

~~142 Chapter Six~~

1996). At different localities the primary dispersers may variously be defecators (Docteurs van Leeuwen 1954; Reid 1989; Sargent 1994; Martinez del Rio et al. 1995) or regurgitators (Godschalk 1985; Monteiro et al. 1992). Regurgitators have been found to be more effective as dispersers of mistletoe seeds than defecators (Godschalk 1985) or peckers (Monteiro et al. 1992) at the same site.

From an extensive review of the literature, mainly anecdotal, Godschalk (1983) concluded that in tropical Africa the predominant dispersers of mistletoes are tinker barbets {Pogoniulus spp, family Capitonidae). The only two quantitative studies in the region found that tinker barbets accounted for 100 % (Dowsett-Lemaire 1982) and 64 to 80 % (Godschalk 1985) of seeds removed from Loranthaceae. Tinker barbets are regurgitators with respect to mistletoe seeds. At the Darwendale study site there is only one species of tinker barbet, the yellowfronted tinker barbet {Pogoniulus chrysoconus\ T. Gordon, personal communication, from data collected for the National Bird Survey). This species was expected to be the primary disperser of all mistletoes at the site.

In Chapter Four I found that isolated hosts of E. dregei were less likely to be occupied than hosts in large woodland clumps, but that isolated hosts of E. virescens were equally likely to be occupied as hosts in large woodland clumps (Tables 4.5 and 4.9). Hence, if differences in occupancy with patch isolation are due to differences in between-patch dispersal, I hypothesise that isolated hosts of E. dregei are less likely to receive E. dregei seeds than hosts in large woodland clumps, while isolated hosts of E. virescens are equally as likely to receive E. virescens seeds as hosts in large woodland clumps. In order to test this hypothesis it would be necessary to measure dispersal events to unoccupied isolated and non-isolated hosts. Since actual dispersal events are difficult to track, because birds that take seeds cannot easily be followed over any distance, I used visits by frugivorous birds to fruiting mistletoes in large woodland clumps and on isolated trees as a proxy of dispersal events. If fruiting mistletoes on isolated trees are visited less frequently than fruiting mistletoes in large woodland clumps, it can be assumed that non-infected isolated trees will also be visited less frequently than non-infected trees in large woodland clumps.

~~143 Chapter Six~~

In Chapter Four I also found that mistletoes of both E. dregei and E. virescens were highly aggregated within particular individual hosts (Table 4.2) and furthermore spatially aggregated within the canopies of occupied hosts (Section 4.3.6). Hence my second hypothesis in this chapter is that mistletoe seeds taken from any parent plant are not randomly dispersed among the local set of trees but are more likely to be dispersed within the host which supports the parent plant. Therefore I attempted to estimate the proportion of seeds taken by frugivorous birds that were dispersed within the host tree and away from the host tree. Unfortunately it was not possible to make objective estimates of the spatial aggregation of seed deposition relative to adult plants within the canopies of hosts.

~~6.2. Methods~~

During the fruiting seasons of E. dregei (December 1996) and E. virescens (January to February 1997), observations were made of birds visiting fruiting mistletoes in large woodland clumps and on isolated trees (defined as in Chapter Four). The isolated hosts were all remnants of miombo or terminalia woodland in the case of E. dregei and on either termite mounds or rocky outcrops in the case of E. virescens.

Observation time was divided equally among six time periods of two hours each, from 6 - 8 am till 4-6 pm. A fruiting mistletoe or group of fruiting mistletoes on either one focal host or two adjacent focal hosts would be watched until a seed was taken by a visiting bird. If a bird had not visited by the end of the time period, the watch at that location was abandoned. No more than one observation was made at one location on any one day. Observations were spread out as widely as possible, but could not be randomised because of the paucity of mistletoe fruits, particularly on isolated hosts of E. dregei that could be kept in view by a hidden observer.

For each observation, the number of mistletoes in view and the number of ripe fruits in view were recorded. When a bird arrived, it was identified to species, following Maclean (1984). If a group of birds arrived, the number in the group was recorded, and one focal bird was chosen for observation, generally the first bird to be seen removing fruits in view. The number of seeds swallowed and the number dropped by

144 Chapter Six the focal bird were recorded, as well as the duration of its stay in the host of the mistletoe after feeding, and the length of the waiting time prior to its arrival. The fates of seeds dislodged by feeding birds were observed as far as possible. Note that each mistletoe fruit contains one seed and that in taking the seed from the fruit a feeding bird swallows only the seed and not the epicarp.

The recorded waiting times to the visit of the focal bird were analysed in GLIM Version 3.77 (Royal Statistical Society, London), using a censoring technique to include both the times less than two hours, correct to the nearest minute, and the cases in which no visit had been made within two hours (Muenchow 1986; Crawley 1993).

~~6.3. Results~~

A total of 98 hours was spent waiting for and observing frugivorous birds visiting mistletoes. Fifty-three visits by birds were recorded and 137 seeds were observed being removed from mistletoe plants. In general, the focal bird dislodged the single seed without disturbing the fleshy epicarp of the fruit (see Chapter Two and Section 6.2). The immediate fates of the dislodged seeds were as follows: 120 were swallowed, 16 were dropped and fell to the ground and one was wiped on a branch of the parent mistletoe. The precise later fates of the swallowed seeds could not be tracked in any instance.

The numbers of ripe fruits on display within view (usually on one or more plants on one host, but in some cases on two hosts) did not differ between the observations of mistletoes on hosts in large clumps of woodland and those on isolated hosts for either E. dregei (mean for non-isolated = 7.63, s.e. = 1.08, n = 24, mean for isolated = 5.55, s.e. = 1.59, n = 11, t = 0.59, p > 0.05, Student's t-test) or E. virescens (mean for non- isolated = 4.56, s.e. = 0.818, n = 9, mean for isolated = 5.22, s.e. = 0.909, n = 9, t = 0.29, p > 0.05). The overall numbers of mistletoe plants were also similar on non- isolated and isolated focal hosts or pairs of hosts for E. dregei (mean for non-isolated = 3.83, s.e. = 0.630, mean for isolated = 2.64, s.e. = 0.607, t = 1.17, p > 0.05) and E. virescens (mean for non-isolated = 5.00, s.e. = 1.14, mean for isolated = 6. II, s.e. = 1.78, t = 0.65, p > 0.05).

