The Behavioural Ecology of the Gliding Marsupial, Petaurus Australis Ross Lindsay Goldingay University of Wollongong
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1989 The behavioural ecology of the gliding marsupial, Petaurus australis Ross Lindsay Goldingay University of Wollongong
Recommended Citation Goldingay, Ross Lindsay, The behavioural ecology of the gliding marsupial, Petaurus australis, Doctor of Philosophy thesis, Department of Biology, University of Wollongong, 1989. http://ro.uow.edu.au/theses/1077
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THE BEHAVIOURAL ECOLOGY OF THE GLIDING MARSUPIAL, Petaurus australis.
A thesis submitted in fulfilment of the requirements for the award of the degree of
Doctor of Philosophy
from
THE UNIVERSITY OF WOLLONGONG
by
Ross Lindsay Goldingay B.Sc. (Hons.) UNSW
Department of Biology
1989 DECLARATION
This thesis is submitted in accordance with the regulations of the University of Wollongong in fulfilment of the requirements of the degree of Doctor of Philosophy. The work described in this thesis was carried out by me and has not been submitted to any other university or institution.
Ross L. Goldingay November 1989 1
ABSTRACT.
The yellow-bellied glider (Petaurus australis) is one of only a few mammal species which feed on plant and insect exudates. The studies described in this thesis were aimed at assessing the importance of the diet on the behavioural ecology of the yellow-bellied glider. Gliders were studied in detail at two sites in New South Wales in quite different forest habitats. One site was near Bombala on the southeast tablelands and the other was near Kioloa on the south coast. The following features of the behavioural ecology of the yellow-bellied glider are presented in this thesis: (i) the diet and foraging behaviour, (ii) a detailed examination of the influences on the sap feeding behaviour, (iii) the socioecology, (iv) the size of home-ranges, and (v) influences on the use of vocalizations. At both study sites, a detailed assessment was made of the contribution of various food resources to the diet. Direct observation was necessary to assess the diet because exudates are almost wholly digested and, the use of exudate indicators in the faeces allow only presence or absence to be ascertained. Exudates (eucalypt sap, insect honeydew, manna, nectar) accounted for approximately 75% of the diet of gliders at Bombala (based on the proportion of the observed feeding time) whilst arthropods accounted for the remaining 25%. Arthropods are believed to be harvested primarily to provide dietary protein which is virtually absent from exudates. In contrast, exudates accounted for 99% of the diet at Kioloa and arthropods only ca. 1%. Gliders at Kioloa spent 70% of their feeding time engaged in feeding on nectar (and presumably pollen) from eucalypt blossom. Most of the protein requirement of gliders at this site may have been satisfied by pollen digestion because glider faeces contained substantial numbers of pollen grains, most of which had lost their cell contents. Eucalypt sap was important in the diet of gliders at both sites on some occasions. Gliders obtained sap by cutting into the trunks of trees with their lower incisor teeth and licking the sap that exuded. This occurred on only a small proportion of trees within a home-range. The incidence of rainfall and the availability of alternative food resources have been suggested recently to account for this seemingly enigmatic behaviour. However, the occurrence of sap feeding was not related to rainfall at either Bombala or Kioloa. Moreover, neither hypothesis accounts for the selection of only a small number of trees for sap feeding. Gliders were also selective in the species of tree utilized, with only a few of the available species being incised. An index of sap flow in both sap-site and non sap-site trees was obtained periodically. Gliders fed on sap only at times of high sap flow and trees used for ii
sap feeding tended to have a greater propensity to elevate sap flow than trees not incised by gliders. Feeding bouts during the main sap feeding periods were of a long duration {ca. 65 min) but outside these periods gliders occasionally made brief (ca. 6 min) 'test' incisions into both sap-site and non sap-site trees. It is suggested that this behaviour of gliders allows them to assay trees for the amount of sap flow and it is only when this is above a certain threshold that gliders engage in sap feeding. At Kioloa, high levels of sap flow were measured at times when sap feeding did not occur. This suggests that the abundance of alternative food resources, particularly of nectar, may on occasion influence the use of sap by gliders. Thus, elevated sap flow may provide a necessary precondition for sap feeding rather than ensuring its occurrence. An examination of the foraging behaviour of gliders at both sites revealed that gliders spend more than 80% of the time outside their dens feeding. When feeding time is coupled with time spent in other behaviours essential for foraging (i.e. gliding and climbing), approximately 90% of this time is accounted for. This is one of the highest values yet found for a mammal. It is suggested that this is due to the nature of the diet. Exudates are continuously renewed and can be quickly assimilated, but these food types are never sufficiently abundant to permit much time to other activities. Gliders spent significantly longer periods in trees when feeding on exudates than when feeding on arthropods. Also, gliders tended to forage together in the same trees when feeding on exudates compared to when feeding on arthropods. Data collected at both sites suggest that the foraging behaviour of gliders is influenced, not only by the abundance of their food resources, but also by the rates of renewal. At Kioloa, when eucalypts were flowering, gliders often had a choice of remaining in single trees for long periods of time or visiting more trees and perhaps encountering higher standing crops of nectar. Gliders were always highly selective in their choice of flowering trees in which to feed, choosing those with more than twice as many flowers as on a randomly selected sample of trees. Trapping of gliders was conducted at both sites and this, coupled with extensive spotlighting, allowed the social organization of gliders to be monitored. At Bombala, gliders lived in groups consisting of an adult pair and occasionally a subadult. Thus, glider groups almost always contained two or three individuals which shared an exclusive home-range. In contrast, glider groups at Kioloa never contained fewer than three individuals and initially two groups contained six individuals each. Both these groups contained an adult male and at least two adult females, suggesting a polgynous mating system. Subsequently, group sizes declined to three individuals which included an adult pair with subadult. This iii
decline in group size coincided with the failure of flowering in the most abundant tree species at this site, Eucalyptus maculata, over three successive years. It is argued that the mating system of these gliders is determined by the abundance and continuity of their food resources. At Kioloa, eucalypt blossom can be available throughout the year, providing a constant supply of both energy and protein. Gliders at the two study sites gave birth to a single young. At Bombala, young were born predominantly between July and September while at Kioloa, there was a predominance of births between February and March. This difference is suggested to be related to the timing of late lactation and weaning to coincide with the availability and predictability of certain food resources. At both sites, glider groups occupied exclusive home-ranges. At Bombala, these averaged 55 ha (using 95% isopleths based on the harmonic mean distance minimum) compared to 30 ha at Kioloa. The difference in the size of the home- range may reflect a greater abundance of food resources at Kioloa. Exclusive use of a home-range is often considered suggestive of territorial behaviour. The gliding capability of these possums allowed extraordinary mobility within their home-ranges which is one prerequisite for territorial behaviour. I propose that the extensive use of vocalizations by yellow-bellied gliders, which parallels the behaviour of many primates, mediates this intergroup spacing. Calling rates by gliders were higher when they foraged in the periphery of their home-range compared to when they foraged in the core of their home-range. Experimental playback of vocalizations within glider home-ranges resulted in increased calling rates by the resident gliders and in 50% of tests, led to a resident glider moving into the playback area. These results suggest that the home-ranges of glider groups are in fact, territories. This study shows that the extensive use of exudates by yellow-bellied gliders has a strong influence on their behavioural ecology. Exudates display a set of traits (a clumped spatial distribution, a continuous rate of renewal, can be quickly digested, have the potential to be available year-round and to be at times superabundant) which produce (i) an uncommon time-activity budget, (ii) a flexible mating system and (iii) apparent territoriality. Finally, the requirement of the yellow-bellied glider for very large home-ranges and the allocation of an enormous amount of time to foraging suggest that this species may be adversely affected by habitat alteration. Studies which examine the impact of logging on the behavioural ecology of this species are now required. iv
ACKNOWLEDGEMENTS
To study yellow-bellied gliders was not an easy undertaking and, like all field- based studies, was only possible with the help and support of many people. First and foremost, I would like to express my sincere gratitude to my supervisor, Rob Whelan. For keeping me employed on a more or less full-time but very flexible basis, for the six years whilst I conducted this research and also for providing judicious supervision. I am very grateful to Rod Kavanagh who was instrumental in my commencement of research at Bombala and who also provided considerable critical input to many aspects of this research. Also, for sharing the frustration of trapping gliders at Bombala and collaborating with the home-range analysis. This research, by its very nature, has caused me many sleepless nights and I would like to thank those people who shared these nights with me in the forest at Bombala and Kioloa, many of whom are mentioned in the papers at the end of this thesis. In particular: Michael Andren, Sue Carthew, Jon Howard, Rod Kavanagh, Amanda Sullivan and Patric Tap. I extend considerable gratitude to the following people for offering critical comments on the various drafts of thesis chapters and manuscripts from this research: David Ayre, Sue Carthew, Andy Davis, Tony Hulbert, Rod Kavanagh, Yan Linhart, Ros Muston, Patric Tap and Rob Whelan. The content of this thesis has also benefitted from discussions with Steve Craig, Stephen Henry, Rod Kavanagh and Rupert Russell. Rob Whelan also provided extensive editing of this thesis for which I am extremely grateful. I take full responsibility for any remaining split infinitives. My gratitude is extended to the Joy London Research Fund, the Australian Ecological Society and the Forestry Commission of N.S.W. for providing critical funding for this research. I am extremely grateful to this Biology Dept. in this regard also. I wish to thank Ann Lee for providing much needed help in ordering and hiring 'things' during this research and I thank many of the department's other staff (Linda Deitch, Elsina Meyer, Marina McGlinn, Julie Read, Judy Gordon) for providing other assistance. The Forestry Commission of N.S.W. and the Edith and Joy London Foundation are thanked for providing facilities at Bombala and Kioloa, respectively. I also thank John MacFarlane for providing assistance with facilities at Kioloa and Stuart Davey for showing me potential study sites at Kioloa. I extend boundless thanks to my parents for tolerating, over many years, my zoological interests and all sorts of animals in their home. I am grateful to them for enduring support. V
Lastly, I thank the Australian Cricket Team for providing considerable late- night entertainment during the most intensive period of writing this thesis. This is the last word.
• vi
TABLE OF CONTENTS
ABSTRACT i ACKNOWLEDGEMENTS iv TABLE OF CONTENTS vi LIST OF TABLES xii LIST OF FIGURES xiv LIST OF PLATES xvi Chapter 1. INTRODUCTION. 1
1.1. ARBOREAL MAMMALS. 1
1.2. INFLUENCE OF FOOD TYPES AND THEIR DISPERSION. 2 1.2.1. Body size. 3 1.2.2. Population density and social spacing. 4 1.3. EXUDIVOROUS MAMMALS. 5 1.4. OBJECTIVES OF THE THESIS. 7
Chapter 2. THE FEEDING BEHAVIOUR OF THE YELLOW-BELLIED GLIDER, Petaurus australis, AT BOMBALA.
2.1. INTRODUCTION. 8 2.2. METHODS. 8 2.2.1. Feeding behaviour. 10 2.2.2. Indices of food availability. 11 2.3. RESULTS. 12 2.3.1. Eucalypt sap. 12 2.3.2. Honeydew. 12 2.3.3. Arthropods. 14 2.3.4. Manna. 15 2.3.5. Nectar. 15 2.3.6. Overall diet. 15 2.3.7. Food resource indices. 16 2.4. DISCUSSION. 17
Chapter 3. INFLUENCES ON THE SAP FEEDING BEHAVIOUR OF THE YELLOW-BELLIED GLIDER, Petaurus australis. 22 3.1. INTRODUCTION. 22 Vll
3.2. SAP FEEDING BY THE MARSUPIAL Petaurus australis'. AN ENIGMATIC BEHAVIOUR? 26 3.2.1. Methods. 26 3.2.1.1. Feeding behaviour. 26 3.2.1.2. Sap measurements. 26 3.2.1.3. Incising experiment. 27 3.2.2. Results. 27 3.2.2.1. Sap feeding. 27 3.2.2.2. Sap measurements. 29 3.2.2.3. Incising experiment. 29 3.2.3. Discussion. 31 3.3. USE OF SAP-SITE TREES AT KIOLOA AND CALLALA BEACH. 35 3.3.1. Study sites. 35 3.3.2. Incidence of sap feeding at Kioloa. 35 3.3.3. Influence of rain on sap feeding. 35 3.3.4. Sap measurements at Kioloa and Callala Beach. 38 3.4. DISCUSSION. 42 3.4.1. Index of sap flow. 42 3.4.2. Examination of hypotheses to explain glider sap feeding. 46 3.4.3. Model of sap flow in eucalypts. 48 3.4.4. Comparison with sap feeding by sugar gliders. 50 3.4.5. Influences of sap composition. 51
Chapter 4. TIME BUDGET AND RELATED ASPECTS OF THE FORAGING BEHAVIOUR OF THE YELLOW-BELLIED GLIDER, Petaurus australis, AT BOMBALA, N.S.W. 54 4.1. INTRODUCTION. 54
4.2. METHODS. 55 4.2.1. Study area. 55 4.2.2. Time budgets. 55 4.2.3. Pattern of activity. 55 4.2.4. Time-utilization of trees. 55 4.2.5. Occurrence of group foraging. 55 4.2.6. Foraging distance. 57 4.3. RESULTS. 57 4.3.1. Activity pattern. 57 4.3.2. Time-activity budgets. 58 4.3.3. Time-utilization values of trees. 59 4.3.4. Occurrence of group foraging. 60 4.3.5. Foraging distance. 60 4.4. DISCUSSION. 62 vm
Chapter 5. USE OF NECTAR RESOURCES BY THE YELLOW-BELLIED GLIDER, Petaurus australis, AT KIOLOA, N.S.W. 65
5.1. INTRODUCTION. 65
5.2. METHODS. 65 5.2.1. Study area. 65 5.2.2. Flowering phenology. 66 5.2.3. Foraging observations. 66 5.2.4. Nectar sampling of Eucalyptus gummifera. 67
5.3. RESULTS. 67 5.3.1. Diet of Gliders at Kioloa. 67 5.3.2. Flower measurements. 69 5.3.3. Flowering phenology. 70 5.3.4. Nectar Parameters. 70 5.3.4.1. Temporal variability in secretion. 70 5.3.4.2. Influence of sampling interval on secretion. 70 5.3.4.3. Inter-tree variability in secretion. 72 5.3.4.4. Standing crop. 72 5.3.4.5. Nectar sugar concentration. 72 5.3.5. Foraging behaviour. 72 5.3.5.1. Tree selection. 72 5.3.5.2. Duration of visits to flowering trees. 75
5.3.6. Time budget. 77 5.3.7. Occurrence of group foraging. 78 5.3.8. Number of mammals feeding in flowering trees. 78
5.4. DISCUSSION. : 79 5.4.1. Diet. - 79 5.4.2. Nectar foraging behaviour. 81 5.4.2.1. Nectar production. 82 5.4.2.2. Influence of flower number. 82 5.4.2.3. Group foraging. 83 5.4.2.4. Nectar losses to other animals. 84 5.4.3. Pollination by gliders? 85
Chapter 6. SOCIOECOLOGY OF THE YELLOW- BELLIED GLIDER, Petaurus australis, AT BOMBALA AND KIOLOA. 88 6.1. INTRODUCTION. 88 IX
6.2. METHODS. 89 6.2.1. Trapping 89 6.2.1.1. Bombala. 89 6.2.1.2. Kioloa. 89
6.2.2. Glider marking and measurement. 94 6.2.3. Reproduction. 94 6.2.4. Food resource abundance model. 95
6.3. RESULTS. 95 6.3.1. Bombala. 95 6.3.1.1. Trapping. 95 6.3.1.2. Body weight measurements. 96 6.3.1.3. Glider groups. 96 6.3.1.4. Reproduction. 100 6.3.1.5. Dispersal. 101 6.3.1.6. Longevity. 101 6.3.2. Kioloa. 102 6.3.2.1. Trapping. 102 6.3.2.2. Body weight measurements. 103 6.3.2.3. Glider groups. 103 6.3.2.4. Reproduction. 104 6.3.2.5. Dispersal. 105 6.3.2.6. Longevity. 105
6.4. DISCUSSION. 105 6.4.1. Trapping. 105 6.4.2. Weight variation. 106 6.4.3. Groups dynamics. 107 6.4.4. Reproduction. 108 6.4.5. Food resource abundance model. 110
Chapter 7. HOME-RANGE OF THE YELLOW- BELLIED GLIDER, Petaurus australis, AT BOMBALA AND KIOLOA. 116 7.1. INTRODUCTION. 116
7.2. METHODS. 117 7.2.1. Bombala. 117 7.2.1.1. Study area. 117 7.2.1.2. Animal locations. 117
7.2.2. Kioloa. 120 7.2.2.1. Study area. 120 7.2.2.2. Animal locations. 120
7.2.3. Estimation of home-range. 120 7.2.4. Density estimate. 120
7.3. RESULTS. 122 X
7.3.1. Bombala. 122 7.3.1.1. Estimates of home-range area. 122 7.3.1.2. Glider density. 124
7.3.2. Kioloa. 124 7.3.2.1. Estimates of home-range area. 124 7.3.2.2. Glider density. 126
7.4. DISCUSSION. 126 7.4.1. Home-range area. 126 7.4.2. Comparison with other exudivores. 128 7.4.3. Management implications. 129
Chapter 8. VOCALIZATIONS AND TERRITORIAL BEHAVIOUR OF THE YELLOW-BELLIED GLIDER Petaurus australis. 131
8.1. INTRODUCTION. 131
8.2. TERRITORIAL ADVERTISEMENT BY PRIMATES. 132 8.2.1. Overt defense. 133 8.2.2. Olfactory advertisement. 133 8.2.3. Auditory advertisement. 133
8.3. SPACING AND RANGING BEHAVIOUR OF Petaurus australis. 135
8.4. CALLING BEHAVIOUR. 135 8.4.1. Temporal distribution of calls. 137 8.4.2. Calling by other gliders in group. 137 8.4.3. Calling in relation to food type. 137 8.4.4. Calling with respect to position in home-range. 140 8.4.5. Calling when neighbouring groups present. 141 8.5. DISCUSSION. 142
Chapter 9. CONCLUDING DISCUSSION. 147
9.1. INTRODUCTION. 147
9.2. TIME BUDGET. 147
9.3. SOCIALITY OR TERRITORIAL DEFENCE? 148
9.4. MATING SYSTEM. 150
9.5. MANAGEMENT CONSIDERATIONS. 153 XI
REFERENCES 155 APPENDIX 175 xii
LIST OF TABLES
TABLE
1 -1. Food niches of arboreal mammals. 2 1-2. Species of Primates which feed on exudates. 3 1-3. Exudivorous Australian marsupials. 4 2-1. Seasonal changes in the abundance index of loose shedding bark on six species of eucalypt. 16 2-2. Honeydew abundance index. 17 3-1. Glider feeding behaviour for wet and dry nights at Kioloa and Bombala. 38 3-2. Sap flow indices for E. gummifera at Kioloa and E. punctata at Callala for different times within a 24h period. 39 4-1. Activity pattern of gliders at Bombala. 58 4-2. Time-activity budget of gliders at Bombala. 59 4-3. Time-utilization of trees whilst engaged in harvesting different foods. 59 4-4. Occurrence of group foraging. 60 5-1. Diameter of flower capsules for different eucalypt species. 69 5-2. Flowering tree abundance and tree selection by gliders. 75 5-3. Regressions of time per tree by gliders versus the number of flowers in those trees. 77 5-4. Time-activity budget of gliders at Kioloa. 78 5-5. Occurrence of group foraging for different food types. 78 5-6. Influence of flowering tree number on the presence or absence of fruit bats at Kioloa. 79 5-7. Mean number of mammals nectar feeding in trees in which' yellow-bellied gliders were observed. 79 6-1. Trapping data for yellow-bellied gliders at Bombala. 95 6-2. Reproductive events of gliders recorded at Bombala. 101 6-3. Trapping data for yellow-bellied gliders at Kioloa. 102 6-4. Glider population survey at Kioloa. 104 6-5. Reproductive events recorded at Kioloa. 105 6-6. Glider group sizes for different sites. 107 7-1. Determination of the home-range area of yellow-bellied gliders at Bombala using different techniques. 122 7-2. Determination of the home-range area of yellow-bellied XU1
gliders at Kioloa. 124 8-1. The number of calls audible at various distances from a calling glider. 137 8-2. Calling rates by gliders when harvesting different food types at Bombala. 140 xiv
LIST OF FIGURES
FIGURE
2-1. Location of study sites at Bombala and Kioloa. 9 2-2. Monthly feeding observations on gliders at Bombala. 13 3-1. Incidence of sap feeding at Bombala. 28 3-2a. Measurements of sugar concentration in sap of E. viminalis for February 1985-July 1986. 30 3-2b. Sap flow measurements for E. viminalis. 30 3-3. Incidence of sap feeding at Kioloa. 37 3-4. Sugar concentration in sap of E. punctata. 40 3-5. Sugar concentration of sap for an individual E. punctata sap-site tree (a) and non sap-site tree (b). 41 3 - 6. S ap flow measurements for Eucalyptus punctata. 43 3-7. Sap flow for an individual E. punctata sap-site tree (a) and non sap-site tree (b). 44 3-8. Sap flow measurements for three Eucalyptus gummifera sap-site trees. 45 3-9. Theoretical model of sap flow in eucalypts. 49 4-1. Frequency distribution of 100 measured gliding distances of yellow-bellied gliders at Bombala. 61 5-1. Monthly feeding observations of gliders at Kioloa. 68 5-2. Rates of nectar secretion of flowers of five Eucalyptus gummifera. 71 5-3. Standing crop of nectar in flowers of four E. gummifera sampled in 1988. 73 5-4. Sugar concentration for E. gummifera tree 1 flowers sampled at different times. 74 5-5. Relationship between number of flowers per tree and time spent feeding in trees by gliders. 76 6-1. Study site at Waratah Creek, Bombala, and the location of trap trees contained within three glider group home-ranges. 92 6-2. Study site and location of trap trees at Kioloa. 93 6-3. Body weights of male and female gliders captured at Bombala. 97 6-4. Composition of six glider groups occupying three XV
home-ranges at Bombala. 98 5. Food resource abundance model at Bombala. Ill 6. Food resource abundance model at Kioloa. 112 1. Distribution of forest types at Waratah Creek, Bombala. 119 2. Forest habitat at Kioloa. 121 3. Home-ranges of five glider groups at Bombala. 123 4. Home-range of three glider groups at Kioloa. 125 1 (a). Distribution of calls and glides by one glider under observation for three nights in January 1986. 138 1 (b). Distribution of calls by one glider under observation and by other gliders nearby for three nights in June/July 1986. 138 2(a). Frequency of calling by gliders under observation at Bombala in response to three call types of gliders nearby. 139 2(b). Number of calls by gliders under observation at Bombala when foraging in periphery and core of home-range. 139 2(c). Number of calls by resident gliders before and following the transmission of a single full call at Kioloa. 139 LIST OF PLATES
Typical 'V'-shaped incisions made by the yellow-bellied glider (Petaurus australis) on a Eucalyptus saligna. 23 Lower incisors of a yellow-bellied glider which are used to cut into the trunks of eucalypts in sap feeding. 23 Test incisions on a Eucalyptus viminalis non sap-site tree at Bombala. 34 Eucalyptus punctata sap-site tree with incisions of various ages. 36 Yellow-bellied glider from group 2 emerging from den after dark. 56 Two sap-site trees with permanent ladders attached used for trapping gliders at Bombala. 90 A Eucalyptus viminalis den tree with a permanent ladder and trap attached. 91 A trapped glider showing prominent yellow belly fur. 91
Forest habitat at (a) Bombala and (b) Kioloa. 118 1
Chapter 1.
INTRODUCTION.
1.1. ARBOREAL MAMMALS. Among the world's arboreal mammal fauna, the Primates have received a disproportionate amount of attention in studies of behaviour and ecology. This is because primates occupy a dominant position in many tropical ecosystems (Terborgh & Schaik 1987) and also because most are diurnal and will readily habituate to the presence of a human observer, thus facilitating observational studies (Terborgh 1983, Terborgh & Janson 1986). Nocturnal primate species, despite often occurring at high densities (e.g. Petter et al. 1971, Hladik et al. 1980), have been studied mostly using indirect methods such as trapping and radio-telemetry (e.g. Hladik et al. 1980). This situation emphasises the difficulty in conducting observational studies of nocturnal mammals in general (e.g. Charles-Dominique & Bearder 1979). Arboreal species from other mammalian groups are also important members of their ecosystems (e.g. sloths may contribute substantially to nutrient cycling; see Montgomery & Sunquist 1975) but they have been largely overlooked. Such species may occur at low densities and thus are difficult to capture or observe (e.g. forest felids; see Terborgh 1988), presenting intractable difficulties for detailed research. The Australian arboreal marsupials, of which there are 31 species (24% of Australian marsupial species; determined from Strahan 1983), are predominantly nocturnal and also tend to fall into the intractable category. The ecology of only six species (Trichosurus vulpecula, Pseudocheirus peregrinus, Petauroides volans, Petaurus breviceps, Petaurus australis, Phascolarctos cinerius) has been studied in any detail at more than a single site (Smith 1980, Henry 1984, Henry & Craig 1984, How et al. 1984, Kehl & Borsboom 1984, Kerle 1984, Pahl 1984, R. Russell 1984, Suckling 1984, Kavanagh 1987c, Lee & Martin 1988, Howard 1989). Even for these species, some of which can be extremely abundant (e.g. P. peregrinus may occur at densities of 12.4-15.8/ha; How et al. 1984), their role in the forest and woodland ecosystems in which they occur is still poorly understood. For example, a recent study (Goldingay et al. 1987) has suggested that the sugar glider (P. breviceps), may be a major pollen vector of some plants. Further studies on arboreal species are therefore essential if an understanding of whole ecosystems is required. The discussion below is primarily directed at showing that a species' diet has a profound influence on all aspects of its behavioural ecology. This discussion only presents a cursory view of this, outlining several of the more obvious influences. A more detailed coverage of these points was unnecessary here as these points are
3 0009 02898 2622 2
developed further in the chapter discussions. Also included here is a preliminary account of the diet of exudivorous mammals and a broad statement of the aims of this thesis.
1.2. INFLUENCE OF FOOD TYPES AND THEIR DISPERSION. Arboreal habitats offer as great a diversity of food niches ("macroniches" sensu Eisenberg 1981; see Table 1-1) as terrestrial habitats. If only truly terrestrial or truly arboreal mammal species are considered, nine macroniches can be recognised for each (Eisenberg 1981). Arboreal habitats offer gumivore and nectarivore niches which are unique (Lee & Cockburn 1985). These are better considered as a single 'exudivore' niche (see Henry et al. 1987) because many species utilize both gum, nectar and other exudates. Moreover, there is only one true non-volant nectarivore, the honey possum (Tarsipes rostratus), among all mammalian orders (Turner 1982, 1983).
Table 1-1. Food niches of arboreal mammals.
Herbivore/browser. Feed primarily on plant stems, twigs, buds and leaves and require microbial enzyme systems (mammals do not possess cellulases) to aid digestion of structural carbohydrate (Eisenberg 1981). Other dietary adaptations include low total energy requirements and reduced feed intakes, low maintenance nitrogen requirements and caecotrophy (Hume et al. 1984, see also Hume 1982). Frugivore/herbivore. Feed on leaves, fleshy fruiting bodies and some seed (Eisenberg 1981). Frugivore/omnivore. Feed primarily on fruits (generally the fleshy pericarp) but supplement the diet with invertebrates and occasionally vertebrates (Eisenberg 1981). Most tropical didelphid marsupials belong to this category (see Charles-Dominique 1983). Fru givore/gran i vore. Feed on fruit as well as seeds and nuts (Eisenberg 1981), the latter being cached (see Emmons 1980). Carnivore. Feed primarily on vertebrates; distinguishing them from arboreal insectivores. The extinct Thylacoleo is the only species of marsupial believed to have occupied this niche (Lee & Cockburn 1985). Insectivore/omnivore. Feed primarily upon arthropods but may supplement the diet with small vertebrates and fruit (Eisenberg 1981). Myrmecophage. Feed on colonial insects, mostly ants and termites, but other invertebrates may be eaten (Montgomery & Lubin 1977, Eisenberg 1981). This niche includes the neotropical antcatcrs and old world pangolins (Eisenberg 1981) but may include the Striped Possum, Dactylopsila trivirgata , (Smith 1982b). Exudivore. Feed predominandy upon plant and insect exudates such as tree sap, gum, nectar, manna and insect honeydew. These species supplement their diet with arthropods presumably to provide protein which is virtually absent from these exudates (e.g. Basden 1965,1966, Paton 1982, Stewart et al. 1973). Pollen is also ingested by species feeding on nectar and this may provide some protein (Turner 1984a,b, Smith & Green 1987). 3
1.2.1. Body Size. It has been suggested that a food niche actually sets limits to body size among mammals (Smith & Lee 1984, Lee & Cockburn 1985). Within particular phylogenetic groups, the largest species are folivorous whilst smaller species feed on energy-rich food items and arthropods (Clutton-Brock & Harvey 1977a,b). Diets of herbivores tend to be low in nutritional value and require long rates of passage through the gut, thus precluding small body size (Clutton-Brock & Harvey 1977a, Hume 1982, Smith & Lee 1984). For example, the smallest marsupial folivore, the common ringtail possum (P. peregrinus ; ca. 600g), possesses particular digestive adaptations such as coprophagy, which allows it to cope with a low nutrient diet (Hume et al. 1984). Rates at which mammals harvest arthropods appear independent of body size so that as body size increases in omnivorous species, the proportion of arthropod biomass in the diet decreases (e.g. Charles-Dominique 1974, Petter 1978, Smith & Russell 1982). Most arboreal insectivores weigh less than 220 g (Smith 1982b) and this seems to reflect the size and dispersion of arthropod prey (Kay & Hylander 1978). Only those that specialize on social insects have been able to achieve larger body size.
Table 1-2. Species of Primates which feed on exudates. Only those species that use nectar and/or other exudates as a significant component in the diet are listed. Where detailed data were not present an indication is given of the likely proportion of each in the diet; ++ = present, — = absent, ? = unknown contribution.
Species Weight (g) Exudates; fruit; arthropod;j Location Reference
Prosimians Galago elegantulus 300 75%; 5%; 20% Africa 1,2 Galago demidovii 60 10%; 19%; 70% Africa 1,2 Galago senegalensis 200 ++; -- ;++ Africa 3 Galago crassicaudatus 1300 70%; 21%; 5% Africa 3 Perodicticus potto 1100 21%; 65%; 10% Africa 1,2 Microcebus murina 65 ++;++;++ Madagascar 4,5 Microcebus coquereli 300 >50%; ?; ? Madagascar 6 Phaner furcifer 300 90%; -; 10% Madagascar 5,7 Cheirogaleus medius 170 nectar, ++; ++ Madagascar 5 Simians Saguinus imperator 500 10%; 23%; 67% South America 8,9 Saguinus fuscicollis 400 22%; 28%; 50% South America 8,9 Saguinus oedipus 508 14%; 38%; 39% Central America 10 Callithrix jachus 240 70%; --; 30% Central, South Am. 11 Callithrix humeralifer 400 ++;++;++; verts South America 12 Cebuella pygmaea 100 67%; --; 33% Central, South Am. 13 Saimiri sciureus 900 some nectar South America 8,14
1 Charles-Dominique 1971; 2 Charles-Dominique 1974; 3 Crompton 1984; 4 Martin 1972; 5 Petter 1978; 6 Pages 1980; 7 Hladik et al. 1980; 8 Terborgh 1983; 9 Terborgh & Stern 1987; 10 Garbcr 1984; 11 Fonscca & Lachcr 1984; 12 Rylands 1981; 13 Ramirez et al. 1977; 14 Janson et al. 1981. 4
Among primate exudivores, body weight is restricted to species within the range 60-1300g (Table 1-2). However, exudivorous species in Australia range from 7g (Cercartetus lepidus) up to 590g (P. australis) (Table 1-3). Exudivorous species attain a greater body size than insectivores (Smith 1982b), presumably due to the abundance and energy content of exudates. It is not known whether the constraint on larger body size for exudivorous species is energy or protein. Exudivores may generally have low nitrogen requirements (e.g. Smith & Green 1987). However, species feeding extensively on floral nectar may obtain sufficient protein from pollen digestion (e.g. Turner 1984a,b). Rates of energy intake are probably more limiting (Smith 1984c, Smith & Green 1987) because exudates are often widely dispersed (e.g. Smith 1982a), preventing specialisation on this resource by large species. It is a salient point that four of the ten Australian exudivores are gliding species.
Table 1-3. Exudivorous Australian marsupials.
Species Weight (g) Diet Reference
Petaurus australis 590 mostly exudates and some arthropods 1,2,3 Petaurus norfolcensis 230 exudates and arthropods important 4 Petaurus breviceps 130 67% exudates, 33% arthropods 5 51% exudates, 49% arthropods 6 95% exudates, 5% arthropods 7 Gymnobelideus leadbeateri 145 80% exudates, 20% arthropods 8 Acrobates pygmaeus 12 eucalypt nectar and pollen 9 Cercartetus nanus 24 nectar, pollen, arthropods, fruits 10,11 Cercartetus lepidus 7 some nectar 12 Cercartetus longicaudatus 30 some nectar 13 Cercartetus concinnus 13 nectar and arthropods 14 Tarsipes rostratus 10 nectar and pollen 10 1 Smith & Russell (1982); 2 Henry & Craig (1984); 3 Craig (1985); 4 MenkhOrst & Collier (1988); 5 Smith (1982a); 6 Nagy & Suckling (1985); 7 Howard (1989); 8 Smith (1984a); 9 Turner (1984b); 10 Turner (1984a); 11 Turner (1985); 12 Green (1983); 13 Russell (1980); 14 Morcombe & Morcombe (1979).
1.2.2. Population Density and Social Spacing. The abundances of food resources will also have an effect on population densities. For example, a folivorous diet involves "a dense and relatively predictable food supply" (Clutton-Brock & Harvey 1977b). For primates, population density is positively related to the proportion of foliage in the diet whilst home range size is negatively related to this (Clutton-Brock & Harvey 1977a). Such a relationship is a consequence of the energetics of different diets as stated above. Insectivorous species will require relatively larger areas from which to obtain their food because arthropods tend to be widely dispersed resulting in lower mammal densities. Omnivorous species 5
such as exudivores have densities intermediate between folivores and insectivores. Moreover, the dispersion of food resources will influence the sociality of species. Insectivorous species tend to be solitary whereas folivorous species often live in groups (e.g. Clutton-Brock & Harvey 1977b). Waser (1981) contended that the rate of food renewal influences sociality and thus, was able to explain the enigmatic sociality of group-forming insectivorous mammals. Exudates, with high rates of renewal should also allow group formation amongst mammals. The distribution of food resources is probably most fundamental to the spatial strategy exhibited by mammals due to the economic defensiblity of such resources and the influence on social organization. For example, Terborgh (1983) found different degrees of territorial behaviour among five species of Peruvian primate. He contended that the spatial and temporal continuity of food resources determined the extent to which territorial behaviour was expressed. Territorial behaviour was favoured by species utilizing food resources which were: "relatively common, small, evenly distributed in space and displayed a high continuity in time". In contrast, species which seek out "resource bonanzas" (e.g. exceptional concentrations of fruit) "exploit them to exhaustion" so that site fidelity would be counterproductive. Thus, home ranges were ill defined and habitats were used seasonally. Potentially, different exudate resources could be perceived either way (e.g. Paton 1980, Lee & Cockburn 1985) so that the spatial strategy of exudivores may depend on the particular food items utilized. In conclusion, many of the patterns present in the behavioural ecology of animals can be explained, largely in terms of the influence of a species' food types (and their dispersion) and the interplay with body size.
