INTERACTIONS BETWEEN FIGS (FICUS SPP., MORACEAE) AND FIG WASPS (CHALCIDOIDEA, AGAONIDAE) THESIS Submitted in fulfillment of the requirements for the Degree of Doctor of Philosophy at Rhodes University by ANTHONY BRIAN WARE December 1992 CONTENTS PREFACE .......•.•....................................................... iv LIST OF FIGURES ...••..•............•...•.•..•.•.......................••. v LIST OF TABLES ...................•.....••................................ xii ABSTRACT ................................................................ xvi CHAPTER 1: Introduction ................................................... 1 CHAPTER 2: Fig WJSp host specificity ....................•.................... 17 Paper 1: African figs and fig wasps: the wasps eye view of Ficus species. Mitteilungen aus dem Institut fur Allgemeine Botanik Hamburg 24, in press. (Compton, S.G.,Ware, A.B. and van Noort, S.) ...............•........... 17 Paper 2: Host specificity in some African fig wasps. Submitted to Annals of the Missouri Botanical Garden (Ware, A.B. ,Compton, S.G. and Phillipson, P .B) . ...................................................... 29 CHAPTER3: Biological evidence for the presence of volatile attractants ................. 48 Paper 3: Pollinator specific volatile attractants released from the figs of Ficus burtt­ davyi. South African Journal of Science 85,323- 324 (1989). (van Noort, S., Ware, A.B. and Compton, S.G.) .............................. 49 Paper 4: Fig wasp responses to host plant volatiles. Submitted to Journal of Insect Behavior. (Ware, A.B. and Compton, S.G.) .........•............ 51 CHAPTER 4: Chemical evidence for the presence of Ficus attractants ........•.......••• 67 Paper 5: Fig volatiles: their role in attracting pollinators and maintaining pollinator specificity. Plant Systematics and Evolution (In press). (Ware, A.B., Kaye, P.T.,Compton, S.G. and van Noort, S) ......................... 68 CHAPTERS: Studies of fig wasp behaviour ...................••....•............ 83 Paper 6: Dispersal of adult female fig wasps I. Arrivals and departures. Submitted to Emomologia Experimelltalis et applicara. (Ware, A.B. and Compton, S.G.) ................................................... 84 i i Paper 7: Dispersal of adult female fig wasps II. Movements between trees. Submitted to Elltomoiogia E'{perimelltalis et applicara. (Ware, A.B. and Compton, S.G.).................................................. 100 CHAPTER 6: Perception of volatiles ............................................ 118 Paper 8: Preparation of small, delicate insects for scanning electron microscopy. Proceedings of the Electron Microscopy Society of southern Africa 19,39-40 (1989). (Ware, A.B. and Cross, R.H.M.) ...................••.. 119 Paper 9: Repeated evolution of elongate multiporous plate sensilla in female fig wasps (Hymenoptera: Agaonidae: Agaoninae). Proceedings of the Koninlijke Nederlandse Akademie vall Wetenschappen 95,275-292 (1992). (Ware, A.B. and Compton, S.G.) ............•..•............•.......... 121 CHAPTER 7: Breakdown of host specificity .................•.................... 139 Paper 10: Studies of Ceratosolen gaZili, a non-pollinating agaonid fig wasp. Biotropica 23, 188-194 (1991). (Compton, S.G., Holton, K.C., Rashbrook, V.K., van Noort, S., Vincent, S. and Ware, A.B.) .........•.•............. 140 Paper 11: Breakdown of pollinator specificity in an African fig tree. Biotropica 24, in press. (Ware, A.B. and Compton, S.G.) .............•.......... 147 CHAPTER 8: Fig wasp parasitoids..................•..•..•.................... 153 Paper 12: African fig wasp parasitoid communities. In Parasitoid Community Ecology (Eds Hawkins, B.A. and Sheenan, W.) in press. (Compton, S.G. Rasplus, J.- Y. and Ware, A.B.) ........................................ 154 CHAPTER 9: Synopsis ...................................................... 179 iii PREFACE Natura nusquam magis quam in minimis tota est (Nature is nowhere more perfect than in the minutest of her works) Pliny: Roman naturalist and philosopher 1 A.D. Most research cannot be done in isolation and these studies are no exception. Although the contribution of colleagues is acknowledged in each section, I would like to make special mention of . of the following people: my senior supervisor, Dr Steve Compton, for providing me the opportunity to investigate fig/fig wasp biology and for his considerable input in the investigations; Prof. Perry Kaye provided much needed assistance in the chemical aspects of the study; Profs M. Brown and V. Moran for having enough faith in my ability to give me a second chance at Rhodes University; the 'fig team', in particular Sally Ross, Simon van Noort and Costas Zachariades, provided many hours of field assistance and company. Finally I would like to thank my wife, Kathy Holton, for her support and encouragement during my studies. iv FIGURES CHAPTER 1 Fig. 1. An electon micrograph of the interior of a fig showing the ostiole (0) with accompanying bracts (B) and the ovules (F) lining the inside of the flowers ......3 Fig. 2. Electron micrograph of the mandibles used by the pollinating fig wasp to force its way through the ostiole in order to gain access to the flowers within the fig ....