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Annu. Rev. Entomol. 1995. 40:297-331
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INTERSPECIFIC
INTERACTIONS IN
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PHYTOPHAGOUS INSECTS:
Competition Reexamined and
Resurrected
Robert F. Denno
Depar tment of Entomology, University of Maryland, College Park, Maryland 20742
Mark S. McClure
The Connecticut Agricultural Experiment Station, Valley Laboratory, Cook Hill
Road, Box. 248, Windsor, Connecticut 06095
James R. Ott
Department of Biology, Southwest Texas State University, 601 University Drive,
San Marcos, Texas 78666
KEY WORDS:
facilitation, competition-mediating factors, competitive exclusion, niche,
. resource partitioning
ABSTRACT
This review reevaluates the importance of interspecific competition in the
biology of phytophagous insects and assesses factors that mediate
competition. An examination of 193 pair-wise species interactions, repre­
senting all major feeding guilds, provided information on the occurrence,
frequency, symmetry, consequences, and mechanisms of competition. Inter­
specific competition occurred in 76% of interactions, was often asymmetric,
and was frequent in most guil d s (sap feeders, wood and stem borers, seed and
fruit feeders) except free-living mandibulate folivores. Phytophagous insects
were more likely to compete if they were closely related, introduced, sessile,
a g gr e g a tive, fed on discrete resources, and fed on forbs or grasses. Interference
population
0066-4170/95/0101-0297$05.00
297
298
DENNO, McCLURE & OTT
competition was most frequent between mandibulate herbivores living in con­
cealed niches. Host plants mediated competitive interactions more frequently
than natural enemies, physical factors, and interspecific competition. Sufficient
experimental evidence exists to reinstate interspecific competition as a viable
hypothesis warranting serious consideration in future investigations of the
structure of phytophagous insect communities.
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INTRODUCTION
The importance of interspecific competition as a force affecting the distribu­
tion, abundance, and community structure of phytophagous insects has expe­
rienced a controversial history, to say the least (107, 152, 174). During the
1960s and 1970s, field investigations of interspecific competition among her­
bivorous insects consisted mainly of observational studies of resource parti­
tioning (e.g. 108, 143, 147, 179, 184). The rationale for such studies stemmed
from classical competition theory, which predicted that two species could not
occupy the same niche and coexist, and that coexistence could be achieved
only through divergence in resource use (reviewed in 152). Thus, many insect
ecologists sought differences in the way herbivorous insects divided up their
host plants or habitats and implicated competition as the cause of such differ­
ences when they were found. We also contributed to this fashionable but
deductive approach (36, 127), for which the precedent had been set largely by
vertebrate ecologists (reviewed in 151, 161). During these decades, experi­
mental field studies documenting the occurrence of interspecific competition
in phytophagous insects were rare (126, reviewed in 26, 153). Nevertheless,
there was sufficient experimental support for competition emerging from ma­
rine invertebrate and terrestrial vertebrate systems (26, 153) to persuade many
insect ecologists to accept interspecific competition as the paradigm for the
organization in phytophagous insect communities.
During the early 1980s, however, the role of competition in structuring
phytophagous insect communities was challenged severely, and within a few
years its status fell from a position of prominence to that of a weak and
infrequent process (89, 102-104, 106, 107, 174). Two major lines of criticism
led to this downfall. The first had its roots in a theoretical paper by Hairston
et al (74), who argued that because defoliation was rare, food must rarely be
limiting for herbivores, and that predators, parasites, and pathogens were
largely responsible for maintaining herbivore densities below competitive lev­
els. The few insect studies included in reviews at the time (26, 107, 153, 174)
seemed to substantiate this contention.
The second avenue of criticism stemmed from analyses of phytophagous
insect distributions and cooccurrences. Positive interspecific associations, the
failure to find repulsed distributions (19, 102, 170, 171), and the presence of
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COMPETITION IN PHYTOPHAGOUS INSECTS
299
vacant niches and unsaturated communities (102) led some ecologists to ques­
tion the importance of competition. Notably few experimental field studies of
competition in phytophagous insects had been added to the literature at this
time, and the insect studies responsible for both the deification and demise of
interspecific competition were overwhelmingly observational and pattern
rather than process oriented.
By the mid 1980s the scientific community had responded to a plea for a
more experimental approach (26, 153), and more controlled, manipulative
investigations of competition between insect herbivores were instigated (e.g.