1.3. EXUDIVOROUS MAMMALS. The exudivore niche is occupied by prosimian primates (ca. 9 spp) in Madagascar and Africa, simian primates in South and Central America (ca. 6 spp) (Table 1-2) and by marsupials in Australia (ca. 10 spp) (Table 1-3). These species feed, at least during part of the year, on exudates. This list is not exhaustive because there are other species such as the marsupial Antechinus stuartii, long considered an insectivore (e.g. Hall 1980, Statham 1982), which makes extensive use of nectar at certain times of the year in some habitats, but the importance of this to the overall diet is still unknown (Goldingay et al. 1987). The reason why so many Australian marsupials occupy this food niche is difficult to explain. Australian heathlands, woodlands and forests have particularly diverse 'vertebrate-pollinated' floras (Ford et al. 1979, Keighery 1982, Ford 1984). Due to the long association of the flora with the bird and marsupial fauna, many plant species may have evolved with a generalised flower morphology suited to both bird and mammal visitors (Turner 1982). Australia has the only species of non-flying 6
mammal (the honey possum) with a diet consisting solely of nectar and pollen (Turner 1982,1983). The apparent reliance by the Australian flora on vertebrate pollen vectors may have allowed a diverse array of marsupial exudivores to evolve. The consequences for pollination of nectar-feeding visits by non-flying mammals were recognised by Sussman and Raven (1978). In fact, Carpenter (1978) and Rourke and Wiens (1977) observed that certain groups of plant species possessed traits which may be more conducive to mammal pollination than to bird pollination. Early investigations into the veracity of these claims were not supportive (Hopper 1980, Hopper & Burbidge 1982) but the methodology employed may have severely underestimated the potential of mammal pollen vectors (Goldingay et al. 1987). The latter study indicated that mammals (i.e. marsupials) may indeed be the most effective pollinators at some sites. Exudivorous mammals also feed on sap, gum, manna and insect honeydew. All of these exudates undergo seasonal variations in abundance and, therefore, utilization by mammals (e.g. Smith 1982a). However, documentation of the seasonal usage of exudates is difficult because exudates are almost totally digested and leave little trace in the faeces (Smith 1982a). For the primates, 11 species at least supplement their diet with tree exudates such as sap and gum (Coimbra-Filho & Mittermeier 1977, Garber 1984). However, only three species of primates (Phanerfurcifer, Callithrix jacchus, Cebuella pygmaea ) incise trees for exudates, and three others (Microcebus murinus, Galago senegalensis, Euoticus elegantulus ) use their modified lower dentition (i.e. tooth comb) to collect gums (Coimbra-Filho & Mittermeier 1977). Two species of marsupial (P. australis and P. breviceps) regularly incise trees to obtain sap (Wakefield 1970, Smith 1982a). Leadbeaters possum (Gymnobelideus leadbeateri) and the sugar glider regularly feed on Acacia gum (Smith 1982a, 1984a, Henry 1985) with the former using its lower incisors to notch acacia trees, presumably to stimulate the flow of gum (Smith 1984a). Gum production has been examined by Smith (1982a) and Henry (1985). Henry suggested that gum was used extensively when the rate of production was highest (i.e. summer and autumn) but Smith found a high utilization of gum throughout the year. Furthermore, a strong correlation between sugar glider density and acacia density has been reported (Suckling 1984), suggesting a dependence on this resource at some sites. Two other exudates utilized by arboreal mammals are manna and insect honeydew. The former is an exudate commonly exploited by Australian honeyeaters (Paton 1980, 1982). Although, it is not known in the diets of primates it has been found in the diet of a few marsupials (e.g. Smith 1982a, 1984a, Henry & Craig 1984). It leaves no trace in faeces (Smith 1982a) and there is some ambiguity among researchers as to whether animals observed feeding are actually harvesting it (see Kavanagh 1987a, Smith 1982a). Insect honeydew is another food item whose importance has not been fully appreciated by researchers (Smith 1982a). Studies on 7
the mouse lemur (Microcebus coquereli) have revealed that honeydew may account for 50% of the diet of this animal at certain times of the year (Pages 1980, Hladik et al. 1980) but its use by other primates is less well documented. Honeydew has been found in the diets of several exudivorous marsupials (Smith 1982a, 1984a, Henry & Craig 1984) but its importance has probably been underestimated for the same reasons as that for manna. Species referred to here as exudivores feed on arthropods for dietary protein. The availability of this may influence the timing of reproduction (e.g. Smith 1982a, Suckling 1984). The smaller species often have a greater proportion of their diet comprised of arthropods than do larger species because insect harvesting rates do not increase with size but may in fact decline (Charles-Dominique 1974, Smith 1982a,b). Terborgh (1983) found that different-sized frugivorous primates devoted different amounts of time to feeding on arthropods and due to other aspects of their ecologies (e.g. group size), also had to employ different foraging strategies and utilize different substrates. Those exudivorous species that make extensive use of nectar may also be capable of digesting pollen from which they may obtain dietary protein (e.g. Turner 1984a,b, Goldingay et al. 1987) but adaptation to low protein avalability may have led to some species having reduced requirements for nitrogen (Smith & Green 1987).
1.4. OBJECTIVES OF THE THESIS. This thesis examines in detail, at two sites, the diet of the yellow-bellied glider (Petaurus australis). This diet has been treated in such detail (Chapters 2,5) because previous studies on this species have not examined it adequately, primarily due to the methodological problems outlined in Chapter 2. One aspect of the diet, the sap feeding behaviour, has received specific investigations (Chapter 3), because many aspects of this behaviour appear enigmatic. The foregoing discussion has suggested the importance of the distributional properties of food resources. The selection of two sites, containing quite different forest habitats, allowed investigation of the spatial and temporal components of food resource abundance and how this may affect the foraging behaviour and the socioecology of gliders. Chapters 2,3 and 4 form the basis of the published papers contained in the Appendix. 8
Chapter 2.
THE FEEDING BEHAVIOUR OF THE YELLOW-BELLIED GLIDER, Petaurus australis, AT BOMBALA.
2.1. INTRODUCTION Although studies have shown that diet has an important influence on a mammal's overall biology (e.g. McNab 1983), little is known about the feeding ecology of many Australian species. The yellow-bellied glider (Petaurus australis), which weighs up to approximately 700g (Chapter 6), is the largest of the arthropod- and exudate-feeding marsupial gliders (see Smith & Lee 1984). It has a widespread but patchy distribution in eastern Australia and is characterized by low population densities (Henry & Craig 1984, Kavanagh 1984). It has been difficult to study in the field owing to difficulties in detection and capture (Craig & Belcher 1980), and until recently, relatively little research had been centred upon this species. Wakefield (1970) described the 'V'-shaped incisions made by yellow-bellied glider into the trunks of various species of eucalypt to obtain sap. However, he concluded that arthropods comprised the bulk of the diet. This conclusion was based on limited feeding observations and the irregular occurrence of these 'sap-site' trees. Smith and Russell (1982), Henry and Craig (1984) and Craig (1985) conducted faecal analyses on samples from north Queensland and Victoria respectively. These studies found the presence of arthropods, eucalypt sap, nectar and honeydew. However, insect and plant exudates are almost totally digested and leave little trace in the faeces. Indicators must therefore be used to infer their use (Smith & Russell 1982). For example, bark is used as an indicator of eucalypt sap. Therefore faecal analysis does not allow a precise determination of the relative importance of each dietary item. Henry and Craig (1984), Craig (1985), Kavanagh and Rohan-Jones (1982) and Kavanagh (1987a,b) made qualitative observations upon feeding gliders (i.e. each observation is scored equal, regardless of duration) but again these data indicate only the presence or absence of food items in the diet. Thus, a study employing the use of timed (i.e. quantitative) feeding observations is necessary to give a better resolution of the species dietary requirements. This study was aimed at achieving this by addressing the following question: are different food resources exploited in different proportions throughout the year?
2.2. METHODS.
This study was conducted at Waratah Creek (37°01'S, 149°23'E), in the Coolangubra State Forest, approximately 20 km southeast of Bombala, New South <4
Fig. 2-1. Location of study sites at Bombala (B) and Kioloa (K). The dashed line indicates the approximate distribution of Petaurus australis. After Strahan (1983). Wales (Fig. 2-1.). The study area contained six species of eucalypt (Eucalyptus radiata, E. viminalis, E. fastigata, E. obliqua, E. ovata, E. cypellocarpa). See Chapters 6,7 and Kavanagh (1984) for further details. Thirteen field trips were conducted at the following times:- 9-18 January, 2-12 April, 13-18 May, 22 June-1 July, 30 August- 3 September, 28 October- 1 November, 3-9 December 1984; 2-8 February, 15-24 April, 8-14 July, 2-8 September 1985; 5-17 January and 23 June- 5 July 1986. Gliders were trapped in the study area and ear-tagged with coloured reflective tape to enable assessment of the number of individuals observed during each field trip (see Chapter 6). Yellow-bellied gliders were located with a 12V 100W spotlight. Initial location was greatly facilitated by their extraordinary vocal behaviour (Kavanagh & Rohan-Jones 1982). After locating a glider, it was followed for as long as possible (up to 3hr in 1984 but often for an entire night in 1985 and 1986; see Chapter 4) and observed with a 55W 'red' spotlight and a pair of binoculars. All feeding activities were timed to the nearest 1/2 min and recorded on tape. Observations commenced at dusk (when the gliders left their dens) and continued until approximately 0300h unless followed for an entire night. During each field trip except December 1984, at least one observation period was conducted throughout the night.
2.2.1. Feeding Behaviour. A total of 122.4 hr was spent observing feeding by yellow-bellied gliders. The following feeding behaviours were identified on the basis of the spotlighting observations. Daytime observations of the substrate at which gliders were observed foraging were made in order to confirm the identity of the food types being ingested. Eucalypt sap feeding:- gliders were observed clinging to the trunks of eucalypts and licking at the 'V-shaped incisions they had made into the bark. Licking was interspersed with relatively short bouts of bark gouging to extend the incisions or create new ones. Honeydew feeding:- gliders were presumed to be harvesting honeydew when engaged in branch- and leaf-licking activities (Smith 1982a). Honeydew is the substance excreted by sap-sucking insects and, as found in the study by Smith (1982a), was produced at Bombala by coverless psyllids concealed under the bark of eucalypts and by scale insects present on the smaller branches and leaves of eucalypts. Scale insects were clearly seen with binoculars and were present on the leaves occasionally discarded by gliders when leaf-licking. Trees containing psyllids were uncommon and could be distinguished by the blackening of the branches (owing to a mould growing on the bark) under which the psyllids were living. One blackened branch collected from a E. cypellocarpa regularly used for brach-licking showed that these insects were common under the bark. Arthropod feeding:- gliders were observed to harvest arthropods by peeling 11
back eucalypt bark and by searching through (gleaning) clumps of foliage. Bark arthropds were harvested in three different ways; by peeling back the bark being shed by the tree and consuming any exposed arthropods (Craig 1985, Kavanagh 1987a), by searching through and breaking open the bark ribbons which had accumulated in the forks of E. viminalis and by shredding the rough bark of E. fastigata in search of beetle larvae (Kavanagh 1987a). Manna feeding:- This behaviour consisted of biting and licking the small branches and leaves of eucalypts (Kavanagh 1987a). Manna is the crystaline sap which forms at sites of insect damage on leaves and branches (Smith 1982a). Leaves and small branches were often discarded during feeding and examination of these showed the remains of manna. Nectar feeding:- gliders were observed climbing amongst the canopy of eucalypts and drawing clumps of flowers toward the mouth so that these could be licked.
2.2.2. Indices of Food Availabilty. Owing to the large home range of these gliders (34-88 ha; Chapter 7) and the complexity of the forest habitat, it was only possible to collect indices of food availability at regular intervals. Sap flow measurements were made during each trip, and this forms the basis of Chapter 3. Within lOOha of the forest, a grid with 100m intervals had been laid out for a previous study (see Kavanagh 1984). Within this area, 150 tagged trees (out of the 250 used by Kavanagh 1984, 1987a) were visited during each sample period between February 1985 and July 1986, and scored for the number of flowers present and the amount of bark being shed. The invertebrates harvested by gliders at other localities were predominantly those that live beneath the smooth bark of eucalypts (Henry & Craig 1984, Craig 1985, Goldingay pers. obs.). These arthropods become available to gliders only when the smooth bark is being shed. Gliders also harvest honeydew produced by psyllid nymphs which live under this bark (Henry & Craig 1984, Goldingay pers. obs.). The availability of this food resource (i.e. arthropods and honeydew) is therefore determined primarily by the bark-shedding pattern of the eucalypts. To assess the change in the abundance of shedding bark, each marked tree was given a score (0 = 0-10%, 1 = 10-30%, 2 = 30-50%, 3 = 50-70%, 4 = 70-100%) based on the proportion of 2m sections of smooth bark on the trunk and branches which had peeling bark present. This index was averaged for each species to give an abundance index. Flower abundance was estimated by counting the number of flowers in a recognizable canopy unit and multiplying this by the number of such units in the entire canopy (Kavanagh 1984, 1987a). Kavanagh (1987a) provides data on this for this site for May 1981-January 1985. The E. cypellocarpa producing honeydew could be readily identified because of the blackening of branches caused by a mould growing on the bark in the sugary exudate (see above). Five such trees (identified in 1984) were examined during each trip between April 1985 and July 1986 and the number of blackened branches on these trees was scored as an index of honeydew abundance. Eleven E. cypellocarpa used for flower- and bark-shed scores were also examined for blackened branches during each of these field trips.
2.3. RESULTS. 2.3.1. Eucalypt Sap. Two species of eucalypt were frequently incised by yellow-bellied gliders at Bombala to obtain sap. The sap of E. viminalis accounted for 94% of the feeding observation time (FOT) during January 1984, 1% in February 1985, 83% in April 1985 and 3% in January 1986 and 14% in July 1986 (Fig. 2-2). Eucalyptus fastigata sap accounted for 44% of the FOT during May and 58% in June and 48% in January 1986. Fresh incisions were observed on E. viminalis during the Oct./Nov. 1984 field trip, suggesting that sap had been harvested prior to this time. One glider group, consisting of 4-6 individuals, made almost continual use of E. fastigata sap (suggested by relatively fresh incisions) from May through to December 1984 (pers. obs., Kavanagh 1987a). However, frequent checks on these sap-site trees (4 individual trees) during the last three field trips in 1984 did not reveal gliders feeding. Within the home range of a group of gliders, only a small number (3-6) of each of these two eucalypt species was incised for sap, although each species was very abundant. This aspect of their feeding behaviour is treated in greater detail in Chapter 3.
2.3.2. Honeydew. This activity varied seasonally from 0% of the total observed feeding time in July 1985 and January 1986 to 68% in July 1986 (Fig. 2-2). It was a more common feeding behaviour in winter in two of the years of this study. It was absent during the winter of 1985 but only two gliders could be located on one night so that these data may not be indicative. Two types of honeydew were harvested. One type, produced by hemipterans (Family Psyllidae) living under the bark of E. cypellocarpa was responsible for 65% of the honeydew feeding observations in April, 76% in May, 49% in June and 87% in Aug./Sept. 1984, 85% in April 1985, and 21% in July 1986. Gliders harvested this type of honeydew only by branch-licking. These observations were principally made upon one group of gliders (January 1984-July 1985) which utilized four E. cypellocarpa for this resource. Another group used E. ovata in the same manner to obtain this type of honeydew but to a lesser extent. The areas from which gliders I •§
o fftD « a> I W < I S Z ini^Qi
o(-. rt rt rt ,H r/n on so- so >. PQ T.53 ,—^l ft >* A §e f on o rt 1) TJ c o o o o o o £ Q •£ o CO (£> T 1— to T3 H Q) aiuii uojiBAjasqo jo % anim a obser- v No . o f harvested this type of honeydew were characteristically blackened (see above) and droplets of honeydew could often be seen on this substrate glistening in the spotlight beam. Also, in June/July 1986 76% of the honeydew feeding was on the outer branches of E.fastigata where gliders (of another glider group) licked honeydew produced by psyllids under the bark. At no time while feeding would gliders have contacted the psyllids producing this honeydew as these would have been protected by the overlying bark. The second type of honeydew was produced by scale hemipterans (Family Coccidae) living on the outer branches and leaves of E. fastigata, E. obliqua, E. viminalis and E. radiata. Utilization of this coccid honeydew (by branch and leaf-licking) was significant during May, June, Aug./Sept., Oct./Nov. and December 1984 when it comprised 9%, 51%, 13%, 96%, and 100% of the total honeydew feeding observations respectively. During Oct./Nov. 1984, February and April 1985, gliders harvested honeydew only from the foliage of E. radiata where it could be seen glistening in the spotlight beam. Some ingestion of these insects would be expected during this feeding activity. 2.3.3. Arthropods. Little time was spent harvesting arthropods during January, October, December 1984, February, April 1985 and January 1986 (Fig. 2-2). However, this changed dramatically at certain times of the year. In April 1984 and July 1985 bark-peeling accounted for 86% and 98%, respectively, of the observed feeding time. This feeding activity was concentrated on E. fastigata in April but E. viminalis in July. During Aug./Sept., Oct., Dec. 1984, February, Sept. 1985 and January 1986, gliders were observed peeling back the back of E. radiata, E. viminalis and E. ovata and licking along the exposed surface. Licking of the branch was not observed at other times of bark peeling. This behaviour accounted for 36%, 61%, 35%, 97%, 49% and 25% of the observed feeding times respectively. Eucalyptus radiata accounted for most of the observation time during Aug./Sept. 1984 and examination of recently felled E. radiata nearby showed a large abundance of psyllids beneath bark being shed from the upper branches. Each psyllid had an associated droplet of honeydew so that gliders were probably ingesting both honeydew and arthropods simultaneously. Eucalyptus ovata accounted for all of these observations during Oct./Nov. and December 1984. This species was shedding bark from its entire surface and examination of recently fallen trees displaying bark-shed showed an abundance of psyllids and also other arthropods, in particular Coleoptera. Eucalyptus viminalis accounted for most of these observations in February 1985 and January 1986. During May 1984, 22% of the observed feeding time was spent gleaning arthropods from the foliage of E. viminalis. This activity consisted of systematically searching through the foliage, rapidly drawing clumps of leaves toward the nose and eyes for inspection. This behaviour was very different to that associated with harvesting honeydew or manna from foliage. 2.3.4. Manna. Gliders were only observed gleaning manna from the smaller branches and leaves of E. viminalis. This occurred during December 1984 and January 1986 when this activity accounted for 29% and 24% of the observed feeding time, respectively (Fig. 2-2). Observations were made on two gliders in 1984 in one tree which they visited on at least two consecutive nights. Similarly, in 1986, one tree accounted for all observations and this tree was visited on consecutive nights. Manna was harvested in a similar fashion to that of the sugar glider (Petaurus breviceps) (Smith 1982a), spending long periods within a clump of foliage, examining leaves individually, licking them, but also nipping the manna off from along the finer branches. This feeding activity was similar to the second type of honeydew feeding but examination of discarded branchlets clearly showed the remains of manna and not hemipterans. These two gliders remained within this tree for at least three hours, foraging and occasionally grooming. Two feathertail gliders (Acrobates pygmaeus) and at least two sugar gliders were also observed in this tree feeding upon manna during this observation period. 2.3.5. Nectar. At various times during the study, all eucalypts flowered in the study area (Kavanagh 1984, 1987a). Certain individuals of all of these species showed an abundance of flowers and presumably also nectar. However, only during June/July 1986 were observations made of gliders using this resource, although on numerous occasions they were observed foraging in trees adjacent to these flowering individuals. During 1984, E. ovata flowered lightly in the study area during October-December, but only 1 min of nectar feeding was observed and that occurred in December. Other trees which flowered in 1984 were apparently ignored by foraging gliders. One E. viminalis was in flower in June/July 1986 and the two gliders in the area made extensive use of it, visiting it on consecutive nights. 2.3.6. Overall Diet. The diet of the yellow-bellied glider at Bombala consisted at times almost exclusively of plant and insect exudates (Fig. 2-2). Exudates (sap, honeydew, manna and nectar) accounted for 63.1% of the feeding observation time (FOT) during the whole study (122.4h) while arthropods alone made up 14% of FOT. However, a further 22.9% of the FOT was of gliders peeling back loose shedding bark during which they harvested arthropods and honeydew together but the proportion of each could not be determined (see above). If it is assumed that each were harvested in equal proportion then exudates account for 74.6% of FOT and arthropods 25.4%. Only during April 1984 and July 1985 did arthropods feature as a main item in the diet. At othertimes i t formed a consistent but minor portion of the diet. 2.3.7. Food Resource Indices. Kavanagh (1984, 1987 a) provided details of flowering and bark shed at this site for November 1981-January 1985. During this time nectar was usually seasonally abundant at Bombala and relatively evenly dispersed but during the 18 months when its abundance was quantifiedin this study (February 1985-July 1986), only seven of the 150 marked trees were observed to possess flowers. All of these were in February 1985 and averaged approximately 500 flowers each. Observations of nectar feeding were few and apart from 1 min in December 1984, were made only during June/July 1986 (Fig. 2-2) when one E. viminalis, heavily laden with flowers (ca. 16,000 flowers), was visited regularly by one pair of gliders. This was the only flowering tree seen in the study area. Table 2-1. Seasonal changes in the abundance index (ranging from a minimum of 0 to a maximum of 4) of loose shedding bark (see text for determination of the index) on six species of eucalypt (species names have been abbreviated). Numbers of trees monitored are in parentheses beside species. Numbers in parentheses beside indices represent the proportion (%) of trees with >10% bark shed scores. 1985 1986 February April July Sept January June/July Species E.v. (39) 1.1 (64) 0(0) 0(3) 0 (0) 0.8 (59) 0(0) E.r. (45) 2.3 (82) 0.4 (27) 0.1 (7) 0.9 (56) 0 (2) 0.1 (7) E.f. (20) 2.6 (95) 0.3 (25) 0(0) 0.1 (10) 0(0) 0 (0) Ex. (12) 1.2 (50) 0.3 (17) 0.4 (8) 0.6 (25) 0.1 (8) 0.1 (8) E.ov. (21) 1.4 (71) 0.6 (29) 0.6 (43) 0.4 (29) 0.5 (29) 1.4 (57) E.ob. (13) 1.6 (54) 0.2 (15) 0.1 (8) 0.5 (31) 0.1 (8) 0 (0) Bark-shedding by eucalypts in the study area was spread across the year with substantial overlap between species (Table 2-1). These data corroborate those of Kavanagh (1987a) for earlier years and show that during any visit, some shedding bark could be observed on individuals of several species and at least one species had a large proportion of individuals with >10% bark-shed. Furthermore, E. viminalis, which has a very narrow period of bark-shed in summer, retains the bark in ribbons (after being shed) on its major lateral branches, providing further substrate for invertebrates (Smith 1982a, Henry & Craig 1984, Goldingay pers. obs.). These may persist for more than one year so that arthropod abundance from this substrate is probably not markedly seasonal (e.g. Smith 1982a, Henry & Craig 1984). Eucalyptus radiata and E. obliqua shed bark only from their smaller branches which probably provides a substrate for honeydew-producing arthropods only. Insect honeydew was a resource which was extremely difficult to quantify. It was mainly obtained by licking the branches of a few trees (15-40m above the ground) which appeared to be highly productive for this resource, particularly during autumn and winter in 1984 (Fig. 2-2). The availability of honeydew changed during the year but average scores of its abundance were generally low due to a protracted bark shedding pattern by these individuals greatly reducing the number of suitable branches at any one time. Trees, when observed in use by gliders, had values much higher than these average scores. One tree in April 1985 had 23 blackened sections and a new tree located in July 1986 had 70 sections. The trees tagged for flower counts and bark shed scores showed little if any branch blackening (Table 2-2). Table 2-2. Honeydew abundance index represented by the mean number of 2m blackened tree sections for five E. cypellocarpa used extensively by gliders for honeydew in 1984 and 11 trees not used. 1985 1986 April July Sept Jan June/July Honeydew trees 10.2 • 11.8 5.4 4.8 7.2 Trees not used 0 0.3 0 0 0 Gliders were observed to harvest manna from only two E. viminalis (one in December 1984 and one in January 1986). The availability of this resource could not be assessed but this observation suggests that it was highly seasonal and patchy in distribution. 2.4. DISCUSSION. The diets of many of the arthropod and exudate-feeding arboreal marsupials have been investigated during the last few years. These have included: P. breviceps (Smith 1982a, Howard 1989), P. australis (Smith & Russell 1982, Henry & Craig 1984, Craig 1985, Kavanagh 1987a,b), P. norfolcensis (Menkhorst & Collier 1988), A. pygmaeus (Turner 1984a), Cercartetus nanus (Turner 1984b), and Gymnobelideus leadbeateri (Smith 1984a). Only Smith (1982a) and Howard (1989) combined quantitative feeding observations (i.e. where feeding behaviours are precisely timed) and faecal analysis. The remainder employed faecal analysis and/or qualitative feeding observations (i.e. where feeding behaviours are scored equal regardless of duration). The latter techniques will allow determination only of the presence or absence of items in the diets, not the proportions of such items. Thus, an assessment of the diet using qualitative feeding observations may not be indicative unless large numbers of such observations are obtained. Faecal analysis does allow quantification of the arthropods ingested but not of exudates, which leave little trace (Smith & Russell 1982). Quantitative feeding observations, such as those employed in this study, allow seasonal variations in resource use to be more accurately assessed, giving a better understanding of how these species utilize their environment. However, feeding observations also have associated biases. For the yellow-bellied glider, the main difficulty is in the detection of individuals in the field owing to their large home range, rapid cross-country movement and the species' shyness of being spotlighted. These factors limited the number of individuals which could be observed during each field trip. For the yellow-bellied glider, the difficulty in capturing individuals will restrict the number of faecal samples for analysis. Henry and Craig (1984) analysed the diet based on faecal samples for nine seasons from autumn 1980 through to winter 1983. For four of the seasons they had only one or two samples, which may not be representative of feeding preferences. Smith and Russell (1982) had samples for four months in 1979. One month had two samples and another had four. Both studies augmented these data with opportunistic observations on gliders feeding. Henry and Craig (1984) used direct observation to support the faecal analysis but inconsistencies were apparent. Craig (1985), with more samples, realised the futility in this and lumped all samples in spring/summer and autumn/winter for all years. Thus for yellow-bellied gliders at least, there are severe limitations to diet determination from faecal analysis. Sap, honeydew and arthropods were found to be the major dietary items of yellow-bellied gliders at Bombala (Fig. 2-2). Nectar was a notable omission from the diet (except in July 1986) although flowering eucalypts were present in the study area during many field trips. During previous years, E. ovata has flowered prolifically during winter and spring, and its nectar was considered to be an important dietary item (Kavanagh 1984, 1987a). However, during 1984 there were few individuals flowering, and only with low intensity (Kavanagh 1987a). Henry and Craig (1984) suggested that only the larger-flowered eucalypt species are utilized for nectar. However E. cypellocarpa flowers, which were used in Victoria (Henry & Craig 1984, Craig 1985) and at Eden, N.S.W. (Kavanagh 1987b), were totally ignored at Bombala. Also the smaller-flowered E. viminalis was used only once. At Bombala, gliders displayed a marked seasonal variation in the use of their food resources. Sap, arthropods, honeydew and manna were predominantly exploited by gliders during some months but were virtually absent from the diet during others (Fig. 2-2). For example, E. viminalis sap was the main constituent in the diet during January 1984 but was not used again until April 1985. This pattern of seasonality is in agreement with that of other researchers in south-eastern Australia and appears to be largely determined by the abundance and seasonal availability of food resources. It appears, based on the limited data of food item abundance, that all items tend to vary seasonally in their availability, but although they may be quite productive, they are often patchily dispersed. For example, the major group of gliders observed between January 1984 and July 1985 was observed to harvest sap from only six trees, honeydew (by itself) from six trees, manna from one tree but arthropods and arthropods/honeydew from more than 100 trees. This indicates that specific trees are very important to the energetic requirements of these gliders. Only a very few individuals of certain species of eucalypt are utilized for sap feeding (Wakefield 1970, Craig & Belcher 1980, Henry & Craig 1984). Consideration of the influences on sap feeding have been treated more fully in Chapter 3. The sap-site trees at Bombala were heavily scarred and have probably been utilized for many years. The condition of these trees does not appear to have been adversely affected by the activities of gliders. Honeydew has been an underrated food resource in the diets of non-folivorous arboreal vertebrates (Smith 1982a). The Madagascan prosimian Microcebus coquereli feeds upon honeydew produced by hemipterans and at times, this may account for 60% of its feeding time (Petter 1978, Hladik et al. 1980). In Australia, honeydew is frequently harvested by honeyeater birds (Paton 19-80). Sugar gliders and Leadbeaters possums are also known to harvest honeydew but it has been considered to account for only a small proportion of the diet (Smith 1982a, 1984a). At Bombala, honeydew was often found to account for 30-68% of the observed feeding time of yellow-bellied gliders. Smith and Russell (1982) did not find this resource important for gliders in north Queensland possibly because faecal analysis may underestimate its relative importance. Whether the availability of honeydew varies between sites is not accurately known at present. The presence of hemipterans in the faeces has been used by researchers to indicate the use of honeydew but when gliders were harvesting the psyllid honeydew in this study by branch-licking, it is unlikely that these insects would have been ingested as the psyllids remained beneath the bark. Henry and Craig (1984) and Craig (1985) suggested that honeydew was more important at Cambarville than at Glengarry North. However, the use of honeydew has probably been underestimated at both these sites if it can be harvested without ingestion of the 20 psyllids. During June 1984 at Bombala, one group of gliders appeared to specialize on this resource while a neighbouring group made a greater use of the sap of E. fastigata. During three nights of continuous rainfall, the group specializing on honeydew remained within their den for most, if not all of that time (determined by observing the den for 3 hr after dusk and radio-tracking one glider, Goldingay and Kavanagh unpubl. data), presumably because honeydew is washed away by rain. However, the group feeding upon sap continued to do so for part of this time. The availability of honeydew at Bombala appeared to be greatest during autumn and winter. Its availability will be influenced by two major factors in addition to weather, as stated above. Firstly, the abundance and life cycles of the hemipterans producing the honeydew. Some species only have one life cycle during the year while others have many (White 1971). This can result in a seasonal or continuous availability of this resource (Paton 1980) as honeydew will not be produced during all phases of the life cycle. For example, Paton (1980) found that the honeydew-producing psyllids were more common during autumn and winter. Secondly, the honeydew-producing psyllids living beneath the bark of the eucalypts will become exposed and possibly removed when this bark is shed. Consequently the small number of E. cypellocarpa which were frequented by gliders from April through to September were apparently not visited in Oct./Nov. and December 1984 when the bark had been shed. In 1985, these trees shed their bark earlier and were not used with the same intensity as in 1984. Also, gliders were observed to harvest these psyllids and the associated honeydew when the smooth bark was being shed from E. ovata and E. radiata. Manna was harvested by gliders during only two sample periods, both in summer. Paton (1980) found that manna was available on E. viminalis foliage in summer and early autumn and commonly 50% of trees sampled had it. Manna can be produced at rates equivalent to those for nectar (Basden 1965, Paton 1980) and the large amount of time gliders spent harvesting this resource on consecutive nights (mean = 125 min, see Chapter 4) suggests that it was also highly productive at Bombala. In fact, observations of the substrate from which it was harvested (i.e. the discarded branchlets showing where the gliders were nipping off the manna) indicated that harvesting of the manna actually facilitated its production. The manna formed at the cuts made by the gliders as well as at sites of insect or mechanical damage (see Basden 1965, Smith 1982a). Eucalypt sap, honeydew and manna are composed mainly of various sugars and contain little or no protein (Basden 1965, 1966, Paton 1982, Stewart et al. 1973). Therefore arthropods or pollen need to be harvested to meet the protein requirements of the yellow-bellied glider. At Bombala, gliders harvest arthropods principally by peeling back loose shedding bark or by searching through hanging bark ribbons which 21 persist on the trunk and branches of E. viminalis. Loose bark, being shed from the smooth trunks and branches of eucalypts, is an important substrate,rich in arthropods and associated carbohydrates (i.e. insect honeydew), (Recher et al. 1983, 1985, Henry & Craig 1984, Goldingay pers. obs., Kavanagh 1987b) and for the present study accounted for 23% of the total feeding observation time. The value of this resource may be greater during winter as many arthropods, in particular coleoptera, overwinter under bark (Smith 1982a, Recher et al. 1983, pers. obs.). However, the usefulness of this substrate will be determined by the bark-shedding pattern of the different tree species. In the present study there was always some trees which had loose bark present (with attendant arthropod fauna) and different species tended to have staggered patterns of bark shed (see also Kavanagh 1987a). However, E. viminalis showed a more synchronised bark shed than any other species and probably provides a very abundant resource. The low rates of renewal of arthropods (Smith 1982a, Henry 1985) probably requires that gliders must forage over large distances to meet their protein needs. Gliders often harvested arthropods when gliding to major resource trees such as sap-site trees and manna trees. This is similar to the behaviour of some frugivorous primates which supplement their diet with arthropods harvested whilst moving between fruiting trees (Terborgh 1983). Only during May were gliders observed to glean arthropods from the foliage of eucalypts and this was confined to E. viminalis. Arthropod abundance upon eucalypt foliage has been shown to be typically low by a number of researchers (Smith 1982a, Henry & Craig 1984, Woinarski & Cullen 1984). Therefore sap and honeydew may have been in abundance at this time which might enable gliders to forage for arthropods at an energy loss so that they could obtain protein. One of the three gliders observed engaging in this activity was a lactating female which presumably required an increased protein intake. Paton (1982) found that new holland honeyeaters often foraged for insects at an energy loss throughout the-year in order to meet their protein requirements. Surprisingly gliders did not forage for flying insects although these were present at various times of the year. On numerous occasions, large moths were observed flying close to yellow-bellied gliders but these were totally ignored while sugar gliders in the same tree would attempt to capture them. Henry and Craig (1984) similarly reported the reluctance of yellow-bellied gliders to attempt to capture flying insects. This activity may be energetically too expensive for the protein rewards. This study has confirmed the conclusion of Smith and Russell (1982) that the yellow-bellied glider does rely heavily upon exudates. In their study, eucalypt sap was considered to be the main dietary item. At Bombala, honeydew has been found to be of equal importance to sap and therefore it is questionable whether previous studies of the yellow-bellied glider have not in fact, underestimated the importance of honeydew in the diet. Chapter 3. INFLUENCES ON THE SAP FEEDING BEHAVIOUR OF THE YELLOW-BELLIED GLIDER, Petaurus australis. 3.1. INTRODUCTION. The utilization of tree sap (i.e. phloem sap) as a food resource has been documented for several groups of vertebrates. The best known is that by the yellow-bellied sapsucker (Sphyrapicus varius), a species of woodpecker which drills holes into the trunks of various tree species in order to obtain sap (Kilham 1964). Other vertebrates which incise trees to obtain sap are a few species of marmoset (Coimbra-Filho & Mittermeier 1976, 1977, Ramirez et al. 1977, Fonseca & Lacher 1984, Lacher et al. 1981,1984, Rylands 1984) and two species of gliding marsupial, Petaurus australis and Petaurus breviceps (Fleay 1947, Wakefield 1970, Smith 1982a, Smith & Russell 1982, Chapter 2). Phloem sap is rich in sugar, primarily sucrose (Crafts 1961, Stewart et al. 1973) and can provide a significant amount of food for these animals (e.g.Tate 1973, Smith & Russell 1982, Lacher et al. 1984, Chapter 2). Although sap feeding by these vertebrates has been documented for some time, there has been little attempt to quantify this behaviour. Furthermore, the factors governing selection of particular trees (referred to as 'sap-site' trees) are poorly understood and the response of these trees to incising has not been adequately examined. Sap feeding by S. varius is believed to be facilitated by the wounding of the trees by these birds which stimulates sap flow (Kilham 1964). Moreover, the flow of sap induced by S. varius has been found to be greatest during the day when these birds feed (Sutherland et al. 1982). The yellow-bellied glider (Petaurus australis) is an arboreal marsupial which feeds predominantly on plant and insect exudates such as sap, manna, honeydew and nectar (Smith & Russell 1982, Henry & Craig 1984, Chapter 2, Kavanagh 1987a,b). It obtains sap by cutting 'V-shaped notches (Plate 3-1) into the trunks of certain eucalypts with its procumbent lower incisor teeth (Plate 3-2) (Fleay 1947, Wakefield 1970, Smith & Russell 1982). Its sap feeding behaviour appears enigmatic because only a very small number of trees of certain species are selected. These trees are used periodically during the year in southern Australia (Wakefield 1970, Craig & Belcher 1980, Henry & Craig 1984, Craig 1985, Kavanagh 1984, Chapter 2). In contrast, gliders feed on sap throughout the year in north Queensland (Russell 1980, 1981, 1984, Smith & Russell 1982) but not all trees are used concurrently (Russell 1981, R. fp 5t •MJBMB H9HH • ^ -OFM . Plate 3-1. Typical 'V'-shaped incisions made by the yellow-bellied glider (Petaurus australis) on a Eucalyptus saligna. Note the claw marks surrounding the incisions. Plate 3-2. Lower incisors of a yellow-bellied glider which are used to cut into the trunks of eucalypts in sap feeding. 