Oecologia
9 Springer-Verlag1989
Oecologia (1989) 79:15-22
Variation in selection pressures on the goldenrod gall fly
and the competitive interactions of its natural enemies
Warren G. Abrahamson, Joan F. Satfler, Kenneth D. MeCrea, and Arthur E. Weis*
Department of Biology, Bucknell University, Lewisburg, PA 17837, USA
Summary. Larvae of the tephritid fly Eurosta solidaginis
induce ball-shaped galls on the stem of tall goldenrod, Solidago altissima. Survival probability depends on gall size;
in small galls the larva is vulnerable to parasitoid oviposition, whereas larvae in large galls are more frequently eaten
by avian predators. Fly populations from 20 natural old
fields in central Pennsylvania were monitored in 1983 and
1984 to examine the distribution of the selection intensity
imposed by natural enemies, the parasitoids Eurytoma gigantea and E. obtusiventris, the inquiline Mordellistena unicolor, and the predatory birds Dendrocopus pubescens and
Parus atricapillus. Mordellistena and E. obtusiventris are
able to attack galls of all diameters while E. gigantea and
the predatory birds preferentially assaulted small and large
diameter galls, respectively. Eurosta in intermediate sized
galls had the highest survivorship, hence selection had a
stabilizing component. However, parasitoid attack was
more frequent than bird attack, and the two did not exactly
balance, thus there was also a directional component. The
mean directional selection intensity on gall size was 0.21
standard deviations of the mean, indicating that larger gall
size was favored. Interactions among the insect members
of the Eurosta natural enemy guild are complex and frequent.
Key words: Bird predation - Eurosta solidaginis - Parasit o i d s - Selection pressures - Solidago altissima
Herbivore populations typically sustain heavy attack from
intricate arrays of natural enemies (Bergrnan and Tingey
1979; Price etal. 1980). Gallmakers, for example, frequently support complex guilds of parasitoid wasps (Varley
1947; Askew 1961 : Price and Clancy 1986) and avian predators (Spofford 1977; Schlichter 1978; Confer and Paicos
1985). Although many studies have described the interactions of natural enemy guilds with their gallmakers, we
know of no studies, except those of Weis and Abrahamson
(1986) and Price and Clancy (1986), that have measured
the selection intensities on gallmakers that are created by
these enemies. The study reported here provides such selection information for 20 old fields in central Pennsylvania.
* Current address: Department of Biological Sciences, Northern
Illinois University, DeKalb, IL 60115, USA
Offprint requests to: W.G. Abrahamson
The natural enemies of a gallmaker clearly influence
the survival of individual gallmakers. If survivorship varies
among gallmakers with different traits, natural enemy attack can potentially alter gallmaker traits in subsequent
generations. The relationships of E. solidaginis with its natural enemies have been described in a number of studies
(e.g., Fitch 1855; Harrington 1895; Beck 1947; Uhler 1951;
Judd 1953; Stinner and Abrahamson 1979; Abrahamson
et al. 1983), however, none of these efforts determined the
selection pressures these enemies create. The study reported
here expands on these earlier works by (1) measuring the
selection pressures on gall size that are caused by natural
enemy attack and (2) examining the potential for competitive interactions among the guild of insect natural enemies.
The probability of E. solidaginis survival depends on
gall size since at least some of the gallmaker's natural enemies differentially attack galls of various sizes (Milne 1940;
Miller 1959; Uhler 1961; Cane and Kurczewski 1976; Weis
and Abrahamson 1986). Gallmakers in small galls have
been shown to be more vulnerable to oviposition by the
parasitoid wasp E. gigantea (Weis and Abrahamson 1985;
Weis et al. 1985) and large galls are more frequently attacked by downy woodpeckers and black-capped chickadees (Confer and Paicos 1985; Weis and Abrahamson
1986). While Abrahamson et al. (1983) studied the insect
natural enemy guild as a whole and reported its impact
on gallmaker survival, the present study examines the impacts of the individual species comprising the guild (both
insect and avian) and measures the selection pressure each
exerts on the gallmaker.
Although the gall is plant tissue, aspects of the gall phenotype are likely influenced by the insect. A genetically
coded stimulus from the insect induces the development
of a gall from normal tissue (Weis and Abrahamson 1986;
Abrahamson and Weis 1987; Carango et al. 1988). Since
some of the gallmaker's natural enemies differentially attack galls of various diameters, the natural enemies should
exert selection pressure on the gallmaker that could influence the evolution of the gallmaker's contribution to gall
diameter (Weis and Abrahamson 1985). We have determined Eurosta mortality in relation to gall size and natural
enemy attack, and thus we are able to measure selection
intensities. Specifically, we asked the questions: (1) What
are the abundances of the gallmaker and its insect natural
enemies? (2) To what extent is Eurosta mortality caused
by insect and bird enemies? (3) Which natural enemies exhibit gall size preferences, what are these preferences, and
16
what selection pressures result?, and (4) To what extent
do the insect natural enemies compete for the gallmaker?