31, 41, 45, 50, 63, 81, 92, 94, 96, 114, 123, 124, 129, 132, 134, 135, 167).
Accompanying such studies has been a growing body of evidence suggesting
that herbivorous insects indeed do compete, and recent assessments reflect this
reversal in thinking (34, 48, 49, 169).
The focus of this review is to reevaluate the importance of interspecific
competition in the population biology of phytophagous insects and to assess
those factors that promote its occurrence. Previous treatments have emphasized
folivores (34, 107), and current perceptions of the importance of competition
for phytophagous insects are based largely on conclusions drawn from this
guild. Here, we examine interactions for food and space in all guilds of
herbivorous insects (e.g. folivores, seed feeders, wood borers, gall makers, root
feeders) except pollinators. Interactions involving detritivores (e.g. 156 in part,
187) are also excluded.
Our specific objectives are to: (a) update and expand the database on
interspecific interactions for phytophagous insects; (b) compare evidence for
and against competition and facilitation within and among guilds and contrast
the occurrence, frequency, symmetry, consequences, and mechanisms of com­
petition; (c) examine four factors that mediate (promote or diminish) interspe­
cific competition including host plants, natural enemies, physical factors, and
intraspecific competition; (d) determine whether taxonomic relatedness, vari­
ous life-history traits, diet breadth, and host plant growth form predispose
herbivorous insects for competition; (e) establish a link between resource
partitioning (temporal and spatial), niche shifting, and interspecific competi­
tion, and assess the relationship between repulsed distributions and interspe­
cific competition; and (j) examine facilitative interactions between
phytophagous insects and assess their symmetry, causes, and consequences.
By using the comparative approach, we address suggestions in the literature
that competition occurs more frequently in the Homoptera and Hemiptera (41,
92, 135, 174); is more intense between closely related taxa (133); is more
likely between species feeding on discrete resources (e.g. seeds, fruits, stems)
(54, 71, 166); and is more frequent between species in introduced systems,
managed habitats, and concealed feeding niches, which are situations in which
the action of natural enemies is often reduced (28, 72, 73).
300
DENNO,
McCLURE & orr
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THE DATABASE
We limit our treatment of phytophagous insects to those feeding on the living
tissues of vascular plants. Thus, insects feeding on rotting fruits or dead wood
are not considered. From the remaining literature, we extracted 193 pair-wise
interspecific interactions that provided infonnation on competition and facili­
tation (Table 1). These interactions represented 104 study systems [e.g. the
investigations of Addicott & Antolin on fireweed aphids (1-4, 9) constituted
one study system and offered one interaction between two species]. We in­
cluded in our analysis only those interactions for which there was direct
evidence for or against competition and facilitation. Direct evidence included:
(a) experimental demonstrations (41, 92, 114), (b) displacement or exclusion
following the introduction of a competitor (84, 123, 124, 125, 130, 158), and
(c) observations with verification of mortality or niche shift [e.g. the dissection
of galls or stems with confinnation of competitor death (6, 167), or alterations
in gallery construction in the case of bark beetles (138)]. In large part, we did
not include interactions in which competition was assessed indirectly (e.g.
nonexperimental studies of resource partitioning, niche overlap, or dispersion
and density correlation). Some studies provided direct evidence of competition
for some species pairs and nonexperimental, distributional evidence for others
(e.g. 70, 143). In these cases, we included only those species pairs for which
competition was measured directly.
Of the 193 pair-wise interactions, 148 were experimental demonstrations, 9
were exclusively examples of competitive displacement, 31 were observational
with direct evidence for death or niche shift, and 5 were nonexperimental.
Most pair-wise interactions (166 examples) were studied in the field; however,
supplemental laboratory assessments of competition were made in many of
these cases. Studies in which leaves were either naturally or artificially dam­
aged in the field and then later assayed in the laboratory for delayed competitive
effects were scored as having a field component (e.g. 75, 137, 186). The
remaining 27 interactions were appraised exclusively in the laboratory or
greenhouse. These were included because they provided valuable infonnation
on the mechanism or symmetry of competition. Two of these 27 interactions
involved aphids in greenhouses (175, 181), and 6 involved bruchid pests of
stored beans, which is their primary habitat (e.g. 71, 177).