24 Russell pers. comm.). The basis for tree selection and periodic usage is unknown. Early examination of sap feeding by the yellow-bellied glider (Wakefield 1970, Craig & Belcher 1980) was confined to documenting the species of eucalypt incised and authors offered no explanation for the underlying causes of the specificity. In fact, Wakefield demoted the importance of sap feeding by concluding that it "evidently constitutes the least important of the gliders' food-getting operations". This was later questioned by Smith and Russell (1982) who concluded that the bulk of the gliders' energy requirements was satisfied by eucalypt sap. They however, offered no account of whether the diet of gliders in north Queensland was typical of that at other sites with respect to the relative utilization of different food resources. Russell (1980) considered sap a staple in some months and observations of the regular use of sap by gliders led him to suggest that sap-site trees may act as meeting places for glider social interactions. Moreover, he observed that one of the sap-site trees, which are few in number, may be used more frequently and may accommodate several gliders. However, those group members which failed "to secure a good feeding site .... visit other feeding trees [sap-site trees] where fresh incisions ooze sap just as freely as those on the most used tree". The inference from his observations is that the sap-site trees were equivalent (although sap-sites per se may vary in utility) but that regular use of particular trees facilitated social interaction. Henry and Craig (1984) suggested that the species of tree selected was related to its ability to produce a flow of sap when the tree was incised with a chisel but they did not account for selectivity among trees within a species. Craig (1985) stated that the sap-site trees were particularly vigorous individuals. This observation has been verified by Mackowski (1988) using measures of cambial electrical resistance (which reflect some nebulous physiological parameter) but he noted that many such individuals were ignored for sap feeding by gliders. More recently, further observations by researchers have resulted in a reconsideration of the sap feeding behaviour. Two general hypotheses have been advanced to account for the sporadic occurrence of sap feeding. They are: i) the availability of alternative food resources (R. Russell 1984, Kavanagh 1987a) and, ii) the incidence of rain (R. Russell 1984, Kavanagh 1987a). The latter hypothesis implies that it is less costly energetically for a glider to feed on sap than to forage actively for other food types during rain. Russell's (1980) suggestion above (i.e. social facilitation) is the only explanation to date which has attempted to account for the use of a small number of trees. Site differences among sap-site and non sap-site trees appear unlikely to account for the selectivity. All sap-site trees located by Craig (1985) occurred mid-slope. 25 Kavanagh (1987a) invoked site differencs to account for differences in the species of eucalypt used in coastal and tablelands forest in southern N.S.W. but such an explanation does not account for the observed differential use of sap-site trees themselves (Henry & Craig 1984, Craig 1985). Henry (1985) examined the sap-sugar concentration of both sap-site trees and non sap-site trees using a hand-refractometer and investigated the effect of difference in tree girth and species of eucalypt on this parameter. He observed no relationships. Kavanagh (1987a) found no relationship between the timing of sap feeding by gliders and the 'flushing' of new leaves by the species incised. Thus, to date, there is no unifying hypothesis to account for this seemingly enigmatic behaviour. The parameter related to sap which is most obviously worthy of examination is sap-flow. Many exudivorous vertebrates respond primarily to the quantity or abundance of their food resources rather than the quality (e.g. Paton 1985). Arguments involving optimal foraging theory could be invoked to explain this (e.g. Pyke 1978a, 1981). Hummingbirds respond to changes in nectar concentration (see Hainsworth & Wolf 1976, Gass 1978, Wolf & Hainsworth 1983) but the influence of exudate quality would be expected to be more pronounced for vertebrates of small body size which would be disadvantaged by filling their crops or stomachs with lower quality food resources if higher quality resources are available. Thus it seemed reasonable that gliders may feed on sap when this resource was most abundant. However, if sap flow is relatively invariable and sap feeding is determined by the availability of alternative food resources then there may still be detectable differences in sap flow among sap-site and non sap-site trees. Therefore, a third hypothesis that sap feeding is influenced by the sap flow in sap-site trees can be postulated. Sap composition may also vary in response to glider sap feeding and may in fact be used by trees as a mechanism to deter such possibly destructive feeding behaviour by gliders. However, it seems unlikely that trees could mobilise toxins quickly enough to avoid losses to such feeding. Moreover, the pattern of gliders repeatedly utilising the same few trees for sap feeding (see Chapter 2) is inconsistent with such an explanation that trees may 'forcibly' conclude glider sap feeding periods. The production of kino (containing polyphenols) to block sites of injury appears to be the only mechanism available to these trees and this may take several weeks (e.g. Smith 1982a, Mackowski 1988). The objective of this chapter is the resolution of what determines the sap feeding pattern of P. australis by examining the three hypotheses outlined above. This chapter is presented in two parts. Firstly, data were collected on sap feeding and sap measurements at Bombala (this study has been published; see Appendix 1). Secondly, data were collected on sap feeding at Kioloa and, sap measurements from Kioloa and 26 another site, Callala Beach. This second part was designed to test the generality of conclusions obtained from the research at Bombala. 3.2. SAP FEEDING BY THE MARSUPIAL Petaurus australis: AN ENIGMATIC BEHAVIOUR? 3.2.1. Methods. 3.2.1.1. Feeding Behaviour. Observations were conducted on P. australis in the Coolangubra State Forest, Bombala, N.S.W., Australia (37°01'S,149°23'E) from September 1983 - July 1986. Gliders are strictly nocturnal and were observed with binoculars at night using a 12V 55W spotlight. The duration of all their feeding activities were timed to the nearest 1/2 min and recorded on tape (see Chapter 2). 3.2.1.2. Sap Measurements. Eight Eucalyptus viminalis trees which had been heavily incised by P. australis for sap were located during 1984/85 (see Chapter 7 for location). These trees occurred within the home ranges of three groups of P. australis and were widely dispersed through a study area occupying approximately 150ha. During field trips from February 1985- July 1986, these eight trees (only seven were measured in February) were each incised with a 'V shaped 23cm metal peg measuring 1.2cm in width and 4mm in depth. This peg was hammered up into the smooth bark of the trunk at approximately 45°, to a depth of 1.5cm. Because of the small size of the incision, only a small quantity of sap exuded and collected on the peg. Sap flows usually ceased within 5 minutes. The volume of sap that exuded was measured with a lOul capillary tube and was assayed for sugar concentration using a 0-50% Brix temperature-compensated hand refractometer. The latter measurement was considered a reasonable index of sugar concentration because eucalypt sap has been shown to be comprised mostly of sucrose (Stewart et al. 1973). Repeated peg incisions were made on each tree in the vicinity of the incisions made by gliders until six incisions had yielded a flow of sap for measurement. Glider incisions tended to be on the smooth bark, above the area of rough bark which E. viminalis has near the base of the trunk. The height of incisions varied considerably between trees independent of tree girth. When each tree was sampled, it was scored as either 'in use' or 'not in use' by gliders depending on the presence of fresh incisions on the trunk and fresh bark peelings on the ground. Eight trees of similar girth which had not been incised by gliders were used as controls and were monitored concurrently. Only seven were measured in February 1985 and for this sample, these were trees randomly selected in the vicinity of the sap-site trees. For the rest of the study, the same nearest non sap-site tree of the same species was used. These trees were sampled below 2m but above the rough bark at 27 the base of the tree. Measurements on all trees were made during the day. 3.2.1.3. Incising Experiment. The influence of incising on the sap flow was tested during the last sample period by making six, 4-5 cm wide incisions on two 'not in use' sap-site trees and their adjacent non sap-site trees for nine days. From observations of gliders feeding, it was considered that this intensity of daily incising would approximate that by gliders during a given night. Sap flow and quality were measured before commencement of the incising and again 10 days later. Another 'not in use' sap-site tree and its associated non sap-site tree that were not incised by me were measured for the same period in case differences were detected in the measured parameters of the experimental trees. The logistics of conducting this experiment prevented a larger number of trees from being tested. 3.2.2. Results. 3.2.2.1. Sap Feeding. Gliders made incisions into the bark of two species of eucalypt (E. viminalis, E. fastigata ) at Bombala by gouging out pieces of bark with their lower incisor teeth. They then licked the exudate which flowed from these incisions. Licking was interspersed with relatively short bouts of bark-gouging to extend the incisions or create new ones (Chapter 2). Incisions were probably only useful for a given period of time as the tree eventually secrets kino to block the incisions (Smith 1982a). Within a lOOha study grid at Bombala, there were approximately 2900 E. viminalis and 2200 E. fastigata > 30cm diameter at breast height (DBH) (estimated from Kavanagh 1984) but only seven (0.2%) and six (0.3%) individuals of these species, respectively, were incised. The incidence of sap feeding by P. australis was very sporadic but when it did occur it was often the predominant feeding behaviour (Fig. 3-1). For example, one glider observed for a whole-night period in January 1986 fed at a single sap-site for all of this time. Foraging gliders were followed for up to 3h in 1984 but often for whole nights in 1985 and 1986. These observations are therefore considered a good indication of the frequency of the gliders' feeding activities. Two bouts of sap feeding were observed on sap-site trees and 12 bouts were observed on other trees outside the main sap-feeding periods during 89.8h of directly observing gliders feeding. These bouts were only of a very short duration (6.2 min ±1.3 s.e.) whereas feeding bouts on sap-site trees at times of major sap feeding (27 bouts completely observed) were of 65.4 min (± 10.2 s.e.) duration. Three gliders remained on sap-site trees for whole night periods during observations but time constraints prevented further quantification of the duration of sap-feeding visits to the sap-site trees. 28 UJ LU s 3 CD ~3 CO CO ~3 -5 c ^^ n a CD CO o XE3 CO "5 C«3 03 ~3 O C/3 co c3 4—1 CD D. T— CU o < Ui O CD H CD n sz c > CD ««—' C Li. 'cd O c O o 2o E CD Q) rt Q o Ot3- o o a E cq CD 4—1 oD> 01 cd c3 3 M < 5 a E°* C3 c "St CO Eta en —) >, "3 en C/3 §Si 2 -^ • CD c n < .CD o ° .0 c c 4—t CO •rj CO +-• W -3 CD & X-) —• o CD •s .*? 00 X) 1 m 3 CD o : ''B euiji uoiiBAjasqo jo % —> o 3.2.2.2. Sap Measurements. The number of sap-site trees 'in use' (determined by the presence of fresh incisions on the trunk) during any sample period varied from one in February 1985 to three in July 1985 and four in January 1986. Sugar concentrations of E. viminalis sap measured with a refractometer were quite variable among individual trees during any sample period (largest range 18.0-37.1%) but were more constant for individual trees between sample periods. However, there were no consistent significant differences in the sugar concentrations using a single factor analysis of variance (Zar 1974) between sap-site trees in use, not in use, and non sap-site trees (Fig. 3-2a). Sap flow was greater for 'in use' sap-site trees than for 'not in use' or non sap-site trees (Fig. 3-2b). A single factor analysis of variance was used to test the significance of differences in sap flow among sap-site trees and non sap-site trees. A Tukey Test (Zar 1974) was then used to provide multiple comparisons among sap-site trees and among the non sap-site trees. This determined whether the sap flow measurements for these trees were in fact different within the two groups. None of the non sap-site trees had sap flows which were significantly different to each other. However, measurements for the 'in use' trees were significantly different from the 'not in use' trees for February, April and July 1985 but were not significant for September 1985, January and June 1986. Pair-wise comparisons (paired t-tests) were used to test for differences between each pair of trees (i.e. sap-site and non sap-site trees) because possible site differences (e.g. in soil moisture) made it inappropriate to pool data from all trees to make such comparisons. Fourty seven comparisons were made between sap-site and non sap-site trees. Of these, 14 were comparisons involving 'in use' sap-site trees and these had significantly higher flow values from the adjacent non sap-site trees for eight comparisons. Only 15 out 33 'not in use' tree comparisons showed significantly different values and for three of these, the non sap-site trees had the higher value. The influence of rain on the sap flow of the trees was investigated by relating the rainfall pattern at Bombala during each field trip and the two week period prior to it, to the sap flow values for the 'in use' trees. However, there was no apparent relationship between the incidence of rain and the fluctuations in the sap flow of the 'in use' trees (Spearman rank correlation P >0.05). Furthermore, the highest sap flow measurements for an 'in use' sap-site tree were made during July 1985, when no rain fell during the preceeding two weeks and very little fell during the field trip. 3.2.2.3. Incising Experiment. Measurements of sap flow and sap-sugar concentration, taken both before and after tree incising, showed no significant differences (Mann-Whitney U-test). Another pair of trees measured during the same Feb Apr July Sept Jan July Sample Month • iu 0 NIU 100- o 80 - o E 3 O > Q. 20 - Sample Month Fig. 3-2. a. Measurements of sugar concentration (% sucrose equivalents) in sap of Eucalyptus viminalis for February 1985-July 1986. b. Sap flow measurements for E. viminalis. Numbers above bars represent the number of trees 'in use' by gliders for sap feeding. IU = sap-site tree in use, NIU = sap-site tree not in use, Non = non sap-site tree. 31 period also did not show a difference for these measurements. 3.2.3. Discussion. The present study and others on the yellow-bellied glider in southern Australia have all found a sporadic use and selectivity of sap-site trees (Wakefield 1970, Henry & Craig 1984, Craig 1985, Kavanagh 1987a,b) but no previous study has been able to account for this apparently enigmatic behaviour. The yellow-bellied sap-sucker (S. varius ) also selects a small proportion of trees to tap for sap (Kilham 1964, Tate 1973). This selectivity contrasts with the finding of Lacher et al. (1984), that sap feeding marmosets incised trees in the proportion in which they occurred. However, in other areas, marmosets concentrate their sap feeding activities on only a few individuals of a few tree species although all individuals of such species had some indication of prior use (Ramirez et al. 1977, Maier et al. 1982). Measurements of sap-sugar concentration varied substantially between trees but fluctuations within a tree were not synchronised with glider use. This is consistent with the finding of Henry and Craig (1984). However, sap feeding by gliders occurred when sap-site trees had high measurements of sap flow. When not in use, these trees often had sap flows no different to non incised neighbouring trees. The cue for this increase in sap flow is not understood. Kilham (1964) stated that wounding of trees drilled by yellow-bellied sap-suckers stimulated increased sap flow. Increases in sap flow at Bombala were apparently not caused by the incising behaviour of the gliders. For example, one sap-site tree, which was in consistent use from April 1985 through to July 1986, showed substantial variation in its flow and the highest measurement occurred at a time when gliders were not actually observed sap feeding. Furthermore, there was no significant difference in the sap flow measurements of trees experimentally incised in order to stimulate increased sap flow. If the non sap-site trees always have low sap flow and are representative of other trees in the forest, then the sap-site trees may be unusual in their ability to elevate their rate of sap flow. Changes in sap flow are known to occur in the trees drilled by sap-suckers but on a defined seasonal basis. This is because of the obvious changes in sap flow associated with the annual shedding of leaves in deciduous trees (e.g. Kilham 1964) or in the case of conifers, because sap freezes in the phloem vessels during the winter (Tate 1973). Even so, this does not explain why only a small proportion of available trees is drilled by these woodpeckers. The reasons why the sap-site trees showed large increases in sap flow and the non sap-site trees did not are unclear. The most obvious explanation would be differences in soil moisture but this was not the case. For example, one sap-site tree on the bank of a creek was surrounded by numerous non-incised trees of the same 32 species. These trees should experience a similar microhabitat but the difference in the sap flow measurements between the sap-site tree and the adjacent non sap-site tree was considerable. Furthermore, the pattern of sap flow for this and the other sap-site trees was not associated with the rainfall pattern. The pattern of flow in other sap-site trees also appeared independent of microhabitat. In another study (Craig 1985), the glider sap-site trees were all located midslope and therefore would be expected to experience the same soil moisture conditions but were not all used concurrently. It may be that the rate of sap flow is governed by the endogenous rhythms of the tree which are under genetic control and therefore, a small number of trees in the forest are able to show unusually high rates of sap flow. Gliders at Bombala were quite selective in the sap-sites chosen for feeding as some fresh sap-sites (possibly of low sap flow) were apparently ignored by feeding gliders and one glider was observed to feed at a single sap-site for a whole night. This perhaps reflects variability in the phloem vessels conducting sap (e.g. Marvin 1958). Measurements of sap flow in this study, which were from six places on the trunk, may therefore underestimate the potential of the tree to the gliders. Diurnal measurements may also underestimate sap flow as this may be greater at night. For example, Crafts (1961) reported that sap flow from the palmyra palm (Borassus flabellifer) was greater at night but sap flow from trees utilized by S. varius has been found to be greater during the day (Sutherland et al. 1982). It has been suggested that the availability of alternative food resources influences the sap feeding behaviour of P. australis (R. Russell 1984, Kavanagh 1987a). In north Queensland, sap is apparently harvested throughout the year (Russell 1981, Smith & Russell 1982) and therefore the duration of sap feeding each night may be related to the availability of arthropods (which are necessary to provide protein) and possibly any, more energy-rich food resources. In southern sites, sap utilization is more sporadic (Henry & Craig 1984, Craig 1985, Chapter 2) but this does not correspond with the time when energy demands are expected to be greatest and food abundance lowest (i.e. winter). However, observations at Kioloa (see below), revealed extensive sap feeding on eucalypts only during the winter months of some years when the eucalypts that usually provide abundant nectar have failed to flower (unpubl. data) but periods of low food availability may occur at different times in different areas. Other evidence for the influence of the availability of other food resources is equivocal. During the present study, the alternative exudates for gliders were honeydew and manna (Chapter 2). Nevertheless, sap was often used even when these other resources were being used extensively and therefore were probably abundant. If, however, other resources were limiting and sap was necessary to supplement these, 33 it may be expected that all sap-site trees would be used with the same intensity. This was not the case and the particular sap-site trees incised changed during the 18 month sample period. Two, in particular, were not used at all although they were heavily scarred from use in 1984 and previous years. The interpretation of sap utilization and its relationship to the availabilty of other resources is confounded by an inability to distinguish between the differing intensities of sap feeding when scoring tree use. For example, low sap flow values for 'in use' trees as in 1986, may reflect a tapering off or commencement of sap feeding, as a response to changes in sap flow rates. However, the relationship between sap flow and sap feeding (Fig. 3-2b) implies a relationship with sap availability so that changes in sap flow in the sap-site trees seem to be the key to this interaction. Furthermore, gliders were observed to make small incisions into both sap-site and other trees (Plate 3-3) during months when they weren't engaged in sap feeding, suggesting that they may in fact, test for the level of sap flow. Such sampling behaviour has also been observed in sap-feeding marmosets (Fonseca & Lacher 1984). It is clear that further studies are required to investigate several outcomes of this study. First, what is it about sap-site trees which allows them to increase their sap flow so dramatically? Is it a genetic trait and if so, are there any more such trees in the forest not detected by gliders? Second, do other tree species display similar patterns of sap flow as described here for one species used by P. australis. Finally, an investigation of sap flow in the trees used by the yellow-bellied sapsucker and the sap-feeding marmosets would make an extremely useful contribution to understanding the dynamics and evolution of this specialized dietary niche. 34 Plate 3-3. Test incisions on a Eucalyptus viminalis non sap-site tree at Bombala. Kino can be seen exuding from the middle incision. 3.3. USE OF SAP-SITE TREES AT KIOLOA AND CALLALA BEACH. The methods used in this section are essentially the same as those described above and are explained only where they differed. 3.3.1. Study sites. Gliders were studied at a site in the Kioloa State Forest (35°35'S, 150°19'E) approximately 25 km northeast of Batemans Bay. The climate for another site within this state forest has been described in detail by Pook (1984, 1986). The annual average rainfall for Batemans Bay is 1065mm and mean daily temperatures only occasionallyrise above 25°C or drop below 10°C (Pook 1984). The forest habitat for this site is described in detail in Chapter 6. Observations were made on gliders from February 1985 through to August 1989. Glider sap-site trees were located on Crown Land at Callala Beach, approximately 20 km southeast of Nowra. At this site, gliders utilized E. punctata for sap feeding (Plate 3-4) but other common species in the the forest were E. gummifera, E. pilularis, and E. haemostoma. 3.3.2. Incidence of sap feeding at Kioloa. Overall, sap feeding accounted for 14.2% of the total feeding observation time (72.3h) at Kioloa. In comparison, gliders at Bombala spent 26.7% of the total feeding observation time (122.4h) engaged in sap feeding. Sap feeding occurred extensively on E. gummifera during August, October 1986 and July 1987 (Fig. 3-3). Sap-site trees at other times (e.g. July 1988) were observed with fresh incisions but gliders were not observed on these trees despite frequent checks and following gliders as they foraged, suggesting that this behaviour was of minor consequence at this time. The small observation time in July 1988 was due to the difficulty in observing gliders feeding in the crowns of E. maculata. Six gliders were followed extensively to record ranging behaviour and none visited any sap-site trees. Sap feeding also occurred very infrequently on E. maculata and E. piperita. Two incised E. maculata were located in one home range in early 1985 but were not used during the remainder of the study. One glider was observed making small incisions into the trunk of a E. maculata with no previous incisions in May 1989. This animal made several incisions during a 30 min period as it climbed up the trunk. Other gliders nearby fed extensively on eucalypt nectar. One E. piperita was located in October 1986 at which one glider was observed feeding. 3.3.3. Influence of rain on sap feeding. Nights when spotlighting was conducted were categorized as either 'wet' or 36 Plate 3-4. Eucalyptus punctata sap-site tree with incisions of various ages. 37 oo 1 e" I f- J8 c « 1-1 o NO _ 1 oo o fe. ota l nth , lin g la < 2 &H -Q TT D 01 > O ca p P3 Ui 5 •-> a t oo sa p t o 9 , th e din g £ g-4- 3 .•*—2* ra oo _o rt 1/3 =££ o < O 3 tj to o 00 o O ti m c 85 - ide n • —< fe. O ON < c CJ •—1 VJ C4-. CO• >>~>"'- rtS _>. (— c-An 53 u>. O o o O o t-c U c •3" 0 o 00 CD U-c tL. O E euui uojiBAjasqo jo % 'dry'. The former were those nights when at least persistent light rain fell. Also included in this category were nights when heavy rain had fallen throughout the day leaving trees very wet, but rain did not continue into the night. All other conditions were scored as dry nights. Nights were then categorised as either "sap-feeding observed" (a single animal was sufficient) or "not observed". The latter indicated that gliders were feeding on other food types. On three nights of heavy rain gliders were not actually observed but glider vocalizations were heard and examination of known sap-site trees failed to reveal any gliders sap feeding or any fresh incisions on those trees. Analysis of data for Kioloa (Table 3-1) showed that the occurrence of sap-feeding was not dependent on wet or dry nights. Data for Bombala (Table 3-1) also showed that sap feeding occurred independently of wet or dry conditions. Table 3-1. Glider feeding behaviour for wet and dry nights at Kioloa and Bombala. Kioloa3 Bombalab Dry Wet Dry Wet Sap feeding observed 11 0 13 7 No sap feeding observed 33 9 40 8 Totals 44 9 53 15 a Fisher Exact Test P = 0.101; bG = 2.609 P>0.1 3.3.4. Sap measurements at Kioloa and Callala Beach. Measurements of both sap flow and sap-sugar concentration were taken following the procedures of Section 3.2. However, sampling of sap was from six regularly spaced points around the trunk at 1-1.5m above the ground. This was within the height range of glider incisions on E. punctata but 2m lower than incisions on E. gummifera. However, measurements were only considered an index of sap flow. At Kioloa, trees were monitored from January 1987 through to July 1989. When sampling from E.gummifera, the outer rough bark was scraped back to reveal the live phloem and the sample peg was then driven in. Attempts to sample with the rough bark intact resulted in the exuding sap soaking into the bark. Similarly, gliders shaved back this rough bark to feed (pers. obs.). In July 1987, a transect through the forest at Kioloa was traversed in order to determine the proportion of E. gummifera incised by gliders. Only trees >30 cm DBH were scored. Of 100 individuals examined, 10 were heavily incised and a 39 further six had recent test incisions present (see Section 3.2.3.). Two of the latter had further test incisions which may have been up to a year old. In July 1989, a census of 50 E. punctata at Callala Beach showed that 10 (20%) had old scars of major incisions, indicating sap-feeding in the past but only two (4%) had extensive recent scarring. Several individuals of sap-site and non sap-site trees were monitored from Dec 1986 through to July 1989. Eucalyptus gummifera was also common in the forest at Callala Beach but no individuals incised by yellow-bellied gliders were observed although many were incised on the upper branches by sugar gliders. Measurements of E. punctata showed large variations in sap-sugar concentrations with no apparent pattern (Fig. 3-4). Individual trees tended to show relatively little variation in this parameter Q?ig. 3-5). Most variation for the E. punctata grouped data is due to the fact that not all trees were sampled each month. Apparent increases in concentration in some months are due to the sampling of a tree with a high sap-sugar measurement which was not sampled in the other months. Measurements of sap-flow at different times of the day and night were taken for each species to examine variation in this parameter over 24h. There was no difference in these measurements for five trees at Callala sampled in the morning and afternoon, and no difference for three trees sampled at Kioloa in the morning, afternoon and near midnight (Table 3-2). Table 3-2. Sap flow indices for E. gummifera at Kioloa and E. punctata at Callala for different times within a 24h period. Values are mean ± s.e. microlitres. Values for Callala were tested for significance using Wilcoxon paired-sample tests, while for Kioloa Friedman analysis of variance was used. NS = not significant (P >0.05). Tree No. Time of Sample (h) Prob Kioloa 1015-1055 1650-1720 2330-2425 2 29.9 ±7.5 20.7 ± 3.5 20.6 ± 5.0 NS 3 34.4 ±7.2 29.3 ± 4.1 33.1 ± 3.7 NS 4 40.7 ±6.8 38.1 ± 8.4 41.9 ±3.1 NS Callala 1000-1110 1705-1800 1 19.8 ±3.7 22.3 ± 3.3 NS 2 34.8 ±4.1 34.4 ± 6.3 NS 4 22.2 ±2.6 32.4 ± 7.3 NS 7 26.0 ±2.3 24.8 ± 2.3 NS 9 35.8 ±3.4 32.9 ± 4.2 NS 40 • iu 40 -i 0 NIU H Non tn c 30 - 0) ca > i] '5 i I cr 20 - CD O CO f o o 10 3 P V) II I i I Jl II 12/86 4/87 6/87 7/87 10/87 12/87 9/88 10/88 12/88 1/819 2/89 3/89 I i Sample Month II Fig. 3-4. Sugar concentration in sap of E. punctata. Notation as for Fig. 3-2. 40 (a) 0) CO 30 > 3 cCDr CD 20 CO O »— o3 CO 10 -5 12/86 4/87 6/87 7/87 10/87 12/87 9/88 10/88 12/88 1/89 2/89 3/89 40 -i CO *-« c 30 - o CO > '5 cr CO CO CO o 1— o 3 CO 12/86 4/87 6/87 7/87 10/87 12/87 9/88 10/88 12/88 1/89 2/89 3/89 Sample Month Fig. 3-5. Sugar concentration of sap for an individual E. punctata sap-site tree (a) and non sap-site tree (b). Values are means of six samples (± s.e.). Only single samples were taken after 10/87. NS = no sample. 42 At Callala Beach only one E. punctata sap-site tree (Tree 2) was recorded as 'in use' during the study and at such times its average sap-flow measurements were higher than for 'not in use' sap-site trees and non sap-site trees (Fig. 3-6). A single factor analysis of variance was used to test for statistical differences among the sap-flow measurements for each sample month. Where a significant F value was obtained, a Tukey Test (Zar 1974) was employed to provide multiple comparisons (see Section 3.2.2.2.). Where only two trees were sampled at Callala Beach, a t-test was used to examine differences. The sap-flow of Tree 2 was significantly different to that of other trees when 'in use1 in September 1988 and when 'not in use' in January, February and June 1989. Gliders tended to select only a few specific sites on tree trunks to incise at a given time, so that sampling of sap from regularly spaced points around the trunk may have underestimated the sap flow. Sap-site Tree 1 had a consistently low sap flow (<23|il) throughout the study and accounted for other statistical differences among trees. This tree had not been used since the study began. Statistical comparisons were made between the sap flow measurements of Tree 2 and the nearest non sap-site tree (Fig. 3-7). These trees showed significant differences for nine out of 14 comparisons and in each case Tree 2 had the higher values. At no time during the sample periods was any of the trees at Kioloa 'in use'. However, the indices for three sap-site trees sampled (Fig. 3-8) illustrate the temporal and between tree variability in sap flow that exists. For example the sap flow for Tree 4 in May 1987 averaged three times that of the two other sap-site trees sampled. These trees occur within 100m of each other and could be sampled within 30 minutes of each other. Three adjacent non sap-site trees were sampled along with the sap-site trees for four sample periods in 1989 but there were no significant differences (Kruskal-Wallis single factor analysis of variance) among the six trees during any period. 3.4. DISCUSSION. 3.4.1. Index of sap flow. The index of sap flow used in this study is considered a reliable approximation of the availability of sap to gliders and indicative of temporal changes in sap flow of individual trees. Similar procedures to measure sap flow are standard practice of plant physiologists (e.g. Milburn 1979). However, it is not an absolute measure from which food intake can be extrapolated. When phloem tissue is cut, there may be a high initial rate of sap exudation due to the release of high turgor pressure in the sieve tubes (e.g. Kallarackal & Milburn 1985). After a period of time exudation is reduced due to a sealing mechanism 2 Z Z „ kssssssssssssssj OO ;HH Cs « ES^H^H! 00 4—J c-v-;<«*X"tv:<- OS ^^^^^^^^^>^^^^^^^N^^N OO i n O s *~.ara . (U c O (a) 12/86 4/87 6/87 7/87 10/87 11/87 12/87 9/88 10/88 12/88 1/89 2/89 3/89 6/89 7/89 (b) 12/86 4/87 6/87 7/87 10/87 11/87 12/87 9/88 10/88 12/88 1/89 2/89 3/89 6/89 7/89 Sample Month and Year Fig. 3-7. Sap flow (mean ± s.e.) for an individual E. punctata sap-site tree (a) and non sap-site tree (b). IU = tree in use by gliders, NS = no sample. Tree 2 1/87 4/87 5/87 7/87 9/87 12/87 7/88 10/88 11/88 1/89 2/89 4/89 5/89 6/89 7/89 Tree 3 1/87 4/87 5/87 7/87 9/87 12/87 7/88 10/88 11/88 1/89 2/89 4/89 5/89 6/89 7/89 Tree 4 1/87 4/87 5/87 7/87 9/87 12/87 7/88 10/88 11/88 1/89 2/89 4/89 5/89 6/89 7/89 Sample Month and Year Fig. 3-8. Sap flow measurements (mean ± s.e.) for three Eucalyptus gummifera sap-site trees. whereby sieve-plate pores are blocked by P-protein (Kallarackal & Milburn 1983). Sieve plates prevent gas embolisms and sealing when sieve tubes are severed will prevent loss of sap but this can be circumvented if the phloem is recut (Milburn 1979, Kallarackal & Milburn 1983). This accords with observations on gliders engaged in sap feeding which interspersed licking of sap-sites with gouging to extend incisions (Chapter 3). Presumably sealing of the severed sieve tubes prevented sustained sap flow when measuring sap flow in this study. Milburn and Zimmermann (1974) expressed surprise that yellow-bellied sap-suckers (Sphyrapicus varius) were able to tap into palm trunks to feed on sap because the sealing mechanism of palms apparently operates instantaneously. Mackowski (1988) suggested that introduction of saliva into the sieve tubes whilst yellow-bellied gliders feed may create a small sugar gradient and prevent sealing. Trnis, combined with occasional re-incising of a sap-site, may lead to sustained flows over long periods. For example, one glider at Bombala was observed to feed continuously from a single sap-site for 7h. 3.4.2. Examination of hypotheses to explain glider sap feeding. The objective of this chapter was to examine the present hypotheses which try to account for glider sap feeding. Both R. Russell (1984) and Kavanagh (1987a) suggested a relationship between sap feeding and rain. An examination of sap feeding by gliders at two sites with respect to 'wet' nights revealed no obvious association. In fact, contrary to the hypothesis sap feeding by gliders at Kioloa was only observed on dry nights. R. Russell (1984) and Kavanagh (1987a) also suggested the availability of alternative food resources may affect sap feeding. This hypothesis does not account for one of the major characteristics of glider sap feeding behaviour, namely the irregular use of the same small number of specific trees. If gliders must resort to sap feeding due to rain or changes in the availability of alternative food resources then why do they return to the same few trees? Often only a few of the available sap-site trees were used. For example, at Kioloa and Callala Beach, the sap-site trees sampled occurred within a relatively small area but were not used concurrently. Furthermore, at Bombala in January 1989 one glider was observed to travel 600m (in 20 min), after emerging from its den at dusk, to a sap-site tree where it fed for at least 3h. This was in spite of its den being located within 170m of a sap-site tree displaying fresh incisions. The above hypotheses are also inadequate because they do not explain why not all eucalypt species available at a site are utilized for sap. For example, at Bombala E. viminalis and E. fastigata were used for sap at essentially different times of the year 47 (Kavanagh 1987a) even though glider groups had access to six species. Examination of sap flow and the incidence of sap feeding by gliders at three sites now allows a more detailed hypothesis to be constructed. Variable sap flow appears to account for the differences stated above namely, the sporadic use of a few individual trees. Measurements of sap flow demonstrate clearly that within these eucalypts there is a pronounced variability throughout the year. Individual sap-site trees varied their sap flow independent of each other and it was at times of heightened flow that they were utilized by gliders. At no time did sap feeding coincide with low sap flow. The period of high sap flow could be determined by gliders making test incisions into trees. These incisions are relatively small and gliders only spent short periods of time feeding at them. Many of the sap-site trees examined during this study at all three sites bore such incisions on occasion but gliders may also assay other trees. For example, 6% of £. gummifera (n =100) examined during July 1987 at Kioloa had such incisions. At Kioloa and Callala, there were numerous periods of apparently high sap flow in certain sap-site trees when gliders did not feed on sap. This may provide partial support for an influence of alternative food resources. Sap feeding at Kioloa was mostly confined to the winter months (sap-site Tree 2 & Tree 3 showed some use in early November 1988) when flowering trees (providing the main food resource - see Chapter 5) were absent. However, absence of nectar did not ensure the use of sap as gliders fed extensively on insect honeydew in September 1987. It is not known whether honeydew was abundant then and absent at other times. Also, one glider was observed to briefly engage in sap feeding in May 1989 despite an abundance of flowering trees nearby (see above). The use of different eucalypt species for sap feeding at different sites is quite puzzling. Some species, although used at some sites, are ignored at others (Kavanagh 1987a,b). For example, E. gummifera was present with different species at Kioloa and Callala but only used for sap at Kioloa. Kavanagh (1987a) implicated the influence of microsite of the incised species as being responsible. He argued that E. obliqua and E. cypellocarpa (present at Nadgee and Bombala) were used on the coast (Nadgee) because they occupied the "most fertile and productive sites" but were not used at Bombala where they occurred on theridges. Thi s over-simplifies the fact that some E. obliqua and E. cypellocarpa at Bombala occupied the same microsite as the E. viminalis sap-site trees. At Kioloa, E. gummifera was the main species incised but at Callala Beach it was ignored although it was adjacent to the E. punctata sap-site trees. If sap-site trees are used due to sap flow changes then perhaps choice of different species at different sites reflects the ability of different species to elevate sap 48 flow at different sites. Alternatively, it may reflect a difference in the amplitude of the variation and hence, gliders may exercise a preference among species. The causes for the temporal variation in sap flow are not understood. As stated above, the variation does not accord with the microsite occupied. Examination of the rainfall pattern preceeding field trips to Bombala showed no relationship with the measurements of sap flow. The variation in sap flow may be a natural rhythm shown by a small proportion of trees in the population. However, this necessitates clarification of whether trees with the capacity to elevate sap flow are more common in the population than suggested by the incidence of glider utilization. Linhart (1989) considered that much of the morphological and biochemical variation in trees to be genetically based and that there is clustering of genetically-related individuals. Sap-site trees tend to be spatially separated and very few in number at some sites (e.g. Bombala). A further implication from this research is that glider distribution may be determined by the presence of eucalypts with this capacity. However, Mackowski (1986) has surveyed some areas in northern N.S.W. where P. australis were observed but no sap-site trees were located. This may simply reflect inadequate surveys, particularly if gliders use sap-site trees in some years and not in others as at Kioloa. However, if some glider populations do not use sap-site trees, then this requires further investigation. 3.4.3. Model of sap flow in eucalypts. A graphical model can be proposed to illustrate the observed changes in the sap flow of the sap-site trees. This model (Fig. 3-9) depicts an hypothetical sap flow profile for a sap-site tree over several months. Sap flow within the tree is depicted as following some sort of wave function. Based on comparisons of sap flow in sap-site trees 'in use' and 'not in use' and non sap-site trees there appears to be a sap flow 'threshold' above which gliders will feed on sap but below which they will not. Sap flow in sap-site trees occasionally rises above this threshold and during this time gliders may be observed sap feeding. Sap flow in non sap-site trees generally does not rise above this threshold but sap flow still shows variation. At time c the sap flow is much greater than the threshold and statistical comparisons of this tree with other sap-site and non sap-site trees will reveal a significant difference. At time d gliders are still sap feeding but this may be tapering off and statistical comparisons may or may not be significantly different. At time b gliders are not sap feeding and sap flow in this tree is no different to other 'not in use' or non sap-site trees. Overall comparisons of sap volume measured at point d and point b may not show a great difference. This can be seen in Fig. 3-2b 49 80 - "v> 70 - Q) i_ *^ 60 - O >~ o 50 - E CD 40 - E 3 30 - O > Q. 20 - TO in 10 - 0- a bed Sample Month Fig. 3-9. Theoretical model of sap flow in eucalypts. Dashed line represents the sap feeding threshold. See text (p 48) for further explanation. 50 (Section 3.2) comparing January 'in use' with Sept 'not in use' sap flow. Occasionally a non sap-site tree may elevate sap flow above the sap feeding threshold and may further mask statistical comparisons of sap flow in trees used by gliders. At point a sap flow has increased above the threshold but not long enough for gliders to make use of it, or the abundance of other food resources may preclude sap feeding. Gliders may make decisions based on energetic considerations which determine whether to sap feed or not. A necessary precondition for sap feeding is that sap flow be elevated above some particular threshold but if an alternative food resource is abundant with respect to the cost of active foraging, then gliders may not engage in sap feeding (see Chapters 5). Gliders occasionally make test incisions (Plate 3-3) into trees (sap-site and non sap-site trees) presumably to monitor sap flow. Although some non sap-site trees occasionally have high sap flow values, mostly they do not. However, caution should be exercised here because this conclusion is based on a sample of only eight trees at Bombala, three at Kioloa and two at Callala. Most of the sap-site trees have been used periodically by gliders over many years. Of the eight sap-site trees sampled at Bombala, two which were originally located by R. Kavanagh in late 1981 were still showing signs of recent use in January 1989, over seven years later. Also, one glider group at Bombala which established itself after the disappearance of the original resident pair utilized the same sap-site trees as the former residents (see Chapters 6,7). Such trees are easily identified and immature gliders probably learn to identify such trees whilst living in the natal home range. Occasionally new trees are located by gliders and may become important sources of sap. 3.4.4. Comparison with sap feeding by sugar gliders. The sugar glider is another petaurid marsupial which feeds extensively on eucalypt sap (Smith 1982a, Howard 1989). Does sap feeding by both glider species respond to the same factors? Sap feeding by the yellow-bellied glider is ubiquitous among populations but this is not the case for the sugar glider. For example, at Barren Grounds Nature Reserve where sugar gliders use the nectar of Banksia spinulosa extensively throughout winter (Goldingay et al. 1987, Goldingay unpubl. data, S.M. Carthew unpubl. data), no incised trees have been observed (pers. obs.). Also, sugar gliders have only been found to incise two species, E. bridgesiana (Smith 1982a) and E. gummifera (pers. obs., Howard 1989), while yellow-bellied gliders incise a large number of species (see Wakefield 1970, Craig & Belcher 1980). Perhaps one advantage that large body size confers on the yellow-bellied glider is its much larger incisors which allow it to incise the hard trunks of many eucalypt species. Alternatively, small body size may allow sugar gliders to utilize exudates which occur 51 in smaller quantities. Smith (1980, 1982a) observed sugar gliders feeding on sap throughout the period of his study which suggests that eucalypt sap was a dietary staple at his site (but one glider group did not utilize sap), perhaps a similar situation to that for the yellow-bellied glider in north Queensland. This continued use of sap-site trees suggests that the factors determining sap feeding may be quite different for this species but Howard (1989) found more of a seasonal use of sap at a site in N.S.W. Also, the proportion of trees incised by sugar gliders is much greater (Howard 1989, Goldingay pers. obs.). The much larger size of the yellow-bellied glider would imply that it is subject to vastly different foraging constraints than is the sugar glider. Only a few individual trees in a forest may display a pattern of sap flow that is profitable to a mammal the size of the yellow-bellied glider (450-735g) while the sugar glider (90-160g) may be able to feed on sap less selectively because trees with low flow rates are still profitable. Howard (1989), in his study of sugar gliders, employed a similar technique to sample sap flow and was able to demonstrate consistently higher values for sap-site compared to non sap-site trees. 