~~145 Chapter Six~~

The mean waiting times until the arrival of the first bird to remove one or more seeds from the mistletoe fruits in view ranged from 44 to 71 minutes (Table 6.1). These means do not take into account the many occasions when no bird had visited after two hours, which were included in the overall analysis through a censoring technique. This analysis showed that the waiting time till bird arrival was significantly shorter for hosts of E. dregei in large woodland clumps compared to isolated hosts (x^ = 5.11, df = 1, p < 0.05) but not different for hosts of E. virescens in large woodland clumps compared to isolated hosts = 0.22, df = 1, p > 0.05). The mean measured waiting times for isolated hosts of E. dregei compared to isolated hosts of E. virescens appeared to be very different, but in fact there was no significant difference between them, taking into account the times over two hours = 2.34, df = 1, p > 0.05).

~~Mean measured s.e. n (measured n (times over waiting time waiting times) two hours) (minutes) E. dregei Isolated hosts 71.3 &49 11 9 Non-isolated hosts 46.7 5^9 24 6~~

~~E. virescens Isolated hosts 44.0 7.92 9 3 Non-isolated hosts 64.7 11.6 9 3~~

The observed visits were made by twelve species of birds: plumcoloured starling {Cinnyricinclus leucogaster), glossy starling {Lamprotornis nitens), lesser blue-eared starling {Lamprotornis chloropterus), crested barbet (Jrachyphonus vaillantii), blackcollared barbet (Lybius torquatus), Whyte's barbet (Stacolaema whytii), blackeyed bulbul {Pycnonotus barbatus), redfaced mousebird (Colius indicus), blue waxbill (JJraeginthus angolensis), streakyheaded canary {Serinus gularis), redheaded weaver (Anaplectes rubriceps) and grey lourie {Corythaixoides concolor). Yellowfronted tinker barbets, which were locally resident, were never observed eating mistletoe fruits during the designated bird-watching periods. Plumcoloured starlings consumed the greatest numbers of seeds of both E. dregei and E. virescens (Table 6.2). The common visitors (more than five visits) were all observed consuming seeds of both species of Erianthemum at both localities (large woodland

~~146 Chapter Six clumps and isolated trees). The visits were spread evenly among the six two hour watching periods (6 am to 6 pm).~~

~~Table 6.2. Numbers of visits and numbers of seeds consumed by birds feeding on mistletoes.~~

~~Bird species Erianthemum dregei Erianthemum virescens~~

Number of Number of Number of Number of visits seeds visits seeds Plumcoloured starling 11 35 5 8 Glossy starling 7 10 2 4 Crested barbet 4 13 3 4 Blackeyed bulbul 5 10 2 7 Lesser blue-eared starling 4 8 1 2 Blackcollared barbet 1 3 1 3 Redfaced mousebird 0 0 2 4 Whyte's barbet 1 1 0 0 Blue waxbill 1 1 0 0 Streakyheaded canary 0 0 1 1 Redheaded weaver 0 0 1 1 Grey lourie 1 5 0 0

The single blue waxbill pecked at the fruit and wiped the seed on a branch of the parent mistletoe. The other species removed seeds from their epicarps and swallowed them whole. Regurgitation or defecation were not observed. The usual post-feeding behaviour of the observed birds was to hop away from the fruiting mistletoe and rest in a denser part of the host canopy, invariably out of sight of the observer, before flying away from the tree. Two other species, redeyed dove (Streptopelia semitorquata) and familiar chat {Cercomela familiaris), were observed eating mistletoe fruits on the ground.

The numbers of seeds removed by birds did not differ between hosts in large woodland clumps and isolated hosts for either E. dregei (mean for non-isolated = 2.65, s.e. = 0.531, n = 24, mean for isolated = 2.18, s.e. = 0.658, n = 11, t = 0.53, p > 0.05, Student's t-test) or E. virescens (mean for non-isolated = 2.11 per host, s.e. = 0.540, n = 9, mean for isolated = 1.67, s.e. = 0.287, n = 9, t = 0.73, p > 0.05). For both species of mistletoe in both localities the seeds of approximately half of the visible fruits were dislodged (either eaten or dropped) by the focal bird.

The durations of the focal birds' stays in host trees after feeding were generally short and did not differ between large woodland clumps and isolated trees for E. dregei (mean for non-isolated = 5.39 minutes, s.e. = 1.21, n = 24, mean for isolated =

~~147 Chapter Six~~

4.82 minutes, s.e. = 1.93, n = 11, t = 0.26, p > 0.05, Student's t-test) or for E. virescens (mean for non-isolated = 4.78 minutes, s.e. = 1.50, n = 9, mean for isolated = 3.00 minutes, s.e. = 0.749, n = 9, t = 1.06, p > 0.05). Only one bird, a crested barbet, stayed longer than 20 minutes in the host tree after feeding.

For the six species of starlings and barbets, which together removed the greatest number of seeds from mistletoes, the proportion of seeds of E. dregei that were removed before shorter (less than two minutes) and longer (more than two minutes) post-feeding stays in the host tree was the same for isolated and non-isolated hosts (Table 6.3; = 0.31, df = 1, p > 0.05). However, it was apparent that birds tended to stay longer in the host tree after eating larger numbers of seeds. Fourteen visits each with post-feeding stays of less and more than two minutes were recorded, but for those of less than two minutes 23 seeds were removed, giving a ratio of 1.64 seeds per visit, while for those of more than two minutes 47 seeds were removed, giving a ratio of 3.36 seeds per visit.

~~Duration Isolated hosts Non-isolated hosts~~

~~Stays less than 2 minutes 8 seeds 15 seeds Stays more than 2 minutes 13 seeds 34 seeds~~

For E. virescens, there were a smaller number of visits in total by starlings and barbets, too few to conduct chi-square analysis, but as with E. dregei, there did not appear to be any marked differences in the durations of the stays after feeding in large woodland clumps or on isolated trees (Table 6.4). Eleven seeds were removed in six visits with post-feeding stays of less than two minutes, giving a ratio of 1.83 seeds per visit, and eight seeds were removed in four visits with post-feeding stays of more than two minutes, giving a ratio of 2.00 seeds per visit.

~~Duration Isolated hosts Non-isolated hosts~~

~~Stays less than 2 minutes 6 seeds 5 seeds Stays more than 2 minutes 2 seeds 6 seeds~~

~~148 Chapter Six~~

~~6.4. Discussion~~

Contrary to the results of comparable African studies (Dowsett-Lemaire 1982; Godschalk 1985), the yellowfronted tinker barbet did not take the majority of seeds at the Darwendale site. In fact they were never seen to visit mistletoe plants during the entire period of bird-watching (though they were seen feeding on mistletoes outside the designated field work carried out for this chapter). Seeds of both species of mistletoe were removed by a wide variety of birds, rather than a select group of specialist frugivores. For example, two observed consumers, the blue waxbill and the redheaded weaver, are mainly insectivorous (Maclean 1984). While it is possible that none of the removals of seeds observed in this study led to effective dispersal events, for example because only yellowfronted tinker barbets are effective dispersers, Godschalk (1985) recorded successful dispersal of mistletoe seeds by several of the species observed here, including plumcoloured starlings, crested barbets, blackcollared barbets and blackeyed bulbuls.

