Oecologia (1992) 91:68-74
Oecologia
9 Springer-Verlag 1992
Determinants of species richness in southern African fig wasp assemblages S.G. Compton 1'2 and B.A. Hawkins z
1 Department of Zoology and Entomology, Rhodes University, Grahamstown, South Africa 2 NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berks. SL5 7PY, UK Received January 6, 1992 / Accepted in revised form February 24, 1992
Summary. We investigated the species richness of 24 fig wasp (Hymenoptera) assemblages associated with southern African fig trees (Ficus species, Moraceae). Assemblage sizes ranged between 3 and 30 species on different host tree species, with parasitoids slightly outnumbering gall-forming phytophages. Ten potential taxonomic, geographic and ecological determinants of assemblage richness were examined. Galler richness differed significantly between taxonomic sub-groups of Ficus and was significantly correlated with several ecological characteristics of the host trees, but there was no species-area effect. Parasitoid richness was strongly correlated with galler richness. We conclude that both ecological and historical factors have combined to determine the numbers of species that form fig wasp assemblages. Key words: Agaonidae - Cospeciation - Figs Galls
Ficus
Fig trees (Ficus spp., Moraceae) and pollinating fig wasps (Agaoninae, Agaonidae, Hymenoptera, sensu Boucek 1988) are partners in an obligate mutualism. Female agaonines are the exclusive pollinators of the trees, which in turn provide the wasps with the ovules where their larvae develop (Galil 1977). The relationship is highly specific, with each species of tree typically pollinated by only one wasp species and each wasp associated with only one tree species (Wiebes and Compton 1990; Michaloud et al. 1985). Related trees are generally pollinated by wasps belonging to the same genus (Wiebes and Compton 1990) and Wiebes' (1982) cladogram of agaonine genera showed a generally close correspondence with the relationships of the host trees. This evidence for parallel phylogenies of the trees and their pollinators has led to the suggestion that they have cospeciated (Jermy 1984; Thompson 1989).
Correspondence to: S.G. Compton, Dept. Zool & Entomol., Rhodes University, Grahamstown 6140, South Africa
Cospeciation is not the only explanation for parallel phylogenies between fig trees and agaonines, which could also have resulted from secondary radiation of the wasps after the trees had speciated (sequential/radiating speciation: Jermy 1976). Transfers by the wasps are more likely to have occurred between closely related tree species (Connor et al. 1980) and subsequent isolation of the populations could have resulted in each Ficus supporting different species of wasps. Examples of sequential evolution may include insects on thistles (Zwolfer 1982), tephritids in flower heads (Straw 1989) and lycaenids on Eriogonum (Shields and Reveal 1988), while Farrell and Mitter (1990) concluded that cospeciation was more likely in the case of Phyllobrotica leaf beetles and Lamiales. In addition to the agaonines, figs are host to numerous non-pollinating fig wasps. Non-pollinating fig wasps have traditionally been placed in several different families of the Chalcidoidea (Boucek et al. 1981), but most have recently been combined with the pollinating fig wasps into a much-enlarged Agaonidae (Boucek 1988). These fig wasps include both gall-forming phytophages and parasitoids. All the parasitoids oviposit from the outside of the figs, whereas the non-pollinating gallers include some species which, like the pollinators, have females that enter the figs before ovipositing. Tree specificity of non-pollinating fig wasps also appears to be well developed, with almost all the described species recorded from only a single host (exceptions in Boucek et al. 1981 ; Wiebes 1981). This may be partly a consequence of the small number of fig wasp communities that have been studied, although Ulenberg's (1985) revision of the parasitoid genus Apocrypta demonstrated extreme host specificity. She also showed that related Apocrypta species were associated with related trees. Thus, evidence of some parasitoid fig wasps having phylogenies that parallel Ficus is as strong as for the phytophagous agaonines. Given that evolutionary history influences both phytophagous and parasitoid fig wasp assemblage composition, what is the interplay between these evolutionary constraints and other, ecological factors that are known to influence insect communities (for example
