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OIKOS 73: 109-119. Copenhagen 1995 Phloem-feeding specialists sharing a host tree: resource partitioning minimizes interference competition among galling aphid species Moshe Inbar and David Wool Inbar, M. and Wool, D. 1995. Phloem-feeding specialists sharing a host tree: resource partitioning minimizes interference competition among galling aphid species. - Oikos 73: 109-119. This study deals with a guild of specialist, phloem feeding aphids (Homoptera; Pemphigidae; Fordinae) which form galls on Pistacia trees (Anacardiaceae). In Israel, each of two Pistucia species carries five common species of galling aphids, which may occur in large numbers on the same individual tree, shoot, leaf or even leaflet. These Fordinae have very similar life cycles, they all feed on phloem sap, and all of them need very young, unfolding leaves for gall formation. Our data show, however, that most pairs of species are unlikely to compete for galling sites because their niches are separated either temporally (fundatrices arrive at different times and, therefore, occupy different leaves) or spatially, by attacking different sites on the tree, shoot, or leaf. In 1991-1993, we calculated niche breadth (B) of each species, and proportional similarity (PS) between each species pair on shoots colonized by more than one species. PS between different species pairs on leaves within shoots ranged between 0 and 0.48. This means that, on the niche dimension represented by the shoot, the two species may share some of the habitat units. If the two species compete, we expected that niche breadth of at least one of them would be reduced on the cohabited shoots. This was not the case. B was not negatively affected when pairs of species occupied the same shoot, compared with shoots where only one species was present. B was positively correlated with density: the chance of niche overlap increased when more galls occupied the same shoot. In species sharing leaves within shoots. B showed similar trends. On P. utlanrica, Srnynthurodes betae and Forda riccobonii had the highest PS. Both species make their galls on leaflet margins and occur frequently on the same leaves. Only at this level did we detect negative interactions: the frequency of co-occurrence of galls of both species on the same leaflet (within galled leaves) was significantly less than expected by chance. Taking into account our deliberate non-random selection of trees. shoots, and leaves, where competition was likely to occur, we conclude that interspecific interference competition for galling sites is not a major determinant of the resource partitioning of these closely-related herbivores. M . Irlbar (Bursrein) and D. Wool, Dept of Zoology, George S . Wise Faculty of Life Sciences, Tel Avi). Univ., Rantat Aviv 69978, Israel. Theoretical ecology has emphasized for many years the centrality of interspecific competition, as a determinant of the distribution of organisms in space and time, and the issue occupies considerable space in ecological textbooks Accepted 13 October 1994 Copyright 0OIKOS 1995 ISSN 0030-1299 Printed in Denmark - all rights reserved (e.g. Ricklefs 1979, Price 1984a). Schoener (1982) concluded that despite criticism, competition must still be considered of major ecological importance. An overwhelming majority of field experiments reported evi- dence for interspecific competition (Schoener 1983), largely supporting Hairston's et al. (1960) suggestion that phytophagous animals compete less than other groups. Recent studies tend to play down the importance o f competition in natural communities (e.g., Strong et al. 1984),and dismiss the "ghost o f competition past" (Connell 1980) as irrelevant (e.g. Strong 1984). Price (1984b) focused attention on specialists, which use only a small subset o f the seemingly available resources. He makes the point that when different species o f specialists coexist, they do not necessarily compete for a shared, limited resource and that many "empty niches" may be available to them. But the issue is certainly not dead: Competition and resource partitioning were reported among four species o f bark beetles (Scolytidae) attacking phloem tissue in pine trees (Paine et al. 1981). More recently, Schlyter and Anderbrant (1993) demonstrated "scramblen-type competition for that resource in Norwegian spruce. Many specialists may be found among phloem-feeding insects such as aphids. Several species o f aphids may co-exist on an individual tree, but occupy different niches. Moreover, the morphology and lengths o f their feeding stylets show correspondence with their feeding sites (Dixon 1985: 25-28, Hajek and Dahlsten (1986)), and thus competition among them is unlikely. Addicott (1978) mentions 3 conditions which must be met for interspecific competition