3.4.5. Influences of sap composition. Sap-sugar concentration was also measured during this study. This was found to be variable among trees but given trees did not display much temporal variability. Only a single study (Stewart et al. 1973) has determined the chemical composition of eucalypt sap. Samples of phloem sap from E. regnans contained less than 10% soluble dry matter of which sugars, primarily sucrose (>50% of sugar component), comprised an average of 42%. Amino acids accounted for < 2% of the total dry matter. Inorganic components accounted for 32% of the dry matter which was considered to be mostly salts of inorganic acids but 25% of the soluble dry matter was unaccounted for and was suggested to be polyphenolic substancs such as ellagitannins (Stewart et al. 1973). As pointed out by Inouye et al. (1980) and Hiebert and Calder (1983), amino acids and inorganic salts will bias determinations of sugar concentrations using hand refractometers. The temporal variation in these components is unknown so that whether these change with or independently of the sugar component (or with glider sap feeding) is also unknown. However, the amino acid component would presumably be of greatest importance to gliders as a way of providing nitrogen but the low overall contribution of this to sap composition suggests it unlikely that glider sap feeding might be influenced by its temporal variation. Nitrogen requirements of the sugar glider are low and may be easily met for a mammal with a high-energy diet (Smith & Green 1987) suggesting a similar capacity for yellow-bellied gliders. Some 52 authors (e.g. Bearder & Martin 1980a, Garber 1984) have suggested that mammals such as bushbabies and tamarins may feed selectively on plant exudates because they may contain high levels of calcium (lOx more than in arthropods). Garber (1984) suggested that intrasexual differences in the use of exudates may occur during late lactation when females would be expected to have a greater requirement for calcium. Extensive sap feeding by yellow-bellied gliders was observed for all individuals and at times of the year when females were not reproducing thus precluding such an explanation. Moreover, Hume (1982) considered that the bulk of an omnivore's mineral requirements would be met by the arthropod component of its diet. Possibly of greater relevance to glider sap feeding is whether eucalypts have chemical defences to avoid loss of sap to consumers. The cost to the tree of such feeding behaviour is indeed difficult to determine (Janzen 1979). Farentinos et al. (1981) implicated certain secondary compounds (monoterpenes) in the selection of individual pondersa pine (Pinus ponderosa) for feeding on cortical tissue by tassel-eared squirrels (Sciurus aberti). Repeated use of the selected trees by squirrels suggests that the level of the secondary compounds did not differ temporally. Thus, an analogous situation in eucalypts would not explain the sporadic use of sap-site trees. One mechanism available to eucalypts to prevent loss of sap from sites of phloem damage is the production of kino to block the wound (Smith 1982a, MacKowski 1988). Smith (1982a) stated that this occurred over a period of weeks. MacKowski (1988) inferred that the activity of incisions should be limited to approximately 15 days. In the present study, one incision out of thousands made during sap sampling (from a E. gummifera ) produced a flow of kino within minutes of incising the phloem but generally they did not; some were clogged with kino by the next sampling period. Thus, there is presently no evidence to suggest that glider sap feeding is influenced by the chemical composition of the sap. The bark feeding behaviour of some mammals has relevance to sap feeding by gliders. Bark is an important food resource to beavers (Castor canadensis) during autumn and winter (Jenkins 1975, 1979). Jenkins (1978) described how beavers often sampled the bark of trees which were not felled. This behaviour was observed at two sites and must be part of the regular foraging behaviour of beavers. Jenkins suggested that beavers may sample the bark of trees to assess nutritional status of available trees. Moreover, temporal changes in nutritional value of different tree species has been inferred to account for seasonal and annual differences in tree selection (Jenkins 1979). Little consideration was given to the presence of toxic compounds affecting tree selection (e.g. Belovsky 1984, Jenkins 1979). However, recently Basey et al. (1988) demonstated that tree selection by beavers at two sites was 53 influenced by the occurrence of phenolic compounds. In contrast, although some studies on snowshoe hares (Lepus americanus) have suggested that the selection of twigs, which form the basis of their winter diet, is influenced by the presence of defensive chemicals, supporting evidence is equivocal (Sinclair & Smith 1984). Thus, although the chemical defenses of plants may provide some influence on diet selection by snowshoe hares it does not provide a major constraint (Sinclair & Smith 1984). Indeed, although there are few similarities between the herbivory displayed by the above rodents and sap-feeding by yellow-bellied gliders it is instructive to show that chemical defenses may not be ubiquitous solutions in understanding the complex feeding behaviours of such mammals. However, an examination of the chemical composition of sap from 'in use', 'not in use' and non sap-site trees would contribute substantially to understanding the interaction between gliders and the trees selected for sap feeding. Other useful studies now required to further an understanding of this interaction include detailed investigations of sap flow in species used as sap-site trees by yellow-bellied gliders and species not used. If the sap flow hypothesis has general application then eucalypt species which are never used by gliders could be predicted to always have low sap flow indices. A detailed examination of sap flow in a species that is used as a sap-site tree at some locations but not at others would provide a further test of this hypothesis. The reliance on the same small number of sap-site trees also requires examination and an experiment which denies gliders access to these trees during periods of heavy use of sap would provide important information. Chapter 4. TIME BUDGET AND RELATED ASPECTS OF THE FORAGING BEHAVIOUR OF THE YELLOW-BELLIED GLIDER, Petaurus australis, AT BOMBALA. 4.1. INTRODUCTION. Time budgets of animals are behavioural measures of energy acquisition and utilization (e.g. Wolf & Hainsworth 1971). The particular budget adopted will be influenced by the animal's diet and, in particular, by the dispersion and availability of its food resources (e.g. Wolf et al. 1975, Terborgh 1983). This aspect of animal behaviour has been widely examined for nectar-feeding birds because their food resources can be easily quantified and empirical values of energy expenditure for various activities allow time budgets to be directly converted to energy budgets (e.g. Wolf & Hainsworth 1971, Wolf 1975, Wolf et al. 1975, Gill & Wolf 1975, Paton 1982). Research on the time budgets of mammals has been largely confined to the primates (e.g. Clutton-Brock & Harvey 1977a) because of the difficulty in observing the behaviour of other mammals in the field. However, several studies have examined the time budgets of arboreal marsupials but these have been confined to folivorous species (Smith 1979, Winter 1976, Kehl & Borsboom 1984, MacLennan 1984). Generally these species spend a large proportion (45%) of their time inactive and a smaller proportion (25%) actually feeding or foraging. The yellow-bellied glider (Petaurus australis) is a non-folivorous species of arboreal marsupial which can be readily observed in the field (e.g. Henry & Craig 1984, R. Russell 1984, Chapter 2). It has a diet consisting predominantly of plant and insect exudates, such as eucalypt sap, manna, honeydew and nectar, and to a lesser extent arthropods (Smith & Russell 1982, Kavanagh & Rohan-Jones 1982, Henry & Craig 1984, Kavanagh 1987a, 1987b, Chapters 2,3). Whether such a diet imposes constraints on the time spent active or indeed foraging is not known but examination of the time budget of this species would provide an interesting comparison with that of the folivorous marsupials mentioned above. In addition to describing the time budget of the yellow-bellied glider this study examines the activity pattern and several important aspects of the foraging behaviour. 55 4.2. METHODS. 4.2.1. Study area. This study was conducted in the Coolangubra State Forest, approximately 20 km south-east of Bombala (37<>01'S,149o23'E) New South Wales. Data were collected during 13 field trips between January 1984 and July 1986. 4.2.2. Time budgets. Gliders were followed for as long as possible at night (six all-night periods were used in 1986, see below) so that time budgets could be estimated. Activities were timed to the nearest 0.5 min and classed as either feeding (gliders actually engaged in some sort of feeding behaviour, see Chapter 2), climbing, grooming, gliding, social behaviour (interaction between gliders), resting or collecting foliage (removing clumps of foliage, placing in a twist of the tail and carrying back to the den). Times when gliders could not be seen were classed as lost. This generally occurred when gliders departed from trees and could not be relocated. Gliders were trapped (see Craig & Belcher 1980, Henry & Craig 1984) during field trips and tagged with colour-coded ear tags which enabled recognition of individuals. 4.2.3. Pattern of activity. The times that gliders emerged from and retired to their den hollows (Plate 4-1) were recorded. Gliders that were followed late in the night were often observed as they returned to their dens. This allowed retiring times to be recorded. These trees were subsequently watched at dusk on a number of occasions and the emergence times of gliders from hollows were recorded. Times of emergence and return to hollows were recorded and activity durations calculated for three whole night observations in January and three in July 1986 (see below). 4.2.4. Time-utilization of trees. Whilst following foraging gliders I was often able to record the times that gliders entered and left trees when harvesting particular food types. Thus the duration of these visits to trees for different food types was recorded and referred to as tree time-utilization values. Gliders only harvested the stated food type during these visits. 4.2.5. Occurrence of Group Foraging. When gliders were observed feeding on particular food items, the number of gliders in the trees was recorded. Observations of two or more gliders feeding in the same tree were scored as 'group feeding' records. Thus, solitary foraging is defined as one individual only, foraging in a tree. '^-'Xm lliilll -x Plate 4-1. Yellow-bellied glider from group 2 (see Chapters 6,7) emerging from den after dark. Photograph by P. Tap. 57 4.2.6. Foraging Distance. In January 1986, three gliders were followed for an entire night each (as above), one glider from each of three different groups. In July 1986, two gliders from one group were fitted with collars containing single-stage "Biotrack' transmitters. These gliders were then followed for three nights (one was followed twice). Radio-telemetry was essential at this time because the much longer night time period in winter made it difficult to follow gliders continuously by spotlight alone. Trees in which gliders were observed during these whole-night periods were marked with flagging tape and mapped during the day. From the mapped routes, the total distance traversed was determined. For some whole-night periods, the glider followed was occasionally lost from sight so that every tree it visited could not be tagged. On those occasions, the glider was assumed to have continued in a straight line to the next tree in which it was observed. This has resulted in a slight underestimate of distances moved. For 100 occasions when complete glides were observed, the trees were taped and the distance between them measured. The distance was a slight overestimate because gliders usually left trees from the outer foliage rather than near the trunk. 4.3. RESULTS. 4.3.1. Activity pattern. Gliders emerged from nest hollows at quite precise times after sunset (Table 1). Data for summer and winter were not significantly different (Mann-Whitney U-test, U =119.5, P >0.1) and the mean throughout the year was 49.7 min (s.e.= 3.7, n = 53) after sunset. Retiring times however, were quite different between summer and winter (Table 4-1) but due to the variability in the winter data, were not significantly different (Mann-Whitney U test, U = 4.0, P > 0.1). In summer, gliders often retired shortly after sunrise whereas in winter, they always retired before sunrise. One glider was observed to return to the den at 0100 h. Although the duration of the gliders' activity increased from summer to winter there was an actual decrease in the proportion of the night that gliders were active (Table 4-1). Table 4-1. Activity pattern of gliders at Bombala. Values are means ± s.e. (n = number of observations). The percentage of the dark phase utilized was determined by dividing the duration of activity by night length. Night length was that for the three nights in which gliders were continuously followed. Summer Winter Emergence time (minutes after sunset) 45.9 ± 7.2 (n = 13) 58.3 ± 5.9 (n =25) Retiring time (minutes before sunrise) 10.6 ± 10.*6 (n =11) 140.3 ± 77.9 (n =4) Night length (h) 9.6 14.2 Activity Duration (h) 9.2 ± 0.2 (n =3) 10.4 ± 2.6 (n =3) Percentage of dark phase utilized 96% 73% 4.3.2. Time-activity budgets. Only those observations of more than 15 min duration were used for the time-activity budget so as to avoid possible biases due to glider detectability and observer presence. Feeding accounted for the greatest proportion of the gliders' activity (81% of time outside the den averaged for all seasons). This declined from 90% in autumn to 71% in winter (Table 4-2). Climbing was often an integral part of the feeding behaviour so that it was not always possible to score it separately and therefore this activity has been underestimated. Furthermore, if those behaviours which constitute foraging (feeding, climbing, gliding) are considered together, 90% of the time budget is accounted for. Grooming occupied a minor proportion of the gliders' activity but increased during the winter months. The salient feature of these data is that only a very small proportion of time was spent inactive (i.e. resting). This ranged from 1% (summer) to 2.4% (autumn) of the gliders' time. A single glider was observed collecting eucalypt foliage and transporting it back to the den in winter 1984. Foliage is used for lining the nest (Fleay 1947) and probably serves to reduce heat loss during winter (see Smith et al. 1982). Table 4-2. Time-activity budget of gliders at Bombala. Values are the percentage of the total observation time 82.6 h. Activity Spring Summer Autumn Winter Mean a. Feeding 81.1 82.9 89.8 70.9 81.0 b. Climbing 9.4 7.5 3.1 11.5 7.9 c. Gliding 1.2 0.7 0.3 0.9 0.8 Foraging 91.7 91.1 93.2 83.3 89.7 d. Grooming 6.8 8.0 4.3 11.7 7.7 e. Resting 1.5 0.9 2.4 2.3 1.8 f. Social Behaviour 0.5 1.4 0.5 g. Foliage Collecting 2.4 0.6 Total obs. time (min.) 282 1577 1519 1575 4953 4.3.3. Time-utilization values of trees. The amount of time spent in a tree by a glider was clearly related to the type of food item being consumed. Data were significantly different using a Kruskal-Wallis analysis of variance (H= 506.7, P <0.001) and the mean ranks from this were used in a nonparametric multiple comparison test (Zar 1974). Significantly more time was spent in trees from which exudates (sap, manna, and honeydew) were harvested than in those from which food items were harvested from within bark ribbons (arthropods) or from under loose shedding bark (arthropods/honeydew) (Table 4-3). The latter involves a feeding behaviour where gliders peeled back loose shedding bark, licked the exposed surfaces and presumably ingested both arthropods and honeydew (see Chapter 2). One group of gliders observed extensively between January 1984 and July 1985 was observed to harvest sap from only six trees, honeydew (by itself) from six trees, manna from one tree but arthropods and arthropods/honeydew from more than 100 trees. Table 4-3. Time-utilization of trees whilst engaged in harvesting different foods. Values (mean ± s.e.) were determined for completely observed bouts of foraging in trees. Values with the same superscript are not significantly different. Values in parentheses are numbers of trees. Food type Time(min) per tree Sap 184.0 ± 56.6 (6)a Manna* 125.0 ± 21.2 (5)a Honeydew 48.6 ± 9.6 (13)a Arthropods 10.2 ± 0.9 (84)b Arthropods and/or honeydew 12.7 ±1.9 (43 )b * underestimated as four bouts were not fully observed. 60 4.3.4. Occurrence of group foraging. Gliders, although living in family groupings of 2-6 individuals (Henry & Craig 1984, Russell 1984, Goldingay unpubl. data), mostly foraged alone in trees but were often in vocal contact with group members (see Chapter 8). From 268 discrete foraging observations during 1984-86, 86% were of solitary animals (Table 4-4). Gliders tended to feed in the same tree more often when involved in sap feeding (46% of all group foraging observations) than for any other food type. In order to statistically analyse these data, three groups were formed by pooling some of the data (arthropods and arthropods/honeydew were pooled into one group and honeydew, manna and nectar into another group). A chi-square analysis revealed significant heterogeneity among the three groups (%2= 31.5, df = 2, P <0.001). The large chi-square value was due to a larger than expected value for group feeding on sap and a smaller than expected value for group feeding on the arthropods and arthropods/honeydew. 4.3.5. Foraging distance. The distance glided was measured on 100 occasions and averaged 39.2 m (s.e. = 2.3) (Fig 4-1). The total distance traversed during a night was determined for gliders followed for three whole-night periods in summer and three in winter. Average distance traversed for summer and winter was 1803 m (range 1060-2350) and 1110 m (range 590-1670), respectively. Shortest distances were recorded when gliders were feeding on sap and honeydew because only a small number of trees were visited. Largest distances were traversed when gliders were harvesting items from beneath loose bark and spending shorter periods in trees. For example, one glider followed for 4h in July 1985 traversed approximately 2km visiting more than 40 trees whilst foraging for arthropods. Table 4-4. Occurrence of group foraging. Values are numbers of observations, with percentages in parentheses. Food type Group Solitary Total Arthropod 2(3) 60 (97) 62 Arthropods and/or honeydew 6(7) 79 (93) 85 Honeydew 9(14) 55 (86) 64 Manna 2(20) 8(80) 10 Nectar 1(33) 2(67) 3 Sap 17 (39) 27 (61) 44 Total 37(14) 232(86) 268 61 1-10 11-20 21-30 31-40 41-50 51-60 61-70 71-80 81-90 91-100 100+ Distance glided (m) Fig. 4-1. Frequency distribution of 100 measured gliding distances of yellow-bellied gliders at Bombala. 62 4.4. DISCUSSION. Yellow-bellied gliders at Bombala spent a large proportion (81%) of their time outside their dens feeding. Only 2% of the total time in which gliders were observed (82.6h) was spent inactive. This was not compensated for by time in the den as gliders spent a large proportion of the night outside their dens. In contrast, the folivorous brushtail possum and the greater glider spend approximately 45% of their time outside the den inactive (Winter 1976, MacLennan 1984, Kehl & Borsboom 1984). The above value obtained for the yellow-bellied glider is possibly the highest value of time devoted to feeding yet obtained for a mammal (e.g. Clutton-Brock & Harvey 1977a), though few data are available for other exudivorous mammals. Other small homeothermic vertebrates for which comparable time budget data exist mostly have been found to spend less than 40% of their active time foraging (e.g. Wolf & Hainsworth 1971, Gill & Wolf 1975, Wolf 1975, Johns 1986). Terborgh (1983) found that three species of omnivorous primate spent more than 60% of their time budget feeding and attributed this to their large size (0.9 - 3.0 kg) and their need to procure sufficient arthropods to provide dietary protein. Paton (1982) found that New Holland honeyeaters (Phylidonyris novaehollandiae) devoted 33-90% of their active time feeding, depending on the availability of their carbohydrate food resources, with birds having to feed for much of the day when the availability of food was low. Food availability may explain the difference in time budget between the yellow-bellied glider, greater glider and brushtail possum. The folivores have a food resource which is abundant and easily obtained. Therefore, little time is required to harvest sufficient foliage to meet energy requirements but long periods are required to digest this food. The yellow-bellied glider, however, may devote a large amount of time to foraging (90% of the time budget) because its food is either well dispersed (arthropods and arthropods/honeydew) or highly clumped (sap, honeydew, manna, nectar) (Chapter 2, Kavanagh 1987a, Goldingay unpublished data). Exudates are renewed continuously (e.g. Paton 1980) and can be quickly digested by vertebrates (e.g. Paton 1982), which presumably allows gliders to feed for extended periods. Food resources are perhaps never sufficiently abundant to allow more time resting. Gliders displayed a similar pattern of activity to that recorded for the sugar glider in captivity (Goldingay 1984). This pattern of activity is also similar to that recorded by Kavanagh and Rohan-Jones (1982) for yellow-bellied gliders at another site, based on vocalizations as an indicator of glider activity. In summer and winter gliders emerged from their dens at a precise time after sunset. In summer, gliders often returned to their dens after sunrise, suggesting maximum use of available foraging time due to a low availability of food resources. In winter, when night length was longer, the time devoted to feeding declined and gliders occasionally retired well before sunrise. 63 In theory, an efficient foraging strategy will maximise the net return of energy relative to that expended in foraging (Schoener 1971). Pyke (1979) examined various hypotheses to account for the time budget of the golden-winged sunbird and found that an hypothesis where daily energy costs were minimised was in close agreement with the observed data. For yellow-bellied gliders during winter, if sufficient food is harvested early in the night, then the extra energy which may be obtained through prolonged foraging may not exceed the energy savings which may be obtained by retiring early when temperatures are low. The yellow-bellied glider has a food resource which has been described as seeming to be at times 'tantalizingly precarious' (Henry & Craig 1984). During the present study, one group of gliders was observed to remain within their den during three nights of heavy rain in June 1984, when honeydew was the predominant food item (Chapter 2). Honeydew is presumably washed away by rain so that the energetic savings obtained on this occasion through inactivity may have outweighed the cost of foraging under such conditions. Interestingly, although the feeding behaviour of gliders changed in response to a change in food resources (Chapter 2, Kavanagh 1987a, Goldingay unpublished data), foraging behaviour comprised the greater proportion of the time budget throughout the year. This has implications relevant to the energetics of foraging gliders. Different food items presumably will have different associated foraging costs. For example, gliders feeding on sap may remain in the one tree and feed at a single sap-site for a whole night (Chapter 3). In contrast, gliders harvesting arthropods and/or honeydew from beneath loose bark (see Chapter 2) actively search through trees pulling back loose bark with their incisors to gain access to this resource. For this behaviour, gliders will spend considerably less time per tree, travel greater distances and their energy expenditure would be expected to be considerably displaced above basal whereas those feeding on sap would not. Thus, in addition to the influence of ambient temperture on thermoregulatory costs (e.g. McCarron & Dawson 1984), energy expenditure whilst foraging will be a function of: a) the dispersion and productivity of food items (this will be reflected in the tree time-utilization values and the distance traversed) and, b) the energetics of the particular feeding behaviour required to harvest those food items. Nagy and Suckling (1985) suggested such differences in foraging costs for different food types may account for differences in field energy expenditure of sugar gliders and Leadbeaters possums. Indeed, the behavioural data presented on the yellow-bellied glider caution against generalising about field energy expenditure based on measurements during single periods. Gliding by the yellow-bellied glider presumably affords considerable energy savings considering the large distances traversed in an entire night whilst foraging 64 (range 590-2350m). Only a very small proportion of the time budget was devoted to gliding which was considerably less than that spent climbing. Being able to glide distances of 40-100m allows rapid cross-country movement which may be essential for an arboreal mammal exploiting patchy or dispersed food resources. Two important aspects of the foraging behaviour of gliders were measured in this study; the time-utilization of trees and the incidence of group foraging. Understanding the differences in these parameters for different food types may extend beyond measurement of the abundance and dispersion of food resources. The rate of renewal is probably a fundamental property of a food item to which the gliders' foraging behaviour will respond. The importance of the rate of food renewal was first proposed by Waser (1981) in a model to explain the cost for a carnivorous mammal of tolerating conspecifics in an area. Thus, it is probably no coincidence that yellow-bellied gliders spent the longest time in trees when feeding on eucalypt sap (184 min) and at such times were often observed feeding with conspecifics (39% of sap feeding observations). Henry and Craig (1984) similarly reported a greater incidence of group foraging when gliders fed on sap. The time-utilization values are probably reliable indicators of the rate of food renewal because gliders devoted most (90%) of their time to foraging. The difficulty in quantifying the rate of renewal of glider food items at Bombala prevent a test of the hypothesised relationship between food item abundance and rate of renewal, and the behaviour of foraging gliders in response to these. However, this relationship could be investigated on occasions when gliders are feeding extensively on nectar (e.g. Henry & Craig 1984, Kavanagh 1987a), a resource which could be more reliably quantified. Finally, Smith et al. (1982) concluded that the cost of food acquisition placed a far greater energy demand on Leadbeaters possum than any other major life process such as fat storage or reproduction. This is probably true for all exudivorous marsupials because of the dispersion of their food resources but is likely to be most pronounced for the yellow-bellied glider due to its much larger body size (450-735g, Chapter 6). Appreciation of the influence of body size will only be gained when time budgets have been described for the smaller petaurids. However, the yellow-bellied glider devotes a very substantial proportion of its active time to foraging which must translate to a very large allocation of energy resources. A study which examines energy intake and expenditure is now needed in order to gain a better appreciation of the metabolic demands on this species. This may help to account for its low fecundity (e.g. Craig 1986) and low population density (e.g. Henry & Craig 1984, Kavanagh 1984). Chapter 5. USE OF NECTAR RESOURCES BY THE YELLOW-BELLIED GLIDER, Petaurus australis, AT KIOLOA. 5.1. INTRODUCTION. Few studies have been conducted on the foraging behaviour of nectar feeding mammals. Most have only superficially considered the foraging behaviour of these mammals and have merely commented on their likely role in pollination (e.g. Heithaus et al. 191 A, Wiens & Rourke 1978, Voss et al. 1980, Steiner 1981, Goldingay et al. 1987). Some have simply considered the diet of these mammals (e.g. Turner 1984a,b, Heithaus et al. 1975). The nocturnal activity of most of these species has probably been responsible for the dearth of detailed studies on their foraging behaviour. In contrast, studies on nectarivorous birds have examined, in detail, many aspects of their foraging behaviour (e.g. Gill & Wolf 1977, Carpenter et al. 1983, Paton & Carpenter 1984) and when combined with data on their energetics, have led to tests of theoretical models (e.g. Pyke 1978a, 1979, 1981). Similar studies on mammals are rare and have been confined to nectarivorous bats (e.g. Howell 1979, Lemke 1984). Before such elaborate consideration can be given to non-flying mammals feeding on nectar, studies on their foraging behaviour need to be conducted. In Australia, there are many species of non-flying mammals which visit flowers (Turner 1982) but the importance of nectar in the diet of such species has been investigated only recently (e.g. Turner 1984a,b, Goldingay et al. 1987). To date, no Australian study has examined the influence of the dispersion and productivity of nectar resources on the foraging behaviour of a non-flying mammal. The yellow-bellied glider (Petaurus australis) is a species of arboreal marsupial which has a predominantly exudivorous diet and may, on occasion, feed extensively on nectar (Smith & Russell 1982, Henry & Craig 1984, Chapter 3). The aim of this chapter was to: i) document the incidence of nectar in the diet at a study site where gliders were known to commonly feed on nectar (S. Davey pers. comm.), ii) examine the dispersion and productivity of the nectar resource and, iii) examine the foraging behaviour of this animal when nectar feeding. 5.2. METHODS. 5.2.1. Study Area. This study was conducted in the Kioloa State Forest, Kioloa, coastal N.S.W. The study area contained five species of eucalypt (Eucalyptus maculata, E. gummifera, E. pilularis, E. pellita, E.piperita). The area encompassed approximately 200 ha and 66 included the home-ranges of three glider groups (see Chapters 6,7). Field trips were made to the study area over a five year period (February 1985 - August 1989). 5.2.2. Flowering Phenology. In April 1987, two one kilometer transects with pegs at 100m intervals were marked out along two roads in the study area (equal to 12 ha of forest). The transects extended 30m on either side of the road. These transects spanned the three home-ranges. This allowed the number and species of flowering tree available to each glider group to be recorded during field trips. During each field trip flower abundance was determined for each of 10 trees randomly selected along each transect. The number of flowers per tree was estimated by examining the tree canopy through a pair of binoculars, counting the number of flowers in what could be regarded as a typical canopy unit and multiplying by the number of such units in the tree (see Kavanagh 1984). It has been suggested that gliders may feed on nectar only in trees with large (>5mm diameter) flowers (Henry & Craig 1984). Therefore, fresh flowers which had been removed by parrots feeding destructively were collected from under trees. The diameter of the capsule of these flowers was measured with callipers in order to assess this hypothesis. In May 1989,1 investigated the relationship between the diameter at breast height (DBH) of 28 flowering E. maculata and the number of flowers present in the canopy of these trees. This was conducted because gliders may be able to select trees with abundant flowers by selecting large trees. Data were collected from the trees randomly selected along the two phenology transects and for trees along another transect on a road adjacent to the study site. 5.2.3. Foraging Observations. Gliders were located in the study area at night with a 100W 12Vspotlight. They were then observed with a 55W red spotlight and a pair of binoculars. Habituation to the spotlight allowed gliders to be observed with a white light without apparent disruption to normal behaviour. Gliders were followed and observed for as long as possible. All feeding behaviours were timed to the nearest 0.5 min and recorded on tape (see Chapter 2). While observing gliders other behaviours were timed and recorded. These data were accumulated to formulate a time budget using continuous observation periods of at least 15 min (see Chapter 4). The number of yellow-bellied gliders feeding in trees was recorded and allocated to either a solitary (one glider in a tree) or group (two or more feeding in the same tree) foraging category. When gliders were observed feeding on nectar, an attempt was made to score the number of other mammal species feeding in these same trees. 67 The trees in which gliders were observed at night were taped with coloured flagging tape so they could be relocated during the day. For observations in flowering trees the total number of flowers in these trees was estimated (see above) and the distance to the nearest flowering tree measured. Where possible, the duration of the period gliders spent in flowering trees was recorded in order to investigate whether this was influenced by flower number. On the few occasions when two gliders were feeding in the same tree the duration of time spent in the tree for both gliders was added together. When recording the duration of these visits, gliders were often not observed under spotlight continuously because the battery life of the spotlight could have been exhausted before the glider departed from the tree. 5.2.4. Nectar Sampling of Eucalyptus gummifera. Sampling of nectar from eucalypt flowers can be exceedingly difficult and at Kioloa, the lower branches of tree canopies were at least 10m above the ground. This precluded a more detailed investigation of patterns of nectar production. In April 1987, a caving ladder was used to gain access to the flowers in one tree. Ten flowers were emptied of nectar at 1300h. These flowers were then covered with fibreglass mesh to prevent access by nectar-feeding animals. The amount of nectar secreted subsequent to this was measured (using capillary tubes) at 6h intervals beginning at approximately 1800h. In April 1988 four trees were sampled for nectar. A mini-cherrypicker was used to gain access to the flowers in these trees. This had the capacity to reach 14m above the ground. For these trees, 6-10 flowers were initially emptied of nectar between 1400h-1700h. These flowers were then covered with fibreglass mesh and sampled at approximately 6h intervals as above (beginning at 1800h). The exact times of sampling were noted and secretion rates are expressed as the volume of nectar produced in the interval between sampling. For each sample of sufficient volume, the sugar concentration of the nectar was determined using a temperature-compensted hand refractometer. For two trees, an additional 6-10 flowers were bagged so that different sampling intervals could be compared. These groups of flowers were sampled 24h after being emptied. Also, measurements were continued for two of the trees so as to compare nectar secretion for different days and different sampling intervals. In addition, whenever nectar volumes from the four trees were being measured for rate of secretion, a random sample of 10 flowers was removed from the tree and measured for the standing crop of nectar. 5.3. RESULTS. 5.3.1. Diet of Gliders at Kioloa. Timed feeding observations indicated that the single most important food item in the diet of gliders at Kioloa was eucalypt nectar (Fig. 5-1). This was obtained from all E.pil. E.pip. E.m. E.pe. 190 190 400 100- 65 556 « 80 - E c .2 60 H 03 > »- CD 40- co £1 O 20- Honeydew 0 Eucalypt Sap Feb Apr Sep Apr Aug Oct Dec Acacia Gum of animals _ 2 3^47 if 2 4 Arthropods observed' Sample Month (1985-86) D Nectar Eg. E.pil.- E.pip. E.m. E.pe. 120 50 395 454 431 114 30 60 62 272 427 186 G) E *-» n o CO > 1— CO Jan Feb Apr May Jul Sep Apr Jun Jan Feb May Aug of animals 4 2 64 46 142 4 10 2 observed5 Sample Month (1987-89) Fig. 5-1. Monthly feeding observations of gliders at Kioloa. Numbers above bars indicate the total feeding observation times (min). Different food types are indicated in the key. Flowering periods of eucalypt species (see Table 5-1 for abbreviations) are shown above sample months. Lines joining consecutive sample months indicate heavy flowering in those samples. five species throughout the study and the only time that other items featured in the diet was during the absence of trees in flower (e.g. during winter/spring 1986, 1987). Faecal samples were collected from six captured gliders (two in April 1988, one in May 1989 and three in Aug/Sept 1989). Each sample had high densities of eucalypt pollen (c.f. Turner 1984a). Digestion of pollen was determined by microscopically examining 100 grains and scoring as to whether the contents were intact or not (Turner 1984a, Goldingay et al. 1987). The number of pollen grains devoid of cell contents averaged 59.3 ± 7.4. Overall, nectar (and pollen) feeding accounted for 70% of the total feeding observation time (FOT) of 74.6h. Gliders in one home-range obtained gum from one Acacia mabelliae. This tree was used extensively by gliders from September 1985 through to October 1986 and again briefly in May 1987. There was six gliders in this group and all were known to visit this tree to feed, based on trapping in the tree and spotlighting in February 1986. Gliders stopped using this tree when it suffered massive die-back in late 1986. Overall, acacia gum accounted for 5% of the total FOT. Two types of honeydew were harvested by gliders. One was obtained by licking the blackened branches of a few E. piperita where psyllids were presumed to be living in the stringy bark (see Chapter 2). These trees could be distinguished by the blackening of the upper branches owing to a mould growing on the bark (see Chapter 2). Two such trees were located in the home-range of Group 1 gliders while one each was located in the home-ranges of Groups 2 and 3. The second type of honeydew was obtained from the fine branches in the canopy of E. maculata in July and September 1987 and July 1988. These trees were shedding bark from these areas and the gliders peeled back the bark and licked the branches. Drops of honeydew were often seen glistening in the spotlight. Honeydew accounted for 9% of the total FOT. Eucalypt sap accounted for 16% of the total FOT and its use by gliders at this site has been described in detail in Chapter 3. Arthropod feeding accounted for only 0.3% of the total FOT. Table 5-1. Diameter (mm) of flower capsules for different eucalypt species. Species Mean (± s.e.) Range N E. gummifera (E.g.) 8.5 ± 0.1 6.9- 11.7 70 E. maculata (Em.) 7.3 ± 0.1 6.2 - 8.8 50 E.pilularis (E.pil.) 5.0 ± 0.1 4.4-5.9 40 E.pellita (E.pe.) 7.7±0.2 6.6-8.4 10 E. piperita (E.pip.) 2.9 ±0.1 2.3-3.7 40 5.3.2. Flower Measurements. Measurements of flower diameter were made for each of the eucalypt species in 70 which gliders were observed nectar feeding (Table 5-1). All but one had large (>5mm diameter) flowers and all species had cream-white flowers. 5.3.3. Flowering Phenology. The flowering periods of eucalypts in the study area (Fig. 5-1) indicate the availability of this resource during the year and the small amount of overlap in the flowering of different species. Different species flowered at different times of the year and E. maculata, the most abundant species in the study site, could flower from autumn through to spring (i.e. for 6 months). Two individual E. maculata were known to flower for at least seven weeks in 1989. This species failed to flower in the study site during the winters of 1986 and 1987, and only a very small number flowered in 1988. The abundance of the flowering resource is indicated for each species from the transect data (Table 5-2). Gliders were only observed feeding in one species when overlap in flowering occurred. In February 1989, there were 29 E. gummifera, three E. piperita, one E. pellita, and one E. maculata flowering and gliders fed only in the flowering E. gummifera so the number for this species alone has been used to indicate the abundance of the flowering resource for that sample (Table 5-2). 5.3.4. Nectar Parameters. 5.3.4.1. Temporal Variability in Secretion. Nectar secretion (microlitres per hour) was found to be highly variable among sample periods (Fig. 5-2). There were significant differences among the different sample times for all except Tree 2 in 1988 (Friedman analysis of variance; 1987 Tree 1: %2 = 11.4, df = 3, P <0.01; 1988 Tree 1: %2 = 25.81, df = 4, P <0.001; Tree 2: %2 = 6.76, df = 4, P >0.1; Tree 3: %2 = 18.36, df = 3, P <0.001; Tree 4: %2 = 25.79, df = 4, P <0.001). There were no consistent differences in the time when trees had peaks or troughs in nectar secretion. 5.3.4.2. Influence of Sampling Interval on Secretion. For tree 4, flowers sampled at 6h intervals did not secrete significantly greater volumes of nectar than those sampled only once in 24h for the same period (Mann-Whitney U-test, z = 1.82; P >0.05). Nocturnal and diurnal rates of nectar secretion for day 1 and day 2 were significantly different (Wilcoxon paired-sample test; day 1: z = 2.19; P <0.05; day 2: z = 1.99; P <0.05). Rates of nectar secretion (u.l/h) for day 1 flowers sampled at 6h intervals were significantly different to that on day 2 sampled at 12h intervals (Mann-Whitney U-test, z = 3.06; P <0.005). For tree 3, flowers sampled at 6h intervals did not secrete significantly greater volumes of nectar than those sampled only once in 24h (Mann-Whitney U-test, z = 4-i 2 o £ 1840 2400 0530 1300 Time of Day (C) 3- CD o 2 1930 0150 0708 1310 1912 0700 1805 2418 0810 1213 2021 Time of Day Time of Day 4-i (d) (e) W 0) o o E 2005 0218 0635 1326 1847 0110 0730 1248 1930 Time of Day Time of Day Fig. 5-2. Rates of nectar secretion (mean ± s.e.) of flowers of five Eucalyptus gummifera. (a) sampled in 1987, (b) - (e) sampled in 1988. 