••••• 2 Fig.3. Fig-fig wasp development cycles. Parasitoids will arrive later than the seed predators and oviposit from outside the fig after probing with their long ovipositors. See text for general description (Modified from Galil and Eisikowitch, 1968) ...•..•.•. 7 CHAPTER 2 Paper 2:Fig. 1. Our distribution records of southern African F. sycomorus and associated pollinator, C. arabicus Co); other southern African distribution records of F. sycomorus (0) are from van Greuning (1990) and von Breitenbach (1986) and are without pollinator records .....................•................................. 35 Fig. 2. Our distribution records of Malagasy and Comorian F. sycomorus (lot) together with their associated pollinators; other Malagasy and Comorian F. sycomorus (0) records are from Perrier de la Bathie (1928, 1952) and are without pollinator records •.• 56 Fig. 3. Our distribution records of F. sakalavarum (e) together with their associated . pollinators; other F. sakalavarum records (0) are from Perrier de la Bathie C1928, 1952) and are without pollinator records ...••..•••••....•............•. 36 Fig. 4. Our distribution records of southern African F. cordata subsp. cordata together with their associated pollinators (e) and F. cordata subsp. salicifolia ~); other F. cordata subsp. cordata (0) and F. cordata subsp. salicifolia records (+) are from van Greuning (1990) and von Breitenbach 1986) and are without pollinator records •...•..•• 39 Fig. 5. Our distribution records of southern African Ficus "thonningii I natalensis" together with their associated pollinators (.); other Ficus "thonningii I natalensis" records (0) are from van Greuning (1990) and von Breitenbach (1986) and are without pollinator records. F. lhollllingii (i) is only associated with one pollinator species while F. lUuaiellsis (ii and iii) is associated with two different agaonines . .....• 41 v CHAPTER 3. Paper 3.Fig. 1. Elisabethiella baijnathi trapped next to control (empty) cotton bags and bags containing receptive F. bunt-davyi or F. thonningii. More wasps were attracted to the figs of F. bunt-davyithan those of F. thollllingii or controls (t[34] = 3.96,P<0.001 and 1[34] = 3.65,P<0.01,respectfully). Equal numbers of wasps were trapped near control bags and those containing F. thollllingii figs (t[34] = 0.41 ,P> 0.05) ....... 49 Fig. 2. Elisabethiella baijnathi trapped next to control (empty) cotton bags and bags containing receptive figs of F. bunt-davyi or F. sur. More wasps were trapped near F. burtt-davyi than F. sur (t[34 = 6.89,P<0.001)or controls (t[34] = 6.97,P<0.OOl). There was no difference in the numbers of wasps trapped at F. sur figs and controls (t[34] = 0.054,P>0.05) .. ........•..........•.....•.......•........ 50 Fig. 3. Elisaberhiella baijnathi trapped next to control (empty) cotton bags containing receptive figs of F. bunt-davyiwith beeswax sealing their ostioles or applied to their bases. Figs with their ostioles covered did not attract wasps when compared with controls U[lS] = 1.17, P>0.1). In contrast, figs with basal wax remained highly attractive (t[18] = 3.37,P<O.0l) .. ...••.•......•.•.................... 50 Paper 4:Fig.1. Portion of the 1820 Settlers Botanical Garden (Grahamstown, South Africa) showing the relative positions of F. thonningii (+), F. burtt-davyi (0) and F. sJA.{rees. Additional exotic fig trees are represented by the open symbol (0). The numbers indicate those trees used to monitor the arrivals and departures of the fig wasps. 55 Fig.2. The effect of bagging pre-receptive (= pre-female) figs (hatched bar) of F. burtt-davyi on the numbers of pollinating wasps, E. baijnathi, trapped. The solid bars indicate the number of wasps trapped on a similar tree which remained unbagged ...... 56 Fig. 3. The numbers of wasps, together with their relative percentages, simultaneously trapped near bags containing receptive figs of F. thollningii or F. burtt-davyi. Empty bags acted as controls •.........•••.•....••..•.••.....••••..•...•. 58 Fig. 4. The fruiting phenologies of 10 fig trees used in the long term monitoring of fig wasp arrivals and departures. Intercrop periods are shown with a thin solid line while the period when trees are bearing fruit are denoted by solid blocks .............. 59 vi Fig. 5. Identity and numbers of fig wasps trapped at a