to be possible: that the species exhibit intra-specific competition, that the species coexist in space and time, and that the presence o f one species decreases the fitness o f individuals o f the other species. These conditions are met for some species o f aphids (review in Dixon 1977, 1985, Moran and Whitham 1990). Factors which reduce interspecific competition may be selection o f different feeding sites, temporal separation, and the effectso f predation and parasitism, which may reduce population sizes to levels too low for competition to have a meaningful effect (Lawton and Strong 1981, Strong et al. 1984). Some recent studies on specialist herbivores do not agree on interspecific competition as a cause o f niche separation. Moran and Whitham (1990) found that leafgalling aphids had a negative effect on density o f rootgalling species on susceptible plants. through competition for phloem sap as a common resource. Fritz (1990) detected significant differences in the magnitude o f competition coefficients o f gall-inducing sawflies among willow clones. Fritz and Price (1990) and Fritz et al. (1986), however, suggest that competition had less effect on densities o f the species concerned than other environmental factors. The two Scolytid species studied by Schlyter and Anderbrant (1993) tend to occupy different parts o f the host tree, but no interference competition was observed at the time o f colonization, and the mechanism o f this niche separation is unclear - perhaps differential response to species-specific aggregation pheromone (loc. cit.).In his study o f Eriosoma galling aphids on Ulmus in Japan, Akimoto (1988) concluded that even i f competi- tion does occur among closely-related species, this is not the main cause o f niche differentiation. W e have been working for many years on an ecological system which satisfies all three o f Addicott's criteria, and therefore has the potential for competition among its component species. Fifteen species o f gall-forming aphids (Fordinae: Homoptera, Pemphigidae) colonize three species o f Pistacia (Anacardiaceae) in Israel (Koach and Wool 1977). Only one species occurs on P. lentiscus, but P. atlantica and P. palaestina each has a distinct "guild" o f several aphid species forming galls on it. These gallers are taxonomically related (some are congeneric, all belong to the same subfamily Fordinae) and have similar life cycles (Wool 1984). All o f them attack newly unfolding leaves on their primary hosts and feed on phloem sap. Two or more species may co-exist on the same shoot, leaf or even leaflet within the same individual tree. Co-existence may be facilitated by resource separation on some dimension o f the species' niche, which could have occurred during the phylogenetic history o f the species. However, we wanted to find out whether presentday distribution on the host plant is affected by presentday competitive interactions between species pairs. In this study we investigated the spatial distribution o f galls on the host trees and examined the possibility o f interference competition for galling sites. (The possibility o f resource exploitation competition for phloem sap (see in Dixon 198.5) is discussed elsewhere (Burstein et al. 1994, Inbar et al. 1995). W e examined the distribution o f pairs o f species at three hierarchial levels: shoots within trees, leaves within shoots, and leaflets within leaves, and calculated niche breadth ( B ) for each species when alone and when co-habiting with another. Competition will be indicated i f B o f at least one species is smaller when co-habiting than when alone. At the lowest level o f the hierarchy, competition would be indicated i f two species occurred on the same leaflet less frequently than expected by chance. Interference competition may be affected by. aggres-sive interactions among colonizing individuals. Intra-specific aggressive territorial behavior was reported in galling aphids (Whitham 1978, Aoki & Makino 1982), but such data have not been published on the Fordinae. Materials and methods Rationale There can be no competition for space (galling sites) unless the niches o f potential competitors overlap at least partly. Therefore our sampling o f units for study was not random: at each stage we deliberately searched for units where both species occur. The choice o f units in the habitat was o f some concern. In the galling Fordinae, a meaningful habitat unit could be a shoot, a leaf,or even a leaflet within the same leaf. W e did not include the entire tree as the highest level in the hierarchy, because occu- Table 1. List of common Fordinae species on Pistaciapalaestina and P. atlantica in this study (rare species mentioned in Koach and Wool (1977) are omitted). Host species Aphid species Galling site on shoot P. arianrica Smpnthurodes betae West. Fordu