Natural history of the system
The univoltine gallmaking fly, Eurosta solidaginis (Fitch;
Diptera: Tephritidae) causes the tall goldenrod (Solidago
altissima L., Compositae) to develop a globose, tumor-like
stem growth. Oviposition occurs in mid- to late May in
central Pennsylvania. The gall appears about 3 wk after
oviposition and reaches full size in another 3 to 4 wk (Weis
and Abrahamson 1985). The larva enters diapause in late
September and pupates within the gall during the following
March or April (Uhler 1951).
Eurytoma obtusiventris (Gahan; Hymenoptera: Eurytomidae) is an internal parasite of Eurosta (Uhler 1951). Parasitism most likely occurs while the gallmaker eggs are hatching and the larvae are boring through the stem (Abrahamson unpubl, data). When attacked, the gallmaker forms
a premature puparium in late summer after which the parasitoid consumes the host. E. obtusiventris larvae remain inside the host's puparium throughout winter and pupate the
following spring (Weis and Abrahamson 1985).
Eurytoma gigantea (Walsh; Hymenoptera: Eurytomidae) is an external parasite that attacks Eurosta after maximum gall size has been reached (Weis and Abrahamson
1985). It consumes the gallmaker by the end of August
and remains in the central chamber of the gall to feed on
plant tissues (Uhler 1951). E. gigantea females probe galls
of all sizes but can only inject eggs when the gall wall is
thinner than the length of their ovipositor. This parasitoid
is therefore limited to smaller galls (Weis and Abrahamson
1985; Weis et al. 1985).
MordeIlistena unicolor (Lec; Coleoptera: Mordellidae)
feeds on gall tissues by chewing narrow channels through
gall parenchyma and vascular regions. Larvae, which hatch
from eggs oviposited on the gall surface in early July (Weis
and Abrahamson 1985), bore into the gall tissue by early
August. Although Mordellistena is considered an inquiline
(Uhler 1951), it usually eats the gallmaker by the end of
the growing season.
Two species of birds attack Eurosta during winter
months, the downy woodpecker, Dendrocopus pubeseens,
and the black-capped chickadee, Parus atricapillus
(Schlichter 1978). The degree of mortality caused by these
birds is highly variable from site to site and year to year
(Weis et al. unpublished data). Milne (1940), for example,
found that bird predation accounted for 44.8% of total
Eurosta mortality whereas Miller (1959) and Uhler (1961)
showed bird predation to be much less at 7% and 2.3%
of total gallmaker population, respectively.
Since the natural enemies attack the same resource but
at different times, there are predatory relationships among
them. Although E. obtusiventris attack occurs first, E. gigantea and M. unicolor larvae incidentally consume E. obtusiventris when they attack the gallmaker. Similarly, Mordellistena larvae typically consume E. gigantea larvae if the
inquilines find their way to the gall's central chamber. Predation of the parasitoids by birds has also been documented. Cane and Kurczewski (1976) found that the larvae of
E. gigantea were taken, but suggested that E. obtusiventris
might be distasteful as it was consistently avoided.
Schlichter (1978) found the Mordellistena larvae were likewise not taken by birds.
Methods
Patterns of gallmaker and enemy abundance were examined
in 20 natural old fields of varying stages of succession within a 15 km radius of Lewisburg, PA USA (40~
76 ~53' W). Analysis of gall abundance was done by systematically placing 50 (0.5 x 1 m) quadrats in an approximately
equidistant grid across each field. Fields were censused by
counting all ball galls in each quadrat between 17 August
and 29 September 1983. During the periods of 12 Nov e m b e r - l l December 1983 and 7-28 April 1984, a minimum of 97 galls were systematically collected from each
of the 20 fields. Galls from both autumn and spring collections were measured to the nearest m m by passing them
through circle stencils and then galls were dissected to determine their contents (i.e., gallmaker, parasitoid, or inquiline). Successful bird predation was recorded when beak
chisel holes penetrated to the central chamber of an empty
gall. Chisel holes to the central chamber with evidence of
Mordellistena presence were not recorded as bird success
since the MordelIistena could have consumed the gallmaker
prior to the bird's attack (unknown bird success). Galls
with chisel holes not reaching the central chamber and still
containing Eurosta or a parasitoid were recorded as unsuccessful bird predation. Evidence of an exit hole of adult
E. gigantea, Mordellistena tunnels, gallmaker death, or
empty galls was also recorded.
To determine the extent of mortality caused by each
natural enemy, percentages of surviving Eurosta, parasitoids, inquiline, and galls successfully attacked by birds
were calculated. This was done for both November and
April data based on the percentages found at dissection
after excluding galls containing dead Eurosta and empty
galls. The November data were used to determine gallmaker
and enemy occurrences before predation by birds and the
April data were compared to November data to assess natural mortality over winter and to determine bird predation
levels. Galls are primarily a winter food resource for these
birds. April data were used to assess the survival at the
end of Eurosta's annual life cycle.