72 0.98; P >0.2). Tree 1 flowers sampled for consecutive nights (the first night at 6h intervals; the second night at 12h intervals) showed a significant difference (Wilcoxon paired-sample test; z = 2.70; P <0.01). Moreover, these flowers secreted significantly more nectar at night than during the day (Wilcoxon paired-sample test; z = 2.60; P <0.01). 5.3.4.3. Inter-tree Variability in Secretion. Nectar secretion in the four trees measured in 1988 was examined for statistical differences among sample periods using a Kruscal-Wallis analysis of variance. Only values determined within 2h intervals were used. Two out of five comparisons showed significant differences in nectar secretion (1805-2005h: H = 17.15, df = 3, P <0.001; 2418-0218h: H = 2.37, df=3, P >0.5; 0635-0810h: H = 6.16, df = 3, P >0.1; 1213-1326h: H = 5.60, df = 2, P >0.05; 1912-2021h: H = 16.73, df = 2, P <0.001). 5.3.4.4. Standing Crop. Measurements of nectar standing crop (Fig. 5-3) were compared both for different periods on the same individual trees and also for different trees sampled within a 3h period. Kruscal-Wallis and Mann-Whitney U-tests were used to detect differences between values. Two trees had standing crops which were significantly different for different time periods (Tree 1: H = 24.97, df = 4, P <0.001; Tree 4: H = 34.94, df = 4, P <0.001) while two trees showed no difference among times (Tree 2: H = 1.71, df = 2, P >0.25; Tree 3: H = 2.76, df =4, P >0.5). There was only one significant difference when comparing standing crops among trees for different times: Day 1 (1413h-1655h: H = 6.69, df = 3, P>0.05); Night 1 (1900-1930h: z = 0.23, P >0.5; 2418-0218h: H = 6.01, P <0.05); Day 2 (1248-1326h: H = 4.46, df = 2, P >0.1; 1715-1740h: z = 0.23, P >0.2). Therefore, most variation detected in standing crop occurred over time rather than among trees. 5.3.4.5. Nectar Sugar Concentration. Data were arcsine transformed (Zar 1974) and compared for different times of the day. For tree 1, the concentration of nectar (% sucrose equivalents) did differ significantly (Friedman analysis of variance: % = 22.51, df = 4, P <0.001) among the time periods (Fig. 5-4). For tree 2, due to the small quantities of nectar obtained it was not possible to measure sugar concentrations of the nectar. For trees 3 and 4, the nectar concentration did not differ significantly (% = 3, df = 3, P >0.25) among the time periods (range: Tree 3, 7.5-17.5%; Tree 4, 6.0-10.0%). 5.3.5. Foraging Behaviour. 5.3.5.1. Tree Selection. For six sample periods gliders were associated with trees which had significantly more flowers than that on random trees (Table 5-2). The 12-i (b) 0) 10- o 8 a 6 o 4 o 2H E 0 1413 1930 1310 0700 1715 1455 1710 2418 Time of Day Time of Day CO o w CD o o E 1530 0218 0635 1326 1832 1655 1900 0110 1248 1930 Time of Day Time of Day Fig. 5-3. Standing crop (mean ± s.e.) of nectar in flowers of four E. gummifera sampled in 1988. 74 1930 0150 0708 1310 1912 0700 Time of Day Fig. 5-4. Sugar concentrations (means ± s.e.) for E. gummifera tree 1 flowers sampled at different times. degree of selection by gliders for trees with greater than the average number of flowers on transect trees can be expressed as a ratio of the number of flowers in glider selected trees divided by the number of flowers in the transect trees (Table 5-2). During most sample periods, gliders selected trees with 2-3 times as many flowers as may be encountered on random trees. During June 1988, when very few trees were in flower and transect trees contained very few flowers, gliders selected E. maculata with less than half as many flowers as were present on trees they selected during May 1989 when flowering E. maculata were numerous. However, these trees in 1988 had more than one hundred times as many flowers as on transect trees. As the abundance of flowering E. gummifera declined from April to May 1987, there was a subsequent increase in the distance (mean ± s.e.) to the nearest flowering tree (April: 13.0 ± 4.4 m, n = 20; May: 50.3 ± 44.4 m, n = 4) measured from the trees gliders were seen in. This distance was also reduced in May 1989 (15.0 ± 1.2 m, n = 15) when flowering trees were very abundant. During May 1989, the relationship between tree size (DBH cm) and the number of flowers borne was examined for flowering E. maculata. There was a significant relationship between tree DBH and 2 flower number (Y= 309.4 + 65.3x; F1>26 = 10.29 , P < 0.01; r = 0.28). Thus, not surprisingly, larger trees carried more flowers than smaller trees. Table 5-2. Flowering tree abundance and tree selection by gliders. The abundance of flowering trees (different species are represented by their initials; see table 1) was assessed by the number along two one km transects (equal to 12 ha). Values for flowers per tree are mean ± s.e. Mann-Whitney U-tests were used to test for statistical differences. The small sample sizes in June 1988 precluded testing. Ratio is the mean number of flowers/glider tree divided by the mean number of flowers/transect tree. Month No . flowering trees No. flowers/transect tree No.flowers/glider tree Ratio Prob. April 87 196 {E.g.) 5865.0 ± 993.9 (n=20) 12700.0 ± 1632.0 (n=20) 2.2 <0.001 May 87 13 {E.g.) 989.2 ± 607.8 (n=12) 3005.7 ±981.4 (n=7) 3.0 <0.02 June 88 3 {E.m.) 28.3 ± 16.7 (n=3) 2933.3 ± 556.0 (n=3) 103.7 - Jan 89 9 {E.pil.) 15296.7 ± 5053.2 (n=6) 45612.0 ± 7923.6 (n=5) 3.0 <0.02 Feb 89 29 {E.g.) 5166.0 ± 1958.6 (n=10) 11487.8 ± 2088.3 (n=9) 2.2 <0.02 May 89 65 {E.m.) 2413.9 ±701.1 (n=20) 6185.7 ± 783.7 (n=17) 2.6 <0.001 Aug 89 16 {E.m.) 3962.0 ± 1020.2 (n=10) 11209.1 ± 1929.8 (n=ll) 2.8 <0.02 5.3.5.2. Duration of Visits to Flowering Trees. The relationship between the estimated total number of flowers a tree possessed and the duration of glider visits to those trees was examined for several sample periods (Fig. 5-5). Only during May 1989 was such a relationship significant (Table 5-3). Small sample sizes may explain the lack of significance for February 1989 and May 1987 but for April 1987, the coefficient of determination was extremely low (r2 = 0.04), suggesting that total April 1987 May 1987 30000 -i CD El • 0) | 20000 - o u_ i? 10000- • • I ' I ' I • I • I • I • I u - i i i i i i i 20 40 60 80 100 120 140 Time (min) Time (min) February 1989 May 1989 30000 -i •"2000 CD CD g> oooo-l 20000 - 2 8000 H o | 6000 - 10000 4000 - o o z 2000 —I—'—I—'—I—'—I 0 l • l • l • I • I ' l ' I 20 40 60 80 20 40 60 80 100 120 140 Time (min) Time (min) Fig. 5-5. Relationship between number of flowers per tree and time spent feeding in trees by gliders. See Table 5-3 for regression parameters. 77 flower number was a poor indicator of the amount of time gliders spent feeding. In February 1989, one incomplete observation of a glider nectar feeding lasted for 280 min (in a tree with 20700 flowers). A complete observation of a glider visit to the same tree on a previous night was of 45 min duration. During other field trips (in which this relationship was not examined) when few trees were in flower, gliders remained in flowering trees for long periods. For example, in December 1986 when few trees were flowering two gliders remained in a flowering E. pilularis for at least 236 min. Table 5-3. Regressions of time (min) per tree by gliders versus the number of flowers in those trees. Month No.flowering tree s Regression parameters ANOVA r2 a b n F P April 87 196 (E.g.) 0.04 12674.7 46.0 9 0.29 0.609 May 87 13 (Kg.) 0.50 845.0 28.4 5 2.94 0.182 Feb 89 29 (E.g. ) 0.28 6553.0 127.9 7 1.96 0.202 May 89 65 (E.m. ) 0.37 2203.1 48.7 15 7.78 0.015 5.3.6. Time Budget. Feeding accounted for an average of 85% of time gliders spent outside their dens throughout the year (Table 5-4). In autumn, grooming occupied a larger proportion of time than for other seasons and less time was devoted to feeding. Climbing was often an integral part of feeding as gliders moved between clumps of flowers within the tree canopy and therefore is underestimated as a separate behaviour. Gliding has also been underestimated as the dense understorey often made it difficult to remain in constant contact with gliders as they moved between flowering trees. When all behaviours associated with foraging are considered together they account for approximately 90% of the time budget. Social behaviours such as allogrooming (i.e. gliders grooming each other) were observed on occasion but often early in the night after gliders emerged from their dens. At such times they tended to move out of sight making it difficult to quantify. Vocal exchanges, whilst gliders foraged, were a more common form of interaction between gliders (see Chapter 8) and occurred throughout the night and was not quantified as a separate component in the time budget. Resting occupied, on average, less than 1% of the time budget during the year. In May 1989, females from two glider groups had young in their dens and were occasionally observed to return to the den during the night. 78 Table 5-4. Time-activity budget of gliders at Kioloa. Values are the percentage of the total observation time. Activity Spring Summer Autumn Winter Mean a. Feeding 98.0 96.8 79.4 94.6 85.0 b. Climbing 0.2 2.3 5.1 2.6 4.0 c. Gliding 0.5 0.4 0.5 0.4 Foraging 98.7 99.1 84.9 97.7 89.4 d. Grooming 1.3 0.9 14.4 2.3 10.2 e. Resting 0.6 0.4 f. Social Behav. Total obs. time (min.) 224 217 1324 194 1959- 5.3.7. Occurrence of Group Foraging. Gliders were commonly seen feeding together for all food types resulting in 38% of all observations being of more than one glider feeding in a tree at once (Table 5-5). Few observations were made for arthropod foraging and therefore may not be representative of usual foraging associations among gliders. The data were analysed by pooling into one group those data for the three groups with observations of less than six. A chi-square test of independence revealed no significant difference (x = 0.14, df = 2, P >0.9) among the three groups of food types. Table 5-5. Occurrence of group foraging for different food types. Values are the numbers of observations. Food Type Group Solitary Total Nectar 28 (36%) 49 77 Eucalypt sap 6 (40%) 9 15 Acacia gum 3 (38%) 5 8 Honeydew 3 (33%) 6 9 Arthropods 2 (67%) 1 3 Total 40 (38%) 65 105 5.3.8. Number of Mammals Feeding in Flowering Trees. Three other mammal species, the sugar glider (Petaurus breviceps), the feathertail glider (Acrobates pygmaeus) and the grey-headed fruit bat (Pteropus poliocephalus) were recorded during this study feeding in the same flowering trees in which yellow-bellied gliders were observed. Fruit bats were only recorded in the study area when at least moderate numbers of flowering trees were present (Table 5-6). Table 5-6. Influence of flowering tree number on the presence (+) or absence (-) of fruit bats at Kioloa. Month No. of flowering trees Bats April 1987 196 (E.g.) + May 1987 13 (E.g.) - June 1988 3 (E.m.) - Jan 1989 9 (E.pil.) - Feb 1989 29 (E.g.) + May 1989 65 (E.m.) + July 1989 60 (E.m.) + Aug 1989 16 (E.m.) . A multiple regression analysis (Zar 1974) was used to determine whether the number of sugar gliders and feathertail gliders in flowering trees (Table 5-7) was influenced by the presence of yellow-bellied gliders (the dependent variable). This 2 was not a significant relationship (F229= 0.179, P = 0.84, r = 0.012). This is illustrated by an observation in February 1985 of a single flowering E. pellita (approximately 15m tall) in which two yellow-bellied gliders, two sugar gliders and two feathertail gliders were nectar feeding. Table 5-7. Mean (± s.e.) number of mammals nectar feeding in trees in which yellow-bellied gliders were observed. These data represent only those observations when the number of other mammals could be assessed accurately. No. observations yellow-bellied glider sugar glider feathertail glider 30 1.5 ±0.1 0.4 ±0.1 0.4 ±0.1 5.4. DISCUSSION. 5.4.1. Diet. Yellow-bellied gliders fed extensively on eucalypt nectar of all species, whenever flowering trees were present in the study area. Such a predominance of 80 nectar in the diet has not been recorded at any other site (Smith & Russell 1982, Henry & Craig 1984, Kavanagh 1987a,b, Chapter 2). Different eucalypt species tended to flower at different times during the year. Thus an assessment of the number of flowering trees along two one km transects (equal to 12 ha) through the forest gave an average for April 1987 to August 1989 of 3.9 ± 2.2 flowering trees per ha per sample period. Only on a few occasions were more than one species flowering together. At such times one flowering species predominated and it was only that species in which gliders were observed feeding. Henry and Craig (1984) suggested that gliders only fed on nectar from species of eucalypt with large (>5mm) flowers. At Kioloa, gliders fed in all species when they flowered including E. piperita which has flowers ca.3mm in diameter. At Bombala, gliders were observed during one field trip feeding extensively in the small-flowered E. viminalis (Chapter 2). This was an individual flowering profusely out-of-season. At other times at Bombala, flowering trees were ignored despite the heavy flowering of a large flowered species such as E. cypellocarpa. Thus, nectar feeding appears less related to flower size than to some component of the abundance of other food resources. This requires further investigation. At Kioloa, other food types tended to be important in the diet only in the absence of eucalypt blossom. The abundance of the other food types at such times is unknown. However, the extensive use of sap in winter 1986 and honeydew in winter 1987 suggests these food types had varied in abundance from one year to the next. One individual Acacia mabelliae was used by one glider group for gum in spite of this species being relatively common throughout the study area. Why more individual trees were not used by this and other glider groups is not known. Gliders made typical incisions into the trunk of this tree from which gum exuded day and night. This suggests that other individual trees did not freely exude gum, and this may represent a situation analogous to that of glider sap feeding, where feeding appears contingent on the sap flow idiosyncrasies of a few trees (see Chapter 3). Only a very small proportion of the feeding observation time was devoted to arthropod feeding. This may be slightly underestimated due to the difficulty of maintaining visual contact with gliders as they moved between exudate trees. However, also of importance was the much lower abundance of suitable substrates as sources of arthropods at Kioloa. At Bombala (see Chapter 2) arthropods were principally harvested by stripping back loose bark or by breaking open hanging bark ribbons. At Kioloa, E. maculata was the only tree which had a completely smooth trunk from which to shed bark. When this species shed its bark the pieces flaked off in small patches (giving the so-called 'spotted' appearance) but most importantly, it did not provide refuge for arthropods (pers. obs.). Only when the very fine branches (ca. lcm diameter) in the canopy shed their bark were the gliders observed utilising this substrate, and then to feed on the honeydew underneath. Eucalyptus pilularis is a tree 81 with two-thirds of its trunk consisting of smooth bark. However, no field trip coincided with the bark shed of this species. Some loose bark did usually hang from the boundary with the rough bark from which gliders occasionally peeled back the bark in search of arthropods. In general, hanging loose bark, which was an important substrate for arthropods at Bombala (Chapter 2) was absent at Kioloa. The dearth of observations of gliders feeding on arthropods may also be explained by the abundance of an alternative source of protein. Turner (1984a,b) suggested that some marsupials which regularly feed on nectar may obtain dietary protein from pollen. Since then field studies on the sugar glider have reported the apparent digestion by gliders of banksia and eucalypt pollen (Goldingay et al. 1987, Howard 1989). Smith and Green (1987) found that the sugar glider has a very low nitrogen requirement which may be satisfied by a relatively small component of pollen in the diet. The faeces of yellow-bellied gliders examined when trees were flowering contained very high densities of eucalypt pollen, and a large proportion (ca. 60%) of the pollen was devoid of cell contents suggesting that the pollen had been digested (cf. Turner 1984a,b, Goldingay et al. 1987). Thus, it appears that most dietary protein may be obtained by pollen digestion. 5.4.2. Nectar Foraging Behaviour. Since 1974 there has been a steady increase in the number of studies which have examined some aspect of the foraging behaviour of nectar-feeding bats (Heithaus et al. 1974, 1975, Sazima & Sazima 1977, 1978, Gould 1978, Lack 1978, Howell 1979, Howell & Hartl 1980, Helversen & Reyer 1984, Lemke 1984). Most of the studies on nectar-feeding bats (Baker & Harris 1957, Start & Marshall 1976, Lack 1978, Howell 1977, 1979, Gould 1978, Sazima & Sazima 1978, Heithaus et al. 191 A, Voss et al. 1980, Kress 1985, Crome & Irvine 1986) have examined foraging specifically to assess the probable role of bats in pollination. The foraging behaviour of non-flying nectar-feeding mammals has been virtually overlooked. Two exceptions are Hopper and Burbidge (1982) and Terborgh and Stern (1987). The former study provided some preliminary data on flower probing and visitation by the honey possum (Tarsipes rostratus), the sole nectar- and pollen-dependent non-flying mammal. This study was unusual in that these possums, although normally nocturnal, may be observed feeding during daylight under cloudy conditions (Hopper & Burbidge 1982). The latter study provided basic information on the abundance of a nectar resource and visitation to it by the saddle-backed tamarin (Saguinus fuscicollis), a diurnal non-flying mammal. The majority of non-flying mammals which visit flowers are small nocturnal rodents, prosimians and marsupials (Turner 1982, 1983), which probably accounts for the absence of studies detailing the influence of changes in the abundance of a nectar resource on the foraging behaviour of a non-flying mammal. The present study is the first to provide details of the nectar foraging behaviour of a nocturnal non-flying mammal. 5.4.2.1. Nectar production. Various sampling regimes revealed substantial variation in nectar secretion both within and among individual E. gummifera. The length of the interval between sampling did not influence the secretion rate although this has been reported in other plants (Gill 1988b). Secretion varied from 0.8-3.0 microlitres per hour. Four of the five trees sampled showed significant temporal variability in secretion rate but no consistent pattern was observed. Temporal variability in nectar production has been described in detail by Zimmerman and Pyke (1986) for an herbaceous perennial plant and by Frankie and Haber (1983) for several species of mass flowering trees. However, several previous studies which examined nectar production in eucalypts have failed to consider such variability (e.g. Bond & Brown 1979, Pyke 1985). There also apppeared to be differences in nectar secretion among the trees sampled in this study. Whether variation exists within a tree is not known but this is likely since flowers of different ages occur within a given tree and may secrete at different rates. Standing crops of nectar measured for two out of four trees were considerably higher at night than during the day. However, considerable variation was observed (range: 0-9.2 [il/flower). Time constraints prevented conducting observations on foraging gliders during the field trip when nectar sampling was conducted so it is not known whether the trees sampled were in fact similar, in total number of flowers, to those that gliders were feeding in. The main conclusion to be drawn here is that trees were continuously secreting nectar over 24h, but the rate of secretion may vary within the forest. 5.4.2.2. Influence of flower number. Gliders were highly selective when nectar feeding, choosing trees with 2-3 times as many flowers as those on transect trees. This was a feature of their foraging behaviour during periods of both abundant flowering and sporadic flowering. Generally, gliders accommodated decreases in the abundance of the flowering resource (i.e. the total number of trees in flower) by choosing trees with relatively fewer flowers than at times when flowering trees were abundant. For example, during April 1987 flowering E. gummifera were extremely abundant (ca. 16/ha) and gliders fed in trees with an average of 12700 flowers. One month later the number of flowering trees had declined dramatically (1/15 of the earlier abundance) and gliders fed in trees with an average of approximately 3000 flowers. However, in doing so they were still choosing trees with three times as many flowers as transect trees. The number of flowers in a tree was positively correlated with tree girth. Therefore, gliders may simply select larger trees which are flowering. Leighton and Leighton (1982) similarly invoked a relationship between tree girth and fruit crop 83 to explain aspects of monkey foraging. Olfaction would certainly play a role in locating flowering trees, and familiarity with the home-range would allow gliders to know the location of particular flowering resources. This may be critical at times when few trees were in flower, such as in June 1988 when there was only one or two flowering trees in each of two home-ranges. Similarly, at Bombala in July 1986, one pair of gliders fed extensively in a flowering E. viminalis, the only flowering tree observed throughout the whole study area (Chapter 2). Clearly, gliders showed a preference for trees containing greater than average numbers of flowers. This leads directly to an examination of whether the number of flowers present in a tree determined visit duration. Gliders spent the greater proportion (90%) of their time outside their dens foraging. The amount of time spent in a tree (tree time utilisation; see Chapter 4) should therefore reflect some trait of the abundance of that food resource. When flowering trees were super-abundant (e.g. April 1987) there was no apparent relationship between the number of flowers in a tree and the duration of visits by gliders. Flowering trees were very close to one another (13.0m) so that it may have been more profitable for gliders to move to new resource patches more often (e.g. Charnov 1976, Pyke 1978a). At intermediate levels of floral abundance (e.g. May 1989) gliders foraged in trees for a time related to the number of flowers in a tree. At low abundance levels, flowering trees were much further apart so that on some occasions it may have been more profitable for gliders to remain for longer periods in trees. This was apparent for one glider in February 1989 which fed in a large flowering tree for more than 4.7h compared to a glider on the previous night which had fed in the same tree for only 0.8h. Moreover, in April 1987 one glider fed in two nearby trees for over 6h. Thus, although largely unquantified, it appears that at extremely low abundances of flowering trees, gliders may choose to feed for long periods (possibly whole nights) in just a few trees. This is analogous to when gliders feed on eucalypt sap. At such times only one or two trees are available for use and gliders may remain feeding in the one tree all night (Chapter 3). When nectar feeding, gliders systematically foraged through a tree and therefore probably harvested nectar from nearly all available flowers before having to revisit any flowers, by which time nectar will have accumulated (see Pyke 1978b, 1982). Thus, gliders employ a foraging strategy which utilizes two options. Either they remain feeding in one tree for very long periods of time or they can move more frequently if food resources are abundant. Studies are now required on the energetics of foraging gliders in order to understand this foraging strategy. Until such a time it is pointless speculating on the number of flowers from which a glider must harvest nectar or pollen in order to satisfy its energy requirements (see Henry 1985 concerning P. breviceps). 5.4.2.3.Group foraging. Leighton and Leighton (1982) demonstrated a relationship between the size of the feeding aggregate in howler monkeys (Alouatta 84 palliata) and the size of a food patch. Yellow-bellied gliders have been reported to be normally solitary when they forage (Henry & Craig 1984). At Kioloa, gliders were often (38% of observations) observed foraging together in the same trees and there was no difference among different food types. This probably reflects a greater density of gliders at Kioloa (see Chapter 7) but highlights the point that the rate of renewal of exudate resources allows group foraging (cf. Waser 1981). Gliders at Bombala only tended to feed together when engaged in sap feeding (Chapter 4). This food type was the most highly clumped and probably had the highest rate of renewal. In contrast, food obtained from beneath loose bark (e.g. arthropods) would be removed with the substrate and would be slowly renewed (i.e. as further substrate becomes available as bark continues to be shed from a tree) or not renewed. Henry (1985) found sugar gliders also made extensive use of the loose bark substrate and suggested that the slow renewal would result in sugar gliders foraging in different patches on consecutive nights. For the yellow-bellied glider, the slow rate of renewal would make it disadvantageous for more than one glider to forage in the one tree together and this presumably accounts for the small number of observations of group foraging for that substrate. 5.4.2.4. Nectar losses to other animals. Several other mammal species were observed feeding on nectar in the same trees as yellow-bellied gliders. An attempt was made to record the abundances of these animals. However, the smaller size of the feathertail glider (lOg) and the sugar glider (120g) made this difficult except in trees with good visibility into the canopy. Grey-headed fruit bats (Pteropus poliocephalus) were also common visitors during several sample periods. Borsboom (1982) described several observations of interactions between bats and gliders from which he inferred support for an hypothesis of Sussman and Raven (1978). This hypothesis, based largely on the world-wide distribution of flower-visiting bats and non-flying mammals, states that "there appears to have been .... competitive exclusion on a grand scale involving flower-visiting bats". Inferred from this is that bats are competitively superior and Borsboom then described what he considered to be interference competition. However, two out of the four observations described involved the folivorous greater glider (Petauroides volans), which generally only supplements its diet with flowers by eating them whole (Kavanagh 1987c) and therefore it was not an appropriate comparison. At Kioloa, several interactions were observed between grey-headed fruit bats and yellow-bellied gliders. In May 1989, a subadult glider was observed as it was chased down the trunk of a flowering tree by a vocalising bat advancing along a major branch. The glider glided out of the tree and the bat returned to the blossom and resumed feeding. On subsequent nights an adult glider was observed to vocalise at a bat which had approached and vocalised at it. The glider continued nectar feeding 85 without any apparent concern for the presence of the bat. On another occasion when a fruit bat directed vocalisations at a subadult glider, an adult glider in an adjacent tree emitted a loud vocalisation which was answered by the subadult. On another night a glider climbed past a fruit bat which directed calls at it. The glider called back and continued climbing. These observations suggest that yellow-bellied gliders are not aggressively excluded from flowering trees by fruit bats. The inverse relationship between nectar-feeding bats and non-flying mammals referred to by Sussman and Raven (1978) can probably be explained in terms of the feeding specialisation and requirements of the two groups. Fruit bats can only obtain enough nectar from certain habitats when there is a high intensity of flowering, otherwise they will feed on fruits, a resource not present in eucalypt forest (Parry-Jones 1987). At Kioloa, fruit bats were only observed during sample periods when there was an abundance of flowering trees (Table 5-6). It is possible that their protein requirements preclude the permanent occupation of temperate areas. Non-flying mammals can obtain protein from arthropods scattered throughout the habitat whereas bats do not eat arthropods (possibly because their anatomy prevents them from searching for both concealed and surface active prey) and must obtain protein from pollen digestion. They also live in large groups and so cannot remain in an area unless there are sufficient flowering trees to meet the protein requirements of many individuals. Their mobility allows them to make use of areas of superabundant flowering on occasion. However, it is this mobility which allows them "superiority" in tropical areas as nectar feeders. Also, tropical forests have an abundant diversity of plants with fleshy fruits, a food resource notably absent from temperate forests. Thus, nectar-feeding non-flying mammals with a diet of other exudates and a more easily satisfied nitrogen requirement can survive in such forests. 5.4.3. Pollination bv Gliders? An important adjunct to an examination of the foraging pattern of yellow-bellied gliders is to consider whether they actually effect pollination of these trees. Several factors are relevant to this: (i) whether gliders transfer pollen as they feed, (ii) whether they groom pollen from their fur after they feed, (iii) how much time they spend in a given tree (this may reflect how much self-pollen versus cross-pollen they may transfer), and (iv) how far they move between trees. Undoubtedly, gliders accumulate large loads of pollen on their snouts during their prolonged periods of nectar feeding, and high densities of eucalypt pollen were observed in the faeces of gliders. Such a situation has been described for sugar gliders when feeding at Banksia spinulosa inflorescences (Goldingay et al. 1987). It is unlikely that yellow-bellied gliders deliberately groomed pollen from their snouts as they fed because gliders were not observed to give undue attention to their snouts when they groomed. In May 1989, on only two out of 10 occasions when gliders were observed immediately before they 86 departed from a flowering tree did they engage in grooming. Typically, gliders travelled from one flowering tree to another and recommenced nectar feeding without engaging in grooming. Presumably, when they visited successive flowering trees they carried heavy loads of pollen from the previous tree. A similar conclusion has been reached by Goldingay et al. (In prep.) for sugar gliders feeding on nectar from Banksia spinulosa, despite observations that these gliders, at least occasionally, deliberately harvest pollen from flowers. Pollen harvesting has been observed in the honey possum when feeding at the flowers of Banksia and Eucalyptus (Russell 1986). Yellow-bellied gliders presumably transfer considerable amounts of cross-pollen to the first few flowers or inflorescences of successive trees, in a way similar to that found for insects and hummingbirds (e.g. Thomson & Plowright 1980, Waser & Price 1982, Thomson et al. 1986), but substantial carry-over of cross-pollen may occur within a tree (i.e. many flowers may receive a few grains). The length of time gliders spent in individual flowering trees is of particular importance. The longer the visit the greater the amount of self-pollen that will be transferred to flowers (e.g. Paton and Ford 1983). Mass-flowering, such as that by trees like Eucalyptus, is expected to lead to "pollinator constancy" in the one tree (Augspurger 1980). This did indeed occur and in May 1989, yellow-bellied gliders spent an average of 70.1 (± 9.5 s.e.; n=15) minutes per tree. In contrast, fruit bats spent only 8.9 (± 1.7; n=7) minutes per tree, indicating that different mammalian visitors were capable of different nectar feeding strategies. This suggests a large capacity for self-pollen to be transferred by gliders whereas bats may transfer considerable amounts of cross-pollen. However, pollen deposition on glider snouts may occur in layers (see Lertzman & Gass 1983) and accumulation of pollen may be substantial. Thus, pollen may not be quickly transferred or lost after feeding is recommenced in each subsequent tree. Examination of the pollen loads carried on the snouts of sugar gliders feeding in Banksia spinulosa revealed the capacity to carry thousands of grains of pollen (Goldingay et al. 1987, In prep.). Also worthy of note is the distances travelled by gliders between flowering trees. When flowering trees were at high density, as in May 1989, gliders could sometimes simply climb between adjacent flowering trees and therefore not transfer pollen over large distances. This is reflected in the distances between flowering trees which averaged 15m (trunk to trunk) at this time. Waser (1982) suggests that interactions between plants and their pollinators probably involve a "conflict of evolutionary interest" such that pollinators will tend to move short distances between flowering plants. However, at other times such as May 1987, flowering trees were on average 50m apart so that although gliders may still only move minimum distances between trees, pollen would in fact be carried larger distances. Furthermore, unless all pollen is lost in the first tree (see Waser & Price 1982) gliders may be responsible for the transfer of cross-pollen over considerable distances (see above). 87 Whether or not gliders predominantly transfer self or cross-pollen may have little significance if these eucalypts exhibit preferential outcrossing. Previous studies on eucalypts have shown that although production of seed from self pollination can occur (Brown et al. 1975), seed set may be greater from cross-pollen and in the presence of both self and cross pollen, the latter may be favoured (Griffin et al. 1987). Whether the predominant transfer of self-pollen, as may occur when yellow-bellied gliders are feeding, leads to stigma clogging or pre-emption of cross-pollen (e.g. Bertin 1986, Waser & Fugate 1986, Bertin & Sullivan 1988) is not known. However, the relatively rare events when gliders transfer cross-pollen may in fact, be very important in maintaining high levels of outcrossing among seeds (see Lertzman & Gass 1983). Eucalypts tend to have morphologically unspecialised flowers which allows visitation and perhaps pollination by a wide range of vertebrates and invertebrates (Ford et al. 1979). Such a generalised pollination system may provide better options for preferrential seed development (e.g. Crome & Irvine 1986). Only in very specific circumstances could it be expected that selection might favour the evolution of a eucalypt pollination system suited to only one group of pollinators (Hopper & Moran 1981). The flowering eucalypts in this study secreted nectar continuously day and night, and typical of mass-flowering species (Augspurger 1980), attracted a large array of potential pollinators. This included three other mammal species and numerous birds and insects. These other vectors may individually transfer much greater amounts of cross-pollen than that by yellow-bellied gliders because they spent shorter periods visiting individual trees (pers. obs.). Further studies are obviously required for a better resolution of the role of mammals in the pollination of eucalypts. Chapter 6. SOCIOECOLOGY OF THE YELLOW-BELLIED GLIDER, Petaurus australis, AT BOMBALA AND KIOLOA. 6.1. INTRODUCTION. The mating system, reproduction and group size of the yellow-bellied glider (Petaurus australis) have been the subject of study at three sites; Herberton in north Queensland (Russell 1980, 1984), and Glengarry North (Henry & Craig 1984) and Cambarville (Craig 1985) in Victoria. In Victoria, gliders occupied exclusive home-ranges and showed a monogamous mating system. In north Queensland, gliders also occupied exclusive home-ranges but a polygynous mating system was evident. Yellow-bellied gliders have therefore been considered facultatively monogamous (Lee & Cockburn 1985). It has been suggested that the difference in the mating system among sites reflects a difference in the abundance and cost of harvesting food resources (particularly arthropods) in temperate and tropical eucalypt forest (Lee & Cockburn 1985). In temperate eucalypt forest, food resources are presumed to be seasonally sparse and temperatures relatively lower, thus resulting in higher energetic demands. Implicit here is a limitation on breeding opportunities due to such foraging constraints. The diet of the yellow-bellied glider consists predominantly of plant and insect exudates (Chapters 3,4, Smith & Russell 1982, Henry & Craig 1984, Craig 1985, Kavanagh 1987a,b). Dietary protein is provided mostly by arthropods (Chapter 3, Henry & Craig 1984, Kavanagh 1987a,b) but pollen digestion may also provide protein on occasion (Chapter 5, Smith & Russell 1982). Protein is of fundamental importance to the growth and development of all young animals and its relative scarcity in the environment is thought to be a major factor regulating their numbers (White 1978). If protein is only seasonally abundant, it may influence the timing of reproduction for petaurid marsupials (e.g. Smith 1982a). If, however, arthropod abundance is relatively invariable then exudate availability may become crucial (Smith 1984a). Studies on the socioecology of the yellow-bellied glider are presently too few to allow generalisation of the factors responsible for differences in mating systems among sites but existing studies do suggest that gliders occurring in comparable habitat (e.g. tall open forest in Victoria) will display the same mating system. Furthermore, consideration of reproductive data from Victorian sites, including a coastal site (Wingan Inlet), led Craig (1986) to suggest that gliders tend to produce one young in alternate years. In contrast, gliders in north Queensland often produced young in successive years (R. Russell 1984) which may further corroborate the suggestion of Lee and Cockburn (1985) of a greater arthropod abundance in north Queensland. The aim of the present study was to provide data on the mating system, group dynamics, reproduction and longevity of the yellow-bellied glider at two sites in N.S.W. The absence of studies from this state have been apparent in discussions of the socioecology of this species to date. Furthermore, data on the availability of the food resources and their use by yellow-bellied gliders at both sites are sufficient to construct a model which is related to the pattern of reproduction. 6.2. METHODS. 6.2.1. Trapping. 6.2.1.1. Bombala. Wire cage traps (measuring 20 cm x 20 cm x 56 cm) were attached to horizontal platforms on tree trunks and placed at heights of 2-12 m above the ground. Traps were baited with creamed honey and a honey-water solution was squirted on to the tree's trunk above the trap using an oil can. In 1984, an aluminium ladder was used to set traps but the logistics of carrying this to all trap-trees necessitated the construction of permanent ladders fixed to these trees (Plates 6-la,b). Traps were usually placed only on sap-site trees (trees incised by gliders to obtain sap; Chapter 3) but two den trees (trees containing hollows to which gliders retired during the day) were trapped briefly, one in August 1984 and the other in July 1985 (Plate 6-2a). Neither den tree yielded any captures and were not used in subsequent trapping. Traps were widely spaced throughout the study site (Fig. 6-1), being contained within the home-ranges of three glider groups (A, B, C) (see Chapter 7). At least two other glider groups had home-ranges adjoining those of the study groups. In home-range C, several traps were placed on E. fastigata sap-site trees at a height of 5 m above the ground. No captures were made here until two fixed ladders were constructed in 1986 enabling traps to be placed at 8 m and 12 m above the ground. Trapping of gliders at Bombala occurred between January 1984 and Januray 1989. 6.2.1.2. Kioloa. Gliders were captured as described above for Bombala. Trap platforms were attached to 10 trees (Fig. 6-2), eight of which had permanent ladders erected on them. Five of these trees were E. gummifera sap-site trees, one was a E. gummifera non sap-site tree, two were large E. maculata at the northern end of the study site, three were E. piperita honeydew trees and one was an Acacia mabelliae in which gliders had been observed feeding extensively on gum. Regular censuses of three yellow-bellied glider groups were conducted to allow an accurate assessment of the number of gliders in each group. Observations of marked individuals in 1986 indicated the approximate boundaries of glider group 90 ~^~^~t •• JR.--' X-'J--- sSsjS^^e JQ c 5) t) CM c P. a rci (L)« * Ui /** fs •r1 £X i^* *-£ Fig. 6-1. Study site at Waratah Creek, Bombala, and the location of trap trees (solid circles) contained within three glider group home-ranges (A,B,C). The approximate boundaries to these are indicated by the large dashed line. The smaller dashed lines indicate creeks. The large square represents the study area (100 ha) of Kavanagh (1984). The area to the left of this had forested margins adjoining the Coolangubra State Forest which were cleared by January 1986. Fig. 6-2. Study site and location of trap trees (T) at Kioloa. Single dashed lines indicate creeks and the double dashed line indicates a logging track. 94 home-ranges which consequently enabled censuses of the number of gliders in a group to be conducted at least annually. Attempts were made to locate den trees during most field trips in 1987, 1988 and 1989 by conducting observations at dusk in areas located either from calls of gliders early in the night or by following gliders prior to their return to dens before dawn. Two observers were often employed to do this. Although specific den trees could not be located initially, the approximate position was determined for the three groups under study and the number of gliders departing (at dusk) and arriving (at dawn) was determined. The vocalizations of gliders facilitated this. 6.2.2. Glider Marking and Measurement. Captured gliders were weighed, sexed, reproductive condition noted and dentition examined. Adult gliders were distinguished by their deep-yellow ventral fur (Plate 6-2b), and by the presence of cracked and discoloured incisor teeth. Subadults could be distinguished by their white ventral fur (which could also be detected with binoculars and spotlight), their white unworn incisors and sometimes their smaller size (when juvenile). Adult females often showed evidence of reproduction (see below) and adult males had obvious, secreting scent glands (Craig 1985). Metal tags (fingerling fishtags) to which a piece of reflective "scotchlite" tape had been attached using "supaglue", were placed at the base of the ear of each captured glider. Thus, gliders were given a unique colour-tag-ear combination which enabled identification of individuals by spotlight while conducting extensive observations on their foraging behaviour (see Chapters 4,5). Spotlighting was particularly useful for establishing the presence of known animals in the area when gliders could not be trapped. In addition, six gliders at Bombala and four at Kioloa were fitted with radio-transmitters at various times during the study. Known den trees were monitored (see Chapter 4) and assisted in establishing the presence of particular individuals. 6.2.3. Reproduction. Pouches of females were examined to assess reproductive condition. Several reproductive events (i.e. small teats indicative of non breeding; pouch young; mammary tissue indicative of lactation; elongated teat) were identified. On occasion a nestling was observed climbing near a den hollow and this was considered indicative of late lactation. From these observations it was possible to extrapolate back to the possible month of birth, assuming a pouch life of 100 days and nestling life of 50 days (R. Russell 1984). It is further assumed that young are weaned by the end of the nestling stage and that the teats then regress over the ensuing month. Descriptions by Suckling (1984) and Craig (1985) assisted in assessing pouch condition. 