riccobonii (Stephani) Forda sp. B Geoica spp. " Slavun~werrheimae HRL Forda formicaria von Heyden Forda murginaru Koch Puru~,letu.rcin?iciformi.r von Heyden Geoicri spp. Bai:on~irr pistczciae L. leaflet margin leaflet margin leaflet margln leaflet midrib axillary bud P. palaestincr leaflet margin leaflet margin leaflet margin leaflet midrib apical bud No. gall types in life cycle Total no. galls on sampled shoots 2 2 1 1 1 :Weferred to as G. utric,uloriu in Koach and Wool 1977. Now known to be a complex of several taxa. LEAFLET F1 pancy of a tree by one or more species is probably determined by factors other than competition (e.g. colonization rates of different species, distance from secondary hosts etc.). Rather than argue which is the best unit to use. we decided to study then1 all in hierarchic order. In one case we studied competition at a still lower level: galling sites within a leaflet (see below). Trees Pistacia palaestina and P. atlaiztica are important components of the natural forest in Israel. The former is common in northern and central forests in the country. The latter has a wider distribution from Iran to the Canary Islands (Zohary 1952) and in Israel it partly overlaps with P. palaestirta but is found also in desert habitats. The study was carried out in the spring and summer of 1991 and 1992. A supplementary study was done in 1993 at one site. We examined over 200 naturally growing trees in search of some that were colonized by more than one species of gallers at high enough frequencies to provide useful data. Since there are 5 common species of gallers on each of the two host species (Table l ) , we tried to find trees with all combinations of the gallers. Suitable trees of P. palaestina were selected at 3 sites. P. atlantica were selected at 5 sites, one (CP) in common with P. palaestina. In all. 26 P, palaestina and 13 P. atlarzticu trees were used. The numbers of trees for each "competing" pair were unequal: some trees provided data for more than one galler pair while others gave data for one comparison and not for others. Data of all trees were used regardless of location. Fig. 1 . Galling sites of common Fordinae on Pistacia paluestina (top) and P. atlantica (bottom). Species names are abbreviated: Bp = Baiiongia pisruciae: G = Geoica sp.; Ff = Forda fornticaria;Fm = Forda marginata; PC = Paraclet~lscinriciformis; Sw = Slavum wertheimae; Sb = Smynthurodes berue; Fr = Forda riccobonii; FspB = Forda sp. B; F, = "temporary" galls. (Drawing by W. Ferguson). Shoots and leaves On each suitable tree, we examined many shoots (all galls are formed on new shoots of the same year) and sampled only shoots carrying at least one gall of any species. We considered only major shoots and disregarded short, lateral shoots produced later in ihe season. The location and numbers of galls on the shoot were recorded (the oldest. basal leaf was labeled 1) for all species present. Table 2. Total numbers of galls on 12 dwarf (< 50 cm tall) P. palaestinu trees and the distribution of the galls of the same species on two non-dwarf trees at the same site (CP). Species F. murginafa F. formicaria B . pistuciae Geoicu spp. P. ci~nicfirrnis Dwarf trees (n= 12) >1000 0 12 2 0 Normal-size trees (n=2) less than 1 m 1 4 m above above ground ground 450 0 16 6 18 2 147 39 30 53 G test of independence: G = 786.21*** (4 df) In October 1993 we sampled shoots from 18 P. palaestina trees at Canada Park (CP). Two species - Geoicu spp. and Fordu forrnicaria - were very abundant on these trees. We 1) randomly chose 10 shoots per tree to get an estimate of the proportion canying at least one gall; 2) \ampled 5 galled shoots per tree and recorded the location and numbers of galls of the 2 species on the leaves along the shoot. Taken together, the sampled shoots carried very large numbers of galls (Table 1). The leaves of pistar& are pennate (Fig. 1). For some of the species we examined each leaflet on galled leaves as a unit, and recorded the cases where more than one fpecies occupied the same leaflet, and whether the species' galls were on the same side or opposite sides of the leaflet midrib. within leaves and treated similarly. Means + SE are given in the tables below. Since B may not be a normally distributed character, non-parametric tests (Sokal and Rohlf 1981) were used in comparisons among means. Regression analysis was used to test for linear dependence of B on density, and Chi-square tests for comparing frequencies. Results Niche separation at the tree level Only 39 of more than 200 trees surveyed were colonized by more than one species at densities suitable for analysis. This shows that niche separation at the tree level may be common. However, as explained in the Methods section, colonization of trees is likely to result from factors other than competition, and this level