69 S t r o n g et al. 1984)? C o m m u n i t i e s in w h i c h p l a n t s a n d insects h a v e c o s p e c i a t e d s h o u l d differ in s t r u c t u r e f r o m t h o s e w h e r e s e q u e n t i a l e v o l u t i o n has o c c u r r e d . I f the l a t t e r was the case, e c o l o g i c a l c h a r a c t e r i s t i c s o f the h o s t p l a n t s s h o u l d h a v e a g r e a t e r influence o n insect c o m m u n ity size a n d s t r u c t u r e (Ricklefs 1987; L a w t o n et al. in press). I n p a r t i c u l a r , h o s t f e a t u r e s w h i c h f a v o u r c o l o n i s a tion, such as a r e a o f d i s t r i b u t i o n a n d " a p p a r e n c y " (tree size etc.) s h o u l d be less i m p o r t a n t in t i g h t l y c o s p e c i a t e d systems. Similarly, i f p a r a s i t o i d s a n d their insect h o s t s h a v e c o s p e c i a t e d , links b e t w e e n p a r a s i t o i d c o m m u n i t i e s a n d their h o s t s s h o u l d b e d o m i n a t e d b y t a x o n o m i c relationships, w i t h e c o l o g i c a l c h a r a c t e r i s t i c s o f h o s t s o r h o s t f o o d p l a n t s ( A s k e w a n d S h a w 1986; H a w k i n s a n d L a w t o n 1987; H a w k i n s 1988) p l a y i n g a s e c o n d a r y role in determining parasitoid community composition. I n this p a p e r we e x a m i n e the c o m p o s i t i o n o f s o u t h e r n A f r i c a n fig w a s p a s s e m b l a g e s to d e t e r m i n e w h e t h e r hist o r y r e p r e s e n t s the o n l y d e t e r m i n a n t o f a s s e m b l a g e richness, o r if e c o l o g i c a l f a c t o r s are also i m p o r t a n t . Because it is likely t h a t forces o p e r a t i n g o n p h y t o p h a g o u s a n d p a r a s i t o i d fig w a s p s differ, we e x a m i n e s e p a r a t e l y the c o r r e l a t e s o f a s s e m b l a g e richness for the t w o g r o u p s .
Methods Our classification of Ficus follows Berg (1990). Figs were collected at the stage when the wasps were beginning to emerge and placed in netting-covered containers. After emergence the insects were killed and card-mounted for identification. Most of the non-pollinating wasps are undescribed and were placed as morpho-species. The biologies of most of the species are unknown and wasps were therefore assigned to each trophic level by extrapolation from information on their congeners. Among the better-studied groups of fig wasps trophic relationships are generally consistent within genera (and even subfamilies, Compton and van Noort, unpublished). A sampling unit consisted of the wasps reared from an individual tree. Samples considered to be unrepresentative, such as those collected outside the natural range of the plants, were excluded from the analyses. A total of 268 representative collections were obtained from the following southern African countries: South Africa, Zimbabwe, Botswana, Namibia, Zambia and Malawi. The collections covered 23 of the Ficus species recognised by Berg (1990), plus one subspecies which had a distinct fig wasp fauna, including the pollinator (Wiebes and Compton 1990). A s s e m b l a g e species richness
We examined ten taxonomic, geographical and ecological factors that we thought might influence the species richness of the 24 fig wasp assemblages. Factors 1 and 2 and 4-8 (below) are potential determinants of assemblage richness for both gallers and parasitoids, factors 3 and 9 are relevant to gallers only, and factor 10 is relevant to parasitoids only. 1. Sample size. More extensively sampled tree species should have more wasps recorded from them, at least until sufficient samples have been obtained for species-recruitment curves to have levelled out, at which time it can be assumed that effectively all members of the regional pools of wasp species have been collected. 2. Taxonomy. The Fieus species were grouped into six taxa, based on the subsections delimited by Berg (1990), except that subsections Platyphyllae and Chlamydodorae were combined because they have similar wasp faunas. Because two of the remaining taxa had only one species, and a third had only two species in southern Africa, we supplemented the data set with extralimital
collections of four additional species. These were F. asperiifolia Miq. (Sycidium, from Uganda), F. vallis-choudae (Sycomorus, from Cameroun and Uganda), F. saussureana DC and F. chlamydocarpa Midbr. & Burret (both Galoglychia, from Uganda and Cameroun respectively). These species were not included in any other analyses. If fig wasp assemblages have evolved in parallel with Ficus, a genus that has been traced back to the Cretaceous period (Arnold 1947), then the wasps associated with its various subgroups will have had long periods of isolation. Phylogenetic inertia will necessarily determine which wasp taxa are represented and thus their contribution to the overall species richness of each community. 3. Host tree taxon size. The numbers of southern African species in each subsection of Ficus were obtained from Berg (1990). Colonisation of new plant hosts is more likely to occur between closely related species. This can result in plants with more close relatives supporting more species of herbivores (for example Lewinsohn 1990). 