Fruiting E. dregei on isolated hosts were visited significantly less frequently by feeding birds than fruiting E. dregei on hosts in large woodland clumps, but there was no significant difference in the frequency of visits to fruiting E. virescens on isolated hosts and hosts in large woodland clumps (Table 6.1). Using visits to occupied hosts as a proxy for visits to unoccupied hosts, these data support the hypothesis that that isolated hosts of E. dregei are less likely to receive E. dregei seeds than hosts in large woodland clumps, while isolated hosts of E. virescens are equally as likely to receive E. virescens seeds as hosts in large woodland clumps. It seems a reasonable assumption that visits to unoccupied hosts will follow a similar pattern to occupied hosts comparing between isolated and non-isolated localities, rather than a completely independent set of dynamics, and in both localities they would most probably be visited less frequently than their occupied counterparts (as discussed below).

However, it is possible that the observed differences had nothing to do with isolation. Obvious confounding variables were controlled as far as was possible in a non- experimental investigation. Most importantly, previous studies have found both for mistletoes (Sargent 1994; Larson 1996) and for other plants (e.g. Howe 1977; Davidar and Morton 1986; Sargent 1990) that frugivorous birds pay more frequent visits to

149 Chapter Six larger local displays of fruits. The numbers of mistletoe plants and fruits on the focal host or pair of hosts did not differ between isolated and non-isolated hosts in this study. One outstanding concern is that the observer was less well hidden at the isolated sites than within large woodland clumps. Overall, considering the potential dependence of the results on the visibility of the observer or some other unidentified variable, and the lack of observed dispersal events (particularly of any to unoccupied hosts), the data provide only a weak confirmation of the proposed hypothesis.

If the observed differences were due to isolation, they indicate an interesting contrast between E. dregei and E. virescens. Although the result that isolated hosts of E. dregei but not E. virescens are visited less frequently than non-isolated hosts accords neatly with the respective differences in host occupancy by the two species, taken by itself it is surprising that there could be an effect of isolation for one species and not the other. The most likely explanation is the different habitats of isolated hosts of the two species of mistletoes, miombo woodland remnants in the case of E. dregei and termite mounds or rocky outcrops on dambos in the case of E. virescens. Woodland outcrops on dambos may well attract higher densities of birds because of overall higher availability of mistletoe fruits, other food or safe perching and nesting sites. African savannas are known to be mosaics of eutrophic and dystrophic sites, where the eutrophic sites, which can include dambos and termite mounds, support higher biomass and/or diversity at all trophic levels (Scholes and Walker 1993). The important distinction between eutrophic and dystrophic sites and its implications for the results of this study are discussed further in Chapter Seven.

A second hypothesis was that within-host dispersal is more frequent than between- host dispersal. Deposition of seeds was not observed, but estimates of the proportion of seeds that are dispersed within and away from the host supporting the parent mistletoe can be made from the number of seeds taken by birds and the durations of their stays in the host after feeding. Godschalk (1985) found that all of the starlings and barbets which consumed mistletoe seeds at his study site (namely plumcoloured starlings, blackcollared barbets, pied barbets, yellowfronted tinker barbets and crested barbets) were regurgitators rather than defecators of mistletoe seeds. He found mean times from consumption till regurgitation of 36.4 to 77.7 seconds for the first four of these species feeding on two species of Loranthaceae, with a total range of 18 to

~~150 Chapter Six~~

153 seconds. Using these data to assume firstly that all starlings and barbets regurgitate seeds of the two Erianthemum species, and secondly that post-feeding stays of less than two minutes correspond to dispersal away from the host while post- feeding stays of more than two minutes correspond to within-host dispersal, an estimated 67 % of E. dregei seeds (47 out of 70) and 38 % of E. virescens seeds (8 out of 21) taken by regurgitators were dispersed within the host supporting the parent mistletoe at the Darwendale site (Tables 6.3 and 6.4).

These data support the hypothesis that the negative binomial distribution of mistletoes among hosts is caused by a high rate of within-host dispersal relative to dispersal off the host which supports the parent mistletoe. Many other studies have found similarly high levels of within-host dispersal. Godschalk (1985) found that 42 % (n = 317) and 47 % (n = 75) of two species of Loranthaceae were dispersed within the host by all species of birds, mainly regurgitators but also defecators, while plumcoloured starlings alone deposited a greater than average 78 % (n = 50) of seeds within the host. Considering defecators only, Overton (1994) estimated that 18 % and 58 % of seeds of one species of Loranthaceae at different subsites were deposited within the host, and Sargent (1994) estimated levels of within-host dispersal of between 2 % and 34 % in neighbourhoods of different densities of one species of Viscaceae. Further evidence comes from the field studies of Martinez del Rio et al. (1995) and Larson (1996), which both found that previously infected hosts were far more likely than uninfected hosts to receive seeds of bird-dispersed mistletoes.

Birds other than starlings and barbets accounted for only 16 out of 86 seeds taken from E. dregei and 13 out of 34 seeds taken from E. virescens. Of these birds, the blackeyed bulbul and redfronted mousebird are known to defecate undamaged mistletoe seeds (Godschalk 1983, 1985). The mean time from consumption till defecation is much longer than till regurgitation, in the order of 20 minutes (Godschalk 1985; Murphy et al. 1993). At the Darwendale site none of the bulbuls or mousebirds stayed in the host supporting the parent mistletoe for this length of time. Godschalk (1983) speculated that while regurgitators disperse most seeds of African Loranthaceae, and disperse them primarily within the host, defecators such as mousebirds are responsible for infrequent long-distance dispersal events.

~~151 Chapter Six~~

Longer post-feeding stays by frugivorous birds in the vicinity of the parent plant will increase the likelihood that seeds are deposited near the parent (Pratt and Stiles 1983). Observations at the Darwendale site suggested that starlings and barbets stayed more frequently for long enough in the host to regurgitate the seeds of E. dregei in situ after eating greater numbers of seeds. This will result in a greater chance that seeds deposited within hosts will be clustered (Godschalk 1985). If dispersers tend to consume a greater number of fruits when a greater number are on display, for example in larger within-host populations of mistletoes, the outcome will be positively density- dependent deposition of fruits, so that already highly infected hosts will be disproportionately likely to receive further seeds. Positive density-dependence could be further reinforced by higher frequencies of visits by frugivorous birds to larger displays of fruits (references above), although high frequencies of visits to local mistletoe populations may not increase the amount of fruit removed per individual plant (Larson 1996).