If competition was found, regardless of its intensity or frequency, the inter­
action was scored as competitive (Table 1). If evidence for competition was
found, but only at densities above those nonnally encountered in the field, the
interaction was scored as noncompetitive (e g. 77).
We also assessed the frequency (not strength) of the competitive interaction,
based on the investigators' opinion-s
interactions were classified as frequent, infrequent (occasional to rare), or not
.
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COMPETITION IN PHYTOPHAGOUS INSECTS
301
detennined. Competitive interactions resulting in exclusion were scored as
frequent (23, 35, 84, 97, 114, 123, 124), as were cases when competition
occurred across most seasons or years (6, 31, 41, 47), and during or following
frequent herbivory or outbreaks (137, 185). Interactions were also scored as
frequent if the removal or addition of one species was followed by a significant
population change in the other (92, 94, 132,142, 167). Interactions were scored
as infrequent when competition occurred only on susceptible plants or clones
and not on resistant ones (63, 134, 135), in dense but not in sparse plantings
(96), in certain plant patch sizes (70), on stressed but not on healthy plants
(85), on some host plant species but not on others (128, 129), and during or
following rare defoliations (87, 136, 163).
The symmetry of interactions was evaluated and was scored as symmetric,
asymmetric, or not detennined. Instances of reciprocal deterrence (17, 20, 21,
54), reductions in fitness (85, 126, 165), and population size (175) were scored
as symmetric. Strong one-way effects on survival (6, 124, 166), fecundity (82,
114), and population size (35, 92, 135, 145) were considered asymmetric, as
were cases in which previous herbivory influenced the perfonnance of sub­
sequent herbivores (75, 78, 81, 136, 185). If only the competitive effect of one
species on another was tested (129, 131, 134), and not the reverse, then the
symmetry of the interaction could not be detennined.
The consequences of competitive interactions were scored as: (a) competitive
exclusion on the geographic or habitat scale, (b) local displacement from the
feeding or oviposition site on a plant, or (c) fitness reduction or population
change. Consequence b could result from overt kiIling, niche preemption, niche
shifting, avoidance, or emigration, and c from adverse effects on survival,
development time, fecundity, and body size, and from changes in population size
in the presence or absence of competitors. Single pair-wise interactions could
exhibit various combinations of these outcomes and were scored accordingly.
The mechanism of competition was scored as exploitative, interference, or
both for each pair-wise interaction. Exploitative competition occurs when
in dividuals, by using resources, deprive others of the benefits to be gained
from those resources (153, 154). Interference competition results when indi­
viduals harm one another directly through fighting and killing, or indirectly
by the aggressive maintenance of territory or the production of chemicals that
deter other individuals (153).
Exploitative competition may be direct or indirect and effects may be felt
either immediately or at a later time (34). Exploitative interactions mediated
through the host plant are difficult to categorize. When a mandibulate defoliator
removes tissue that is no longer available to another species, a direct and
immediate adverse effect can result (18, 84). In contrast, sap-feeding Homop­
tera can reduce plant nutritional quality, which in turn can have indirect
negative effects on cooccurring species (114). The competitive effect may
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Table 1
w
0
N
Interspecific interactions in phytophagous insectsa
HAUSTELLATE MOUTHPARTS
(I] Free living (26)
(2] Gall Mak.r (1)
[3] Free Living X Gall Maker (I)
Compo
36
5
(4] Gall Maker X Root Feeder (I)
Total (Haustellate) (29)
MANDIBULATE MOUTHPARTS
Frequency
Interaction
[Guild]b
(No. Study Systems)
Facilit.
None
Freq.
Infreq.
0
0
22
5
0
1
0
Sym.
Asym.
Not Det.
Excl.
Loc Dis.
16
14
5
19
5
16
20
24
0
27
42
Consequences of Interaction
Symmetry
Not Det.