4. Pollinator taxon size. The numbers of southern African species present in each genus of agaonines was obtained from Wiebes and Compton (1990), supplemented by our own samples. There is not always a close correspondence between the currently recognised taxonomic affinities of the trees and their pollinators. Consequently, pollinator taxon size provides a second measure of the numbers of tree species closely related to each Fieus, as well as the numbers of relatives of each of their pollinators. 5. Host plant latitudinal range. The distributions of the Ficus species were obtained from Berg et al. (1985), Friis (1985), Berg and Hijman 1989 and Berg (1990). Accurate mapping of the trees' distributions was impractical and an alternative indicator, the northsouth range of each species (in degrees of latitude), was employed. More widely distributed host plants generally support more herbivores, and more widely distributed insects support more parasitoids (Strong et al. 1984; Hawkins and Lawton 1987). One contributor to this species-area effect is habitat heterogeneity (widely distributed plants may occupy a wider range of habitats, Strong et al. 1984) allowing more animals with relatively narrow environmental requirements to utilise the plant. Plants which occur over a wide latitudinal range, for example, can potentially support both temperate- and tropical-adapted herbivores. The same arguments apply to parasitoids and their hosts. 6. Habitats of host trees. The primary habitats of each Ficus species were graded in order of their increasing humidity: (i) semidesert, (ii) savanna woodland, (iii) woodland or (iv) forest, based on summaries in Berg (1990). Species regularly occupying more than one category were given intermediate values. Adult fig wasps are small insects, prone to rapid dehydration. Hot, dry habitats may therefore require specialised adaptations, and thus exclude certain species (Compton et al. 1991). 7. Plant height. Values for the typical maximum height of the tree species were obtained mainly from Berg et al. (1985). Large trees may be easier for insects to find, and may produce larger crops. This increased apparency of large plants can result in larger numbers of associated insects (Moran 1980; Strong et al. 1984), and host insects feeding on larger foodplants support more parasitoids (Hawkins et al. 1990). 8. Fig size. The diameters of dried figs were extracted mainly from Berg et al. (1985). As fig diameter increases, so does the distance of the ovules from the outer surface of the fig (Compton and Nefdt 1990). Consequently, gallers and parasitoids that oviposit from the outside of the figs may be excluded from large figs if their ovipositors are too short. 9. Seed size. Fig seed diameters were obtained mainly from Berg et al. (1985), supplemented by measurements of seeds removed from the samples. No data were available for four species. Fig seeds are often extremely small and may be of insufficient size to support the development of the larger fig wasps. 10. Galler richness. The galler species richness of each tree species represents the number of potential host species available for the parasitoid fig wasps. If parasitoids are oligophagous or monophagous, a positive correlation would be expected between galler and parasitoid richness.
70
the lowest numbers of gallers (mean = 1.5), whereas the other subsections were relatively more species-rich, with the average number of gallers ranging between 2.5 and 6.0. ANOVA of galler richness between pairs of subsections were only significant in combinations which ineluded Sycidium. Galler richness was positively correlated with pollinator taxon size, plant height and sample size (Table 2, Figs. 1-3). That is, galler-rich assemblages were associated with larger trees, trees pollinated by wasps in species-rich genera, and trees that were more regularly sampled. The relationship between sampling effort and galler species richness remained significant even when we included only the 15 species which showed a levelling out in their species-recruitment curves (Fig. 4, r=0.616, P = 0.013). Tree taxon size, tree latitudinal range, habitat aridity, fig size and seed size had no significant effects on galler richness (Table 2).
The importance of plant taxon for (log-transformed) galler and parasitoid species richnesses was examined using model 1 analysis of variance (ANOVA). The other variables were investigated using simple and multiple regression. Relationships among independent variables were examined by comparing cross correlations and with principal component analysis. Only groups of mutually statisticaUy independent variables were included in the multiple regressions.