The gall diameters for each content class were approximately normally distributed, but their variances were not
equal. This prohibited the use of a parametric one-way anova or multiple comparison test such as the Student-Newman-Keuls procedure. We therefore used the Kruskal-Wallis non-parametric one-way anova, and multiple Student's
t-tests using separate variance estimates, correcting to give
an experiment-wise error rate of P_< 0.05 (Sokal and Rohlf
1981).
Selection intensities on gall size exerted by natural enemy attack were calculated as the difference between the
mean gall diameter of the selected individuals and the mean
gall diameter of the entire population, divided by the population standard deviation (Falconer 1981). This index is
a measure of the magnitude and direction of a selective
pressure but not of the evolutionary response to that pressure. We will separately present the results of a five-year
study in which we measured the evolutionary responses to
selection pressures (Weis et al., unpublished work).
The standard statistical tests used to determine if a single selection intensity is different from zero, or if several
selection intensities significantly differ from one another,
are flawed when assessing mortality selection. A case in
point is the regression test based on the discovery by Price
17
Table 1. Density of ball galls based on quadrat sampling and percentages of galls (excluding empty galls and those in which no living
occupant was found, D/E) containing living Eurosta soh-daginis (Eur.), Mordellistena unicolor (Mord,), Eurytoma gigantea (E. gig.),
Eurytoma obtusiventris (E. obt.) or which were successfully attacked by birds (bird). N is the number of galls dissected
Field
BVSA
147R
Furn
Pit
147E
Marsh
Hess
Beag
Violet
MP
Ind park
Pott
Owen 1
254
147S
Aikley
Stein
Allen
Owen 2
KF
All fields
combined
Gall
density
per m 2
<0.04
0.08
0.20
0.28
0.36
0.36
0,40
0.44
0.52
0.72
0.84
1.16
1.16
1.24
1.68
1.80
2.04
2.08
3.88
4.00
N
% of galls by content in November
%
D/E
N
Excluding dead or empty galls
% of galls by content in April
%
D/E
Eur.
Mord. E. gig. E. obt. Bird.
Excluding dead or empty galls
Eur.
Mord. E. gig. E. obt. Bird
99
100
100
100
100
105
99
100
145
100
118
100
100
100
100
100
252
100
284
100
39
56
57
49
40
44
40
50
30
36
42
34
38
47
49
53
33
25
40
48
23
50
49
71
70
51
75
44
36
47
48
77
63
53
57
34
15
53
63
71
27
36
30
20
18
14
10
42
39
8
20
9
15
21
20
34
55
33
17
15
28
9
21
4
12
24
10
12
20
16
17
9
18
11
22
13
15
13
13
13
22
5
0
6
0
0
0
2
6
2
13
5
5
2
2
19
14
0
7
0
0
0
0
0
0
12
5
0
0
28
1
0
0
13
0
0
0
0
1
0
100
100
100
100
97
100
101
100
109
100
114
100
100
100
100
287
147
99
100
99
64
57
53
51
58
32
49
52
59
29
54
51
41
50
43
48
58
39
56
46
25
56
36
37
66
34
13
38
49
38
27
65
71
46
40
49
27
62
80
77
28
26
30
14
15
9
6
33
16
21
25
20
12
22
14
23
31
20
9
11
22
9
32
18
20
7
13
21
24
7
15
12
15
8
5
15
23
8
7
8
25
2
0
0
0
0
4
8
9
0
12
0
2
2
0
13
18
3
5
0
0
7
2
31
0
50
63
0
2
34
21
2
0
22
40
1
2
7
0
4
2402
42
50
26
15
6
3
2253
50
47
19
14
6
15
(1970) that the regression coefficient or relative fitness over
phenotypic score was algebraically equivalent to the selection intensity. However, when a fitness c o m p o n e n t with
binary values (i.e., survived vs. died) is used, the basic assumption of a normally distributed dependent variable is
violated and test results invalid. Endler (1987) offered a
modified two sample t-test to determine if the difference
between the m e a n phenotype of the entire p o p u l a t i o n differed from the m e a n phenotype of the selected subset of
the population. W h e n applied to longitudinal studies such
as our's, it violates the assumption of independence of the
two samples because the selected individuals are included
in both samples. This gives the test a conservative bias (i.e.,
real selection will too often go undetected). F o r these reasons we estimated confidence limits on the selection intensities measured in each of the 20 populations by a bootstrapping routine.
Bootstrapping is a technique used to derive the error
distribution of a statistic by intensive resampling of an empirical data set (Effort 1981). A computer p r o g r a m is used
to draw a " s a m p l e " of observations, with replacement,
from the data set and then compute the desired statistic.