was not included in the analysis. Two particular examples deserve notice. Forda marginata on P. palaestinu does not compete with other species. It is sometimes quite common in natural forests, and when it occurs it does so at very high densities of several galls per leaflet, but our investigation sun 50 shade r Calc~llations As measures of the potential for competition among the galler species, we calculated two parameters. For each species, niche breadth, B (Levin's formula; Price 1984a) is where P,? is the proportion of galls on leaf i, and S is the number of leaves on the shoot (or leaflet on a leaf) = the number of available units in the habitat. B was calculated separately for units occupied by a species when alone and when co-existing with another species. For each pair of species we calculated proportional .~imihrity(PS) in habitat occupation (Price 1984: 395) where P,kand P,, are the proportions of species i and j on resource unit k. PS ranges between 0 (no overlap) and 1 (complete overlap). Both formulas were used in ecological studies on aphids (e.g., Hajek and Dahlsten 1986). Statistical analysis Because the numbers of habitat units (leaves) were different from one shoot to another, B and PS were calculated separately for every shoot. Leaflets were used as units 112 Fig. 2. Distribution of Sb and Fr on shoots of old P. atlantico trees. While Sb is more abundant on sunny parts of the canopy, Fr occurs more frequently in the shade. Top: frequency of shoots galled by F, (fundatrices) and F2of the two species on sunny and shady shoots. Bottom: average gall abundance. For statistical analysis see text. OIKOS 73:l (1995) 1 2 3 4 5 6 7 8 9 1 0 1 1 1 2 Leaf position Fig. 3. Distribution of galls along the shoot (pooled from many shoots) on P. palaestina. Note the niche overlap between F,, G and PC galls, and the niche separation between these species and Ff (F, here are the "temporary" galls of Ff; see text). Species names as in Fig. 1. shows that it attacks especially trees which remain small - less than I m tall - as a result of browsing, cutting or other disturbances. This species is almost the sole occupant of dwarf trees. At one site (CP), 12 dwarf and two normal-sized trees were colonized by F. marginata, facilitating a comparison of its gall distribution on the two types of trees (Table 2). When it does (rarely) occur on normal-sized trees, its galls are found on low branches, less than 1 m above ground, where few other galls occur (Table 2). Final galls of F. marginata tend to appear later than other species (Inbar, unpubl.) which may mean temporal separation from potential competitors. On P. atlantica, Srnynthurodes betae and Forda riccobonii had the highest PS of all species (see below). We noticed at two sites, where the host trees were probably > 100 yr old and very large, that the two species tended to occupy different sectors of the canopy. An example from one tree is illustrated in Fig. 2. F, (fundatrix) and F2 1 2 3 4 5 6 7 8 91011121314 leaf position Fig. 4. Distribution of galls along the shoot axis on P. atlantica (pooled from many shoots). Note that FspB and F, overlap, while Sb is distributed on more distal leaves. (F, here are the "temporary" galls of Sb (see text). Species names as in Fig. 1. 8 OIKOS 73.1 (19951 (final) galls are compared separately, using two measures of abundance: the frequency of galled shoots and the average numbers of galls per shoot of each species. S. betae tended to be more frequent in the more distal, sun-exposed canopy, while F. riccobonii was more frequent on shaded shoots within the canopy. The differences in frequencies of the two species on sunny and shady shoots were highly significant both in F , (X2= 15.97, I df) and in F2 (X2=33.41, 1 df; both p < 0.001). The differences in gall abundance, illustrated in Fig. 2, were also significant except F, in the sun (t tests after square-root transformation, p<0.01 at least). We could not detect a similar niche separation within younger, smaller trees, nor in other species. Niche separation at the shoot level It very quickly became clear that some of the common galler species which co-exist on an individual tree, nevertheless cannot compete for galling sites with any others because they occupy a unique position on the shoot (Fig. 1). On P. palaestina, ~ a i z o n ~pistaciae ia alone forms ~ t s large, horn-shaped galls on apical buds (Wertheim 1954). On P. atlanticu, only Slavum wertheinzae occupies leaf primordia in closed, resting axillary buds forming "cauliflower"-shaped galls (Wertheim and Linder 196 l). All of the remaining species occupy leaflets. Geoica sp. forms spherical galls on leaflet midribs, the other species colonize leaflet margins. Some of the species considered here have an extra galling stage in their life cycle (Table 1). The fundatrix F, induces