Unfortunately detailed data on the precise distances travelled by frugivorous birds after feeding, and even more pertinently the precise locations of deposited seeds, are notoriously difficult to gather (Godschalk 1985; Murray 1988). They would certainly provide further insight into the spatial distributions of mistletoes observed in this study. For example, since the spatial aggregation of E. dregei and E. virescens within the canopies of hosts is not explained by variation in establishment success (Tables 5.3 and 5.4), by elimination it appears to be explained by patterns of dispersal, which could be confirmed by detailed records of the post-feeding behaviour of birds. A less obvious and more interesting proposition is that the lack of spatial aggregation of occupied hosts (Section 4.3.5) could be due to a binomial distribution of birds' post- feeding behaviour: perhaps they either hop away a short distance, remaining in the host tree near to the parent plant, or they leave the host and fly a distance far enough that where they land is effectively random with respect to the host.

In summary, despite of the practical limitations to tackling many of the relevant questions about dispersal of the seeds of E. dregei and E. virescens, the bird-watching did provide support for the hypothesis that observed patterns of mistletoe aggregation with distance were due to variation in dispersal. Both the results of this chapter and the literature suggest that the pattern of seed dispersal by frugivorous birds explains

152 Chapter Six the highly aggregated distribution of mistletoes within particular individual hosts, found in this study (Table 4.2) and in many others (Thomson and Mahall 1983; Hoffmann et al. 1986; Reid and Lange 1988; Monteiro et al. 1992; Overton 1994; Donohue 1995; Norton et al. 1997a). The results also provide one plausible explanation for the lower frequency of infection among isolated hosts by E. dregei but not E. virescens. Interpretation of the results only makes sense in the light of the results of Chapter Three, where the potential importance of habitat types to E. virescens was identified, Chapter Four, where some unexpected patterns of mistletoe distribution among trees were found, and Chapter Five, where the roles of establishment and later survival in determining observed patterns were delimited. In Chapter Seven, the closing chapter, I bring together the findings of the previous chapters in greater detail, and comment on the conclusions that can be drawn and the new questions the study has exposed.

~~153 Chapter Seven~~

~~Chapter Seven: Synthesis and discussion~~

~~7.1. Patch size, extinction, isolation and colonisation~~

The broad aim of this study was to assess the effects of insular habitat structure, in terms of the characteristics of individual patches, on the distributions of three species of mistletoes. The working hypotheses were that patch size, quality and isolation would all influence chance of occupancy by mistletoes and that size and quality would affect patch occupancy by limiting the rate of extinction (g), dependent on the rates of establishment and adult survival (within-patch dynamics), while isolation would affect patch occupancy by limiting the chance of receiving seeds dispersed from other patches (between-patch dynamics), or the colonisation rate (m). In the field I found that patch size, quality and isolation were all correlates of patch occupancy, by at least one of the three species, comparing both among woodland clumps (clump scale; Chapter Three) and among individual host trees (tree scale; Chapter Four). There was also spatial aggregation of mistletoes within hosts, at the branch scale, showing that correlation of occupancy with isolation occurred at fine scales.

Did the observed distributional patterns show the expected mechanisms of variation in within-patch processes for patch size and quality and between-patch processes for patch isolation? I concentrated here on a comparison between hosts in large woodland clumps and highly isolated hosts, which occurred singly or in small clusters at a maximum density of three per quarter hectare. In the case of patch isolation the hypothesis was confirmed. Establishment rates did not differ between isolated and non-isolated hosts (Chapter Five), eliminating establishment as an explanation of different occupancy levels. There was supportive evidence that dispersal rates to isolated hosts are lower than to hosts in large woodland clumps for Erianthemum dregei, which showed differences in frequency of occupancy between the two, but not for E. virescens, which had identical levels of occupancy (Chapter Six). Likelihood of occupancy among woodland clumps decreased with distance from the nearest

~~154 Chapter Seven occupied clump for E. dregei, albeit weakly (Chapter Three), which further supports the argument that dispersal accounts for the observed effects of habitat isolation.~~

Comparisons are slightly more complicated in the case of patch size, since correlation of occupancy with patch size will arise even under random distribution, in the absence of any differences in within-patch dynamics with size. However, I did find two non- random patterns with patch size. For E. dregei at the clump scale, the increase in likelihood of occupancy with size deviated from the random model (Chapter Three), but this was most likely due to host aggregation (Chapter Four). At the tree scale, a surprising and interesting decrease in mistletoe density with host size was found. Experimental evidence showed that establishment success can contribute to this pattern and, as predicted, to the pattern of occupancy with patch quality (host species) for E. dregei (Chapter Five). While this provided support for the hypothesis that within-patch processes determine differences in occupancy with patch size and quality, I did not measure relative frequencies of dispersal events to trees of different sizes and species and therefore between-patch dispersal was not eliminated as an explanation.

The working hypothesis of exclusive associations between patch isolation and dispersal and between patch size and in situ survival created a useful framework but is perhaps unrealistically simple, particularly with regard to patch size. If probability of dispersal is random over space, or over habitat space, then it follows that large patches, which are larger targets, will have a greater chance of being colonised than small patches. This has indeed been found in several field studies (Eber and Brandl 1995; Hill et al. 1996; Pfister 1998), and the extinction-size colonisation-distance dogma has been generally criticised (Williamson 1981). Ultimately however, the concepts of patch size and patch isolation can be somewhat interchangeable. The use of different scales in this study illustrates this clearly: a woodland clump can be seen either as a single large patch (clump scale), or as a region supporting many highly aggregated patches (tree scale). If we imagine for heuristic purposes a niche unit which can support exactly one individual of any species, then large patches are conglomerations of many niche units, and patch size is simply patch aggregation in another guise. The dichotomy between patch size and isolation depends on defining

155 Chapter Seven patches in a biologically realistic way, and probably becomes progressively more useful the longer that inter-patch distances are relative to patch size, for example in the oceanic island systems for which the theory of island biogeography (MacArthur and Wilson 1967) was originally envisaged.