W h e n repeated m a n y times, this procedure yields a distribution of values for the statistic, from which confidence intervals can be derived. I n this study a single data set consisted
of the trivariate distribution of gall diameter (in ram), survival from parasite attack (valued as 0 or 1) and survival
from bird attack (also valued as 0 or 1) for one of the
fields. One t h o u s a n d " s a m p l e s " were drawn from this distribution, a n d the selection intensity for the parasite and
bird episodes of selection, as well as total directional selec-
tion, were calculated for each " s a m p l e . " We considered
the 95% confidence interval to extend from the 2.5th to
the 97.5th percentile of the distribution of the intensities
from the 1000 " s a m p l e s . " The whole procedure was repeated for each of the 20 populations. A n observed selection intensity was considered significant if its lower confidence limit was greater than zero, and two selection intensities were considered significantly different if their 95% confidence intervals did not overlap.
Results
Gallmaker mortality sources
The density of Eurosta galls and the attack rate of each
natural enemy were highly variable from field to field for
both the November and April collections (Table 1). I n November, 29.3% of all galls (i.e., n o t excluding dead or empty
galls) contained surviving Eurosta as compared to only
23.6% in April. This difference was significant (X2= 19.30,
P < 0 . 0 0 1 ) and was primarily due to winter exploitation of
galls by birds. After exclusion of dead or empty galls, galls
containing Eurosta larvae accounted for as few as 15%
to as m a n y as 77% of the remaining galls in the N o v e m b e r
sample and as few as 13% to as m a n y as 80% in the April
sample. Eurosta mortality resulting from successful bird attacks was only 1.5% of all galls in N o v e m b e r but increased
to 7.2% by April (X2=91.74, P < 0 . 0 0 1 ) . Excluding dead
or empty galls, successful bird attacks accounted for 3%
of the mortality in N o v e m b e r and 15% by April.
18
Table 2. Results of a Kruskal-Wallis non-parametric one-way anova for mean gall diameter by field for all galls and each content;
and results of a one-way anova on gall diameter by content (twenty fields combined) at two sampling times. All analyses exclude
empty galls and those in which no living occupant was found. Those means followed by the same letter are not significantly different
from one another at P = 0.05 (see methods for details of analysis)
November
April
d.f.
H
Sig. of H
d.f.
H
Sig. of H
Kruskal-Wallis one-way anova gall diameter by field for:
all galls
Eurosta solidaginis
Mordellistena unieolor
Eurytorna gigantea
Eurytoma obtusiventris
Bird attacked galls
19
19
19
19
13
5
146.0
121.4
63.8
31.5
23.3
6.1
< 0.001
< 0.001
< 0.001
0.036
0.039
NS
19
19
19
19
11
14
178.9
93.7
32.9
44.3
25.3
56.5
< 0.001
< 0.001
0.024
<0.001
0.008
<0.001
Kruskal-Wallis one-way anova diameter by :
Content
4
303.0
< 0.001
4
235.7
< 0.001
Mean gall diameters (ram +_std. dev.)
Eurytoma gigantea
Mordellistena unicolor
Eurosta solidaginis
Eurytoma obtusiventris
Bird attacked galls
17.81_+2.78 a
19.81 _+3.52 b
21.63 _ 2.32 c
21.80 _+2.40 c
22.62 _+1.88 c
GalImaker mortality as influenced by gall size
Eurytoma gigantea was restricted to galls of a particular
size range while the other insect enemies were not. This
conclusion results from a one-way anova, performed on
the November data set for gall diameters by gall content,
that showed that the diameters of galls with surviving Eurosta, M. unicolor, and E. obtusiventris varied significantly
among the fields while the diameters of E. gigantea attacked
galls did not.
In order to determine the relationships between natural
enemies and gall sizes, we used the multiple comparison
procedure on the November data to separate galls by contents into three significantly different subsets of gall diameter. Subset 1 consisted of galls containing E. gigantea (2"=
17.81 mm); subset 2 consisted of galls containing Mordellistena (2"= 19.81 mm); subset 3 consisted of galls including
both surviving Eurosta ( X = 21.63 mm) and E. obtusiventris
(2"= 21.80 mm). These results indicate that attack by some
natural enemies is gall size specific. Student's t-tests comparing the mean gall diameters of the surviving gallmakers,
parasitoids, and the inquilines with the mean gall diameter
of the remainder of the population (all 20 fields combined)
showed that the diameters of galls containing surviving Eurosta and E. obtusiventris were significantly larger than the
galls not containing the respective insect (t=12.99, P <
0.001; t=4.66, P < 0 . 0 0 1 , respectively); even though E. obtusiventris can attack galls of all diameters. Galls containing
E. gigantea and MordeIlistena were significantly smaller
than galls not containing the respective insect (t=15.48,
P < 0.001 ; t = 5.36, P < 0.001, respectively); even though
Mordellistena can attack galls of all diameters.