a small gall, in which it matures and reproduces ("temporary gall". Wertheim 1954, Bodenheimer and Swirski 1957). Her offspring (the F2) disperse to other leaves and induce the final galls (e.g., Wool and Burstein 1991). The F, galls usually do not co-occur with F2 on the same leaves (Figs 3, 4) because there is a time delay between the two stages. during which the F, aphids mature. This leaves us with a reduced matrix of species which may be likely to compete. Although shoots with pairs of species were reasonably frequent, shoots carrying three or more were quite rare. Single galls of a third species sometimes occurred on a shoot, but only rarely were three species found at densities that provide meaningful calculations of multispecies co-occurrence. In the following, we examined pairs of species. Proportional similarity (PSI Calculations of PS for species pairs on P. atlanticu and P. pulaestina are listed in Tables 3 and 4, respectively. The numbers of trees listed in Tables 3 and 4 do not add up to the total mentioned in the Methods, since more than one species pair was studied on some trees, and the same trees were thus listed in more than one comparison. Note: For brevity. we often refer to the species by their initial letters. For full names consult the captions to Tables 3 and 4. Table 3. Proportional similarity (PS) between pairs of species on Pistacia atlantica. Abbreviations: Sb - Smynthurodes betae. FspB - Forda sp. B. G - Geoica spp. Fr - Forda riccobonii. F, - "Temporary" galls (of either Fr or Sb). Above diagonal: sample sizes (no. of shootsino. of trees). Below diagonal: mean PS rt SE. All means except Fr-F, are significantly different from zero (t tests, p < 0.05 at least). Sb Sb FspB Fr G 0.007a.002 0.429Hl.045 0.078rt0.012 0.02 1k0.006 FI FspB Fr G F, 3512 175110 4512 - - - - - 2112 - 0.267kO ,064 0.088k0.006 12115 3212 1511 2411 0.353rt0.05 1 0.390?0.048 Pistacia atlantica. PS data for species pairs on this host are listed in Table 3. About half of the galled shoots, randomly selected from trees colonized by both species of a pair, carried galls of only one of the species. Even in shoots colonized by both species, quite often they did not occupy the same leaves, resulting in PS = O (data not shown). The proportion of such cases varied from 94.3% for Sb-FspB to only 4.6% for Sb-Fr, reflecting basic differences in the biology of the species (see Discussion). This variation is also reflected in the PS values. The highest mean PS is for the pair Sb-Fr, indicating that they are often found on the same leaves and thus likely to compete (Table 3). This pair was analyzed in more detail (see below). Other pairs with relatively high PS are G-F,, FspB-F, and G-Fr, contrasting with the very low similarity of Sb-F,, Fr-F,, Sb-G and Sb-FspB. Most of these differences relate to the time delay in colonization (see Discussion). Pistacia yalaestina. A summary of the PS data among species pairs on P. palaestina is given in Table 4. Again, in random samples of galled shoots from trees colonized by both species of a pair, about half the shoots carried one or the other (data not shown). The proportional similarity among species on this host were lower than on P. atlantica. The highest values (still. less than 0.2) were between Ff-G, G-F, and PC-F,; as expected, Ff-F, similarity was very low. Table 4. Proportional similarity (PS) between pairs of species on Pistacia yaiaest~na. Abbreviations: Ff - Forda formicaria. PC - Puracletus cirn- iciformls,G - ~~~i~~sD,,, F, - "TemDorarvW o f ~ f~b~~~ , diagonal: sample sizes ?no. of shootsino. df tGes). Below diagonal: mean PS + SE. All means except G-F, are significantly different from zero (t tests, p < 0.05 at least). Ff Ff G PC Fl G 91125 0.198+0.041 0.085k0.026 0.147k0.031 0.010M.002 0.192a.083 PC FI 8 116 4616 - 1813 1112 2213 0.191+0.042 - - - Niche breadth Estimates of B when a species is alone and when sharing a shoot (Table 5) varied. Wilcoxon two-sample tests (Sokal and Rohlf 1981) were performed for each tree separately, and often showed significant differences between the two values (15 of 24 tests for P. pulaestina species, 8 of 18 for pairs of species on P. atlantica - at p<0.05 (individual tests not shown). However, when there was a significant difference, B when co-existing was frequently somewhat larger than B when the species is alone. To illustrate this point, we pooled B values from all trees for each pair of species. Eleven of 14 comparisons showed this trend (Table 5 ) . This is contrary to what would be expected from competition (see Discussion). The probability of getting three negative signs in 14 comparisons (one-tailed sign test) is 0.0278. We suspected that B and PS should be affected by gall density. Gall density per galled shoot varied greatly (from 1 to close to 100). To examine the possibility, we