~~7.2. Aggregation of mistletoes~~

The contrast between isolated and non-isolated hosts was not the only assessment made of the effects on occupancy of the distance of habitat from sources of seeds. I also examined spatial patterns at smaller scales, among hosts within woodland clumps and within the hosts themselves. The most noteworthy observations were that mistletoes {E. dregei and E. virescens) were highly spatially aggregated within the canopies of their hosts but not at a slightly broader scale, among adjacent hosts. Chapter Four hypothesised that the spatial aggregation within hosts would be explained by dispersal and not by establishment, while the lack of spatial aggregation among infected hosts must be explained by within-patch processes, most likely establishment but otherwise adult survival. Regarding within-host aggregation, the establishment experiments (Chapter Five) confirmed that position in the canopy relative to other mistletoes had no effect on establishment success (except on the same branch) and observations of avian dispersers (Chapter Six) suggested that most dispersal is indeed highly localised.

On the other hand, the establishment experiments showed that the lack of spatial aggregation among infected hosts was not caused by insusceptibility of uninfected hosts, nor by separate host races in the case of E. dregei. If all hosts are equally susceptible, and dispersal is localised, why then does spatial aggregation of infected hosts not arise? Previous detailed treatment of this question has been carried out by Overton (1996), who found the same surprising result that hosts infected by mistletoes were randomly distributed at a dry woodland study site in Mexico. Overton produced a simulation model, which did not generate spatial aggregation despite localised dispersal, and from this he argued that localised dispersal does not lead to spatial aggregation except under particular circumstances. This cannot be true, as the

156 Chapter Seven intuitive notion that locahsed dispersal must lead to spatial aggregation can be demonstrated by very simple models (Tilman et al. 1997). The key to Overton's model is perhaps the rate of host turnover relative to the lifespans of mistletoes, coupled with the tendency for accumulation of mistletoes in particular hosts: when Overton introduced disturbance into the model, so that regrowth produced adjacent trees of the same age, spatial aggregation arose among infected trees, suggesting that it was the continual random deaths of occupied hosts that initially maintained the random distribution of infected hosts.

~~Dispersal probability~~

~~Isolated Extent of host hosts canopy~~

~~Figure 7.1. Hypothesised dispersal function for mistletoe seeds with distance from the parent plant.~~

While Overton's model may well have some validity, I argue that a simpler explanation is quite sufficient to explain the lack of spatial aggregation of mistletoes beyond the immediate environs of the canopy. All that is required is that the probability of dispersal is very high close to the parent mistletoe plant but declines rapidly at a distance within the host canopy (Figure 7.1). The probability of dispersal beyond the host canopy is then so low that the exact shape of the function is irrelevant; it probably declines with distance but could otherwise be constant over distance or even bimodal, as speculated in Chapter Six. With time, the overlay of multiple dispersal functions of this type around infected hosts will give rise to a

~~157 Chapter Seven distributional pattern in which mistletoes form highly aggregated clusters within canopies, but the clusters are effectively randomly located with respect to one another.~~

At the Darwendale site progressively smaller woodland clumps did not show any signs of reduced levels of occupancy by E. dregei or E. virescens (Tables 4.4 and 4.8; Figures 4.4 and 4.6). Only the most isolated hosts were less likely to be occupied than those in large woodland clumps for E. dregei, or than those in small clumps on termite mounds for E. virescens. This is consistent with a very low rate of decline in the dispersal function beyond the immediate vicinity of a parent mistletoe, as illustrated in Figure 7.1; only the most remote hosts will experience a statistically detectable reduction in the chance of receiving seeds by dispersal.

The measured proportions of within-host and off-host dispersal in this study were not as exaggerated as suggested by Figure 7.1. Repeat censuses showed recruitment levels of 50 % for E. dregei and 77 % for E. virescens on already infected hosts (Chapter Five) and calculations from observed post-feeding behaviour of frugivorous birds suggested that 67 % of E. dregei seeds and 38 % of E. virescens seeds were dispersed within the host supporting the parent mistletoe plant (Chapter Six).

Although these figures are rough, they indicate that about half of all seeds dispersed from mistletoes are deposited in the same host as the parent; thus dispersal is highly non-random. Interestingly, the relative figures for dispersal and recruitment do not indicate any differences in dispersal efficiency (Reid 1989; Bustamante and Canals 1995) for seeds dispersed onto the host and those dispersed away from the host. Very low off-host recruitment levels compared to dispersal levels, for example, would indicate that few seeds dispersed off-host arrived at safe sites.

Both my explanation of spatial patterns of mistletoe distribution and that of Overton (1996) depend on the supposition that the negative binomial distribution of mistletoes among hosts is due to accumulation of mistletoes in hosts rather than any of the alternative possible explanations for the highly aggregated distribution. There are two broad types of explanations for the highly aggregated distributions of parasites typically found in hosts: differences in the encounter rate or differences in susceptibility among hosts (Hassell and May 1989). My establishment experiments

158 Chapter Seven showed that apart from complete lack of success on non-hosts and a small difference in establishment success of E. dregei on its two hosts B. spiciformis and /. globiflora, natural hosts did not vary in susceptibility. Hence for these mistletoes, and probably for mistletoes in general, the encounter rate is more likely to account for the negative binomial distribution among hosts. For hosts of mistletoes, the encounter rate is higher for already infected hosts because infection greatly increases the chance of subsequent infections.

Accumulation over time is also the most feasible explanation for the increase in mistletoe numbers with host size/age. Alternative explanations offered in the literature, but not supported by field data, are that avian dispersers are more likely to perch in large hosts even if perching time is allocated randomly (Hoffmann et al. 1986) and that large hosts may be more susceptible to mistletoes (Norton et al. 1997a). My results eliminated both of these possibilities at least for the Darwendale site, since the number of mistletoes per unit branch length actually decreased with host size.

This reduction in mean mistletoe density with host size was a surprising result, particularly as all three species, E. dregei, E. virescens and A. subulatus, showed exactly the same pattern of a linear increase of mistletoe number with host girth (Tables 4.7, 4.11 and 4.15). Chapter Four listed four possible explanations for the reduction in mistletoe density with host size. The first is very unlikely, that avian dispersers prefer not to perch in large trees. Alternative explanations are that there may be changes in host physiology with size which affect the susceptibility of the host to mistletoes, or that density-dependence limits mistletoe population sizes in large hosts, or that rates of population growth of mistletoes are limited by something other than habitat volume and accrual in hosts is not as fast as increases in host volume (a dilution effect). All three of these explanations have found support in this study. Establishment experiments showed that establishment success was reduced in larger hosts, at least in the lower branches of the canopy, and also that negative density- dependence in establishment was very pronounced for mistletoes seedlings on the same branch as an established adult. Density-dependent establishment was not found at any broader scale, within sectors of a host canopy or at the scale of the whole host.

~~159 Chapter Seven~~

Note that for density-dependence to account for the entire observed effect of reduction in mistletoe densities in larger canopies, it would either have to be overcompensatory, or dependent on number per host rather than density per host.