Results Between 3 and 30 species of fig wasps were associated with each host Ficus (Table 1). A N O V A of the 24 southern African and 4 extralimital taxa failed to detect any significant differences between subsections in the numbers of parasitoids (F5.22 = 0.71, P > 0.05), but there was a: marginal difference in the numbers of gallers (F5,22 =2.76, P=0.044). The two Sycidium species had Table l. The southern African Ficus species and fig wasps used in the analyses
No. of Wasp species
Fieus
Subsections
Species
samples Gallers Parasitoids
Sycidium
F. capreifolia Delile
Sycomorus
F. sycomorus L. F. sur Forssk.
Urostigrna
F. F. F. F.
Galoglychia
F. lutea Vahl
Platyphyllae
F. F. F. F. F. F. F.
2
1
2
3
27 30
7 6
6 6
13 12
16 17 11 8
5 2 2 2
9 2 2 5
14 4 4 7
4
5
8
13
bussei Mild. & Burr. 3 glumosa Delile 23 stuhlmannii Warb. 10 nigro-punetata Mild. & Burr. 1 tettensis Hutch. 6 abutilifolia (Miq.) Miq. 17 triehopoda Baker 13
6 11 10 3 2 3 5
9 8 10 1 1 9 14
15 19 20 4 3 12 19
3 18 11 31
5 4 2 12
6 4 3 18
11 8 5 30
5 3 3 5 1
4 3 2 8 5
3 4 3 9 4
7 7 5 17 9
ingens (Miq.) Miq. e. eordata Thunb. c. salieifolia (Vahl) Berg verruculosa Warb.
Chlamydodorae F. fiseheri Mild. & Burr. F. burtt-davyi Hutch. F. ilicina (Sonder) Miq. F. thonningii BI. Caulocarpae
Table 2, Correlations between Ficus species variables and the numbers of their fig wasp gallers and parasitoids, with partial correlations for parasitoids when galier richness is held constant
F . t . tremula Warb. F. p. polita Vahl F. bizanae Hutch. & B-D. F. sansibariea Warb. F. bubu Warb.
Variable
Galler speciesrichness (log)
No. of samples Fig size Tree height Tree taxon size Wasp taxon size Tree latitudinal range Habitat aridity Seed size Galler species nos. * P_
Oecologia
9 Springer-Verlag 1992
Determinants of species richness in southern African fig wasp assemblages S.G. Compton 1'2 and B.A. Hawkins z
1 Department of Zoology and Entomology, Rhodes University, Grahamstown, South Africa 2 NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berks. SL5 7PY, UK Received January 6, 1992 / Accepted in revised form February 24, 1992
Summary. We investigated the species richness of 24 fig wasp (Hymenoptera) assemblages associated with southern African fig trees (Ficus species, Moraceae). Assemblage sizes ranged between 3 and 30 species on different host tree species, with parasitoids slightly outnumbering gall-forming phytophages. Ten potential taxonomic, geographic and ecological determinants of assemblage richness were examined. Galler richness differed significantly between taxonomic sub-groups of Ficus and was significantly correlated with several ecological characteristics of the host trees, but there was no species-area effect. Parasitoid richness was strongly correlated with galler richness. We conclude that both ecological and historical factors have combined to determine the numbers of species that form fig wasp assemblages. Key words: Agaonidae - Cospeciation - Figs Galls
Ficus
Fig trees (Ficus spp., Moraceae) and pollinating fig wasps (Agaoninae, Agaonidae, Hymenoptera, sensu Boucek 1988) are partners in an obligate mutualism. Female agaonines are the exclusive pollinators of the trees, which in turn provide the wasps with the ovules where their larvae develop (Galil 1977). The relationship is highly specific, with each species of tree typically pollinated by only one wasp species and each wasp associated with only one tree species (Wiebes and Compton 1990; Michaloud et al. 1985). Related trees are generally pollinated by wasps belonging to the same genus (Wiebes and Compton 1990) and Wiebes' (1982) cladogram of agaonine genera showed a generally close correspondence with the relationships of the host trees. This evidence for parallel phylogenies of the trees and their pollinators has led to the suggestion that they have cospeciated (Jermy 1984; Thompson 1989).