Birds preferentially attacked larger galls where the probability of finding the gallmaker larva was highest. The density of galls successfully attacked by birds was positively
correlated with the population mean gall diameter ( r =
0.448, P = 0.025) indicating that levels of bird attack were
17.25 + 2.73 a
19.97 _+3.32 b
21.07 + 2.39 c
21.52+_ 1.99 c, d
21.83___2.31 d
higher in fields with more large galls. Total bird-attacked
galls (galls categorized as successfully attacked, unsuccessfully attacked, and unknown success of bird-attack) did
not correlate with gall density. A Kruskal-Wallis nonparametric one-way anova performed on the April data set
showed that the mean diameter o f galls successfully attacked by birds varied significantly among the fields (Table 2). A multiple Student's t-test procedure found that successful bird attacked galls belonged to a mean diameter
subset significantly larger than the galls containing E. gigantea, Mordellistena, surviving Eurosta, and the mean diameter of galls not attacked by birds (latter tested with Student's t-test, t=7.88, P = 0 . 0 1 ) .
Selection intensities
The selection intensities created by Eurosta mortality due
to the various natural enemies varied considerably from
field to field (Table 3). For instance, in the Route 254 field,
we found very small directional selection intensities because
the upward selection by E. gigantea was balanced by the
downward selection by birds. Stabilizing selection predominated in this field. However, the Furnace R o a d field had
fairly strong upward, directional selection as a result of
weak downward bird selection. The Marsh R o a d field had
comparatively weak selection by parasitoids but relatively
strong selection by birds. The net result in this latter case
was significant negative, directional selection. In other
words, the bird attack was so strong in the Marsh R o a d
field that smaller gall size was favored. In this latter case
there is no stabilizing selection because the variance of the
survivors is the same as the variance of the entire field
population that starts the generation.
Considered over all fields, the mean diameter of galls
with surviving Eurosta was larger than the mean of all galls
due to mortality caused by the parasitoid, E. gigantea
(Fig. 1). This mortality in small galls caused an upward
i9
Table 3. Population mean gall diameters (excluding empty galls and those in which no living occupant was found), surviving Eurosta
mean gall diameters, and selection intensities (S.I., in units of standard deviation of mean) exerted on gall diameter by insect natural
enemies (Mordellistena unicolor, Eurytoma gigantea, Eurytoma obtusiventris) and birds. Significance of selection intensities determined
from bootstrapped 95% confidence intervals (95% C.I.)
Field
Mean gall diameters (mm _+s.d.)
Selection intensities from mortality due to :
Original
population
Insects
Surviving
Eurosta
S.I.
November
BVSA
147R
Furn
Pit
147E
Marsh
Hess
Beag
Violet
MP
Ind Park
Pott
Owen 1
254
147S
Aikley
Stein
Allen
Owen 2
KF
21.78 _+2.97
19.45_+2.65
18.64_+3.53
21.00__+2.51
20.62_+2.65
19.69___3.45
20.07-+2.20
19.44_+2.94
21.28_+2.90
21.08-+2.81
19.25_+2.83
21.94_+2.42
20.36_+2.60
21.51 _+2.61
20.86_+2.41
21.06-+3.47
19.17 _+3.86
21.69_+2.80
21.73_+2.79
20.88_+2.18
23.86 + 1.83
20.18___2.42
20.38_+3.07
20.97___2.38
21.50_+1.71
20.33+2.54
20.14_+1.70
21.23_+2.05
22.22_+1.31
21.03_+2.43
19.88_+2.47
22.51-+ 1.97
21.23_+1.68
22.21_+2.41
21.90_+2.01
22.69_+3.11
21.73 _+2.75
22.67_+l.77
22.60-+2.17
21.46_+1.80
All fields combined
20.62_+3.10
21.63_+2.32
0.34*
April
BVSA
147R
Furn
Pit
147E
Marsh
Hess
Beag
Violet
MP
Ind Park
Pott
Owen 1
254
147S
Aikley
Stein
Allen
Owen 2
KF
21.11 __.2.97
21.28_+2.35
18.68+3.02
19.71 +2.80
18.61 _+2.54
21.35_+2.82
19.67_+3.04
19.08 + 3.02
18.73_+2.83
20.54_+3.09
19.13_+2.39
20.73_+2.76
20.02_+ 2.07
20.38+2.86
22.11_+2.95
21.57_+2.47
19.34•
21.83_+2.71
22.25___2.47
10.15___3.05
22.33__.2.40
21.79_+1.86
20.29_+2.76
20.22_+2.02
19.59__+2.54
20.30_+1.94
20.00_+2.08
20.61+ 2.45
19.36_+2.50
20.81+2.40
19.36___2.13
21.62_+1.95
20.50 + 1.76
19.91-+2.41
21.83_+2.95
21.10_+2.04
20.94-+ 1.89
22.22_+2.32
22.46_+2.19
20.85_+2.67
0.41
0.34*
0.57*
0.29*
0.39*
0.21 *
0.16
0.51 *
0.30*
0.23*
0.33*
0.33*
0.23 *
-0.01
0.13
0.22*
0.58*
0.21 *
0.09
0.23*
All fields combined
20.45-+2.97
21.07-+2.39
0.70 *
0.28
0.49*
--0.01
0.33*
0.30*
0.23*
0.61 *
0.32*
0.26*
0.24
0.24*
0.33*
0.28 *
0.43*
0.47*
0.66 *
0.35*
0.29*
0.27*
0.27*
Birds
95% C.I.