95 6.2.4. Food Resource Abundance Model. A stylised model was constructed to represent the annual pattern of availability and abundance of the food resources of yellow-bellied gliders at Bombala and Kioloa. This is based on the indices of food availability and glider feeding observations (Chapters 2,3,5). This model will be described in the discussion and related to the pattern of glider reproduction. 6.3. RESULTS. 6.3.1. Bombala. 6.3.1.1. Trapping. Between January 1984 and January 1989, 17 individual gliders were captured a total of 53 times (Table 6-1). Trap success in any given year was low, varying from 3.6% in 1984 to 9.1% in 1986. However, trapping was conducted during January of each year with trap success ranging from 15% in 1984 to Table 6-1. Trapping data for yellow-bellied gliders at Waratah Creek, Bombala. The number of individuals captured are shown in parentheses. Year Month No. trap-nights No. captures Trap success 1984 Jan 40 6(5) April 72 0 May 40 1(1) June 40 0 Aug/Sept 64 3(3) Oct 32 0 Dec 48 2(2) Subtotal 336 12 3.6% 1985 Jan 45 5(3) Feb 24 0 April 22 4(4) July 32 0 Sept 41 0 Subtotal 164 9 5.5% 1986 Jan 106 6(4) July 67 10(4) Dec 48 4(4) Subtotal 221 20 9.1% 1987 Jan 48 3(3) 6.3% 1988 Jan 29 2(2) 6.9% 1989 Jan 56 7(6) 12.5% Total 854 53 (17) 6.2% 96 5.7% in 1986. Total trap success averaged 6.2% throughout the 61 months of the study. Most (79%) captures occurred during periods of major sap feeding. At these times some individuals became extremely trappable. Other captures probably occurred when gliders were visiting sap-site trees in order to test for sap flow (see Chapter 3). 6.3.1.2. Body Weight Measurements. Gliders fluctuated markedly in body weight. Using data for the weight of adults at the time of first capture, males (x = 631.3 g ± 23.0, s.e.; n = 8) were significantly (t = 2.34, df = 11, P <0.025) heavier than females (556.4 g ± 16.0, n = 5). Only one out of nine adult males ever weighed less than 500 g (485 g when first captured and 494 g two years later) and this was excluded from the analysis above. One subadult female weighed 490-510 g and a subadult male 455 g. Individuals captured at least threetimes illustrate clearly the sort of fluctuations that may occur in body weight over time (Fig. 6-3). Yellow-bellied gliders could be expected to increase in weight with age, as has been found in the sugar glider, Petaurus breviceps (Suckling 1984) and Leadbeaters possum, Gymnobelideus leadbeateri (Smith 1984b), but in this study, maximum weight for some animals occurred at their first capture (F3, M9, F15) and for one, body weight remained relatively constant (Ml). There was no indication that body weight undergoes a regular seasonal fluctuation. For example, some gliders had high and low weights for summer (M9, F3, F15, F6) while others showed little change from summer through to the following winter (Ml, F15). 6.3.1.3. Glider Groups. Yellow-bellied gliders at Bombala had a social group structure similar to that observed by Henry and Craig (1984), consisting of an adult male and female and subadult offspring. At any one time during the study three glider groups occupied the area where traps were located and the home-ranges (A, B, C) of glider groups were exclusive (Chapter 7). Three glider groups were present at the beginning of this study but three different glider groups were present at the completion of the study (Fig. 6-4). Groups 1 and 2 were present in January 1984 in home-ranges A and B, respectively. The adult female in group 1 (F5) had disappeared by October 1984. At this time the adult male (M9) was associating with two untagged gliders. In December 1984 a new adult female (F12) was captured with the adult male (M9). A transmitter was attached to the female (by R. Kavanagh) but this animal disappeared several days later suggesting that it had been a transient. Other individuals to which transmitters had been attached wore these for long periods (up to six months) without obvious alteration to their behaviour. By February 1985, gliders in this group had disappeared and an untagged pair (group 4) was located using this home-range (A). They were not captured until April 97 03 oo oo t-i "-H 00 o a CD 13 £. ^- T3 W>"> •t-H mal e hos e D *-• *~ >, rt o 4-1 CO 2 "SL > w OJ [I I I I I 1 I I I I I ' I • I ' ' ' ' I ' o o o o o o w o m o fs. (O (0 IT) >0 (6) *q6.i9M 1984 J- M9,F5 M8,F3+PY.F4 M- M- 0 y +N M100+ 5U J- : s" ; M9,2U t N- M100+ 1985 J- v : u M1,F6 M8.F3 • M- • • +N I M- < • j- b «• M8 ? S- J_ — N- 1986 J- +S M65.F4 2JJ M- ; M- I J- +PY.M16 F15+ S- N- > +S F15.M59, 1987 J- rot M60 1988 J - F6 + +S 1989 J- F6+N.F20.M61 N •+N M59iM62+ i i i i i 1 4 2 5 3 6 4 , , 1 * ' 1 B Fig. 6-4. Composition of six glider groups occupying three home-ranges (A,B,C) at Bombala. Groups of known composition are indicated by double lines. Dotted lines indicate groups of unknown composition. The plus sign indicates that additional gliders were presumed to be present in the group. The number of untagged (U) individuals is indicated where known. The presence of subadults (S), nestlings (N) and pouch young (PY) is indicated. F4 was a subadult in January 1984. 99 1985, by which time they had a nestling (noticeably smaller in size than the adults) which could be seen peering from the den and occasionally climbing about the den tree but not venturing from this tree. A subadult was observed in this group in January 1986 and possibly the same individual (M16) was captured in July 1986. The adult pair (F6, Ml) were still present in December 1986 but the lower incisors of the adult male were worn right down, protruding only 2mm from the gum and this glider presumably disappeared in the next six months. This group was not censused fully again until January 1988 when the adult female in this group (F6) was present with two untagged animals (Fig. 6-4), all of which used the same den tree. This den had been used predominantly since February 1985 (two other den trees were located during this period; one in January 1986 and another in July 1986). Three animals still shared the same den in January 1989 and two untagged gliders captured; this group then included F6, an adult male M61 and a subadult female F20. Group 2 occupied home-range B and consisted of three animals (an adult pair and one subadult) in January 1984 (Fig. 6-4). The subadult F4 was observed in January 1985 but had disappeared by February 1985. In July the adult female F3 died in a trap and vocalizations were heard from a single animal in September, presumably from adult male M8, but which could not be located. By January 1986 two new gliders (new male M65 was captured) occupied this home-range (Group 5). In January 1987, F4 (the subadult from group 2) was recaptured in this home-range and at this time she had an elongated teat indicating that she had been lactating (she had probably given birth in the previous July-August; see below). The reflective tape had been lost from the ear tag and it is presumed she was the glider observed with M65 in January and July 1986. A third glider was heard calling in this home-range in December 1986 and January 1987 which was presumed to be her offspring. In January 1988, a subadult (small body size and white ventral fur) was observed foraging together with the adult pair. Both adults were present in January 1989 and F4 was lactating. In home-range C only one glider (M100) was tagged before January 1986. This adult male was captured in April 1984 (by R. Kavanagh), using arifle to shoot down branches on which this glider was climbing. It was observed frequently up until December 1984 but not observed subsequently. One observation (R. Kavanagh pers. comm.) in May 1984 indicated that the group in this home-range contained at least six gliders (five untagged gliders were seen on one sap-site tree). At least two gliders were seen in this home-range in January 1986 (an adult female (F15) was captured) but whether this represented a continuance of the original group is unknown. For simplicity the gliders captured in 1986 and subsequently are referred to as group 6. Due to the difficulty in capturing gliders in this home-range it was difficult to assess how many animals were contained in the groups here. Adult F15 was still present in January 1987. One adult male (M59) and a subadult male (M60) were captured in December 1986 (M60 was also captured in January 1987). The latter glider had an adult body weight (535g) but subadult characteristics (i.e. no incisor wear and yellow/white belly fur). In January 1989, M59 (weighing 563g) and a new male glider (M62; weighing 595g) were captured. Both had active scent glands. The latter male had little wear on its incisors. Difficulty in locating gliders in this home-range precluded determining the presence or absence of other gliders in January 1988 and 1989. 6.3.1.4. Reproduction. The reproductive status of females was determined for four gliders captured over at least 12 months (Table 6-2). Although females have two teats, examination of the pouches of these females revealed nine instances of a single young being produced (only a single teat was ever elongated). One further breeding record was obtained (a nestling observed) from an unstudied group adjacent to the study area. Two pouch young were recorded during the study: one born to F3 in December 1983 (in home-range B) and one born to F6 in June 1986 (in home-range A). In home-range B an untagged glider was seen in the den and on some adjacent honeydew trees in June 1984 but not again after this. Examination of F3 during the subsequent 11 months showed no further reproduction (Table 6-2). A nestling, observed exploring the den tree of F6 and Ml (in home-range A) in April 1985 was probably bom in December 1984, assuming a pouch life of 100 days and nestling life of 50 days (R. Russell 1984). In January 1986, F6 was recorded with an elongated teat indicating a birth in 1985. At this time there was only one subadult present and unless the nestling from April 1985 had dispersed at less than 13 months of age, one young had died. A pouch young was bom to F6 in June 1986 and a subadult was present. In January 1988, two untagged gliders were using the - den with F6, which was not breeding. In January 1989, F6 was again lactating and a nestling was observed in the den. The subadult F20 present at this time was inferred to be an offspring of F6. Two adult females from different groups were lactating in January 1987 (Table 2). One glider (F15) had been recorded lactating in January 1986 and the other glider (F4) was again lactating in January 1989. Thus, out of ten reproductive events observed, all births occurred from early winter through to early summer (June - December). Seven occurred from July through to September. Thus, weaning would take place five months later in December-February. One female (F6) reproduced at least four times in five years and another female (F4), at least twice in three years. One female (F3) captured relatively frequently over 18 months had a subadult (F4) in its group (approximately 12 months old) when captured with a pouch young in January 1984 (i.e. two young in two years) but did not breed again in the ensuing 12 months. The fourth glider (F15) also apparently bred in successive years. Table 6-2. Reproductive events recorded at Bombala, N.S.W., from captured females and/or den observation. The extrapolated birth month has used data on pouch and nestling duration from R. Russell (1984). NB= non-breeding; PY= pouch young; L= lactating (mammary gland expanded) and therefore nestling present; N= nestling observed in den tree and therefore soon to be weaned; ET= elongated teat which has not yet regressed indicative of the conclusion of lactation or lactating in previous month. Female Group Month/Year Event Extrapolated month of birth F3 2 Jan 84 ~~~ PY December 83 May 84 L Jan 85 NB April 85 NB F6 4 April 85 ET, N December 84 Jan 86 ET July-Aug 85 July 86 PY June 86 Jan 88 NB Jan 89 N-lateL July-Aug 88 F4 2/5 Jan 84 NB NB Sept 84 NB Jan 85 ET July-Aug 86 Jan 87 L July-Sept 88 Jan 89 ET July-Aug 85 F15 6 Jan 1986 NB July 86 L Dec 86 ET July-Aug 86 Jan 87 N Aug-Sept 84 FU 1317 Jan 85 6.3.1.5. Dispersal. Data suggest that subadults disperse from their natal home-range when 18-24 months old. The subadult (F4) encountered in January 1984 in group 2, when approximately 12 months old (weighing 500g), was last seen in January 1985 at approximately 24 months of age. The pouch young of F3 born in December 1983 was observed on the den tree in June 1984 but had disappeared by August (it would have been nine months old) but the subadult F4 was still present and it is concluded this young had died. A subadult born to F4 in approximately July-September 1986 (see Table 6-2) was present (only spotlighted) in January 1988 when approximately 15 months old but had disappeared prior to January 1989. Subadults may not disperse until they have attained adult weight and characteristics such as yellow ventral fur and, on males, active scent glands. Therefore, gliders would probably not breed before they were two years old. 6.3.1.6. Longevity. A subadult (F4) of approximately 24 months of age (in January 1985) spent up to 11 months as a transient before establishing itself in its natal home-range (see above) where it was still present in January 1989, giving it an age of 102 six years. Another animal (F6) which was first observed in the study area in February 1985 (had reproduced in December 1984-see Table 6-2) was still present in January 1989, giving an age of at least six years, assuming it was two years old when it first reproduced. One male (M65) which became resident in January 1986 was still present in the last survey in 1989. Therefore, assuming it was two years of age when it became resident, it was five years old. 6.3.2. Kioloa. 6.3.2.1. Trapping. Between February 1986 and May 1989, 32 captures of gliders were made from 421 trap-nights averaging 7.6% trap success (Table 6-3). This represented 16 individuals from three distinct home-ranges. There was no statistically significant difference between trap success at Bombala and Kioloa (%2 = Table 6-3. Trapping data for yellow-bellied gliders at Kioloa Year Month No. trap-nights No. captures Trap success 1986 Feb 16 2 April 21 4 Aug 33 11 Oct 30 1 Dec 33 0 133 18 13.5% 1987 Jan 30 0 April 26 0 May 32 2 July 26 2 Dec 26 2 140 ~6 4.3% 1988 April 6 2 May 10 0 June 43 1 July 1 1 60~ 4 6.7% 1989 Jan 15 0 Feb 8 0 May 30 1 July 6 0 Aug/Sept 33 4 92~ 1~ 5.4% Total 425 33~ 7.8% 0.77, P >0.25). Most captures (50%) were made in 1986 when gliders fedextensively on E. gummifera sap in August and Acacia gum throughout much of the year (see Chapter 5). Subsequent to this, all sap-site trees received little attention during field trips and few captures were made. Traps were also set on trees used for honeydew and this yielded some captures during this later period. 6.3.2.2. Body Weight Measurements. Gliders fluctuated markedly in body weight at Kioloa. Adult males (x = 635.8 ± 31.2 g; n = 6; range 555g-725g) were significantly (t=2.22, df=12, P <0.025) heavier than females (529.9 ± 33.8 g; n = 8; range 450-657g). Subadult male weights were 517.5 ± 10.5g (n = 4). Captures of gliders were too infrequent to assess seasonal variation in body weight. 6.3.2.3. Glider Groups. Up to August 1986, traps were set within the home-ranges of two glider groups only (Fig. 6-2). By this time, 11 gliders had been captured from groups 1 and 3 and an untagged glider was known to occur in group 1. Group 3 contained two adult females and four males. One male was clearly a juvenile, being half the size of other gliders (no body weight data were obtained). This glider was not seen after April 1985. Two of the other males were considered subadults as their frontal scent glands were inactive. One had active scent glands when last seen in August 1986. Group 1 consisted of one glider not captured, one adult male, three adult females (two had been lactating concurrently) and one subadult female. The skeleton of a glider (no ear-tag located) was found in December 1986 at the base of a sap-site tree in the home-range of this glider group. Another group (No. 2) was identified in December and specific attempts to capture these gliders failed. At this time only two gliders were seen or heard in this home-range. In April 1987, censuses were begun on the three groups and each group consisted of four free-ranging members (Table 6-4). Only one tagged glider was observed, the remaining individuals being untagged individuals. The skeleton of one glider was found near a sap-site tree in the group 1 home-range. Examination failed to locate any ear tag. By July 1987 a further three gliders had been tagged. Two in group 3 where no previously tagged glider remained. Only one tagged glider from group 1 remained although three other untagged gliders were present. Overall there were four gliders present in each group (Table 6-4). By June 1988 only three free-ranging gliders were present in each group. This was the third successive year in which the chief winter food resource, E. maculata blossom, had failed to develop. Table 6-4. Glider population survey at Kioloa. ? = occasions when group was not fully censused. Sample Month Group 1 Group 2 Group 3 1986 Aug 6 ? 6 Dec 4 2? 2? 1987 April 4 4 4 July 4 9 ? Sept 4 ? 4 Dec ? 4 7 1988 June 3 3 3 1989 Jan 3 ? 3(+7) May 3 4 3 The glider groups observed in 1987 tended to use the same den trees (or at least in the same area) for long periods (>12 months), unlike gliders at Bombala. Group 1 denned in the same area from at least April 1987 through to May 1989; group 2 were known to use only two den trees from April 1987 through to August 1989 and group 3 denned in the same area from April 1987 through to May 1989. In May 1989 groups 1 and 3 numbered three individuals each while group 2 numbered four (including two subadults one of which had received some hostility). Females in groups 2 and 3 had nestlings at this time (see below). 6.3.2.4. Reproduction. Reproductive status was determined for nine female gliders. All of these were considered to be adults (yellow ventral fur) but three were of indeterminate status (see above). Eight reproductive episodes were observed (Table 6-5). Out of eight reproductive events observed, extrapolation revealed that six young were born between February and March. Two females from group 1 were observed lactating in August 1986. It was estimated that these young were born in February-March. One of these females (643) was again captured in May 1987 with an indication of having recently completed lactating. This was extrapolated to the birth of a young in November-December 1986. Thus this female had given birth to two young within 12 months. Another female (853) was captured three times over an 18 month period. This female reproduced three times between June 1987 and February 1989 (i.e. 21 months). This female was observed in April 1988 with a pouch young measuring 1.05 cm (crown-rump length). Table 6-5. Reproductive events recorded at Kioloa, from captured females and/or den observation. See Table 6-2 for explanation. Female Group Date of Capture Event Extrapolated month of birth 638 3 13/8/86 ET Feb-March 1986 645 3 20/8/86 NB 640 1 14/8/86 NB 641 1 14/8/86 NB 637 1 13/8/86 ET Feb-March 1986 643 1 19/8/86 ET Feb-March 1986 29/10/86 NB 23/5/87 ET Nov-December 1986 1 2 12/7/87 NB 853 3 16/12/87 ET June-July 1987 20/4/88 PY April 1988 20/5/89 L February 1989 U 2 20/5/89 PY-N February 1989 In May 1989, an untagged female was observed with an obvious pouch young. The body of this young could be seen through the pouch opening and on occasions the tail was seen hanging from the pouch. The female was seen on subsequent nights without the pouch young which was believed to have been deposited in the den to which the female was observed to return during the night. A young was observed climbing round, but not leaving, the den tree three months later. 6.3.2.5. Dispersal. The change in group composition after 1986 coupled with the difficulty in capturing gliders did not allow any data relating to dispersal of subadult gliders to be collected. 6.3.2.6. Longevity. Few data have been obtained on longevity at Kioloa. Only one individual captured in August 1986 was seen or captured subsequently. This individual F634 (group 1) was last seen in April 1988 when at least 4.5 years old. Another female (853) presumably present in June-July 1987 (i.e. the extrapolated month of birth of its young) was still present in August 1989 when at least four years old. Male 817 which was first captured in May 1987 was still present in January 1989 when aged at least 3.75 years old. Another male (M822), first captured in July 1987, was still present in August 1989 when at least four years of age. 6.4. DISCUSSION. 6.4.1. Trapping. Overall trap success averaged 6.2% at Bombala and 7.8% at Kioloa which is comparable to the 5.8% achieved by Craig (1985) in Victoria. No data on trap success were provided for Glengarry North, Victoria, by Henry and Craig (1984). The reason for the low trap success in such studies is due to the large home-ranges of gliders and the infrequent use of the small number of trees on which traps were set. In the present study, no more than 12 traps could be set and these were spread through an area of approximately 200-250 ha. Studies of the sugar glider have yielded contrasting results. Suckling (1984) reported a trap success of 33-50% where densities varied between 0.7 and 12.8 animals per ha. Smith and Phillips (1984) recorded trap success of 1-9% where densities varied between 0.2 and 1.0 animals per ha and Henry (1985) had trap success of 28% with densities of 1.1 to 2.3 animals per ha. Trap success of yellow-bellied gliders also depended on whether these gliders were feeding extensively on sap because the trees on which traps were placed were those used for sap feeding. Many of the captures occurred when gliders were sap feeding and gliders were rarely observed on these trees when sap was not being exploited (Chapter 4). 6.4.2. Weight Variation. Yellow-bellied gliders at both sites were clearly sexually dimorphic with females on average weighing 86% of average male weight. Body weights of gliders at both sites were similar to those recorded in Victoria (Henry & Craig 1984, Craig 1985) and varied between capture dates at Bombala (where there was more recaptures) by 4-23% for males and 4-16% for females. These variations did not accord well with particular times of the year. In contrast, Craig (1985) suggested a relationship between the time of year and body weight but I consider that this may be a spurious one because he pooled data for months from different years. Lack of an obvious pattern at Bombala may result from gliders in different home-ranges experiencing localized differences in food abundance due to differences in habitat quality. However, small sample sizes prevent resolution of this aspect. Smith (1984b) described a 20% (or more) annual loss of body weight in Leadbeaters possum and found maximun weights occurred during mid-winter. Suckling (1984) found that body weight of sugar gliders showed "strong seasonal fluctuations". Maximum weight was attained in summer and autumn but because of the way these data were presented (all data were plotted for age against weight), it is not possible to see the extent of seasonal weight changes. However, these studies suggest a very regular pattern of nutrient storage in these petaurids presumably reflecting seasonal food resource abundance patterns relative to energy requirements. Weight variation may reflect changes in food availability but the yellow-bellied glider, being a much larger animal and having a food supply which may fluctuate in abundance from one year to another (e.g. Henry & Craig 1984, Kavanagh 1987a), may not undergo regular fluctuations in body weight. 6.4.3. Group Dynamics. At Bombala, the size of the groups tended to remain constant at two or three animals, with the exception of one group which contained at least six free-ranging individuals. Studies in Victoria recorded no more than three individuals per group at Cambarville (Craig 1985) but one group of four free-ranging animals at Glengarry North (Henry & Craig 1984). At Kioloa, groups consisted of 3-6 individuals. In north Queensland, groups often contained five or six free-ranging gliders (R. Russell 1984). The larger group sizes in north Queensland and at Kioloa (Table 6-6) presumably result from a higher reproductive rate and a polygynous mating system. Table 6-6. Glider group sizes for different sites. Group size from each of the study sites (see Henry & Craig 1984, R. Russell 1984, Craig 1985) were determined by considering each change in group size as a separate record. Site Mean group size (no. individuals ± s.e.) N Victoria Cambarville 2.2 ± 0.2 6 Glengarry North 3.0 ± 0.3 7 New South Wales Bombala 2.6 ±0.3 13 Kioloa 4.1 ±0.4 8 Queensland Herberton 4.6 ± 0.3 14 Groups at Bombala always consisted of an adult monogamous pair with or without young. How the formation of a group is achieved is not known but in two instances, when one adult disappeared, the remaining adult disappeared some months later. Craig (1985) observed one adult female with a tagged glider from an adjacent group after her consort of at least 18 months had disappeared. She then took up residence with another glider, having shifted home-ranges (700m), while the former home-range remained vacant for over 12 months. At Bombala, one male (M9) was observed associating with two transients for several months after the disappearance of his consort but failed to establish a new group. Why gliders in such situations fail to establish new bonds is not known. Henry and Craig (1984) reported one adult male glider living alone for at least three months following the presumed death of his consort. However, one female at Bombala (F6) persisted for at least two further years after the disappearance of her consort and mated with a new male. In north Queensland, R. Russell (1984) described how groups persisted when single adult members disappeared. Group vacancies were taken by individuals from adjacent groups which formed new alliances with the original adults. At Kioloa, groups persisted despite the disappearance of many individuals and this probably resembles the situation described by R. Russell (1984). Subadult gliders are believed to disperse from their natal home-range when they have attained adult body weight, yellow belly fur and active scent glands (see earlier). It is not known whether these dispersing gliders become a transient part of the population, moving through the forest seeking a vacancy where one or both adults have disappeared (see above), or whether they may simply visit adjacent home-ranges whilst still resident in their natal home-range. The latter situation has been observed for both subadults (R. Russell 1984) and adults (R. Russell 1984, Craig 1985). At Bombala, home-range B was known to have become vacant after the death of F3 and the apparent failure of M8 to form a new alliance. This resulted in F4 returning to its natal home-range, after an absence of at least eight months, and establishing a new group. Observations of transients at Bombala involved groups which were in a state of flux after a group member had disappeared (group 1: October-Decmber 1984; group 4: January 1988). Such instances were the only times transients were seen with residents. Having untagged residents at Kioloa throughout much of the study precludes such consideration here. Establishment of new groups may be mediated by altered patterns of vocalisations within formerly occupied home-ranges. Yellow-bellied gliders are very vocal animals (Kavanagh & Rohan-Jones 1982, R. Russell 1984) with calls audible by human observers up to 400m away (Kavanagh & Rohan-Jones 1982, Chapter 8) and which may therefore be detected over greater distances by gliders. Furthermore, gliders sometimes vocalised in response to calls of neighbouring groups (Craig 1985, Chapter 8). Therefore, when one or both gliders vacate a home-range, neighbouring glider groups will soon become aware of this. Thus, recruitment may be more likely from nearby. 6.4.4. Reproduction. The contrast between the mating system of the yellow-bellied glider in north Queensland and southern Australia is not as stark as suggested by Lee and Cockburn (1985). The latter situation, where gliders are monogamous, is now represented by studies at three sites (including Bombala) in comparable habitat (two eucalypt species were common to all sites). However, research at Kioloa indicates a situation analagous to that described in north Queensland (R. Russell 1984), where gliders may alternate between polygynous and monogamous groups. The yellow-bellied glider is unique among the Petauridae in almost always giving birth to a single young; there has been only one record of twins (Craig 1986). This study confirms that typically a single young is born. The salient aspect of the breeding biology of this species at Bombala was that all young were born between June and December with a predominance (70%) in July-September. Craig (1986) reported 69% of pouch young of gliders in Victoria between August and December, whilst 63% of pouch young of gliders in north Queensland were recorded between May and September. At Kioloa, there was a predominance (75%) of births between February and March. This preceeds the peak period at Bombala by four months. This is discussed in further detail below. Craig (1985,1986) suggested that most female gliders in Victoria show biennial reproduction. However, Henry and Craig (1984) reported annual births by one female over a 3 year period at one Victorian site. They provided no data for other females. In contrast, most females in north Queensland reproduce in successive years (R. Russell 1984). At Bombala, at least three of the four females examined periodically reproduced in successive years (one reproduced at least four times in five years) but one of these females failed to breed in a year subsequent to breeding. Gliders at Kioloa bred annually also and some appeared to produce successive young within a 12 month period but whether this resulted from the loss of the earlier young is not known. In Victoria, young did not disperse until 18-24 months of age (Henry & Craig 1984, Craig 1985) but in north Queensland they may disperse when 9-18 months of age (R. Russell 1984). Limited data from Bombala suggest that offspring may remain in their natal home-range for up to 24 months of age. Groups at Bombala consisted most frequently of two or three individuals (mean = 2.6) so that if subadults remained for at least 18 months and females bred annually, significant juvenile mortality must have occurred otherwise group sizes would have exceeded three individuals more often. Henry and Craig (1984) reported two occasions of a group with four members; the female in this group bred annually and there was one instance of infant mortality. Henry and Craig (1984) suggested that at Glengarry North in Victoria, gliders showed obvious male parental investment such as babysitting and associating with offspring while foraging. They also cited observations of females with pouch young denning alone. During the few occasions at Bombala when females were known to have pouch young they continued to share a den with the adult male and subadult. There were few observations of individuals within a group denning separately and in such cases it was the adult female with the subadult (at Bombala and Kioloa). The situation depicted by Henry and Craig seems to be an overstatement. Gliders often foraged together when feeding on exudates (Chapters 4,5) and at such times it was often all members of a group together. When gliders foraged for arthropods they did so solitarily but remained in vocal contact with each other. On two occasions group 6 contained two male gliders each of adult body weight (i.e. >500g). This situation probably represented male offspring prior to dispersal. One such male had an active scent gland. Craig (1985) reported a subadult male with an active scent gland when 18 months old. Similarly, at Kioloa, the body weight of two subadult males increased over several months and their belly fur changed from white to yellow (Goldingay unpubl. data). One of these individuals had developed an active scent gland prior to its disappearance. Henry and Craig (1984) also reported an adult male of "uncertain status" in one group prior to its disappearance. These observations suggest that male offspring attain adult characteristics prior to dispersal. Longevity may be approximately equal (at least six years) at Bombala and north Queensland. The cause of the disappearance of many gliders in this study is unknown. At least one individual (Ml) probably died due to a feeding disability after its lower incisors (which are essential for sap feeding; Chapter 3) became worn down to the gums. Kavanagh (1984) observed one instance of a glider apparently starving to death in this study area. Mortality due to predation may be uncommon. Kavanagh (1988) reported one instance of predation on a yellow-bellied glider at this site during a six year period despite the continued presence of a pair of powerful owls (Ninox strenua) and frequent predation on greater gliders (Petauroides volans). Tilley (1982) reported a low incidence of yellow-bellied gliders in the diet of the powerful owl in Victoria. In north Queensland, R. Russell (1984) observed deterioration in condition of animals 5-6 yr old, leading to mortality. 6.4.5. Food Resource Abundance Model. Data on the availability of the food resources and their use by yellow-bellied gliders at Bombala (Chapters 2,3, Kavanagh 1984, 1987a, unpubl. data) and Kioloa (Chapter 5) are sufficient to present a model of annual food availability patterns. Firstly, the pattern at Bombala (Fig. 6-5) will be described and then that at Kioloa (Fig. 6-6). At Bombala, nectar was harvested virtually only from E. ovata (Kavanagh 1987a), a winter flowering species. One individual E. viminalis which flowered in winter 1986 was used extensively (Chapter 2). Only one observation was made of gliders feeding in a flowering tree (E. cypellocarpa) at other times of the year, although flowering trees were often present (Kavanagh 1987a). Therefore the flowering pattern of E. ovata can be used to represent the availability of nectar that is utilized. Manna could not be censused and the small number of trees from which it was harvested extensively (see Chapters 2,4) suggests that it was extremely patchy and only occasionally available. Changes in sap flow have been suggested to influence sap feeding by gliders and the number of suitable trees changes throughout the year (Chapter 3, Kavanagh unpubl. data). Most sap feeding occurred in mid-summer on E. viminalis and mid-autumn through to mid-winter on E. fastigata (Chapters 2,3, Kavanagh 1987a). Moreover, trapping of gliders was highly dependent on gliders engaging in sap 111 J FMAMJJASOND AMJJASOND 0) o c CO •a c < CD > 4—» CD Fig. 6-5. Food resource abundance model at Bombala. This indicates the relative annual abundance of: (a) nectar, (b) manna, (c) sap, (d) honeydew, and (e) arthropods. The initials of the eucalypt species providing arthropods via shedding bark are indicated above the curve depicting its bark-shed pattern (E.v. = E. viminalis, E.f. = E. fastigata, E.r. = E. radiata, E.ov. = E. ovata, E.c. = E. cypellocarpa). See text for further explanation. 112 Q w « u o d >, > 1*1 II IS-S >?« >., >cd II 0) o G< H 3 ° «3 ^ CO >V •*« &o C o cd cd u 5 s« •^ 8 ft so h «cd eouepunqv eA^ey 113 feeding because traps were placed on sap-site trees. Thus, trapping of gliders and the presence of fresh incisions on these trees during all six January field trips suggests that sap was regularly abundant at this time. Honeydew was utilized from autumn through to spring with a peak during winter and assessment of its abundance, based on the number of blackened branches in the few trees from which it was obtained, indicated a greater abundance during winter (Chapter 2). Paton (1980) found that honeydew was more abundant during autumn and winter at a site in Victoria. The data for the availability of arthropods is based on the pattern of bark shed by different eucalypt species (Chapter 2, Kavanagh 1987a). Gliders obtained arthropods, and on occasion both arthropods and honeydew, from beneath loose shedding bark by holding the loose bark in their mouths (and sometimes front feet) and then tearing it back to expose the surface below (Chapter 2, Kavanagh 1987a). Examination of recently fallen and felled trees with shedding bark revealed an abundant food resource (Chapter 2). Eucalyptus obliqua was used rarely by gliders. The other species were all used extensively on occasion (Chapter 2, Kavanagh 1987a). The abundance of the bark substrate of each species differs as only the smooth bark of a tree is shed. This includes the entire surface of the tree for E. viminalis , E. ovata and E. cypellocarpa , the major branches of E. fastigata and the smaller branches of E. radiata (Kavanagh 1987a). Another important consideration is the regularity of these events. Four species (E. radiata, E. ovata, E. fastigata, E. cypellocarpa ) had protracted periods of bark shed (Fig. 4), lasting several months and which may vary in timing (the peak varied by 4-8 weeks) from one year to the next (Chapter 2, Kavanagh 1987a). However, bark shed by E. viminalis was highly synchronous among individuals and predictable in timing (Kavanagh 1987a). Furthermore, once bark was shed from this species, it often persisted in the form of long bark ribbons which enclosed a rich arthropod community (Smith 1982a, Goldingay pers. obs.). Arthropods would be available from this substrate throughout the year (e.g. Smith 1982a) but presumably the abundance of the bark ribbons declined until the next episode of bark shed. The above discussion indicates that the relative abundance of different exudates does vary among seasons and the pattern of abundance for each was different, such that at least one was always available (Fig. 6.5). One critical aspect not apparent from the model is that in some years E. ovata failed to flower (Chapter 2, Kavanagh 1987a). The loose shedding bark (from E. viminalis, E. fastigata, E. ovata and E. cypellocarpa) provided arthropods, and therefore dietary protein throughout the year (pollen from E. ovata flowers may contribute also). Each species had a different pattern of bark shed with that of E. viminalis being the most predictable. Is the timing of reproduction in the yellow-bellied glider at Bombala related to regular occurrence of high food abundance? Many species of primate show adaptive timing in reproduction which has been suggested to be related to female condition, itself contingent on previous reproduction and food availability (Schaik & Noordwijk 1985). Smith (1982a, 1984a,b) implicated seasonal patterns of food availability in the timing of reproduction for sugar gliders and Leadbeaters possums. He argued that a summer abundance of arthropods was most likely to explain the breeding pattern in the sugar glider because late lactation, when protein requirements of females are presumed to be greatest, would coincide with this. In contrast, arthropods may be relatively abundant year-round in Leadbeaters possum habitat but that exudates may be seasonally scarce. All births of yellow-bellied gliders at Bombala occurred between June and December with a predominance in July-September, showing similarities with the sugar glider pattern in Victoria. There was no time of year when exudates appeared to be absent (Fig. 6-5). Winter and spring were times when several food types were available at Bombala. Nectar of E. ovata and insect honeydew were normally abundant and E. ovata, E. cypellocarpa and E. radiata were shedding bark, thus providing both arthropods and honeydew (Chapter 2, Kavanagh 1987a). Late lactation would occur between November-January but possibly of at least equal importance would be the time of weaning (December-February). Therefore, the period November-February would be one of high protein requirement by gliders. Both events coincided with a time of year when the strongly predictable bark shed of E. viminalis provided abundant arthropods (i.e. protein) and sap and manna were often in greater abundance. Moreover, in summer, thermoregulatory demands on females would not be as great as at other times of the year and offspring would be weaned and foraging independently before the ensuing winter. The bark shed of E. fastigata in late summer and autumn would provide further arthropods and thus, essential protein for young gliders before winter. However, survival past weaning may not guarantee the ultimate survival of offspring. Depicting the abundance of the gliders' food resources at Kioloa (Fig. 6-6) is much easier because nectar-feeding was the predominant feeding behaviour throughout the year (Chapter 5). Thus, in a good year, when all species flowered, there could possibly be nectar and pollen available throughout the year. Gliders were able to digest pollen (see Chapter 5) which would provide dietary protein. Thus, when trees are in flower there would be a steady supply of protein throughout the year. Probably the critical resource was the flowering of E. maculata, the winter-flowering species. In two years (1985, 1989) when it flowered properly, this resource persisted from at least April through to September. This provides a third pattern of food availability to the two suggested by Smith (see above), where neither exudates nor protein are clearly seasonal. Gliders at Kioloa gave birth predominantly in February-March, which preceeds the breeding period at Bombala by four months. Such seasonality may result from synchronization with the potentially most prolific food resource because group sizes were larger and may on occasion involve polygyny. This may ensure that females are undergoing late lactation (in July) and that young gliders are emerging from their dens (in August) when E. maculata is in flower. One apparent inconsistency here is that many of the breeding records came from years (1986-88) in which E. maculata failed to flower. However, group sizes declined through this period suggesting the mortality of both adults and offspring. If conception is dependent on body condition, as in some primates (see Schaik & Noordwijk 1985), then the births in early 1986 may have followed the good flowering of E. maculata in 1985. Alternatively, gliders may be unable to predict whether a food resource, such as a flower crop of one species, will eventuate and therefore may reproduce anyway. If at a later date food becomes scarce, then the young can be aborted. In fact, this situation has been documented for Leadbeaters possum where the population density declined by 45% in one year presumably in response to a shortage of food, even though all captured resident females had reproduced prior to this decline (Smith 1984b). Lee and Cockburn (1985) considered the continuous availability of food resources, particularly arthropods, in north Queensland was responsible for the polygynous mating system there. In fact, R. Russell (1984) found that glider groups varied from monogamous pairs through to polygynous groups containing six individuals. This situation is analagous to that at Kioloa. Thus their hypothesis is probably sufficient to explain the mating system at Kioloa also but this study shows that their depiction of a temperate/tropical forest dichotomy is incorrect. Gliders may revert to polygyny whenever the abundance of food resources, particularly those providing protein, is high and continuous throughout the year. Such a situation may occur in habitats which include specific eucalypt species (e.g. E. maculata) or in habitats where eucalypt species diversity is high, such as on the north coast of N.S.W. where as many as 20 species may occur within 100 ha (Mackowski cited in Kavanagh 1987a). Group sizes and polygyny at Kioloa may be dependent on successive years of abundant flowering by E. maculata. Increased group size may influence the time-budget of gliders (e.g. Schaik et al. 1983) such that within-group competition for scarce food when few E. maculata flower, may push time-budgets to unacceptible limits leading to a decline in group size and consequent reversion to monogamy. This study has shown similarities in the socioecology of gliders at Bombala with that in comparable habitat in Victoria (cf. Henry & Craig 1984, Craig 1985). Typically, group sizes are small and fecundity is generally low. The diversity of eucalypts at Bombala provided overlapping availability of food resources and perhaps some buffer against occasional failure of specific resources or adverse weather conditions. In contrast, the socioecology of gliders at Kioloa was similar to that in north Queensland where group sizes alternated between small monogamous groups and larger polygynous groups. 