The remaining explanation, the dilution effect, has gained only indirect evidence in this study, but is probably the most important factor accounting for the reduction in mistletoe densities in larger hosts. This is suggested by the similarity among the three species, whose mean numbers all increased directly with host girth, implying a common mechanism, perhaps limitation by densities of frugivorous birds. The lack of variation in frequency of occupancy with host density in the 50 x 50 m plots supported the supposition that mistletoe population densities are not limited by habitat space (Figures 4.4 and 4.6). Once again, this explanation is predicated on non-random dispersal of mistletoes, by which already infected hosts are far more likely to receive further infections than uninfected hosts.

~~7.3. Linking the branch, tree and clump scales~~

Mistletoes grow on individual branches within host canopies. Perhaps the most conspicuous finding of this study was the strong density-dependent mortality of mistletoe seedlings distal to an established mistletoe on the same branch. The implication is that individual host branches act as single targets for mistletoes, approximating to the theoretical notion of niche units that support one organism each. Characteristics other than prior infection status also influence susceptibility of branches. Importantly, small branches of approximately 5-20 mm in diameter are far more susceptible to infection by mistletoes than branches in other size categories (Sargent 1995; Yan and Reid 1995). Norton et al. (1997b) found that among a number of measures of mistletoe and host anatomy, host branch diameter close to the haustorium was the best predictor of mistletoe age. Thus cohorts of same-aged branches on a host appear to pass through a period of susceptibility to infection, after which they are either infected or uninfected with no further chance of infection. Infected branches are largely safe from establishment by further mistletoes on new

~~160 Chapter Seven growth in the susceptible size category distal to the trunk from the established mistletoe.~~

Adult mistletoes will eventually die from causes which may or may not be associated with the host. Reid and Lange (1988) noted that over time a tree's total branch length in a given even-aged cohort decreases due to branch abscission, meaning that the number of mistletoes supported by branches in that cohort decreases. This pattern may or may not be modified by differences in rates of abscission between uninfected and infected branches. Reid and Lange go on to suggest that the demography of mistletoes may well be determined primarily by the demography of host branches. Certainly, more rapid loss of older branches could be an important reason for the observed reduction in mistletoe density with host size/age found at the Darwendale site. Overall, the branch scale can be seen as the primary scale of importance for mistletoe population dynamics. It has not been given sufficient attention in this or previous studies. For example, the rates of branch growth and abscission in the presence or absence of mistletoes have received only scanty attention (e.g. Sargent 1995; Tennakoon and Pate 1996).

Clearly the tree scale has additional explanatory power regarding mistletoe dynamics over that at the branch scale, since branches within a host are not independent in either the presence or absence of mistletoes. Branches on already infected hosts have a far greater chance of receiving mistletoe seeds than branches on uninfected hosts, particularly those in the same sector of the canopy as an established mistletoe. Branches within a host also share characteristics important to susceptibility to mistletoes. For example host species is a determinant of the likelihood and intensity of mistletoe infections. However, mistletoes themselves do not appear to limit each other at the tree scale; my establishment experiments did not demonstrate any density- dependence within hosts, though Donohue (1995) did find reduced flowering by mistletoes at high within-host densities.

Above the tree scale, trees are aggregated into woodland clumps. Three notable patterns were recognised at the clump scale in this study: variation in occupancy levels by habitat type for E. virescens, a deviation from the strict form of the sampling

161 Chapter Seven hypothesis for E. dregei, and a decrease in hkelihood of occupancy with clump isolation for E. dregei (Chapter Three). The first two of these patterns were better described at the tree scale, as explored in Chapter Four, and were apparently due to differences in densities of the species' hosts, as well as higher frequencies of occupancy by E. virescens on termite mounds. The only emergent pattern at the clump scale then, which was not investigated further at the tree scale, was that likelihood of occupancy by E. dregei declined with increasing clump isolation, suggesting that the observed differences in dispersal between isolated and non-isolated hosts would increase with increasing distance for the isolated hosts.

Metapopulations in the broad sense are networks of local populations connected by occasional dispersal events (Hanski and Simberloff 1997). Regional populations of mistletoes at the Darwendale site, and in general, conform to this definition at the tree scale, since within-host population growth occurs at a faster rate than between-host dispersal. Among host trees, mistletoe dynamics show several fundamental metapopulation characteristics, such as a large number of patches which have the potential to be colonised if vacant or to go extinct if occupied, and frequent asynchronous local extinctions even of the largest within-host populations (Chapter Five). Clearly, distributions of mistletoes within hosts cannot be explained without reference to between-host dynamics, and vice versa. The difference in rates of change between within-host and between-host dynamics is perhaps not sufficient to permit unstructured metapopulation modelling of the system. A higher level of hierarchical nesting was not detected in this study at the clump scale, and probably would only be recognised at a far broader geographical scale.

~~7.4. Interspecific differences~~

The three species of mistletoes, E. dregei, E. virescens and Agelanthus subulatus, exhibited many differences (Table 7.1). Most notably, they did not fit the general prediction that occupancy would rank with abundance of habitat. Both among woodland clumps and among host trees, the species with the rarest hosts, A. subulatus, showed very high frequency of patch occupancy. The high occupancy achieved by

162 Chapter Seven this rare species is very surprising, since the density of its hosts is at least an order of magnitude lower than for E. dregei or E. virescens. The possible explanations for the high levels of occupancy by A. subulatus relative to the two Erianthemum species must be due to higher rates of dispersal, higher rates of establishment or lower rates of mortality. Unfortunately I was not able to measure establishment or dispersal in A. subulatus as it fruited outside my annual field season. Speculatively, however, both low rates of mortality and high rates of dispersal could contribute to the high occupancy by A. subulatus.

Firstly, the host of A. subulatus, Pterocarpus angolensis, is an unusually long-lived tree in miombo woodland, reaching ages of 150 to 200 years, compared to an average of about 60 years (Vermeulen 1990). Longer lived hosts will have a greater net chance of acquiring mistletoes and a lower chance of extinction through host death. Secondly, the long lifespan of P. angolensis is also associated with large maximum sizes (Vermeulen 1990). At the Darwendale site, individuals of P. angolensis were generally larger than hosts of E. dregei or E. virescens (Figure 4.3 compared to Figures 4.1 and 4.2) and their canopies tended to rise above the overall canopy layer of the woodland (personal observation). Since A. subulatus fruits in the dry season, when most trees have only sparse foliage or none at all, it is conceivable that the fruiting mistletoe plants of A. subulatus are far more visible to frugivorous birds than E. dregei or E. virescens which fruit on smaller hosts in the wet season. An interesting aside is that while the sets of dispersers of E. dregei and E. virescens were identical (Table 6.2), the set of dispersers of A. subulatus is probably different; it certainly lacks plumcoloured starlings (the most common dispersers of the two Erianthemum species) which are migrants that visit only in the wet season.