used the 1993 sample of 90 galled shoots from P. palaestiizu at one site (CP). Two species (G and Ff) were present at high densities. Of the 90 shoots, 29 carried only G. 23 only Ff, and 38 carried both. We regressed the calculated B for these shoots on gall density (Fig. 5). There was a clear and significant tendency of niche breadth of G to increase with density (r2=0.55). The pattern for Ff was similar. although not as clear (r2= 0.1 1). When B increases. in one or more species, there is an increasing chance of overlap when 2 species coexist on the same shoot. Niche separation at the leaf level We may look at a pennate leaf of Pistacia as a habitat, divided into 5-12 leaflets (habitat units) and calculate B for each pair of species, when alone and when co-habiting a leaf. This can be done for species which are frequent enough to be co-habiting on a sufficient number of leaves. Two pairs of species were suitable: Sb-Fr on P. atlantica and G - ~ fon P. palaestina. The numbers of co-habited leaves on any- given tree were small. but when pooled from all trees reasonable samples were obtained (Table 6). At the leaf level, proportional similarity for Sb-Fr as well as for G-Ff, was quite low. Comparisons of niche Table 5. Niche breadth (B) of galling species of Fordinae when alone on a shoot, and when co-existing on a shoot with another species. Abbreviations as in Tables 3 and 4. In 11 of 14 comparisons. co-existing species show a larger B than when alone (sign test; P < 0.05). Species B when alone Co-existing with B when co-existing Sign of the difference S FspB Fr G Sb G Fr Sb FspB Sb Sb Sb Fr Fr G G P. palaestina Ff , 1 loo breadth when the species were separated (on different leaves) or together on the same leaf showed the same tendency as at the shoot level: B tended to be slightly higher in co-habited leaves (Table 6). Regression of B on density for the former two species gave significant positive slopes ( r 2 = 0 . 8 4 and 0.76 for S b and Fr respectively), the same response as at the shoot level. values of r2 for the other species pair are r2= 0.54 and r2= 0.67 for G and Ff respectively. Interactions among species sharing the same leaflet within leaves 1 0.00 0.00 3 +, 0.50 1.00 ,,,, 1.50 Some species pairs occur on the same leaflets: on P. atlnntica, this happens quite often with the pair Sb-Fr, especially at high densities. Less often the pairs G-Sb o r Gall density log ( x + 11 - Table 6. Proportional similarity (PS) and niche breadth (B) for two pairs of species at the leaf level. Means and standard errors Smynthurodes betae and Forda riccobonii on P. arlantica. (306 leaves colonized by at least one species) 0501 = z + I I + 1 PS = 0.154 1 Niche breadth (B): I i 0.0266 (n = 157 leaves wlth both ~ p e c ~ e s ) alone co-inhabiting 0.25 - Sb: Fr: 0.257+0.0350 (23) 0.300H.0279 (157) 0.402?0.0418 (126) 0.495i0.0398 (157) I 0.00 0.50 1.00 1.50 2,00 Gall density log ( x + 1 ) Fig. 5. Relationship of niche breadth (B) and gall density for 2 species on shoots of P. palaestina. 1993. Top: Geoica, bottom: F. formicaria. Density is log-transformed. The regression statistics are as follows: Ff, b=0.107 i 0.039, n=61, p<0.001, r2=0.11; G, b=0.302 ? 0.034, n=67, p<0.001, r2=0.55. Geoicu sp. and Forda formicaria on P. palaestina. (217 leaves colonized by at least one species) PS = 0.192 ? 0.0494 (n = 98 leaves with both species) ~ i breadth ~ (B): h ~ G: ~ f : alone co-inhabiting 0.148k0.0189 (50) 0.310i0.0445 (69) 0.173i0.0215 (98) 0.324k0.0392 (98) Table 7. Occurrence of Smynthurodes betae and Forda riccobonii on the same leaflets within leaves. On leaves containing galls of both species (174 leaves): number of leaflets with: Sb Fr Both Neither Total alone alone Observed 212 463 116 322 (proportion) 0.19 0.41 0.10 0.28 Expected from random assortment 157.37 408.36 170.63 376.64 Sign of diff. + + (obs-exp) 1113 G-Fr may occur. On P. palaestina it is mostly G-F6 pairs of Ff-PC or G-PC have not been recorded in the sampled shoots, although they do occur in the field. Interactions between G and Ff, or G and Sb, cannot involve interference competition for galling sites because they require different sites for galling (Fig. 1). However, Sb-Fr may, indeed, compete when they meet on the same leaflet margin. Further examination of the interaction of Sb-Fr: leaflets within leaves To determine the likelihood of competition we studied the Sb-Fr interaction on P. atlantica in detail in a sample of 11 13 leaflets from leaves with both species (Table 7). This time we detected deleterious interactions: there was a significant excess of cases of each species galling a different leaflet, and a corresponding deficiency of cases with both species on the same leaflet, than expected. We also observed that when both species are on the same side of the leaflet, Sb tends to occupy the