Correspondence to: S.G. Compton, Dept. Zool & Entomol., Rhodes University, Grahamstown 6140, South Africa
Cospeciation is not the only explanation for parallel phylogenies between fig trees and agaonines, which could also have resulted from secondary radiation of the wasps after the trees had speciated (sequential/radiating speciation: Jermy 1976). Transfers by the wasps are more likely to have occurred between closely related tree species (Connor et al. 1980) and subsequent isolation of the populations could have resulted in each Ficus supporting different species of wasps. Examples of sequential evolution may include insects on thistles (Zwolfer 1982), tephritids in flower heads (Straw 1989) and lycaenids on Eriogonum (Shields and Reveal 1988), while Farrell and Mitter (1990) concluded that cospeciation was more likely in the case of Phyllobrotica leaf beetles and Lamiales. In addition to the agaonines, figs are host to numerous non-pollinating fig wasps. Non-pollinating fig wasps have traditionally been placed in several different families of the Chalcidoidea (Boucek et al. 1981), but most have recently been combined with the pollinating fig wasps into a much-enlarged Agaonidae (Boucek 1988). These fig wasps include both gall-forming phytophages and parasitoids. All the parasitoids oviposit from the outside of the figs, whereas the non-pollinating gallers include some species which, like the pollinators, have females that enter the figs before ovipositing. Tree specificity of non-pollinating fig wasps also appears to be well developed, with almost all the described species recorded from only a single host (exceptions in Boucek et al. 1981 ; Wiebes 1981). This may be partly a consequence of the small number of fig wasp communities that have been studied, although Ulenberg's (1985) revision of the parasitoid genus Apocrypta demonstrated extreme host specificity. She also showed that related Apocrypta species were associated with related trees. Thus, evidence of some parasitoid fig wasps having phylogenies that parallel Ficus is as strong as for the phytophagous agaonines. Given that evolutionary history influences both phytophagous and parasitoid fig wasp assemblage composition, what is the interplay between these evolutionary constraints and other, ecological factors that are known to influence insect communities (for example
69 S t r o n g et al. 1984)? C o m m u n i t i e s in w h i c h p l a n t s a n d insects h a v e c o s p e c i a t e d s h o u l d differ in s t r u c t u r e f r o m t h o s e w h e r e s e q u e n t i a l e v o l u t i o n has o c c u r r e d . I f the l a t t e r was the case, e c o l o g i c a l c h a r a c t e r i s t i c s o f the h o s t p l a n t s s h o u l d h a v e a g r e a t e r influence o n insect c o m m u n ity size a n d s t r u c t u r e (Ricklefs 1987; L a w t o n et al. in press). I n p a r t i c u l a r , h o s t f e a t u r e s w h i c h f a v o u r c o l o n i s a tion, such as a r e a o f d i s t r i b u t i o n a n d " a p p a r e n c y " (tree size etc.) s h o u l d be less i m p o r t a n t in t i g h t l y c o s p e c i a t e d systems. Similarly, i f p a r a s i t o i d s a n d their insect h o s t s h a v e c o s p e c i a t e d , links b e t w e e n p a r a s i t o i d c o m m u n i t i e s a n d their h o s t s s h o u l d b e d o m i n a t e d b y t a x o n o m i c relationships, w i t h e c o l o g i c a l c h a r a c t e r i s t i c s o f h o s t s o r h o s t f o o d p l a n t s ( A s k e w a n d S h a w 1986; H a w k i n s a n d L a w t o n 1987; H a w k i n s 1988) p l a y i n g a s e c o n d a r y role in determining parasitoid community composition. I n this p a p e r we e x a m i n e the c o m p o s i t i o n o f s o u t h e r n A f r i c a n fig w a s p a s s e m b l a g e s to d e t e r m i n e w h e t h e r hist o r y r e p r e s e n t s the o n l y d e t e r m i n a n t o f a s s e m b l a g e richness, o r if e c o l o g i c a l f a c t o r s are also i m p o r t a n t . Because it is likely t h a t forces o p e r a t i n g o n p h y t o p h a g o u s a n d p a r a s i t o i d fig w a s p s differ, we e x a m i n e s e p a r a t e l y the c o r r e l a t e s o f a s s e m b l a g e richness for the t w o g r o u p s .