1 Chapter 7. HOME-RANGE OF THE YELLOW-BELLIED GLIDER, Petaurus australis, AT BOMBALA AND KIOLOA. 7.1. INTRODUCTION. The home-range of an animal is that area in which it travels in order to obtain food and reproduce (Burt 1943). The size of the area required by an animal for its home-range will depend on the type of diet it has (and associated food availability) and size-dependent metabolic demands (McNab 1963, Mace & Harvey 1983). Knowledge of the size of animal's home-range is central to understanding how it utilizes its environment and is also an important consideration in management plans for the conservation of species' populations. Several studies on the smaller petaurids (Leadbeaters possum, sugar glider) have considered analyses of their home-ranges but as a consequence of the elusiveness of these species, analyses have been based largely on trap-revealed locations (Smith 1984a, Suckling 1984, Henry 1985). In contrast, the yellow-bellied glider (Petaurus australis) offers a major advantage in home-range determination in that habituated animals can be readily spotlighted and followed at night (Chapters 2,4,5). Accordingly, each of the studies of the yellow-bellied glider has given consideration to its ranging behaviour and from this, determined the area of the home-range (Henry & Craig 1984, R. Russell 1984, Craig 1985). All studies to date have found that gliders live in small family groups which occupy an extremely large (30-63 ha) home-range used exclusively by a single group. Gliders are capable of gliding over 100m in a single glide and may traverse several kilometres in a night whilst foraging (Chapter 4). However, these previous studies may have been inadequate in indicating the most realistic size of the home-range. Two of the studies (R. Russell 1984, Craig 1985) approximated the boundaries of the home-range and then determined the area enclosed while all three studies presumably used all possible location data, including temporally related (i.e. non-independent) points (see Swihart & Slade 1985a). There are two main reasons for requiring a more precise determination of the home-range area of the yellow-bellied glider. Firstly, in any consideration of how these animals utilize their forest environment it is necessary to know the size of the area utilized. Secondly, this species occupies many areas in which logging of the forest is occurring and in order to ensure the continued survival of its populations in such areas, it is critical to know the number of home-ranges a given area may include (e.g. Mackowski 1986). 7.2. METHODS. 7.2.1. Bombala. 7.2.1.1. Study area. The study area at Waratah Creek, Coolangubra State Forest, Bombala, encompassed approximately 300 ha of mature eucalypt forest (Plate 7-la). Within the study area seven major forest types occurred (Fig. 7-1). These have been described in detail by Kavanagh (1984) for a 100 ha grid within this area. The height of the forest canopy ranged from 25 m in the open swampy areas dominated by E. ovata, to 45 m in the southeast facing slopes dominated by E. fastigata (Kavanagh 1984). The area has an average winter minimum of 0° C and an average summer maximum of 24° C, and has an annual average rainfall of 1167mm (Kavanagh 1984). 7.2.1.2. Animal locations. In January 1984, a trapping program was begun which allowed captured gliders to be individually ear-tagged using tags covered with reflective tape of different colours (Chapter 6). Subsequent trapping (up to January 1989) and extensive spotlighting in the study area (Chapters 2, 3, 4, Kavanagh 1984, 1987a) allowed detailed data to be collected on the locations of individual gliders which belonged to six glider groups but only three were present at any one time (Chapter 6). The difficulty in capturing gliders in the southern section of the study area made it unclear whether the original glider group was replaced in time with another group (see Chapter 6). As many of the observations (1984-1989) came from the gully containing several E. fastigata sap-site trees, all location data for gliders in this area have been treated as forming a single home-range. Gliders were followed at night as they foraged. The observation time included l-3h per night in 1984 and several whole-night periods in 1985 and 1986 (see Chapters 2, 3, 4). Six gliders were fitted with radio-transmitters for varying lengths of time to facilitate the location of gliders (see Chapter 6). Trees in which gliders were observed were taped with coloured flagging tape and mapped during the day. The derivation of home-range location points from continuously followed gliders results in many points but points which may not be independent of each other (e.g. the location of a glider in one tree is related to the position of the previous tree it was in), and which may bias the home-range area determined (Swihart & Slade 1985a, b, 1986). Thus, a set of independent points was determined from the total set of location points for each glider by selecting points three hours apart. This criterion was chosen because gliders spent the longest periods (ca. 3h on average) in individual trees when engaged in sap feeding (Chapter 4) and these trees were widely spaced. This would therefore ensure that gliders had moved far enough to consider these points independent. 118 WI ffSllll ••.>. J|l§||||l§|lf| ^?llfllPl*i ;Ms wmm 'mm '^m:m:mxx (b) XtMRmme;Jip-l l msMsk mmim iiJISlill Plate 7-1. Forest habitat at (a) Bombala and (b) Kioloa. Fig. 7-1. Distribution of forest types at Waratah Creek, Bombala. Heavy lines indicate roads. Dashed lines indicate creeks. The cross-hatched area was logged in August 1984. Forest occurring inside private property boundary was logged by January 1986. The large square indicates the study area of Kavanagh (1984). Forest types are indicated by the following numbers: lllv = E. radiata- E. viminalis ; 143 = E. ovata- E. viminalis ; 152 = E. obliqua - E. cypellocarpa ; 152A = 152 + E. radiata ; 154 = E. fastigata - E. obliqua ; 154A = 154 + regeneration; 155 = E. fastigata - E. cypellocarpa ; 155v = E. fastigata - E. viminalis ; 159 = E. viminalis. 7.2.2. Kioloa. 7.2.2.1. Study area. The study area in Kioloa State Forest, Kioloa, encompassed approximately 200 ha of mature eucalypt forest (Plate 7-lb). Within the study area, seven major forest types occurred (Fig. 7-2). These have been described in detail by Forestry Commission of N.S.W. (1983). The height of the forest canopy was approximately 30-45 m throughout the area (pers. obs.). The average daily temperatures for the area were rarely below 10° C in winter and rarely above 25°C in summer, and the annual average rainfall for Batemans Bay, which is approximately 20km southwest, is 1008mm (Pook 1984, 1986). 7.2.2.2. Animal locations. Gliders within three home ranges were monitored at Kioloa (Chapter 6). One group (group 1) had one individual which persisted from August 1986 through to April 1988. Although this glider was not observed subsequently, the group in this home-range continued to use a den tree in approximately the same area. Therefore, observations on gliders from this home-range for 1986-1989 have been used. Observations for the other two groups are based on observations from December 1986-August 1989 and February 1987-August 1989. Locations at Kioloa were based both on sightings of gliders, and occasionally on vocalisations when a calling glider could not be observed but its group identity could be established. Generally, only a single location was obtained per individual per night unless locations were widely spaced or separated by more than three hours. Many location records were obtained from untagged gliders from each of the three groups. However, regular following of gliders (both tagged and untagged) from their dens revealed that there was little overlap in adjacent home-ranges and indicated the extent of glider movements from den trees. 7.2.3. Estimation of home-range. The home-ranges of gliders were estimated using the McPAAL programme (Stuwe & Blohowiak 1985). This programme offers several different estimation methods but only three were used to estimate home-range area here: the minimum convex polygon, the harmonic mean distance minimum using 95% isopleths (see Dixon & Chapman 1980) and the Fourier transform method (minimum area vs. probability of 95%; see Anderson 1982). A 95% Ellipse method was available but not used because this method requires that the data be bivariate normal (Jaremovic & Croft 1987). Examination of the cluster of location points around den trees and sap-site trees demonstrated that this was not the case. 7.2.4. Density Estimate. The density of gliders was estimated using two techniques. Firstly, the number Fig. 7-2. Forest habitat at Kioloa. Heavy lines indicate roads. Dashed lines indicate creeks. Doubled dashed line indicates a logging track. Forest types are indicated by the following numbers: 18 = rainforest; 36 = moist forest (on lower slopes and in gullies) dominated by E. pilularis associated with E. pellita, E. piperita, E. gummifera ; 37 = dry E. pilularis (on higher slopes and ridges) with same species mix; 41= E. pilularis - E. gummifera ; 42 = E. pilularis - E. piperita ; 70 = £. maculata ;16 = E. maculata - E. pilularis ; 76A = regenerating 76 after logging; 116 = E. piperita - E. gummifera. of gliders living in the three home-ranges (i.e. foraging independently) was divided by the area which enclosed the three home-ranges. This included the apparently unused areas between the home-ranges of adjacent groups. Secondly, the number of gliders living in a given home-range was divided by the area of that home-range and a mean calculated. 7.3. RESULTS. 7.3.1. Bombala. 7.3.1.1. Estimates of home-range area. Estimates for group 5 were based on a much smaller sample size collected over four field trips compared to the other groups in which location data were collected over at least seven field trips. The smaller sample size resulted in contradictory values (Table 7-1). For example, the MAP (95%) index for each of the other groups was the smallest value but for group 5 gave a value more than six times that of the harmonic mean method. It should be noted that the adult female (F4) in this group was the subadult in group 2 and responsible for many of the location points of that group. Presumably this animal was aware of the extent of the original home-range boundaries. Moreover, one area containing a sap-site tree was used extensively by group 2 but was only observed in use by group 5 during the last field trip in January 1989. This resulted in no location points for the analysis between Table 7-1. Determination of the home-range area (ha) of yellow-bellied gliders at Bombala using different techniques. MCP = minimum convex polygon, 95% MAP = 95% minimum area vs. probability using the fourier transform method. D = duration of group observations (months). Glider Group Home-range Estimation Techniques N D MCP 95% Harmonic 95% MAP Gp 1 75 12 34.4 38.7 13.2 Gp2 250 18 72.9 59.0 9.5 Gp3 82 61 87.7 85.4 26.7 Gp4 80 49 72.6 35.5 34.2 Mean ± s.e. 66.9 ± 11.4 54.7 ± 11.5 20.9 ± 5.8 Gp5 40 37 17.7 10.6 64.2 Fig. 7-3. Home-ranges of five glider groups at Bombala. Home-range boundaries are the 95% isopleths. Den tree locations are indicated by squares and sap-site trees by circles. Numbers associated with sap-site trees show the eight trees sampled for sap flow in Chapter 3. The den tree located outside isopleths was used by Gp 1 after disappearance of adult female. Gp 4 home-range determined after Gp 1 had disappeared and Gp 5 after Gp 2 had disappeared. this area and the other area used morefrequently. The harmonic mean method using 95% isopleths depicts the home-range of this glider group as consisting of a larger part enclosing 10.5 ha and a smaller part of 0.1 ha separated by 350 m (Fig. 7-3). Therefore the data for this group have not been included in determining the mean home-range size or glider density at Bombala. The home-ranges of glider groups at Bombala were large (Fig. 7-3) using any of the estimation techniques, although the different estimation techniques gave quite different values for the home-range area (Table 7-1). The minimum convex polygon (MCP) gave the largest values ranging from 87.7 ha to 34.4 ha. In comparison, the harmonic mean method gave values which on average were 82% of the average MCP value, while the MAP (95%) indices were only 31% of the MCP value. 7.3.1.2. Glider density. The area bounded by the three home ranges (using group 1 and not group 4) was determined to be 238 ha. In May 1984, there were two gliders in home-range A, three in home-range B and six in home-range C. This gives a density of 0.05 individuals per hectare. Using the maximum number recorded in each of the three home-ranges and dividing by the area of the minimum convex polygon of each home-range gives a mean (± s.e.) density of 0.06 ± 0.01 (n = 4) gliders per hectare. Using the minimum known to occupy each home-range gives a density of 0.04 ± 0.01 gliders per hectare. 7.3.2. Kioloa. 7.3.2.1. Estimates of home-range area. The different home-range estimation techniques gave similar values for the size of the home-ranges at Kioloa (Table 7-2). Table 7-2. Determination of the home-range area (ha) of yellow-bellied gliders at Kioloa. Abbreviations as for Table 1. Glider Group Home-range Estimation Techniques N D MCP 95% Harmonic 95% MAP Gpl 55 A3 406 305 52^2 Gp2 88 32 29.5 36.5 31.1 Gp3 86 30 24.7 21.9 27.2 Mean ± s.e. = 31.6 ±4.7 29.6 ± 4.2 36.8 ± 7.8 \ Fig. 7-4. Home-range of three glider groups at Kioloa. Home-range boundaries are the 95% isopleths. Den tree locations indicated by squares. Group 1 den location approximated from observations of gliders soon after dark. Circles indicate E. gummifera sap-site trees and triangles E. piperita honeydew trees, a = Acacia mabelliae used extensively for gum feeding. 126 The minimum convex polygon (MCP) did not give the largest values. In this instance, the harmonic mean method gave values which on average were 94% of the average MCP value, while the MAP (95%) indices were 117% of the MCP value. The position of these home-ranges are shown in Fig. 7-4. 7.3.2.2. Glider density. In August 1986, two home-ranges each contained six gliders. One group had a home-range area (using the minimum convex polygon) of 41 ha. The other group was later replaced (see Chapter 6) but assuming it had approximately the same home range boundaries as the group which replaced it (group 3) the home-range area was 25 ha. This would then give a density of 0.19 ± 0.05 gliders per hectare. In August 1989, there were three gliders in each of the three home-ranges. This gives a density of 0.10 ± 0.01 gliders per hectare. 7.4. DISCUSSION. 7.4.1. Home-range area. There are currently several techniques used to estimate the home-range area of animals. Each of these has advantages and disadvantages (e.g. Schoener 1981, Anderson 1982, Jaremovic & Croft 1987). The minimum convex polygon has been used frequently but includes all location points, giving each equal value, and may include large areas not utilized by the animal (Schoener 1981, Jaremovic & Croft 1987). Jaremovic and Croft (1987) considered that 95% iospleths, from the harmonic mean method, gave a better estimation of the size of the home-range. Using this technique, glider home-ranges at Bombala averaged 54.66 ± 11.49 (s.e.) ha whilst at Kioloa, home-ranges averaged 29.59 ± 4.24 ha. Therefore, the average value at Kioloa was only 54% of that at Bombala. Interestingly, although the other estimation techniques gave quite different results for the data at Bombala, these techniques yielded quite similar values at Kioloa. At sites in Victoria, Henry and Craig (1984) used techniques similar to the minimum convex polygon to estimate the home-range area and found that the size of the home-range was smaller (Glengarry North: area = 52.7 ±6.1 ha; Cambarville: area = 41.7 ± 7.3 ha) than at Bombala in somewhat similar habitat (the three sites had two eucalypt species in common). Using the minimum convex polygon for the Bombala groups, the home-range area averaged 66.88 ± 11.4 ha. At Kioloa, using this method, the home-range area averaged 31.56 ± 4.71 ha. In north Queensland, R. Russell (1984) suggested that two glider groups had home-ranges of 2 and 30 ha. This enormous variation in the size is inconsistent with home-range sizes elsewhere and probably reflects Russell's focus on the social behaviour of gliders at sap-site trees. Thus, most of his observations were confined to the proximity of glider sap-site trees and this may have biased an assessment of the home-range to those core areas. 127 Ear-clipping, the technique he used to mark individuals, is less reliable than reflective ear-tags in establishing identity when gliders are in tree canopies (pers. obs.). In many ways, the ecology of gliders at Kioloa is similar to that in north Qld and it is suggested that the size of the home-range may be of a similar magnitude (ca. 30 ha). Also of importance among all studies of the yellow-bellied glider is that home-ranges were completely exclusive, a situation which is uncommon among marsupials (E. Russell 1984). One important consideration in all attempts to estimate the size of the home-range is that the number of groups studied was quite small and precludes statistical comparisons. Ironically, it is the large home-ranges which have precluded the study of more than three glider groups concurrently. However, the coefficients of variation were comparable. For Henry and Craig (1984) and Craig (1985), these were 20% and 30% respectively. At Bombala, the coefficients of variation for MCP and 95% harmonic were 34% and 42% respectively whilst at Kioloa they were 26% and 28% respectively. In comparison, Jaremovic and Croft (1987) had a coefficient of variation which was 34% (using 95% isopleths) for 15 female eastern grey kangaroos (Macropus giganteus) and Priddel et al. (1988) had a coefficient of variation which was 53% (using minimum convex polygon of the aggregate range) for 21 red kangaroos (M. rufus) and 23 western grey kangaroos (M. fuliginosus). This suggests that despite the small number of glider home-ranges examined at each site the variance among glider groups was not extreme in relation to studies on other mammals which included larger sample sizes. The yellow-bellied glider has a very large home-range for its size (Bombala: 590g). The home-range size for gliders at Bombala (54.7 ha) was approximately three times the size of the home-range of eastern grey kangaroos (19.1 ha; Jaremovic and Croft 1987) which weigh 32-66 kg (Strahan 1983). Home-range is correlated with an animal's body mass and the density of its food resources (McNab 1963, Harestad & Bunnell 1979). McNab contended that this reflected the weight-specific energy requirements of a species. Yellow-bellied gliders feed predominantly upon plant and insect exudates, which are obtained from a small number of trees patchily scatterred through their home-ranges (Chapter 2,3,5). This is apparent from the wide spacing of sap-site trees within home-ranges at Bombala (Fig. 7-3). Yellow-bellied gliders traverse large distances each night whilst they forage (Chapter 4). One glider in January 1989 was observed to traverse 600m in 20 minutes, including time taken to search for arthropods, as it travelled from its den tree to a sap-site tree. Thus, gliding by this species allows the use of an extensive home-range area. More recently, several authors have reiterated the importance of energy requirements (i.e. body mass) and diet on home-range size but state that this relationship is complex (e.g. Harvey & Clutton-Brock 1981, Mace & Harvey 1983) and for some species the apparent complexity may result from intraspecific variation resulting from different habitats (e.g. Gittleman & Harvey 1982). For example, the average home-range size at Kioloa was 55% that at Bombala and I suggest this difference is a reflection of more abundant food resources. An assessment of the number of flowering trees at Kioloa during field trips from April 1987-August 1989 shows that flowering trees averaged 3.9 ± 2.2 per ha (Chapter 5). In contrast, only a small number (<7) of trees were ever used for exudate feeding at Bombala in a given home-range (Chapters 2,3,4). The home-ranges at Kioloa support a greater number of gliders within a group than at Bombala (Chapter 6) which would be expected to place additional demands on the energetic requirements of the group home-range. Harvey and Clutton-Brock (1981) stated that for social mammals, the size of the home-range will also be influenced by the number of individuals in a group (i.e. group energy requirements). 7.4.2. Comparison with other exudivores. The fork-marked lemur (Phaner furcifer) is a prosimian which appears highly convergent with the yellow-bellied glider, having a predominantly exudate diet and using vocal communication extensively (Charles-Dominique & Petter 1980). The prosimian is only half the weight (300g) of the glider and it has a home-range of approximately 4 ha (Charles-Dominique & Petter 1980). Similarly, the mouse lemur (Microcebus coquereli) is an exudivorous prosimian (300g) and it also occupies quite small home-ranges (ca. 6-7 ha; Pages 1980). Such contrasts with the yellow-bellied glider, for animals occupying the same dietary niche, suggest that habitat differences (i.e. food productivity) have a major influence on the size of the home-range of exudivorous species. This may explain why home-ranges at Bombala were, on average, 1.8 times those at Kioloa (using harmonic mean method). The flowering resource at Kioloa provided the most important food resource (Chapter 5) and probably gave home-ranges a greater productivity than those at Bombala (see above). This food resource has been inferred to influence the mating system at Kioloa (Chapter 6,9). At times of low productivity, glider group sizes declined without any apparent increase in the size of the home-range. This can be stated because, although temporal changes in the size of the home-range were not investigated, gliders often ranged widely from one sample period to another as different eucalypt species flowered in different parts of the home-range. Size differences are also important when comparing the exudivorous species mentioned above. Using the equation of Harestad and Bunnell (1979) for omnivores, and relating body mass to home-range area (H = 0.059W-92), a sugar glider (120g) should have a home-range of 4.8 ha. However, Suckling (1984) found that the home-range of sugar gliders in fragmented forest averaged 0.6 ha and 0.5 ha for males 129 and females, respectively, whereas Henry (1985) found home-ranges in continuous forest averaged 3.0 ha and 1.8 ha for males and females, respectively. Both measures are considerably less than predicted. The 300g prosimians listed above should have a home-range area of 11.2 ha. This suggests that exudate food resources may be more abundant (i.e. resulting in smaller home-ranges) than the food resources of other types of omnivore. However, the above equation predicts a home-range of 20.9 ha for the yellow-bellied glider. This is considerably less than most estimates at any of the sites in southern Australia. Thus, there may be a dichotomy in home-range requirements for small versus large exudivores. 7.4.3. Management Implications. Knowledge of the area over which animals range is important not only because it allows determination of the amount of food available (e.g. Priddel et al. 1988) but also because it allows determination of the area an animal requires for continued existence and hence, the number of individuals that may be living in a given area. In instances where animals occupy exclusive home-ranges such as for the yellow-bellied glider, the size of the home-range estimated using the minimum convex polygon would be more appropriate because this would include infrequently used peripheral areas which may be important to animals but only very occasionally (e.g. during drought). Mackowski (1986) used the size of the home-ranges in Victoria to determine approximately how many gliders may occur in forest on the north coast of N.S.W. This is useful provided that home-ranges are not in fact larger, resulting in an overestimate of the number of gliders present. The study area in Coolangubra State Forest has been set aside as a reserve (Waratah Creek Flora Reserve) which encompasses approximately 850 ha of forest (R. Kavanagh pers. comm.). Thus, using the average of the minimum convex polygon (67 ha) such an area would contain only 12-13 home-ranges and thus 12-13 pairs of gliders. This would be quite inadequate if this reserve was isolated from surrounding forest and if the preservation of the yellow-bellied glider was a management objective in this reserve. Density estimates are also useful in determining the number of gliders contained within a block of forest. Henry and Craig (1984) found yellow-bellied gliders at densities of 0.05-0.06 individuals per hectare in Victoria. At Bombala, Kavanagh (1984) determined density estimates of 0.1-0.3 gliders per ha from transect spotlighting through the 100 ha grid in the study area. Braithwaite (1983), in a study which examined the number and distribution of arboreal marsupials recorded during clear-felling of >5000 ha of forest in the Eden-Bega-Bombala region, reported densities of 0.09 yellow-bellied gliders/ha in what was determined to be preferred habitat. However, from the data recorded in the appendix of his paper specifically for Coolangubra State Forest, a density of 0.06 yellow-bellied gliders/ha is determined. In the present study, densities based on home-range area and the number of known gliders in the study area ranged from 0.04-0.06 individuals per hectare. This is comparable to glider densities for other parts of Coolangubra State Forest (see above) and also to that of Henry and Craig (1984) for somewhat similar habitat in Victoria. In contrast, density estimates at Kioloa ranged from 0.10-0.19 individuals per hectare. Thus, densities at Kioloa were on average, 2-3 times higher than those at Bombala or in Victoria. Finally, the impact of logging on the home-ranges of yellow-bellied gliders is unknown. During this study part (ca. one-third) of the home-range of group 3 was logged leaving only 10% of the original canopy cover. Whether the larger home-range of this glider group was due to this is not known but gliders moved through such logged area on occasion and often foraged for arthropods in the trees in these areas. Most of the sap-site trees for this group were contained in a gully which was not logged and gliders continued to use these trees more than four years later. The retention of these trees may have mitigated the impact of logging. Further studies are required to examine the impact of logging on the home-range requirements of this species. Chapter 8. VOCALIZATIONS AND TERRITORIAL BEHAVIOUR OF THE YELLOW-BELLIED GLIDER, Petaurus australis. 8.1. INTRODUCTION. Animals often exhibit particular patterns of spacing behaviour involving exclusive use of a fixed area which is defended against conspecifics (e.g. Brown & Orians 1970). Defence of this area may entail the use of overt aggression, vocalizations, displays and/or scent marking of substrates (Brown & Orians 1970). In short, this is known as territorial behaviour, a concept which has been around for some time (e.g. Carpenter 1958). The most widely accepted definition of a territory is that it is a defended area (Noble 1939). Such an area is fixed and used exclusively by the owner(s). The method by which animals defend their territories has rarely received experimental tests (Davies 1978) and observation of exclusive use of an area has often been interpreted as evidence for territorial behaviour (e.g. Ostfeld 1986). Brown (1964) argued that the spatio-temporal distribution of food resources was the factor most fundamental to whether bird species exhibit territorial behaviour. This was expanded into an hypothesis which stated that such behaviour will evolve if food resources are economically defensible. That is, the benefits gained from defending resources must exceed the costs. Many studies of bird behaviour have constructed time and energy budgets with this in mind. Thus, after quantifying the energy value and abundance of the birds' food resources, researchers have been able to examine the benefits of territorial behaviour over non-territorial behaviour (e.g. Gill & Wolf 1975, Carpenter & MacMillan 1976a,b, Davies & Houston 1981, Carpenter 1987). Birds need not directly defend their territories and, in fact, Paton and Carpenter (1984) have described "defense by exploitation" for territorial hummingbirds which apparently choose to feed on the periphery of their territories early in the day so as to deplete those nectar resources and therefore reduce losses to intruders. Territoriality is uncommon for mammals because most species cannot fly, so the cost of territorial defence is therefore much higher than in equivalent-sized birds, where such behaviour is common (Brown & Orians 1970). Territorial behaviour is expected only in mammal species which feed on concentrated and easily defended food resources (Brown & Orians 1970). This lesser mobility in mammals in general, 1 "prevents them from responding quickly and economically to territorial violations" by conspecifics (Brown & Orians 1970). Few studies have examined territorial behaviour in mammals (Mares & Lacher 1987). Mammals may patrol and defend exclusive home-ranges or core areas (or mates) within the home-range (Mares & Lacher 1987, Ostfeld 1985b), or may use auditory and/or olfactory communication to advertise the occupation of a territory (e.g. Charles-Dominique 1977, Mitani 1987, Ellefson 1968, Kruuk 1978). In some of the preceeding chapters, I have proposed a relationship between glider sociality and the rate of renewal of their food resources. Waser (1981) suggested that the rate of resource renewal would influence sociality in small carnivores. However, little reference was made to whether this should result in territoriality. Various authors have suggested that territoriality will evolve when resources are limited but defendable. Mitani and Rodman (1979) provided data for primates, predicting territoriality when the daily path length of an animal is at least equivalent to the diameter of a cicle with an area equal to the animal's home-range area. This implies that mobility is required for territorial maintenance. Mitani and Rodman (1979) explained that some mobile species may not be territorial because they are not resource limited. It is instructive here to discuss territoriality in primates in greater detail. Although many species are said to be territorial (Mitani & Rodman 1979) few studies provide definitive evidence of this behaviour (e.g. Pollock 1979). Several studies of the same species have conflicted in their interpretation of observed territorial behaviour (e.g. Hamilton et al. 1976). One extreme case is that of the population of howling monkeys (Alouatta palliata) on Barrow Colorado Island where different researchers have reached different conclusions concerning the spacing behaviour, varying from exclusive territories (Carpenter 1934) through to no part of the home-range used exclusively (Smith 1977). Perhaps here the spacing pattern by this species has been dynamic. 8.2. TERRITORIAL ADVERTISEMENT BY PRIMATES. It has often been assumed that exclusive use of home-ranges by mammals is conclusive proof of the existence of territorial behaviour by species under observation. However, there may in fact be underlying discontinuities in resource abundance which have led to the observed distribution pattern. Therefore, to demonstrate the existence of territorial behaviour it is necessary to determine the behaviour(s) which may elicit an exclusive use of habitat by individuals. 133 8.2.1. Overt defence. This is the most obvious form of territorial behaviour where boundaries of a home-range are often visited (e.g. Ellefson 1968, Mason 1968) and if intruders are encountered they are forcibly evicted. This may only involve one animal chasing another because generally few chases result in actual contact, but if contact occurs it may be very brief (Mason 1968, Ellefson 1968). Such overt defence also involves vocalizations and displays (Mason 1968, Ellefson 1968,1974, Gittons & Raemaekers 1980), thus providing ample evidence for territorial behaviour. However, many mammals which exhibit exclusive use of home-ranges (or core areas) may not often encounter conspecifics or may simply show avoidance behaviour, which makes it less obvious as to whether such species can be considered to be exhibiting territorial behaviour (Waser 1976,1977a). Tenaza (1975) described a more passive type of territorial confrontation among Kloss' Gibbons (Hylobates klossi) where trespassing individuals were evicted from a territory, not through overt aggression, but merely by the presence of the resident gibbons. 8.2.2. Olfactory advertisement. Some mammals have developed the use of scent marking as a means of declaring that an area is occupied. This has been best studied in the Carnivora (e.g. Kruuk 1972, 1978, Roper et al. 1986). Along the borders of their ranges these mammals regularly deposit faeces and perhaps anal secretions in sites referred to as 'latrines' and they may also deposit scent marks (Kruuk 1978, Roper et al. 1986). Olfactory advertisment has also been described for primates (e.g. Charles-Dominique 1977, Schilling 1979, Mertl-Millhollen 1988). For species of the prosimian subfamily Galaginae, this consists of micturating on substrates and may also include depositing urine on the soles of the four feet from where it will be transferred to the substrates along which these animals move (Charles-Dominique 1977). The latter type of marking behaviour allows a greater dispersion of the scent. Olfactory communication used in this way has the advantage that the signal (i.e. the odour) is maintained in the absence of the animal responsible for its presence (Croft 1982). Such advertisement may be efficient for mammals with territories small enough to allow patrol of border zones or where defence of a territory is shared by a group (e.g. Meles meles). However, in the case of Galago alleni, olfactory advertisement is supplemented by vocalizations in territorial advertisement (Charles-Dominique 1977). 8.2.3. Auditory advertisement. Vocal advertisement has many advantages over olfactory advertisement but 134 perhaps the greatest is that signals can be transmitted over long distances. This is illustrated by data presented by Waser (1977a) and Mitani (1985a,b) showing that vocalizations by primates can be heard by human observers up to or over 1km from the emitting animal. The use of vocalizations by both simian and prosimian primates, has been described by numerous authors (e.g. Carpenter 1934, Ellefson 1968, Mason 1968, Chivers 1974, Chivers et al. 1975, Waser 1975, 1977a, Charles-Dominique & Petter 1980, Pages 1980, Terborgh 1983, Goustard 1984, Haimoff 1984, Kappeler 1984, MacKinnon & MacKinnon 1984, Mitani 1985a,b,c, 1987, Harcourt & Nash 1986, Nash & Harcourt 1986) and it was suggested very early that such communication serves for both territorial defence and coordination of the movements of members of a group (Carpenter 1934). However, such hypotheses have only recently received experimental tests (e.g. Waser 1977a, Waser & Homewood 1979, Mitani 1985a,b,c, Mitani 1987, Raemaekers & Raemaekers 1985, Whitehead 1987). The use of vocalizations may be quite overt and frequent, as in the gibbons and howling monkeys, and vocal displays may precede chasing (e.g. Ellefson 1968). For some species, the use of vocalizations may be more subtle and result in mutual avoidance without any visual contact as in the mangabey, Cercocebus albigena. (Waser 1976, 1977a). Mason (1968) and Terborgh (1983) described details of territorial behaviour in Callicebus and Sanguinus where vocalizations were used extensively to advertise territories (emitted near boundaries) and overt defence was often observed. It is not surprising that primates use vocalizations for territorial delineation. Those species for which this has been documented occupy extremely large home-ranges (e.g. Bornean gibbon, Hylobates muelleri : ca. 40 ha Mitani 1985c). Waser (1976, 1977a) dismissed territorial behaviour in the mangabey (Cercocebus albig-ena) because home-ranges overlapped substantially between neighbouring groups, site defence did not occur and responses to playback recordings occurred independent of the postion within the home-range (Waser, 1977a). Avoidance behaviour was quite pronounced in the night monkey (Aotus trivirgata) where groups had substantially over-lapping home-ranges, often using the same fruit trees on the same night but at different times and calls were only emitted during encounters (Wright 1978). Mangabeys showed semi-nomadic movements within extremely large home-ranges (410 ha), possibly due to the low predictability in the availability of fruiting trees (Waser 1976). Vocalizations by mangabeys maintained intergroup spacing due to mutual avoidance and only the rare occurrence of encounters between neighbouring groups (one encounter during 120 days of continuous following). Mitani (1985a) observed only seven encounters between neighbouring "territorial" Bornean gibbon groups during 1500h of observation but these gibbons occupied exclusive home-ranges. In contrast to Mitani's observations, frequent interactions involving chases have been reported in other gibbon species (Ellefson 1968, Tenaza 1975, Gittons 1984). 8.3. SPACING AND RANGING BEHAVIOUR OF Petaurus australis. The yellow-bellied glider (P. australis) in common with many of the primates species discussed above, exhibits an intergroup spacing pattern of exclusive home-range use. Such a spacing behaviour is rare among marsupials (E. Russell 1984). This spacing pattern has been described in all five populations examined; two in Victoria (Henry & Craig 1984, Craig 1985), two in N.S.W. (Chapter 7) and one in north Qld (R. Russell 1984). This implies that this is the usual spacing pattern, if not the only one, adopted by this species. Furthermore, these home-ranges are, for the most part, extremely large (22-85 ha; Chapter 7). Gliders are extremely vocal (Kavanagh & Rohan-Jones 1982, Henry & Craig 1984, Russell 1984, Craig 1985) and few observations of overt defence have been made between neighbouring groups (e.g. Henry & Craig 1984, Craig 1985). Scent marking of substrates was not observed at Bombala but on one occasion at Kioloa, two gliders were observed to urinate as they climbed tree trunks soon after gliding onto those trees. Scent marking with secretion from a glider's frontal and sternal glands has been reported by Craig (1985) but the rarity of such observations suggest that these glands are used primarily for transfer of scent to conspecifics which mediates group cohesion (R. Russell 1984). Active glands are possessed only by adult males (pers. obs., R. Russell 1984, Craig 1985). In contrast, Norton (1988) observed that the greater glider (Petauroides volans) "regularly patrolled and scent-marked most of their home range." Thus, despite hundreds of hours of observation of yellow-bellied gliders at several sites there is little to suggest that exclusive use of a home-range is achieved by olfaction. This leaves vocalizations as the most likely behavioural mechanism by which gliders are able to achieve exclusive access to an area. The aims of this chapter are to examine more closely the factors which may influence the vocal behaviour of the yellow-bellied glider to achieve the observed spacing behaviour of discrete home-ranges. Further, I argue that these home-ranges are in fact territories, and that vocalizations by gliders are fundamental to delineation and advertisement of these territories. 8.4. CALLING BEHAVIOUR. Petaurus australis has a varied vocal repertoire (Kavanagh & Rohan-Jones 136 1982, R. Russell 1984) and its regular use of vocalizations probably place it as the most vocal of all marsupials. Surprisingly, this species was overlooked by Eisenberg et al. (1975) in a general account of vocalizations among marsupials. Whilst conducting the detailed observations on gliders (Chapters 2,3,4,5), I also recorded data on the calling behaviour of gliders. Thus, in this section I have dissected out of these observations relevant information on the calling behaviour of gliders. Kavanagh and Rohan-Jones (1982) stated that weather was an important determinant of the calling behaviour of gliders with heavy rain and strong winds having an inhibitory effect (see also Craig 1985) but this may be due to the influence on other aspects of a glider's behaviour. I have not attempted to examine weather due to problems in the replication of similar conditions (and problems associated with discerning calls when rain is falling and strong winds blowing) but instead have used data only from occasions when conditions were still. The following call types, defined by Kavanagh and Rohan-Jones (1982) are referred to extensively below. R. Russell (1984) has provided his own more extensive vocabulary of glider calls. Full call:- is the most characteristic non-gliding call emitted. The onomatopoeia description of Russell (1980) was "skree-uk-skree-uk-wufa-wufa-wufa-wufa". Gliding gurgle:- the typical gliding call described by Fleay (1947) as a "sustained gurgling cry". Gliding moan:- low frequency call emitted just after take off and extending into the glide. Described as "whoo" by R. Russell (1984). Short call:- similar to the full call but with only one shriek (Kavanagh & Rohan-Jones 1982) and repeated many times. Described as "jabber" by R. Russell (1984). Kavanagh and Rohan-Jones (1982) stated that calls by yellow-bellied gliders were audible up to 400 m from the calling individual. Craig (1985) stated that the full call could be heard within a range of 500 m. This was examined at Kioloa using two observers. One remained within 50 m of a glider and the other moved to varying distances away. When a call was emitted, the observer near the glider flashed a spotlight and the other observer noted whether or not the call was heard. Only full calls were monitored. Calls could be heard at 400 m from a calling glider (Table 8-1). Windy conditions were encountered at the time of testing the 400 m distance so few trials were conducted and no larger distances were tried. Table 8-1. The number of calls audible at various distances from a calling glider. Distance from glider (m) Call audible Call inaudible 100 10 0 200 1 0 300 11 0 400 3 1 8.4.1. Temporal distribution of calls. Kavanagh and Rohan-Jones (1982) recorded calls from fixed census points and documented a high incidence of calls early in the night and this was consistent throughout the year. In the study at Bombala, data were collected while following gliders for three whole-night periods in summer and three in winter 1986 (see Chapter 4). These data (Figs 8-la,b) demonstrate a clear bimodal pattern. The calling pattern of gliders is to a large extent, a reflection of the temporal pattern of gliding. Calling and gliding were highly correlated (Spearman rank correlation coefficient, rs= 0.945, P<0.01, n=9) for January (Fig 8-la). Difficulty in maintaining constant contact with foraging gliders in July prevented detailed data on gliding to be collected. However, this relationship is probably always evident as calls were emitted during 88% of all glides observed (n=184 for January and June/July 1986). 