site nearest the petiole, and Fr further distally (Table 8), whether or not the other species is present. Discussion In all stages of the study we made a deliberate effort to find situations in which competition is likely. We selected trees carrying many galls of more than one species; within trees, we selected shoots and within shoots, only leaves carrying galls of more than one species. Despite this deliberate bias for competition, our study detected rather limited niche overlap between pairs of species. Some species have unique niches which do not overlap with others. Even co-existing species which occupy the same shoot, induce most of their galls on different leaves with no overlap with other species. Those species that co-exist on the same leaf, often occupy different leaflets. Only when they meet on the same leaflet, do we find indications of negative interactions between two species, Smynthurodes betae and Forda riccobonii. Based on early theoretical work in mathematical ecology, resource partitioning has often been considered as a mechanism for escape from interspecific competition (review in Schoener 1974). Our results suggest that at present most species do not compete for galling sites. The Fordinae on Pistacia appear to be an excellent example of resource partitioning at least as regards galling sites (Fig. 1). Resource partitioning was described for other specialist, gall-fonning insects by Akimoto (1988), Askew (1984) and Price (1992). Resource partitioning at different hierarchical levels of habitat organization The resource partitioning observed among our galling species can stem from different causes at different levels of the habitat. If entire trees are taken as units, the presence of each species may depend on local (geographical or other) differences in abundance (perhaps absence of some species at some localities). For example, when searching for galled trees in the Galilee (Mt Meiron) in 1992, we often observed large numbers of Forda formicuria galls, but found almost no galls of Geoica, which often co-exists with it at other sites. When the frequency of occurrence of any species on individual trees is very low, competition between two species is unlikely (e.g. Kozar 1987). Therefore, we selected only trees with large numbers of two or more species. Niche separation may occur even within the canopy of the same trees, as illustrated in Fig. 2. When the habitat unit is a shoot, on trees colonized by both species, their presence together may be affected by timing of the gall induction (Burstein and Wool 1993). Like all galling species of insects (Weis et al. 1988). the Fordinae exploit exclusively young, growing parts of the plant (unfolding and expanding leaves). These are available in the right stage for colonization for only a short time (ephemeral resources). The shoot axis represents a time scale for aphid colonization (Burstein and Wool 1993). In order for two galling species to share a leaf, they must arrive approximately at the same time window which may be open no more than a few days. This factor is certainly the reason for the low PS between final and F, galls of Ff and Sb (Tables 3, 4): there is about a 2-week delay between the two galls (generations) during which time the shoots elongate. In our system, four species have Table 8. Microsite differences in position of Sb and Fr galls when on the same leaflet. (Numbers of galls of each species in a sample of leaflets carrying at least one gall). G tests of independence were used (Sokal and Rohlf 1981). Colonizers per leaflet: Basal comer of leaflet Distal part of leaflet Total Sb alone Sb coexisting 186 (85%) 50 (88%) 34 (15%) 7 (12%) Fr alone Fr coexisting 19 (5.6%) 7 (12%) 320 (94%) 50 (88%) 220 57 G = 0.376 ns 339 57 G = 2.991 ns this extra life-cycle complexity (Table 1): Forda formicaria, F, riccobonii, F. marginata and S. betae. Wertheim (1954) thought that Paracletus cimiciformis also has a "temporary" gall, and we assumed earlier that so does FspB. We know now that these species form only one type of gall. as do the species (probably more than one) which we only identified as Geoica sp. The one-gall species coincide temporally with the F, of the 2-gall formers, and thus are likely to be found on the same leaves, as indicated by the PS values in Tables 3 and 4, while the final galls of the latter are found on more distal leaves along the shoot (Figs 3, 4). We suggested (Wool and Burstein 1991) that the F, galls of S . betae may represent the primitive life cycle of that species (a proportion of these "temporary" galls are not deserted and all aphid generations develop in them as in final galls). If this was the case, then by evolving to form a second (F,) gall in their life cycle, these species may, in fact, have escaped competition with the singlegall formers! The only