8
30
21
15
11
27
Subtotal 1 (External Feeders) (21)
30
21
15
II
27
8
[6] Stem Borer (3)
13
1
6
13
13
8
2
IS
2
17
42
0
4
2
2
2
(10] Gall Maker (I)
[11] Root Feeder (1)
Subtotal 2 (loternal Feede...) (31)
14
1
21
0
0
2
0
0
51
0
5
0
0
13
0
0
6
25
[U] Free Living X Leaf Miner (5)
[13] Free Living X Seed/Cone/Stem Feeder (3)
1
{l4] Free Living X Root Feeder (2)
[IS] Free Living X Gall Maker (2)
0
[161 Leaf Miner X Root Feeder (1)
Subtotal 3 (Mancfibolate Guild loteractioos) (13)
16
Tnta1 (Maodibolate) (65)
97
27
36
35
34
17
22
26
22
26
15
0
0
13
10
13
0
0
37
10
4
18
2
0
25
5
0
10
8
2
0
5
15
0
26
20
0
0
0
I
11
26
80
13
11
8
56
55
4
38
37
I
2
0
22
0
5
Total (Haustellate X Mandibolate (10)
Grand Total (104)
16
0
Both
0
3
0
[IS} Free Living (H) X Root Feeder (1)
0
1
0
HAUSTELLATE X MANDIBULATE
[17] Free Living X Free Living (9)
8
0
1
0
0
5
33
Interf.
0
[5] Free Living (21)
(7] Wood Borer (8)
[8] Leaf Miner (1)
(9] Seed/PodfConeiBract Feeder (17)
Mechanism
Fit. Red. Explol.
147
11
35
64
47
36
20
107
20
12
86
95
57
52
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'Evidence for and against interspecific competition is presented by guild,with feeding niche (e.g. free living,stem borer,gall maker) nested within two major
mouthpart guild types. The haustellate group contains piercing-sucking and rasping species (Homoptera,Hemiptera and Thysanoptera),while the mandibulate
group consists largely of species in the Orthoptera, Lepidoptera, Coleoptera, Hymenoptera and Diptera (larval Diptera with mouthhooks were placed in the
mandibulate group). The number of study systems examined for each guild is shown in parentheses (because some studies included mUltiple-species interactions,
there are more interactions than studies).
Interactions are divided into three categories (Competition,Facilitation and None in which no evidence for either
competition or facilitation was found). Also presented are the frequency of the competitive interaction in the field (Frequent,Infrequent,or Not Determined),
the symmetry of the interaction (Symmetric,Asymmetric or Not Determined),the consequence of the interaction (Competitive Exclusion,Local Displacement,
Fitness Reduction/Population Change), and the mechanism of competition (Exploitative,Interference and Both).
b
References for each study system are arranged by guild [Numbers in brackets correspond to numbered guilds/feeding niches in table]
. Letters indicate system
characteristics:
stem, bark),P
G
=
E
=
=
Experimental,S
=
Field survey before and after introduction,D
Non experimental field study;
Greenhouse study,L
=
Laboratory study;
(herbivores and host plants),I
=
F
C
=
Competitive interaction determined by dissection and observation (gall,
=
Field study (bioassays of leaves previosly damaged in the field are included),
=
Field study conducted in cages,0
Introduced system (host plant and/or herbivore),T
=
=
Field study conducted under open conditions; N
Natural habitat, M
=
=
Native system
Managed habitat (Agricultural, Ornamental or
Sylvicultural).
[1] 1,2, 3,4,9 (E, F, L,
0,
N,T); 23, 180 (E, S, L, C,N, M); 32 (E, F,0, N, T); 35 (E,S,0, F,
F,0, N,T); 68,69, 70 (E,F,L,
100 (E,F,L,
0, J, M);
0,
L,
I, M); 38, 41,42 (E,F,L,
0,
N, T); 43 (E,
N,T); 82 (E, G,C, J, M); 85 (E, F,C, N,M); 88 (E,G,F,C,J, M); 92, 93 (E, F,0, N,T); 98 (E,F,C,N,
114,115, 119, 122,125 (E,S,F, G,
0, J,
T);
0, J, M); 119, 122 (E,F, G,0, N, T); 120,121,