S.I.
All combined
95% C.I.
S.I.
95% C.I.
(0.41, 1.03)
(-0.002, 0.55)
(0.24, 0.75)
(--0.20, 0.17)
(0.16, 0.50)
(0.11, 0.51)
(0.08, 0.38)
(0.37, 0.84)
(0.12, 0.54)
(0.10, 0.43)
(-0.003, 0.46)
(0.09, 0.38)
(0.16, 0.49)
(0.07, 0.48)
(0.22, 0.65)
(0.15, 0.80)
(0.41, 0.92)
(0.17, 0.56)
(0.18, 0.41)
(0.07, 0.46)
0
0
0
0
0
--0.10"
--0.07
0
0
-0.28*
-0.01
0
0
- 0.05
0
0
0
0
0.01
0
(0, 0)
0.70*
(0, 0)
0.28
(0, 0)
0.49*
(0, 0)
--0.01
(0, 0)
0.33*
(-0.21, -0.03)
0.19
(-0.16, 0)
0.15
(0, 0)
0.61"
(0, 0)
0.32*
(-0.46, --0.14) --0.02
(--0.05, 0)
0.22
(0, 0)
0.24*
(0, 0)
0.33*
(--0.14, 0.02)
0.27*
(0, 0)
0.43"
(0, 0)
0.47*
(0, 0)
0.66"
(0, 0)
0.35*
(0, 0.03)
0.31 *
(0, 0)
0.27"
(0.41, 1.03)
(-0.002, 0.55)
(0.24, 0.75)
(--0.20, 0.17)
(0.16, 0.50)
(-0.06, 0.40)
(-0.04, 0.33)
(0.37, 0.84)
(0.12, 0.54)
(--0.30, 0.25)
(-0.03, 0.45)
(0.09, 0.38)
(0.16, 0.49)
(0.03, 0.53)
(0.22, 0.65)
(0.15, 0.80)
(0.41, 0.92)
(0.17, 0.56)
(0.20, 0.42)
(0.07, 0.46)
(0.30, 0.39)
-0.02*
(--0.02, --0.01)
0.33*
(0.28, 0.37)
(--0.10, 0.87)
(0.14, 0.56)
(0.28, 0.86)
(0.07, 0.50)
(0.20, 0.60)
(0.09, 0.34)
(--0.05, 0.34)
(0.22, 0.83)
(0.01, 0.61)
(0.06, 0.37)
(0.09, 0.61)
(0.12, 0.52)
(0.07, 0.41)
(-0.25, 0.20)
(-0.04, 0.29)
(0.06, 0.38)
(0.32, 0.84)
(0.02, 0.37)
(-0.11, 0.29)
(0.05, 0.38)
0
--0.10
-0.02
--0.18"
0
-0.60*
--0.29
0
-0.04
-0.19"
-0.17"
-0.01
0
-0.08
-0.23*
-0.01
-0.03
-0.06*
0
0.01
(0, o)
0.41
(-0.10, 0.87)
(0.22, 0.31)
-0.08*
(-0.10, -0.06)
(-0.22,
(-0.08,
(--0.35,
(0, 0)
(-0.83,
(--0.17,
0)
0)
--0.02)
0.22
0.53*
0.18
0.39*
--0.41) --0.37*
0.11)
0.11
(0, o)
(-0.14,
(-0.35,
(-0.33,
(-0.04,
(0, 0)
(-0.23,
(-0.45,
(-0.01,
(--0.10,
(-0.12,
(0, 0)
(--0.01,
0.51.
0)
-0.06)
-0.05)
0)
0.22
0.09
0.10
0.32*
0.23 *
0.02)
-0.16
-0.04) -0.09
0)
0.21 *
0)
0.50*
--0.01)
0.14
0.09
0.02)
0.23*
0.21*
(--0.04, -0.47)
(0.22, 0.84)
(-0.13, 0.49)
(0.20, 0.60)
(--0.72, --0.07)
(--0.42, 0.60)
(0.22, 0.83)
(--0.06, 0.56)
(-0.18, 0.35)
(-0.29, 0.52)
(0.11, 0.51)
(0.07, 0.41)
(-0.47, 0.11)
(-0.47, 0.19)
(0.05, 0.37)
(0.23, 0.78)
(--0.08, 0.33)
(--0.11, 0.29)
(0.06, 0.40)
(0.15, 0.27)
* Significantly different from zero at P_< 0.05
shift in the mean diameter o f galls containing surviving
Eurosta which was partially counter-balanced by bird induced selection favoring Eurosta in smaller diameter galls.