Methods Our classification of Ficus follows Berg (1990). Figs were collected at the stage when the wasps were beginning to emerge and placed in netting-covered containers. After emergence the insects were killed and card-mounted for identification. Most of the non-pollinating wasps are undescribed and were placed as morpho-species. The biologies of most of the species are unknown and wasps were therefore assigned to each trophic level by extrapolation from information on their congeners. Among the better-studied groups of fig wasps trophic relationships are generally consistent within genera (and even subfamilies, Compton and van Noort, unpublished). A sampling unit consisted of the wasps reared from an individual tree. Samples considered to be unrepresentative, such as those collected outside the natural range of the plants, were excluded from the analyses. A total of 268 representative collections were obtained from the following southern African countries: South Africa, Zimbabwe, Botswana, Namibia, Zambia and Malawi. The collections covered 23 of the Ficus species recognised by Berg (1990), plus one subspecies which had a distinct fig wasp fauna, including the pollinator (Wiebes and Compton 1990). A s s e m b l a g e species richness
We examined ten taxonomic, geographical and ecological factors that we thought might influence the species richness of the 24 fig wasp assemblages. Factors 1 and 2 and 4-8 (below) are potential determinants of assemblage richness for both gallers and parasitoids, factors 3 and 9 are relevant to gallers only, and factor 10 is relevant to parasitoids only. 1. Sample size. More extensively sampled tree species should have more wasps recorded from them, at least until sufficient samples have been obtained for species-recruitment curves to have levelled out, at which time it can be assumed that effectively all members of the regional pools of wasp species have been collected. 2. Taxonomy. The Fieus species were grouped into six taxa, based on the subsections delimited by Berg (1990), except that subsections Platyphyllae and Chlamydodorae were combined because they have similar wasp faunas. Because two of the remaining taxa had only one species, and a third had only two species in southern Africa, we supplemented the data set with extralimital
collections of four additional species. These were F. asperiifolia Miq. (Sycidium, from Uganda), F. vallis-choudae (Sycomorus, from Cameroun and Uganda), F. saussureana DC and F. chlamydocarpa Midbr. & Burret (both Galoglychia, from Uganda and Cameroun respectively). These species were not included in any other analyses. If fig wasp assemblages have evolved in parallel with Ficus, a genus that has been traced back to the Cretaceous period (Arnold 1947), then the wasps associated with its various subgroups will have had long periods of isolation. Phylogenetic inertia will necessarily determine which wasp taxa are represented and thus their contribution to the overall species richness of each community. 3. Host tree taxon size. The numbers of southern African species in each subsection of Ficus were obtained from Berg (1990). Colonisation of new plant hosts is more likely to occur between closely related species. This can result in plants with more close relatives supporting more species of herbivores (for example Lewinsohn 1990). 4. Pollinator taxon size. The numbers of southern African species present in each genus of agaonines was obtained from Wiebes and Compton (1990), supplemented by our own samples. There is not always a close correspondence between the currently recognised taxonomic affinities of the trees and their pollinators. Consequently, pollinator taxon size provides a second measure of the numbers of tree species closely related to each Fieus, as well as the numbers of relatives of each of their pollinators. 5. Host plant latitudinal range. The distributions of the Ficus species were obtained from Berg et al. (1985), Friis (1985), Berg and Hijman 1989 and Berg (1990). Accurate mapping of the trees' distributions was impractical and an alternative indicator, the northsouth range of each species (in degrees of latitude), was employed. More widely distributed host plants generally support more herbivores, and more widely distributed insects support more parasitoids (Strong et al. 1984; Hawkins and Lawton 1987). One contributor to this species-area effect is habitat heterogeneity (widely distributed plants may occupy a wider range of habitats, Strong et al. 1984) allowing more animals with relatively narrow environmental requirements to utilise the plant. Plants which occur over a wide latitudinal range, for example, can potentially support both temperate- and tropical-adapted herbivores. The same arguments apply to parasitoids and their hosts. 6. Habitats of host trees. The primary habitats of each Ficus species were graded in order of their increasing humidity: (i) semidesert, (ii) savanna woodland, (iii) woodland or (iv) forest, based on summaries in Berg (1990). Species regularly occupying more than one category were given intermediate values. Adult fig wasps are small insects, prone to rapid dehydration. Hot, dry habitats may therefore require specialised adaptations, and thus exclude certain species (Compton et al. 1991). 7. Plant height. Values for the typical maximum height of the tree species were obtained mainly from Berg et al. (1985). Large trees may be easier for insects to find, and may produce larger crops. This increased apparency of large plants can result in larger numbers of associated insects (Moran 1980; Strong et al. 1984), and host insects feeding on larger foodplants support more parasitoids (Hawkins et al. 1990). 8. Fig size. The diameters of dried figs were extracted mainly from Berg et al. (1985). As fig diameter increases, so does the distance of the ovules from the outer surface of the fig (Compton and Nefdt 1990). Consequently, gallers and parasitoids that oviposit from the outside of the figs may be excluded from large figs if their ovipositors are too short. 9. Seed size. Fig seed diameters were obtained mainly from Berg et al. (1985), supplemented by measurements of seeds removed from the samples. No data were available for four species. Fig seeds are often extremely small and may be of insufficient size to support the development of the larger fig wasps. 10. Galler richness. The galler species richness of each tree species represents the number of potential host species available for the parasitoid fig wasps. If parasitoids are oligophagous or monophagous, a positive correlation would be expected between galler and parasitoid richness.