0, N,T); 130 (S,F,0, I, M); 158 (E, S, F,L, 0, I, M); 159 (E,F,C,N,T);
165 (E, F,C,N,T); 175 (E,G,C,I, M); 181 (E,G,C,I,M); 183 (E, F,L, C,N,T). [2] 5,6,7 (D,F,0, N,T). [3]56 (E, F,C,N, M). [4]135 (E,
F,C, J, N). [5] 14 (E, F,C,N,T); 33 (E, F,0, N,T); 44 (E, F,0, N,T); 45, 90 (E,F,0, N,T); 57 (E, F, 0, C,N,T); 75 (E, F,L, C,N, T); 77
(E,L, C,I,M); 78 (E, F,L, C,N,T); 81 (E,F,L, C,N,T); 84 (S, F,0, L, I,T); 86,87 (E,F,C,N,T); 96 (E,F,0, I, M); 9 9 (E,L, C,I,M); 136
(E,F,C,N,T); 137 (E,F,L, C,N, T); 144 (E,L, C, J, M); 145 (E, F,C, N,T); 155,157 (E, F,0, N,T); 163 (E,F,0, N,T); 171,172,173 (E,F,
L, 0, N,T); 186 (E,F,G,C,N,T). [6]143 (D,F, 0, N,T); 148 (D, F,0, N,M); 166,167 (E,D,F,L, 0, N,T). [7] 15 (E, F,0, N,T); 17,55 (D,
F,0, N,T); 20,21 (E, F,0, N,T); 29,30 (D,F,0, N, T); 109,110 (E,L, C,N, T); 131, 132 (E,F,0, C, N,T); 138,182 (D,F, 0, N,T); 142 (E,
F,L, 0, N,T). [8] 19 (P, F, 0, N, T). [9] 8 (E, L, C, I,M); 13 (E, L, C, I, M); 16,76 (E, F,0, J, T); 2 5 (D,P, 0, N,T); 54 (E,F,C,I, M); 64,
65,66 (E,L, C,I,M); 71 (E,L, C, J, M); 97 (E, S,L, 0, I, M); 112 (E,F,0, N,T); 139 (D,P,F,0, N,T); 141 (E, L, C,I, M); 155,156 (E, F,0,
N,T); 168 (E, F,C,J, T); 176 (E,L, C, I, M); 177,178 (E,L, C,I, M); 188 (E,F,C,N,T). [10]59,60,61,62,63 (E,F, 0, N,T). [11]24 (E, D,
F,0, J, M). [12]46 (E,F,0, N,T); 47 (E, F,0, N,T); 50,51 (E,F,0, N, T); 79 (E,F,L, C, N,T); 185 (E,F,0, N,T). [13]31 (E,F,0, N,T);
134 (E, F,0, N,T); 163, 164 (E,F,0, N,T). [14]52,91 (E, L, C, I, M); 84 (S,F,0, L, I, T). [15]59,60,61,63 (E,F,0, N,T); 84 (S,F,0, L,
J, T). [16]111 (E,L, C,N,T). [17]11 (E, F,0, N,T); 18 (S,F,0, J, T); 44 (E,F,0, N,T); 57 (E,F, 0, C, N,T); 92, 93,94 (E,F,0, N,T); 113
(E,F, 0, M,T); 128,129 (E,F, 0, N, T); 162 (E, F,0, C,N,T). [18]53 (E,L, C, I, M); 67 (E, L, C, N,T).
124,125 (E,F,G, S,0,
J,
M); 116, 117,123, 125 (E,F,G,S,
M); 126, 127 (E,F,C, N,T); 128, 128 (E,F,
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304
DENNO, McCLURE & orr
occur immediately or it may be delayed and carry over to subsequent genera­
tions (122; RF Denno & J Cheng, in preparation). Similarly, mandibulate
herbivore feeding may induce nutritional or allelochemical changes in plants
(95), resulting in either immediate or delayed indirect effects on potential
competitors (75, 78, 81, 136, 185).
Interactions exhibiting interference competition included those involving
direct killing (6, 139, 143, 148, 166, 168, 178), aggressive behavior (69, 128,
129), and the production of chemicals (deterrents and pheromones) that hinder
colonization (17, 55, 109, 110), feeding (144), or oviposition (53, 54, 71, 91,
99). Avoidance of previously damaged leaves (46, 47, 79) and tissues modified
or fouled by other species (16, 25, 112, 130) were considered interference
phenomena. Cases of preemption [the passive occupation of a plant part by
one individual that precludes colonization by another latecomer (183)], and
space overgrowth by scale insects (114, 122), were scored as interference
competition because they contain elements of avoidance. Interactions resulting
in selective emigration (43, 88, 175) or the interspecific triggering of migratory
forms in wing-polymorphic insects (41, 100) were regarded as interference
competition, as were natural enemy-mediated interactions, such as those in
which the intensity or outcome of competition between two phytophagous
species was influenced by predators or parasitoids (15, 122, 158).