Eurosta in intermediate sized galls h a d the highest survivorship yielding a stabilizing c o m p o n e n t to selection. However,
because E. gigantea attack was typically m o r e frequent than
bird attack and since the two mortality sources did not
exactly balance, there was also a directional selection corn-
ponent m most fields (Table 3). The net selection pressure
from all natural enemies on the gallmaker resulted in an
u p w a r d selection differential on mean diameter for galls
containing surviving Eurosta of 0.21 s t a n d a r d deviations
o f the m e a n for the 1983 84 season.
Figure 2 illustrates the percentage o f galls attacked by
E. obtusiventris is shifted to the right because some o f the
smaller galls that were occupied by E. obtusiventris were
20
1o: I Eoro,osodon
30.
All Gaffs
"6
Mordellistena
o~
25
o
~
60
o
:~, 60
b3
._c
40-
~
g
-~
30.
g
20.
40
;2
o
y_
1e0
O0 T
Mordellistena unicolor
~ 1O0 -
X == 29.38
p (0.001
80
10.
0
Eurytome obtusiventris
~
~e 80 -
X 2= 16.02
p = 0.003
"-=
4o
~
40-
2
~
20
z
o
,
. ,-.!
m.
Mordellist
unicolor
(mm)
iI,R,l, oooo
O
~N
b5
.C
a
Eurosta
"l s~
rl 0 , 5 %
~
Eurytoma
~ gigantea
.g%
Fig. 4. Approximate frequencies of interactions among Eurosta solidaginis natural enemies that result in the death of one enemy
by another
1
Observed attack
Estimated total attack
20
C
.
.
.
.
.
-.m
_,_
,
Z0
Eury~orna obtuslventri= - November
.
c
20
Eurytomo
obtusiventr]s
- April
g
15
15
u
L
l,l,lllllIH,l,n,lll=l
(3-
)25
Eurytoma glgantea - April
O
o
24
Eurytorna
obtusiventris
(14 14 16 18 20 22 24 )25
100
40
I
28.
Eurytorna giganteo - November
60.
22
(mm)
145%L%
~=,660
Fig. 1. Gall diameter (mm) by size class for all galls; galls containing surviving Eurosta solidaginis, Mordellistena unicolor, Eurytoma
obtusiventris, Eurytoma gigantea; and galls attacked by birds. The
X 2 values shown compare a given subset to all galls
80.
20
~ o.5
,
20
100,
18
Fig. 3. Percentage of galls by diameter size class (mm) attacked
by the inquiline Mordellistena unicolor at the November and April
censuses
i ~176
40
Call Diameter
16
p ( 0.001
~
{14 14 16 16 20 22 24 )25
14
2&1%
i~ 80
0
<14
Oall D i a m e t e r
~o 60-
i
November
April
o
oe
mm
o
i
So-
20
unicolor
60-
X 2= 85.36
p (0.001
10
(14
14-
16
18
20
22
24
)25
Gall D i a m e t e r
(14
14
16
18
20
22
24
)25
Fig. 2. Percentage of galls attacked by Eurytoma
species according to gall diameter size class (ram) for
November and April censuses. Since one natural
enemy can consume another, both observed attack
levels and estimated total attack levels are shown for
each Eurytoma species at the November and April
censuses
(ram)
also attacked by E. gigantea. Further, we found that Mordellistena experience higher winter mortality in smaller galls
(Fig. 3).
Insect natural enemy competition
A reasonably large fraction of the galls were attacked by
more than one enemy but because the initial attacker was
consumed, only the ultimate survivor in the gall could be
recorded. The approximate frequencies of interactions
among the gallmaker's insect enemies were calculated and
are shown as percentages in Fig. 4. The high levels of interaction among the insect natural enemies prohibits a detailed
analysis of individual species influence on the gallmaker.
MordeIlistena is estimated to have consumed E. gigantea
in 26.1% of the galls originally containing E. gigantea. To-
21
tal galls parasitized by E. gigantea was estimated at 20.3%
of the population. E. gigantea is estimated to have consumed E. obtusiventris in 21.9% of all galls originally containing E. obtusiventris. Mordellistena should have consumed E. obtusiventris in 28.6% of all galls originally containing E. obtusiventris. Total galls originally containing E.
obtusiventris were estimated at 10.5% of the population.