indication of competition was found at the leaflet level on leaves occupied by Sb and Fr; the two species tended to be found on different leaflets more often. and on the same leaflets significantly less often than expected from random distribution based on their frequencies in the sample (Table 8). This is corroborated by videotaped unpublished observations of fundatrix behavior of the two species in the laboratory (M. Inbar unpubl.): the F2 fundatrix nymph of Sb is much bigger and more sclerotized than Fr, and when the latter ventures onto a site occupied by the former, it is inimediately evicted (since there are many unoccupied niches, the loser probably finds an unoccupied leaflet to gall). Similar behavioral evidence for territorial defense in intraspecific interactions was reported by Whitham (1978, 1979) and Aoki and Makino (1982) in other species of galling aphids. Competition and gall density Interspecific interference competition should become more likely as gall density increases; but what level of density is high enough to have an effect is difficult to know. One reviewer suggested to us that interference competition should function to reduce the chance of exploitation competition among species. Therefore a minimum estimate of "high density" should be the point where exploitation competition begins to have a negative effect on fitness. Exploitation competition in galling aphids is difficult to measure, because their resources are the photosynthetic assimilants flowing in the phloem. We have shown (Burstein et al. 1994) that the galls are "sinks" for assimilants and that species vary in their ability to divert these products by their relative "sink" strength (Inbar et al. 1995). The effect of gall density on this variable awaits further study. The fact that we detected no evidence for competition is not due to high levels of parasitism or predation reducing population size (data not shown). It is more likely due OIKOS 73.1 (1995) to the pattern of gall distribution. At all levels within trees (shoots, leaves or leaflets), the distribution of galls is clumped. Therefore, there are plenty of empty niches available for gall induction, as suggested for specialists in general by Price (1984b). In almost all shoots, even those colonized by many galls, many of the leaves carried no galls. On the galled leaves, many leaflets were free of galls. Even on galled leaflets, there was room for additional galls. For example, it is physically possible for 4 galls of F.formicaria to occur on one leaflet of P. palaestina. At Canada Park in 1993, in a sample of 951 leaves, there was one leaf (12 leaflets) with 44 galls of that species, and one with 41, but the median number was far lower (less than 2). The factor here would appear to be timing and density of fundatrices: at the time of gall formation, the simultaneous appearance of many fundatrices of both species on the same habitat unit seems rare, since many more such units are available on the tree than can be colonized. Only very rarely do we find the habitat saturated with galls. Competition and niche breadth The absence of interspecific competition is further indicated by the fact that our estimates of niche breadth at the shoot and leaf levels are very similar whether a species is located alone on the shoot or shares it with another species (Table 5). Competition should cause a shift towards a narrower niche in the latter case: at least one of the competitors should be negatively affected. What we actually find is, that if there is a significant difference between the two estimates. B is wider when the species co-exist with another. The reason, in our opinion, is that when densities are higher, the galls of each species are found on more leaves (B larger). This also increases the chance of niche overlap. When we consider the leaf level, the temporal factor may not be as important: since leaves are only available for galling for a short time and all leaflets expand within that short period, location of galls on the same leaf indicates (almost) simultaneous arrival. This is where interference competition may be effective. and it is at this level that the effect of gall density should be more pronounced. However niche breadth gave no evidence for interference competition even at that level: niche breadth of no species became smaller when they co-habited the same leaves. Why B should be higher on shared shoots or leaves is not entirely clear. As we have shown, B increased with density. We used data from the G-Ff species pair in CP to test some possible explanations (data not shown in detail). We found that gall density of either species was not higher on shared than on singly occupied shoots (actually the means were lower on shared shoots, although not significantly so). 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