We assigned factors mediating the intensity or outcome of competition to
four major categories: host plants, natural enemies, physical factors, and in­
traspecific competition. Host plant effects were further partitioned into imme­
diate effects (plant resistance, plant nutrition, and plant phenological events
such as bud break), delayed effects (plant damage, or feeding-induced changes
in plant nutrition or allelochemistry), and textural effects (plant density, patch
size, plant species composition). If any host plant (e.g. 41, 60, 75, 86, 96, 114,
135), natural enemy (e.g. 15, 43, 47, 115, 158), or physical factor (e.g. 64, 97,
126) influenced the intensity or outcome of the competitive interaction, the
factor was scored as mediating. We considered intraspecific competition to be
a mediating factor if its effect on a particular herbivore species exceeded that
of interspecific competition (e.g. 126).
Evidence for and against interspecific competition and its frequency, con­
sequences, symmetry, mechanism, and mediating factors is compared between
feeding guilds and niches in Table 1. Feeding niche (e.g. free living, stem
borer, gall maker) is nested within two major mouthpart guild types: haustellate
and mandibulate. Based on the concealment of their feeding niche, mandibulate
herbivores are categorized as external feeders (free-living species and leaf tiers
and leaf rollers) or internal feeders (stem and wood borers, leaf miners,
seed/pod/conelbract feeders, gall makers, and root feeders). Interactions be­
tween mandibulate herbivores in different niches that consisted mostly of
interactions between external and internal feeders (e.g. free-living and leaf-
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COMPETITION IN PHYTOPHAGOUS INSECTS
305
miner species) are placed in a separate category for analysis. We also estab­
lished a major interguild grouping that includes interactions between haustel­
late and mandibulate herbivores (most interactions were between free-living
species).
We compared the occurrence of competition between native and introduced
systems (if either herbivore or the host plant was introduced the system was
considered introduced), natural and managed habitats (agricultural, ornamen­
tal, and sylvicultural), forb/grass- and tree/shrub-feeding species, monophages
(feeding within one genus of plants) and polyphages (feeding on more than
one genus of plants), aggregated (feeding in groups at least during early instars)
and solitary species, and sessile and mobile species. To discern if particular
life history traits contributed to competitive success, we compared the fecun­
dity, body size, voltinism, and dispersal ability of the superior and inferior
competitor in each interaction.
Published studies are undoubtedly biased toward detecting competition.
Biases may stem from: (a) the choice of species pairs most likely to interact,
(b) the selection of common species for study, or (c) the failure to publish
nonsignificant results (26, 34). Decisions concerning the inclusion of particular
studies and the scoring of specific parameter states are also subject to bias
(34). To minimize those biases within our control, we limited our assessment
to experimental studies, established uniform criteria for scoring all aspects of
competition, and scored conservatively.
All comparisons were conducted using categorical data analysis of counts
[CATMOD program (58, 149)]. Maximum-likelihood chi-square and prob­
ability values are reported for each comparison. We acknowledge that some
comparisons presented herein are not completely independent. For example,
introduced species often occur in managed habitats. Therefore, comparisons
of competition between introduced and native species, and between species in
managed and natural habitats, must be interpreted with caution.
GENERAL PATTERNS OF INTERSPECIFIC
INTERACTION
Evidence for interspecific competition is widespread, occurring throughout all
feeding guilds of phytophagous insects (Table 1). Of the 193 pair-wise inter­
actions we assessed, 147 (76%) show evidence of interspecific competition,
11 (6%) support facilitation, and only 35 interactions (18%) indicate an absence
of competition. Although competitive effects were detected in the great ma­
jority of cases, their strength .and frequency vary considerably. Nonetheless,
the paucity of hard experimental evidence against interspecific competition
contrasts sharply with the claims of the traditional view. Another recent review
of phytophagous insects (34) also found that the vast majority of experimental
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DENNO, McCLURE & OTT
studies (91 %) provided evidence for interaction (negative or positive) and that
most studies (67%) detected competitive effects.
A comparison between guilds showed that interspecific competition was
more prevalent among haustellate species (93 %) than mandibulate species
(78%) (X2 = 4.57, P = 0.032), and that competition was more common among
haustellate species than in interguild interactions between haustellate and
mandibulate species (62%) (X2 ::: 6.90, P = 0.009) (Table 1). Furthermore,
competitive interactions were scored as frequent more often for haustellate
species (77%) than for mandibulate herbivores (51%) (X2 = 6.47, P = 0.011).