Discussion
The most notable finding of this study was the net upward
selection pressure on Eurosta gall diameter created by Eurosta's natural enemies. Larvae in small galls have low relative fitnesses whereas larvae in intermediate sized galls have
high relative fitnesses. Thus, there is a stabilizing component to the selection pressures created by the natural enemies in this system. At the same time, the selection is directional since the gall size with peak survival is higher than
the average of the gall size distribution. Thus, even though
some of the larvae of the larger galls are eaten by birds,
pressure from E. gigantea is often strong enough that selection is pushing in an upward direction favoring some slight
increase in gall diameter.
The selection intensities reported here indicate the magnitude and direction of the selection pressures created by
the gallmaker's natural enemies. They do not, however, indicate the evolutionary responses to those pressures. The
potential evolutionary responses are determined by both
the heritable variation in gallmakers for gall size and the
selection intensities. Although gall size has a heritable component to the insect (Weis and Abrahamson 1986), plant
genotype has an even stronger genetic effect on gall size.
The limited genetic control of gall size by the gallmaker
will markedly restrain the amount of evolutionary response
possible, We will report on the responses of these gallmaker
populations to natural selection in another paper (Weis
et al., unpublished work).
The selection intensities we measured were highly variable from field to field. The parasitoid E. gigantea created
an upward selection pressure in every field we examined,
but not every field had a downward selection pressure imposed by birds. Since the birds involved in gallmaker attack
are primarily woodland species, bird attack is dependent
on proximity of appropriate bird habitat.
The occupation of the smallest-gall subset by E. gigantea
was expected given that it attacks after galls have reached
maximum size. Thus, E. gigantea is excluded from galls
whose wall thicknesses are greater than their ovipositor
length (Weis and Abrahamson 1985; Weis et al. 1985). Although Mordellistena can attack all gall sizes because of
the beetle's early invasion of gall tissue, it attacked small
galls more frequently. On average, E. obtusiventris occupies
gall sizes larger than the population mean, but this is likely
the result of differential attack on E. obtusiventris by E.
gigantea and Mordellistena in small galls. Thus, E. gigantea
and Mordellistena reduce they number of E. obtusiventris
in small galls in the same way the do Eurosta. E. obtusiventris can be found in galls of all diameters because its oviposition involves egg deposition on Eurosta larvae prior to gall
formation (Abrahamson unpublished data). This natural
enemy is probably the only natural enemy that does not
exert selection on Eurosta for gall size.
The mean of galls successfully attacked by birds was
larger than surviving Eurosta galls and the mean of all galls
not attacked by birds. However, the frequency of bird attack on galls was independent of field gall density but it
was positively correlated with field mean gall diameter. This
suggests that birds select galls based on gall size rather
than gall abundance. This finding is similar to that reported
by Confer and Paicos (1985).
In our study, successful bird attack accounted for 14.5%
of Eurosta mortality whereas E. gigantea parasitism accounted for 20.3% of Eurosta mortality (this figure includes
galls originally occupied by E. gigantea but ultimately consumed by Mordellistena). Uhler (1961) found that E. gigantea accounted for 5.6% of Eurosta mortality while birds
accounted for only 2.3%. Cane and Kurczewski (1976),
however, reported that bird predation can be as high as
20%. These findings and our own data (Weis et al. unpubl.
data) lead us to conclude that site to site and yearly fluctuations in bird predation rates are common.
Annual variation in attack by Eurosta's natural enemies
have the potential to cause shifts in the mean gall diameters
of the surviving Eurosta population. One possible scenario
is that gall size increases do occur as a consequence of
attack by E. gigantea. The resulting population of larger
galls could become more attractive to birds and if so, bird
predation could increase, causing a shift toward a smaller
mean gall size. These two counter-balancing selection forces
could create a dynamic equilibrium in gall diameter that
would fluctuate in different fields in various years. An alternative scenario would see shifts in selection intensity as
primarily the result of environmental effects. In years when
climate promotes vigorous gall growth, the average gall
size would be nearer the peak of the fitness function, and
thus selection would be weak. Under poorer climatic conditions (e.g, drought) the mean gall size would be substantially less than the size conferring peak fitness, hence the
intensity of selection would be strong. Environmental effects on gall development may mask genetic differences in
some generations but not others, thus causing the evolutionary response to selection to occur intermittently, rather
than as a smooth and continuous function (Weis et al., unpublished work). Our study found that interactions among
the insect members of the Eurosta natural enemy guild was
complex and frequent.
Acknowledgements. We thank Chris Abrahamson, Robert Bertin,
Amy Ershter, Irene Kralick, Wayne McDiffett, and Gary Metzger
for their assistance. Financial support was provided by BucknelI
University and NSF grants DEB-8205856 and BSR-8614768 to
W.G.A. A portion of this research was part ofa M.S. thesis submitted to Bucknelt University by J.F.S.
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Received September 7, 1988