Download Phloem-feeding specialists sharing a host tree: resource partitioning

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). Moreoever, densities of the two species
on the shared shoots were not positively correlated (a
low, non-significant negative correlation was observed),
showing that the change in B is not due to some properties of habitat quality to which both species respond. For
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