The dispersal of A. subulatus may be further enhanced by the probable overall lower availability of food for avian dispersers in the dry season. Potentially A. subulatus may show "directed dispersal", in which the pattern of seed deposition is aggregated in favourable sites because they are attractive to dispersers. Directed dispersal has previously been demonstrated for ant-dispersed plants (Culver and Beattie 1980; Davidson and Morton 1981). Perhaps frugivorous birds in the dry season, with less choice of food but highly visible P. angolensis trees, move from one P. angolensis to

~~163 Chapter Seven the next, which would greatly increase the chance of successful within-patch and between-patch dispersal events for A. subulatus.~~

~~Table 7.1. Summary of contrasts between Erianthemum dregei, Erianthemum virescens and Agelanthus subulatus at the study site.~~

Erianthemum dregei Erianthemum Agelanthus subulatus virescens Host characteristics Range of host species Restricted polyphagy Extensive polyphagy Monophagy (4 host species in 2 closely (35 host species in (1 host species) related genera of the sub- many different genera family Caesalpinioideae) and families) Host distribution Hosts are dominants of Hosts occur at greater Host is moderately miombo woodland densities on termite common tree in clumps, rare on termite mounds than in miombo woodland, mounds miombo woodland rare elsewhere Abundance of hosts at Medium High Low clump scale (26 % of clumps) (73 % of clumps) (5 % of clumps) Abundance of hosts at High Medium Low tree scale (48 % of trees) (26 % of trees) (0.3 % of trees) Maximum size of High, potentially many Medium, equal to Low, equal to actual habitat patch at square kilometres maximum size of maximum size of clump scale termite mound individual tree Maximum individual Medium in most localities, Low in most localities, High host tree size rarely high rarely high Life history characteristics Phenology Flowers September- Flowers October- Flowers December- November, fruits November, fruits April, fruits dry December January-February season Fruit display Fruits are red when ripe Fruits are blue when Unknown Usually several fruits are ripe ripe simultaneously on one Usually few fruits are plant ripe at any one time on one plant Occupancy characteristics Occupancy at clump Low Medium High scale (30 % of clumps) (62 % of clumps) (81 % of clumps) Occupancy at tree Low Medium High scale (15 % of hosts) (25 % of hosts) (54 % of hosts) Mean population size More than one More than one More than one per infected host (2.2) (la) Maximum population Low High High size in individual host (13) (47) (51)

~~164 Chapter Seven~~

~~7.5. Termite mounds as nutrient hotspots~~

The prevaiUng view of African savannas is that they do not form a continuum of types but rather fall into two distinct categories: dystrophic savannas and eutrophic savannas (Bell 1982; Huntley 1982). The two types originate from different geological strata, and are reinforced by patterns of erosion. Dystrophic savannas occur on sandy, well- drained soils, where nutrient leaching is high, while eutrophic savannas occur on clay soils which retain nutrients but have less available moisture for plants. Owing to the difference in soil nutrient availability, eutrophic savannas tend to support higher plant biomass, productivity and/or species numbers than dystrophic savannas. Species richness and biomass of consumers are subsequently also higher. The two types form broad zones across Africa: miombo woodlands form the most extensive dystrophic biome and acacia woodlands the most extensive eutrophic biome (White 1983).

At finer scales, mosaics of soil types can give rise to local variation functionally equivalent to the dystrophic and eutrophic types. At these local scales, the patches of high fertility tend to be positively reinforced over time and are very persistent (Scholes and Walker 1993; Belsky 1995). A well known example of nutrient-rich patches in savannas are termite mounds; in fact termites may be the dominant taxon regulating nutrient turnover in African savannas (Jones 1990). Termites forage widely for plant litter and soil clay particles, which are then concentrated in their mounds. The mounds subsequently act as nutrient hotspots, supporting especially productive and species-rich communities of producers and consumers, which can persist long after the disappearance of termites from the mound.

The Darwendale site is typical of the broad dystrophic miombo biome, and no doubt the many termite mounds at the site are nutrient hotspots in a generally nutrient-poor system. If biomass and species richness of taxa at various trophic levels are higher at higher fertility sites, a reasonable prediction is that parasites, including mistletoes, will be more numerous and diverse on hotspots such as termite mounds. A recent study in South Africa found that, among seven biomes, mistletoe species richness (Loranthaceae and Viscaceae) correlated significantly and positively with the average nitrogen concentrations of woody plants in the biome (Dean et al. 1994). The

165 Chapter Seven importance of nutrient status was also evident at a finer scale: in four out of five biomes investigated the mean number of mistletoes per host was significantly correlated with host species nitrogen levels. Polhill and Wiens (1998) provide further evidence from elsewhere in Africa that mistletoes are more abundant in more fertile sites, including on termite mounds.

At the Darwendale site densities of the mistletoe E. virescens were substantially higher on termite mounds than in remnants of miombo or terminalia woodland, or on rocky outcrops. The concentration of mistletoes on termite mounds could be due either to a preponderance of host trees on the nutrient hotspots, or to higher numbers of mistletoes per host. I found that both of these explanations were true: hosts of E. virescens were significantly more common on termite mounds than in the relatively nutrient-poor miombo and terminalia woodlands (Table 4.1). In addition, occupancy and numbers per host were greater (Tables 4.8 to 4.11). Notably termite mounds located on uplands or on dambos did not differ in likelihood of occupancy (Tables 3.3 and 3.4), with the implication that for mistletoes the site as a whole does not function as two broad adjacent systems of uplands and dambos, but rather that the termite mounds act as scattered hotspots regardless of their location.

Unfortunately I did not have the time in this study to pursue investigations into the contrast between termite mounds and other habitat types as sites for the dispersal, establishment and survival of E. virescens, since the system appears to be an interesting example of the repercussions of fine-scale nutrient patterning in savannas. The higher densities of E. virescens per host on termite mounds could be due to better establishment success (and/or reduced adult mortality), or to higher rates of dispersal, since overall densities of frugivorous birds may well be higher on termite mounds (Scholes and Walker 1993). Most likely, both explanations are important, and ultimately the relatively high biomass of the termite mounds is maintained by positive feedback loops between density of host trees (many of which bear edible fruit and attract birds in their own right), density of mistletoes and density of avian dispersers.