70
the lowest numbers of gallers (mean = 1.5), whereas the other subsections were relatively more species-rich, with the average number of gallers ranging between 2.5 and 6.0. ANOVA of galler richness between pairs of subsections were only significant in combinations which ineluded Sycidium. Galler richness was positively correlated with pollinator taxon size, plant height and sample size (Table 2, Figs. 1-3). That is, galler-rich assemblages were associated with larger trees, trees pollinated by wasps in species-rich genera, and trees that were more regularly sampled. The relationship between sampling effort and galler species richness remained significant even when we included only the 15 species which showed a levelling out in their species-recruitment curves (Fig. 4, r=0.616, P = 0.013). Tree taxon size, tree latitudinal range, habitat aridity, fig size and seed size had no significant effects on galler richness (Table 2).
The importance of plant taxon for (log-transformed) galler and parasitoid species richnesses was examined using model 1 analysis of variance (ANOVA). The other variables were investigated using simple and multiple regression. Relationships among independent variables were examined by comparing cross correlations and with principal component analysis. Only groups of mutually statisticaUy independent variables were included in the multiple regressions.
Results Between 3 and 30 species of fig wasps were associated with each host Ficus (Table 1). A N O V A of the 24 southern African and 4 extralimital taxa failed to detect any significant differences between subsections in the numbers of parasitoids (F5.22 = 0.71, P > 0.05), but there was a: marginal difference in the numbers of gallers (F5,22 =2.76, P=0.044). The two Sycidium species had Table l. The southern African Ficus species and fig wasps used in the analyses
No. of Wasp species
Fieus
Subsections
Species
samples Gallers Parasitoids
Sycidium
F. capreifolia Delile
Sycomorus
F. sycomorus L. F. sur Forssk.
Urostigrna
F. F. F. F.
Galoglychia
F. lutea Vahl
Platyphyllae
F. F. F. F. F. F. F.
2
1
2
3
27 30
7 6
6 6
13 12
16 17 11 8
5 2 2 2
9 2 2 5
14 4 4 7
4
5
8
13
bussei Mild. & Burr. 3 glumosa Delile 23 stuhlmannii Warb. 10 nigro-punetata Mild. & Burr. 1 tettensis Hutch. 6 abutilifolia (Miq.) Miq. 17 triehopoda Baker 13
6 11 10 3 2 3 5
9 8 10 1 1 9 14
15 19 20 4 3 12 19
3 18 11 31
5 4 2 12
6 4 3 18
11 8 5 30
5 3 3 5 1
4 3 2 8 5
3 4 3 9 4
7 7 5 17 9
ingens (Miq.) Miq. e. eordata Thunb. c. salieifolia (Vahl) Berg verruculosa Warb.
Chlamydodorae F. fiseheri Mild. & Burr. F. burtt-davyi Hutch. F. ilicina (Sonder) Miq. F. thonningii BI. Caulocarpae
Table 2, Correlations between Ficus species variables and the numbers of their fig wasp gallers and parasitoids, with partial correlations for parasitoids when galier richness is held constant
F . t . tremula Warb. F. p. polita Vahl F. bizanae Hutch. & B-D. F. sansibariea Warb. F. bubu Warb.
Variable
Galler speciesrichness (log)
No. of samples Fig size Tree height Tree taxon size Wasp taxon size Tree latitudinal range Habitat aridity Seed size Galler species nos. * P_