8.4.2. Calling by other gliders in group. Data were collected at Bombala to investigate the influence of conspecific calls on gliders under observation. The vocal response of a glider to calls from group members nearby (within 200m) were recorded (Fig. 8-2a). The response of gliders was not independent of call type (G=26.06, P <0.001). The glider under observation responded very infrequently to both short calls (7%) and gliding calls (10%). Answers to the full call were more common (36%) but fewer than half the calls were answered. 8.4.3. Calling in relation to food type. Here I have collated data on calling rate for times when gliders were feeding on different food types. Due to the potential effect that weather can have on calling rate, I have used data only from nights of similar weather conditions (i.e. still, dry etc.). 15 -i (a) • No. calls E3 No. glides o o 2130 2230 2330 2430 0130 0230 0330 0430 0530 Time of Night 15 -t (b) • Glider observed E3 Other gliders .C ca o 0 | \ 1830 1930 2030 2130 2230 2330 2430 0130 0230 0330 0430 0530 0630 Time of Night Fig. 8-1. (a) Distribution of calls and glides by one glider under observation for three nights in January 1986. (b) Distribution of calls by one glider under observation and by other gliders nearby for three nights in June/July 1986. 120-1 (a) • Short call 100 0 Gliding call H Full call w 80 - O 60- d z40 20 H 0 Yes No Call Answered (b) Periphery Core Location of Foraging Glider c *E in »_ Q. Control Experimental Assessment Period Fig. 8-2. (a) Frequency of calling by gliders under observation at Bombala in response to three call types of gliders nearby. (b) Number of calls (mean ± s.e.) by gliders under observation at Bombala when foraging in periphery and core of home-range, (n = 6 for both) (c) Number of calls (mean ± s.e.) by resident gliders before and following the transmission of a single full call at Kioloa. (n=10) 140 Data were taken mostly from the whole-night observation periods in 1986 because feeding bouts were generally fully observed and weather was similar. I have limited the data set to at least a 300 min total observation period for each food type. The interval for sap feeding was longer because bouts are typically quite long (see Chapter 4) and I wanted a sample size of at least six bouts. Table 8-2. Calling rates by gliders when harvesting different food types (see Chapter 2 for description) at Bombala. Data were collated for feeding bouts totalling at least a 300 min period of gliders harvesting different food items. Only non-gliding calls were recorded for the glider under observation. n= no. observation periods. Kruskal-Wallis analysis of variance, H=9.803, df=4, F<0.05. Food type Mean no. calls/h Total obs.time (min) ± s.e.(n) Sap 0.84 ± 0.42 (6) 611 Honeydew 1.73 ±0.75 (14) 420 Manna 0.73 ± 0.40 (9) 399 Arthropods 4.51 ±1.52 (25) 307 Arthr/honeydew 7.98 ±1.60 (26) 315 Gliders emitted calls at significantly different rates when harvesting different food types (Table 8-2). Calls were emitted much more frequently when gliders were harvesting items from within and beneath loose bark (i.e. arthropods/honeydew, arthropods) than when harvesting just exudates. In particular, the calling rate was 9 times greater for arthropods/honeydew than for sap feeding. This relates directly to the amount of time gliders spent in trees when feeding on different food types (see Chapter 4 - Table 4-3) and probably reflects the greater number of calls made by gliders associated with gliding. That is, although only non-gliding calls are tabulated, gliders often gave such calls when climbing up a tree following a glide. Thus the gliders' feeding behaviour is an important determinant of their calling behaviour. Stationary gliders perhaps have little need to communicate their position frequently. This may also indicate a coordinating function when foraging. Gliders more often fed together when sap feeding (Chapter 4) and had low calling rates. 8.4.4. Calling with respect to position in home-range. It has been suggested by other authors that for mammals using vocalizations to advertise their territories that such behaviour may be concentrated around the periphery because this is the area where incursions are best thwarted. So for gliders it is necessary to ask: Is calling greater near home-range boundaries? Another important aspect of territory delineation by vocalizations may be the position of an individual within the home-range or territory. Territorial animals often display more commonly near the boundaries of their territories (e.g. Ellefson 1968). I attempted to investigate this by collating data on calling with respect to the position in the home-range. The home-range was arbitrarily divided into core and peripheral regions. The latter being anywhere within 200m of what I perceived to be a boundary based on my extensive observations of tagged gliders (see Chapter 7). Data were collated for one hour intervals when individuals were continuously observed. Due to the influence of food type (see above), only data where a glider was harvesting food from within bark ribbons or under loose bark (i.e. arthropods, arthropods/honeydew) were used. Also, only data where the glider remained in the periphery or core for the entire one hour were used and again, I have only considered observations during similar weather conditions. These criteria only allowed six time intervals to be used for each of the two home-range regions. These data, although limited in sample size, do suggest that calling was morefrequent nea r the border of the home-range compared to the core (Fig. 8-2b). 8.4.5. Calling when neighbouring groups are present. At Bombala, only one observation was made of gliders from neighbouring groups coming into close proximity. On that occasion, only one of the gliders appeared cognisant of the other's presence and remained still until the other glider had moved at least 50m away. It then resumed foraging. The silent animal was an untagged subadult while the other animal was an adult male which vocalized frequently as it foraged. On one other occasion, gliders from neighbouring groups were present near the apparent boundary of their home-ranges (i.e. within 100-200m). There were three gliders in the group under observation and two present in the adjacent group. All animals vocalized frequently but the two groups remained more than 100m apart and no attempt was made by the three individuals observed to approach the other group. At Kioloa, during May 1989 gliders from two neighbouring groups used den trees within 150 m of each other. On one night a tagged adult female glider from group 3 came within 40 m of a flowering tree in which the adult female from group 2 was feeding, emitting calls as it moved. It soon moved back towards its own home-range while the group 2 female continued feeding. This observation was the only possible overlap in ranges observed at Kioloa (see Chapter 7). How do gliders respond to calls by intruding individuals? This was examined by conducting an experiment at Kioloa. This involved using the playback of a glider's call to monitor the response of resident individuals. A tape recording of calls of gliders in Nadgee State Forest, which had been used to produce sonograms (see Kavanagh & Rohan-Jones 1982), was obtained from R. Kavanagh. The experiment consisted of entering the home-range of a glider group with a cassette player and if a call was heard then approaching to within 100-200 m of the call. Then all calls from gliders were recorded during a 15 minute period. At the conclusion of that period a single full call was broadcast from the cassette player held approximately 2 m above the ground. Then for a subsequent period of 15 minutes all glider calls were recorded and where possible the movements of gliders monitored. This experiment was conducted on five nights between July and August 1989. Only one test was performed on a given group on a night and not on consecutive nights. Only 10 tests were conducted (Fig. 8-2c). Significantly more calls were heard following the playback period (Wilcoxon Signed Rank Test; T=5.5, P=0.012). On five occasions, gliders glided towards the playback area. One individual was heard calling 200m away before the playback at which time it approached the playback area, remained for 15 minutes and then returned to its former location. Another instance involved an individual gliding into three trees in succession surrounding the playback area but only 15 m from the cassette player. 8.5. DISCUSSION. The yellow-bellied glider has a complex vocal communication system (Kavanagh & Rohan-Jones 1982, R. Russell 1984) which parellels that of many primate species. The functional significance of vocalizations by gliders has received limited consideration. Waser (1977a) listed seven possible functions for the vocalizations of primates which may equally apply to gliders. Vocalizations may: (i) maintain intragroup cohesion, (ii) communicate the location of food resources to group members, (iii) facilitate the attraction of potential mates, (iv) maintain exclusive access to mates, (v) maintain group size and composition, (vi) coordinate group movements and, (vii) maintain territories or other types of intergroup spacing. (i) Gliders in a group spend considerable amounts of time together in the same tree either sleeping in the den or whilst foraging (Chapters 4,5) and therefore would not require an elaborate vocal communication system to aid in group cohesion. Moreover, adult male gliders possess scent glands which are used to transfer scent to other members of a group and thus provide group recognition and cohesion (Russell 1980,1984). (ii) Calls by gliders would certainly communicate to other individuals the type of food being harvested as calling rates differed for different food types. However, the availability of different food types is determined by phenological changes in the forest (Chapters 2,3,5) and thus, changes in availability would occur over a period of several days and not require frequent calling each night. (iii) Gliders form permanent breeding associations lasting several years (see Chapter 6) and so the function of attracting mates when a mated individual or pair died would only rarely be manifest. Mitani (1985b) found no support for this hypothesis for orangutans (Pongo pygmaeus) but Whitehead (1987) cited some support for howling monkeys. (iv) The use of calls to maintain exclusive access to a mate was suggested to account for primates in which one sex was primarily responsible for vocal exchanges (e.g. Mitani 1985b, 1987). All gliders vocalize regularly regardless of sex or status (i.e. adult or subadult). (v) This explanation may be relevant to primates and not to gliders because gliders form breeding association which appear to only be interrupted when one individual dies and group size is only altered by breeding within that group (Chapter 6). (vi) The coordination of group movements while foraging would undoubtedly occur and has been suggested by Kavanagh and Rohan-Jones (1982). This would be advantageous for gliders whilst foraging for arthropods because it would be costly for a glider to search through an area that another group member has searched. However, gliders rarely foraged for arthropods at Kioloa but calling rates were high (see below). Moreover, when feeding on exudates group members fed together often (see Chapters 4,5) but still vocalized occasionally. When conducting the playback experiments at Kioloa, gliders were feeding extensively on eucalypt nectar and pollen, and were often feeding in the same trees (Chapter 5). At such times calling rates were very high (Fig. 8-2c). (vii) If calls serve some sort of spacing function then it would be predicted that at sites such as Kioloa, where group sizes were larger and home-ranges considerably smaller than at Bombala, then gliders may have higher calling rates due to increased need to advertise territories. This was in fact the case. During the control periods of the playback experiments, gliders called at a rate of approximately 32 calls per hour (Fig. 8-2c). This contrasts noticeably to that at Bombala where gliders called at a rate of, at most, only 12 calls per hour (Fig. 8-l,8-2b). Thus, vocalizations are suggested to serve as a way of mediating intergroup spacing by gliders. It is further argued that vocalizations are employed as a type of territorial behaviour as has been suggested for many of the primates. The gibbons and howling monkeys present a paradigm for consideration of territorial behaviour. In these species, vocalizations are given in the form of "interactive singing" (Mitani 1985a). Many of the primates (e.g. siamang, gibbons) have calling bouts of 15-20 min which are given early in the morning but not necessarily every day (e.g. Chivers et al. 1975, Tenaza 1975). In contrast, yellow-bellied gliders vocalize throughout the night, with a distinctive bimodal pattern (see also Kavanagh & Rohan-Jones 1982, Craig 1985) which has now been described at several sites. An important consideration in the use of vocalizations for territorial delineation or advertisement is that calls can be detected over long distances (based on detection by human observers). For primates, this can be over distances of 0.8-2 km (Chivers et al. 1975, Mitani 1985a,b) whilst for yellow-bellied gliders, this is at least 0.4-0.5 km (Kavanagh & Rohan-Jones 1982, Craig 1985, this study). Chivers et al. (1975) found that calls by siamangs were made predominantly in the core area of the home-range. Transgression of home-range borders may lead to chasing (i.e. physical eviction) (e.g. Ellefson 1968, Tenaza 1975, Gittons 1984) but for some species this is rare ( Chivers et al. 1975, Mitani 1985a). R. Russell (1984) described in detail, several instances of fighting between neighbouring groups of yellow-bellied gliders resulting from trespassing to feed on sap-site trees. One fight resulted in two gliders which were clutching each other, falling 12 m to the ground. Such overt defence has rarely been observed at sites in southern Australia (Henry & Craig 1984, Craig 1985). At Kioloa, one fight took place in a flowering tree near a home-range boundary but lasted less than 5 minutes before both individuals left the tree. No fights were observed at Bombala. As noted for the primates above, direct confrontation between individuals from different groups is not necessary as evidence for territorial behaviour. Indeed, efficient spacing of conspecifics should minimise the occurrence of direct conflict (see below). The yellow-bellied glider lives in small family groups which occupy exclusive home-ranges (Chapter 7). Such spacing behaviour has been observed at all sites where this species has been studied (Henry & Craig 1984, R. Russell 1984, Craig 1985). Henry and Craig considered that territorial behaviour in this species to be incongruous because its food resources were not evenly dispersed, predictable and concentrated (but see Waser & Homewood 1979). However, studies on territorial behaviour have stressed that it will arise when resources (food, nest sites, mates) are economically defensible and usually concentrated (Brown 1964, 1969, Brown & Orians 1970). The qualifier normally associated with these statements is that the resources are limited (e.g. Mitani & Rodman 1979, Ostfeld 1985a). Food resources (i.e. exudates) of yellow-bellied gliders are very patchy (i.e. concentrated) in distribution, limited and because the availability of which is determined by the phenology of the forest (Chapters 2,3,5), are to some extent predictable. Thus, the food resources of yellow-bellied gliders are amenable to territorial behaviour. Mitani and Rodman (1979) have equated "defensible" with "highly mobile" in primates and suggest that those species which are capable of traversing a daily distance equivalent to the diameter of their home-range will be territorial. This prerequisite is easily met by yellow-bellied gliders which have a home-range diameter of less than 1 km (Chapter 7) but have been observed to traverse over 2 km in a night (Chapter 4). One individual at Bombala traversed 0.6 km in 20 minutes. Trespassing by gliders into neighbouring territories may generally be uneconomical. Of major importance for yellow-bellied gliders is that due to large home-ranges and wide dispersion of exudates within the home-range, an important component of foraging is memory. For example, sap-site trees at sites in southern Australia appear to be useful only on a sporadic basis (Chapter 3) and are widely spaced (Chapter 7). Thus, the location of such trees may involve considerable searching and then will require assaying over a period of time because not all sap-site tree can be used concurrently (Chapter 3). Moreover, the allocation of 90% of a resident glider's time to foraging (Chapter 4) suggests intrusion into unfamiliar home-ranges would prove very energetically costly. Terborgh (1983) also noted that "intimate familiarity" was an important aspect of territorial behaviour. In north Queensland, eucalypt sap may be available on a more continuous basis (Smith & Russell 1982) and this may have resulted in numerous interactions between adjoining glider groups. Thus, in common with many primate species, yellow-bellied gliders make extensive use of vocalizations. Auditory communication is of advantage because it can be used day or night and can be broadcast beyond environmental obstacles (Croft 1982). Waser and Waser (1977) suggested that vocal communication by primates has been necessary in tropical forest due to the constraints on visibility imposed by the habitat. In the case of P. australis, vocalizations are favoured for communication due to forest structure and nocturnal activity, but also because of the large home-ranges and therefore the large distances between neighbouring groups. Smaller home-ranges as in the greater glider may lead to the use of olfactory marking of home-ranges (see above) and perhaps no vocalizations between adults (Henry 1984). The fork-marked lemur (Phanerfurcifer), which has home-ranges with only a small zone of overlap used by neighbouring males, makes no use of urine and faeces (unlike most other nocturnal lemurs) in social communication (Charles-Dominique & Petter 1980). This species possesses a chin gland, used in allomarking, but it has rarely been observed to use this to mark any substrate. Also, the male and female are in vocal contact throughout the night and close proximity for at least half of it, a situation analogous to that of P. australis. Charles-Dominique and Petter (1980) conducted an experiment to examine the role of vocalizations in the territorial behaviour of P. furcifer. This involved caging a resident male in the middle of its territory. On subsequent nights another male made incursions into this territory and vocalized regularly. On one night a second male entered this territory which led to a fight. The first new male won and chased the other back to its territory. Charles-Dominique and Petter concluded that the presence and vocalizations of the normally established animal were necessary to maintain integrity of territorial boundaries. Dramatic changes in calling rates by yellow-bellied gliders (i.e. when individuals have died) in formerly occupied home-ranges have been suggested to be responsible for the establishment of new glider groups (Chapter 6). In the present study, calls were found to be emitted throughout the night and more calls were given near the boundaries of home-ranges. Experimental playback of calls (simulating an intruder) resulted in higher calling rates by resident gliders and in 50% of tests gliders approached the area of playback; in one instance from a distance of 200 m. Glider calls can be heard by human observers over distances of at least 400-500 m from the calling individual and without doubt, over much longer distances by conspecifics (see Brown 1986 for primates) which would therefore be adequate in maintaining the observed spacing behaviour. Assessment of seven possible functions for calls by gliders indicated that the mediation of intergroup spacing was the most likely but that calls may have secondary roles such as facilitating the coordination of individual foraging movements and the lack of or reduction in calls from formerly occupied areas may also serve to attract dispersing gliders. Chapter 9. CONCLUDING DISCUSSION. 9.1. INTRODUCTION. The principal aim of the studies descibed in this thesis was to examine, in detail, the foraging behaviour and socioecology of an exudivorous mammal. No previous study had done this satisfactorily. Moreover, this study has included investigations of the yellow-bellied glider (Petaurus australis) at two sites (separated by several hundred kilometers) where the forest habitats were quite different. One focus of this study has been the fundamental importance of food resource "traits" (i.e. abundance, dispersion) on the overall behavioural ecology of this species. Several points relating to this, which have not been treated in detail elsewhere in this thesis, require further discussion. 9.2. TIME BUDGET. Exudate food resources display a characteristic temporal and spatial patchiness which is similar to that of some fruit crops (see Terborgh 1983). Perhaps more importantly, exudates (when available) are continuously renewed, have a very high energy content and can be quickly digested. These traits appear to be inextricably related to a time-budget which requires gliders to spend approximately 90% of time outside the den in foraging related activites (Chapter 4). The coati (Nasua narica) is apparently the only other mammal known to invest so much time to foraging and this averages approximately 93% of its time as it forages for invertebrate and vertebrate prey and fallen fruit (Kaufman 1962, Russell 1982). The food types of other mammals (e.g. foliage) have an associated bulkiness which requires protracted digestion times and therefore, increased periods of rest (Chapter 4). An interesting finding from an examination of numerous primate species is that the proportion of time spent feeding increases significantly with increases in body weight but decreases with the amount of foliage in the diet (Clutton-Brock & Harvey 1977a,b). This suggests that the yellow-bellied glider is probably at the upper limit in body weight for an exudivore in similar habitat. It is hard to imagine a mammal having a time budget where more than 90% of its time is devoted to foraging-related activities. Indeed, harvesting rates of arthropods do not improve with increases in body weight (Terborgh 1983) and this could be expected to apply also to exudates. Smaller exudivores such as the sugar glider are expected to devote less time to foraging because the abundance of exudates they would encounter is approximately the 148 same as that for yellow-bellied gliders. However, their total energy requirements would be less and therefore, could be satisfied in less time. Also, body size differences for these two exudivorous species may lead to other differences in foraging behaviour due to relative differences in travel costs and choice of food patches (Price 1983). Galago crassicaudata is a primate exudivore twice the size of the yellow-bellied glider (Table 1-2). This bushbaby has 70% of its diet consisting of exudates (mostly gum) and yet it devotes only 25% of time to feeding on exudates and arthropods (Crompton 1984). This difference may simply reflect vastly different habitats and therefore resource distributions. For example, Terborgh and Schaik (1987) examined convergence among primate communities from different regions of the world. They found that the deviations from a model of convergence in community structure and organization could be explained by "differences in climate-driven phenological patterns of resource production". Such a result cautions against transcontinental comparisons of ecologically similar species when the relative abundances of food resources at the sites considered are unknown. However, it is reasonable to conclude that, although petaurids and prosimians are ecologically convergent, the different environments in which they have evolved has resulted in some divergent adaptations. For example, the evolution of gliding for a mammal the size of Petaurus australis was probably the key which opened an exudivore niche in Australian eucalypt forests. 9.3. SOCIALITY OR TERRITORIAL DEFENCE? Waser (1981) proposed this question largely to examine why some small African carnivores, the viverrids, formed large groups (e.g. the banded mongoose, Mungos mungo) whilst others maintained solitary social systems (e.g. genets). Typically, small carnivores which feed on arthropods live solitarily. The most likely solution to this paradox seemed to be the divergent renewal rates of their respective- food resources; for some species the renewal rate of the insect food resource is. apparently sufficient to allow group formation (Waser 1981). The social organization of the yellow-bellied glider and other petaurids engender a similar question. Indeed, Waser (1981) contended that the "rate of food renewal" hypothesis could explain the social organization of other animals. Many petaurid marsupials live in small family groups and may, on occasion, forage together (e.g. Smith 1982a). Smith and Lee (1984) have listed five potentially adaptive advantages which may account for the social behaviour, in particular sleeping aggregations, of possums and gliders (phalangeroids). They are: (i) energy conservation derived from nest sharing; (ii) predator avoidance; (iii) communication; (iv) mate defence; and (v) group territorial defence. However, Macdonald (1983) argued that, in some situations (e.g. carnivore societies), group and territory sizes may result from resource 149 dispersion which may lead to selective pressures operating on other behaviours associated with sociality. (i) Species for which energy conservation has been suggested are of a small body size and may derive some energy savings by sharing nests (e.g. Fleming 1980). However, field observations on group dynamics for the feathertail glider (lOg) have contradicted this hypothesis (Frey & Fleming 1984). Indeed, the yellow-bellied glider (590g; mean of male and female weight, Chapter 6) may derive less relative benefit due to its larger size but generally group members den together, regardless of the time of the year (unpubl. data). Moreover, the sharing of nests has apparently not resulted from a shortage of nesting hollows. The home-ranges of yellow-bellied gliders encompass 22-85ha of forest which literally include hundreds of suitably-sized hollows. This perhaps enabled some glider groups to utilize several hollows throughout the year (see also Henry & Craig 1984, Craig 1985). (ii) It is unlikely that the social behaviour of the phalangeroids has resulted from predation pressure. Group formation in diurnal primates has been widely mooted to reduce individual predation pressure (Terborgh 1983, Schaik 1983, Schaik & Hooff 1983). Indeed, most nocturnal mammals have solitary foraging systems (Terborgh 1983, Terborgh & Janson 1986). The vocal behaviour of the yellow-bellied glider would tend to alert predators to its whereabouts and thus would negate any possible reduction in predation pressure from group living. Present data indicate that gliders are only occasionally preyed upon by owls (Tilley 1982, Kavanagh 1988). (iii) Calling rates and call type may communicate the types and location of food resources amongst yellow-bellied gliders (Chapter 8). Gliders emit calls during most (88%) glides so that instances when only a few stationary calls are emitted over long periods may indicate to conspecifics that a food clump was being utilized. This may be particularly useful for an animal that devotes so much time to foraging. Instances when many gliding calls are emitted would not indicate large exudate clumps but rather that gliders are feeding on arthropods, and this may be useful in communicating to other group members the area already searched. Such an advantage can easily be invoked for the very vocal yellow-bellied glider which has an extensive home-range but what of other social possums and gliders? For most of the exudivorous species, olfaction and spatial memory are probably more important in locating and exploiting food patches (e.g. flowering trees). (iv) Mate defence would also be of less importance as the impetus for social behaviour among yellow-bellied gliders. Group members associated throughout the year, both in the den and whilst foraging, but only reproduce once a year which would necessitate much less investment in defence. It would be difficult and energetically expensive for males to locate widely dispersed females which come into oestrus once a year (Wright 1986) but, conversely, males would not be forgoing mating opportunities 150 by associating with permanent mates and they would have the advantage of assured mating access (E. Russell 1984). Henry (1984) found that, during the mating season, male greater gliders (Petauroides volans) exhibited a type of mate defence by remaining in close contact with female consorts, thus ensuring exclusive access. Thus, mate defence may be a consequence of social behaviour (i.e. aggregation) but is unlikely as the impetus for it. (v) The clumped but dispersed distribution of the principal exudate food resources (i.e. sap, honeydew, nectar and manna) of yellow-bellied gliders necessitates a large individual home-range to ensure continuity of food throughout the year. Such food types, due to their high rate of renewal, allow several gliders to feed in the same tree at the same time (Chapters 4,5). Clearly, these food types provide the initial impetus for aggregation. Terborgh (1983) suggests a similar situation for some primates (e.g. Saguinus imperator, S. fuscicollis) utilising fruit crops (see also Leighton & Leighton 1982). Terborgh also suggested the need for an "intimate familiarity" with the home-range by such species. This would also apply to yellow-bellied gliders. For example, sap-site trees were widely spaced within a given home-range (Chapter 7) but were rarely "in use" concurrently (Chapter 3). These trees presumably could be readily identified by a glider unfamiliar with an area (due to the extensive scarring on these trees caused by glider incising) but the suitability of these trees may not be predictable and may require occasional visits to assess this. The ability to traverse in a night a distance equal to the diameter of the home-range is also conducive to territoriality (see Mitani & Rodman 1979). One yellow-bellied glider observed at Bombala traversed 600m in 20 minutes travelling from its den tree to a sap-site tree where it fed for over three hours. At other times gliders were observed to traverse over 2 km in a night (Chapter 4) which suggests the ability to defend a large area. Moreover, occupation of an area by more than one individual would facilitate defence of a home-range. Thus, exudate food resources are characterised by a spatial patchiness and high rate of renewal (Chapters 2,3,5). These traits are conducive to group formation (Waser 1981) and for the yellow-bellied glider, are also conducive to territorial defence. 9.4. MATING SYSTEM. Perhaps of great importance in a consideration of the social organization of the yellow-bellied glider is the type of mating system displayed. Emlen and Oring (1977) have defined the mating system of a population as "the general behavioral strategy employed in obtaining mates. It encompasses such features as: (i) the number of mates acquired, (ii) the manner of mate acquisition, (iii) the presence and characteristics of any pair bonds, and (iv) the patterns of parental care provided by each sex." 151 In the present discussion, the term "mating system" refers to the presumed mating relationship between adult animals. The mating system has been variously described as the social system (e.g. Terborgh & Goldizen 1985, Terborgh 1986b) or the mating strategy (e.g. Powell 1989). The term "mating system" has also been used by other authors (e.g. Terborgh & Goldizen 1985, Janson 1984, 1986) to refer more precisely to the copulatory behaviour of individuals within a group. The mating system of the yellow-bellied glider is considered to be facultative monogamy (Lee & Cockburn 1985), due to the observation of monogamous groups in Victoria and polygynous groups in north Queensland. This variation in the mating system has been suggested to reflect a difference in the abundance and cost of harvesting food resources in tropical eucalypt forest compared to temperate eucalypt forest (Lee & Cockburn 1985). The observation of polygynous groups at Kioloa, N.S.W., contradicts any suggestion of a tropical/temperate eucalypt forest dichotomy. Lee and Cockburn (1985) and Henry (1985) have oversimplified the situation in north Queensland where R. Russell (1984) described the association of one adult male glider with several adult females (two of which reproduced concurrently). In fact, one group under intensive study by Russell contained a single adult pair for possibly over two years. This group contained a subadult female during this period which eventually reproduced in its natal group when two years of age. Instances of three adult females in a group probably indicate the presence of a non-breeding animal prior to dispersal. Such an interpretation has been placed on the occurrence of some additional adult gliders in groups at both Bombala and Kioloa (Chapter 6). The social organization of gliders at Kioloa was similar to that at Herberton, north Queensland. Two groups contained six individuals, including several adult females, when first monitored. Two of the females in one group were lactating concurrently, indicating polygyny. The size of these groups and a third group (not studied initially) then declined to a group size of three individuals. This followed three successive years of flower failure by Eucalyptus maculata, the most abundant eucalypt in the study area at Kioloa and that with the longest (April-October) flowering period (Chapter 5). At this time, glider groups consisted of a monogamous pair plus offspring. Thus, it appears that food abundance and continuity may have a large influence on the mating system of this species, as suggested by Lee and Cockburn (1985). Typically, gliders at both Bombala and Kioloa obtained sap, honeydew (by itself) and manna from only a small number (<7 of each) of trees in their home-ranges (Chapters 2,3,4,5). In contrast, on occasion there may have been 40-50 flowering trees present in less than 20% of a home-range at Kioloa (determined from the transect counts presented in Chapter 5). Moreover, due to the staggered flowering periods of the five eucalypt species, blossom could be available throughout the year (although in varying abundances) providing a continuous supply of both nectar (i.e. energy) and 152 pollen (i.e. protein). There has been considerable discussion since Trivers (1972) emphasized the disparity in the reproductive strategies of males and females. For example, among species of microtine rodent there are pronounced sexual differences in the occurrence of territorial behaviour (Cockburn 1988). Differences in perceived sexual strategies (see Clark 1978, Bearder & Martin 1980b for primates) led Wittenburger (1980) to state that female choice rather than male herding ability was responsible for sociality. Powell (1989) presented a resource productivity-variance model which typically applies to food resources but is also relevant to other resources such as nesting sites. This model predicts that where food is highly productive, highly patchy and predictable, then polygyny should evolve. This is the situation with the flowering resource at Kioloa. However, when E. maculata has failed to flower, productivity is low and predictability is low, a situation which the model predicts will favour monogamy. At Bombala, food productivity is generally low and highly patchy and thus should favour monogamy, whether predictability is low or high. Monogamy is commonly considered to evolve when food resources are limiting, thereby preventing social grouping, and where breeding success depends on male parental investment (e.g. Emlen & Oring 1977, Wittenberger & Tilson 1980, Rutberg 1983). Terborgh (1986b) has emphasised the interrelationship between group size and mating system for primates. However, he contended that group size is a tradeoff between the need to reduce per capita predation pressure (which decreases with increasing group size) and the number of individuals that a particular food resource can maintain economically. Group size of yellow-bellied gliders is unlikely to be contingent on predation pressure (see above) but is suggested to be constrained by the abundance of food resources. Eucalypt blossom has the potential to be superabundant, and in good years (e.g. when E. maculata flowers at Kioloa) may result in female philopatry and subsequently lead to polygyny. One instance of a group switching from monogamy to polygyny in north Queensland resulted from a female breeding in its natal home-range, presumably having mated with its father (R. Russell 1984). Such a situation may apply at Kioloa and elsewhere. This may result because mortality of subadults after dispersal is high, so that when food resources are superabundant, the chances of breeding success are greater for philopatric females (e.g. Waser & Jones 1983). This situation is in support of the hypothesis of Macdonald and Carr (1989) who suggested that resource availability, predictability and dispersion determine the framework of an animal's social organization (i.e. territorial behaviour) and within this framework sociological factors operate (i.e. determining the mating system). Also, "when food is dispersed in discrete patches .... territory size will be determined by the dispersion of such patches, while group size is determined by their richness." Food 153 abundance is invariably seen as a precursor to group formation and in the felids actually militates against sociality (Caro 1989). Moreover, home-ranges of gliders tended to be substantially smaller at Kioloa than at Bombala. Davies and Lundberg (1984) found, for a species of bird which displayed a variable mating system, that the dispersion of females was influenced by food resources and when female ranges were relatively smaller, males were able to monopolise several females. They confirmed this in experiments using artificial feeders to alter the abundance of food resources. Thus, it is suggested that alternation between monogamy and polygyny is probably a feature of the yellow-bellied glider mating system in habitats which allow smaller home-ranges and in some years offer superabundant food resources. 9.5. MANAGEMENT CONSIDERATIONS. This study has highlighted several areas of further research needed for the yellow-bellied glider in order that a greater resolution can be obtained of its ecological requirements. These are of direct relevance to the management of this species in areas where hardwood production is a high priority. One such area is in the southeast of N.S.W. where part of the research described in this thesis was conducted. There, the forests are intensively managed by the Forestry Commission of N.S.W. for the production of sawlogs and woodchips (integrated logging). Despite considerable modification to initial logging prescriptions and considerable research into the requirements of forest-dependent fauna (Dobbyns & Ryan 1983, Kavanagh 1983), there has emerged an extensive debate largely concerned with the impact of forestry operations on wildlife (see Andren 1988). The yellow-bellied glider has been placed in a central position in this debate (Glascott 1986). Although this species has a widespread distribution in eastern Australia (Russell 1983), many of its populations occur in areas where they might be considered vulnerable (e.g. Russell 1981). Thus, further research into the ecological requirements of this species should be a high priority of forest managers. This study has shown that gliders show a dependence on a small number of trees of certain eucalypt species for sap-feeding, at least during some periods of a year (Chapter 3). An hypothesis has been generated to explain the use of these sap-site trees by gliders but data from further sites are required to test its general relevance, including experiments which deny access to sap-site trees by gliders. Indeed, the identification and retention of these trees, perhaps by logging crews as forest is being logged, may be a simple but useful management tool for this species. The retention of certain habitats (e.g. gullies) would not ensure that these trees are retained because such trees are not necessarily confined to a particular habitat (Chapter 3). Further elucidation of the role of these specific trees will be central to management which attempts to mitigate the effects of logging on this species. 154 A detailed examination is required of the ecology of gliders specifically in areas where logging is taking place. There are two aspects of the behavioural ecology of this species which require examination in such a study: i) The time budget of gliders could be expected to change in response to extensive habitat alteration (cf. Johns 1986). Gliders ordinarily devote 90% of their time (outside their dens) to foraging (Chapters 4,5). Thus, following logging gliders may spend more time travelling, either searching for food resources or traversing greater distances to more widely dispersed resources. The impact of this may be the long-term consequences for gliders, due to demands on reproduction, rather than immediate mortality, ii) Gliders may alter the size of their home-ranges following logging due to changed spatial distribution patterns of food resources. An assessment of home-range size would also require investigation of the pattern of use of exudate trees, particularly sap-site trees, because variable survival of gliders may result from the differential retention of such trees. Investigating the behavioural ecology of this species following logging would require sufficient replication of glider groups so that definitive statements concerning the impact of logging can be made. Finally, consideration would need to be given to the size and geometry of the forest habitat required by gliders. Forest patches which become isolated may lead to the disappearance of gliders if insufficient in size. For example, the catchment at Waratah Creek, Bombala, has now been set aside as a flora reserve encompassing approximately 850 ha of forest (R. Kavanagh pers. comm.). However, if one group of gliders (consisting of at most three individuals) requires on average, 67 ha of forest for its home-range (Chapter 7), then this flora reserve may only contain 13 adult pairs of yellow-bellied gliders plus their offspring. A maximum of approximately 39 individuals. This is considerably fewer than the number presumably required to maintain a viable population (cf. Frankel 1982) and so, unless this reserve remains part of a larger block of continuous forest, then the continued survival of this species here would remain doubtful. Currently, studies concerned with the impact of logging have only considered the distribution of gliders after logging (e.g. references cited in Craig 1985, Lunney 1987). 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Reproduction in Polemonium: patterns and implications of floral nectar production and standing crops. Amer. J. Bot. 73: 1405-1415. Articles below removed for copyright reasons. Please refer to print copy: Goldingay, R.L. 1986, Feeding behaviour of the Yellow-bellied Glider, Petaurus australis (Marsupialia: Petauridae), at Bombala, New South Wales. Australian Mammalogy, 9:17-25 Goldingay, R.L. 1987, Sap feeding by the marsupial Petaurus australis: an enigmatic behaviour? Oecologia, 73:154-158 182 S- 2 3=> * i Q ' - tL >• 3 le . 3 2 - c = iIT 3. «a J«! -S £ — u . •o S ^ 3-2 o2.5 = E "S * r a 22 • ^•o c 3 5- E H >-s| - i «i !=<=" 2 E » a Ss' 3-2 !•?£ •5 = «r c g %£ Si* * - S - 2- S S'H fi 3 •= S S ° 3 -s :» * *- _ ** v s - ,. - i= " ^ 3 "v, -J; « o « 1 .§ 3 2-.=5 O E " E » _ • "3 .e •OB •= «• O 3 ~ — -C CT M 3 «i S'-a-J J! O SJ „ 1.2 * III S 5! 5.2 *. * 6 — .5 « w» — ci 2* = S E o! 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