~~166 Chapter Seven~~

~~7.6. Effects of habitat fragmentation~~

The natural woodland at the Darwendale site has been extensively cleared for purposes of agriculture, with the consequence that the habitat available to indigenous organisms has been fragmented. Clearance for agriculture has had different impacts on the total habitat available for each of E. dregei, E. virescens and A. subulatus (Figure 7.2). This is mainly because clearance has removed the woodlands of the uplands (miombo and terminalia), leaving the already scattered woodland clumps of the dambos untouched. Therefore habitat fragmentation due to clearance at this site has had a far greater effect on E. dregei and A. subulatus, whose hosts occur predominantly in miombo woodland, than on E. virescens, whose hosts are fairly rare everywhere except on termite mounds. However, E. virescens has a naturally patchy habitat at the clump scale and hypotheses regarding habitat fragmentation can be examined for both Erianthemum species.

The process of habitat fragmentation has three consequences for regional habitat structure: loss of habitat, lower mean patch size and higher mean distance among patches. Probably a general feature of habitat fragmentation is that the effects of habitat loss far outweigh the effects of changes in patch size and patch isolation (Saunders et al. 1991). Where fragmentation has impacts additional to the effects of habitat loss, then consequences may be reduced population densities in smaller patches and/or reduced likelihood of occupancy with patch isolation (see Chapter Three for details and references). In this study mistletoe densities were measured per host (thereby controlling for host density) in large, medium and small woodland clumps, and on isolated hosts, which represented the extreme of isolation at the tree scale and the extreme of patch size at the clump scale.

For E. dregei, mean mistletoe densities did not differ between large woodland clumps and isolated hosts (Table 4.6), but occupancy of isolated hosts was less likely (Table 4.4). This reinforces the conclusion that for E. dregei effects of patch isolation are due to metapopulation dynamics (between-patch dispersal) rather than differences in within-patch dynamics (see Section 7.1). Small woodland clumps tended to lack hosts of E. dregei. Medium clumps showed uneven distributions of mistletoes, with a

167 Chapter Seven bimodal pattern of occupied and unoccupied clumps (Table 4.3). This inconsistency might simply be due to the small numbers of hosts sampled per clump. Alternatively, if all hosts are equally susceptible in spite of location, the implication is that dispersal determines the uneven distribution in medium clumps, and therefore that isolation due to fragmentation is affecting E. dregei even in these fairly extensive clumps.

For E. virescens, mean mistletoe densities were equal in large and medium clumps and on isolated hosts, but were higher in small clumps (Tables 4.10 and 4.11). Comparing among termite mounds only, isolated hosts were less likely to be infected than their counterparts which occurred in bigger groups in the small woodland clumps on termite mounds (Section 4.3.2). For this species it is unknown whether this effect was due to dispersal (i.e. a consequence of being isolated) or within-patch demographic rates (i.e. a consequence of being small). However, it is noteworthy that while isolated hosts were significantly different to those on bigger groups on termite mounds, among the bigger groups the infection rate was constant, with low variance about the mean (Figure 4.6). This shows that the effects of habitat patchiness are discontinuous with patch size for E. virescens. Discontinuous effects of habitat fragmentation are predicted by theory (Doak et al. 1992; Andren 1994; Hanski et al. 1996). In this case the discontinuity is probably caused by the foraging choices made by birds, who perhaps have a cut-off point in terms of risk and energetics which determines the minimum clump size that they are prepared to visit.

~~168 Chapter Seven~~

~~a. total woodland in landscape~~

~~b. Erianthemum dregei~~

~~c. Erianthemum virescens~~

~~d. Agelanthus subulatus~~

Figure 12. Schematic representation of regional habitat distributions for mistletoes at the study site. Habitat is shaded grey. Each of the eight diagrams is divided into a left side representing dambo and a right side representing woodland. The four diagrams on the left represent habitat distributions prior to the 1950s clearance and the four diagrams on the right represent current habitat distributions.

~~169 Chapter Seven~~

~~7.7. Future work~~

The most intriguing findings of this study, which I beheve merit further study, are the scaling of mistletoe numbers with host girth rather than canopy volume and the lack of spatial aggregation of infected hosts. Of these, the first is perhaps the more tractable, as it can be assessed experimentally to some degree. In particular, it would be interesting to compare establishment success at all heights in larger hosts, and to compare rates of branch abscission in hosts of different sizes, and of infected and non-infected branches. Ideally, with better understanding of tree growth and architecture, it would be possible to construct a model of mistletoe dynamics which treated individual branches as single targets for dispersing mistletoe seeds. Branches could be grouped into cohorts, which progress through a susceptible stage when small, into either an infected or uninfected post-susceptible state, with perhaps increasing chance of abscission with age. This could be an interesting way to explore the possible causes of the reduced densities of mistletoes on older hosts. The unexpected pattern of random distribution of infected hosts found at the Darwendale site is not unique (see Overton 1996), and it would be interesting to find out whether the pattern of increase in numbers of mistletoes with girth also holds more generally.

Apart from results concerning mistletoe distributions and habitat occupancy, the findings of this study have also pointed to some areas of more general interest. The relative distributions of E. virescens, its host trees and its dispersers, in various habitat types provides a good system at three trophic levels for examining the persistence of nutrient hotspots in African savannas. Furthermore, while the distinct host ranges of E. dregei and E. virescens may be purely coincidental, it is curious that one parasitises only the dominants of miombo woodland while the other parasitises most of the remaining more common tree species at the site. Perhaps over evolutionary time competitive exclusion has partitioned the full set of hosts between the two closely related species. The exact host ranges of the two species may be specific to this site; for example E. dregei is known to occur on hosts of E. virescens elsewhere (Dzerefos 1995). It would be enlightening to investigate the host ranges of other co-occurring species of Erianthemum, or of E. dregei and E. virescens at other sites. More broadly,

~~170 Chapter Seven mistletoes and their hosts provide fascinating examples of localised evolution of specific host-parasite associations.~~

Overall, mistletoes offer an excellent study system for a variety of studies, not just of the type that I have undertaken here. The drawbacks of the system are the limited scope for experimental manipulation and the relatively slow population dynamics of the mistletoes, but there are many important advantages. The mistletoes, their hosts and their dispersers form a clearly defined tri trophic system. The organisms involved are all easily quantifiable and observable. Some aspects of the field work here were very successful, in particular the establishment experiments, which were logistically straightforward, had the advantage of very high rates of germination, and are open to many adaptations. Altogether, from my experience during this study, I would highly recommend mistletoe-host systems as systems for studies of host-parasite dynamics, plant-frugivore dynamics, or even for studies for which this system has not previously been used, such as the investigation of apparent competition between mistletoes on their exclusive hosts sets via shared natural enemies, or between host trees via the mistletoes themselves.

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