Similarly, interactions tended to be frequent more often among sap feeders
(77%) than between sap feeders and mandibulate herbivores, for which most
interactions were infrequent (80%) (X2 = 4.80, P = 0.029). These findings are
consistent with reports that interspecific competition occurs more often in the
Homoptera and Hemiptera (41, 92, 135, 174).
Within mandibulate phytophages, competition occurred more often in inter­
actions between species occupying internal feeding niches (89%) (e.g. stem
borers, wood borers, and seed feeders) than in interactions between externally
feeding folivores (59%) such as free-living Orthoptera, Lepidoptera, Hymenop­
tera, and Coleoptera (X2= 11.90, P = 0.001). Competition was also detected more
often in interactions between mandibulate free-living folivores and concealed
feeders (100%) (e.g. folivores and leaf miners) than in interactions between
free-living folivores themselves (59%) (X2 = 5.11, P = 0.024). Also, competitive
interactions were more often infrequent between external feeders (79%) than
either between internal feeders (40%) (X2 = 7.02, P= 0.008) or between external
and internal feeders (30%) (X2 = 5.93, p::: 0.015). Thus, for the major guilds of
phytophagous insects, competition was detected least often in free-living,
mandibulate species. When competition occurred in this guild, it was usually
scored as infrequent. One should note that the current view regarding the strength
and frequency of competition in phytophagous insects has generally emphasized
mandibulate folivores (e.g. 107), the guild in which competition appears to be
least likely. Internal feeding guilds (seed and fruit feeders and wood borers), in
which there is abundant evidence for competition (Table 1), have been inexpli­
cably excluded from most previous treatments.
We found that most competitive interactions (84%) are asymmetric (amen­
salistic) (Table 1), a result consistent with the findings of previous critiques
(l05, 106, 174). Although amensalism prevailed in most guilds, nearly half of
the interactions among haustellate sap feeders (44%) were symmetric. An even
greater frequency of symmetrical interactions (53%) occurred among the free­
living sap feeders, especially the Cicadellidae and Aphididae (82, 85, 126, 158,
165, 175). The frequency of symmetrical interactions between sap feeders
(44%) was significantly higher than that observed within mandibulate herbi­
vores (5%) (X2 = 20.50, p::: 0.001). No differences in symmetry were observed
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COMPETITION IN PHYTOPHAGOUS INSECTS
307
between mandibulate herbivores with internal feeding niches, external feeding
niches, or between internal and external feeders (P > 0.05), and all interactions
were strongly asymmetric. The few cases of symmetric competitive interac­
tions in mandibulate herbivores involved bark beetles in which inhibitory
pheromones reciprocally deterred the simultaneous colonization of pine trees
(17, 30, 31, 55, 110, 138, 182).
Certain guilds appeared to be consistently out-competed in interactions with
others. For example, root feeders were adversely affected in all reported
interactions with folivores (52, 84, 91, 111, 135). Also, leaf miners were
usually less successful on leaves previously damaged by chewing herbivores
(46, 47, 50, 51, 185), although free-living chewers may avoid feeding on mined
leaves (79). Haustellate herbivores, however, appeared to prevail in interac­
tions with mandibulate species (113, 129), as often as they succumbed (18,
57, 92, 94). Clearly, more studies are needed to verify these trends.
The consequences of competition also differ among certain guilds (Table 1).
For instance, the frequency of large-scale competitive exclusion, local displace­
ment, and fitness reduction/population change differed between haustellate and
mandibulate herbivores (X2 = 6.04, P = 0.049), a difference largely attributable
to a higher incidence of competitive exclusion (11 vs 3%) for sap feeders, and a
higher frequency of local displacement (49 vs 37%) for mandibulate herbivores.
The consequences of competition also differed significantly between mandibu­
late herbivores feeding in internal and external niches (X2 8.49, P = 0.014).
Local displacements occurred much more frequently among species in con­
cealed feeding niches than in external feeders (59 vs 26% respectively). The high
incidence of local displacement observed for mandibulate herbivores in con­
cealed niches was associated with interference competition (direct killing in
many cases), a mechanism that predominated for internal compared with
external feeders (X2 = 32.10, P = 0.001; Table 1). Interference competition was
also more prevalent among internal feeders than in interactions between internal
and external feeders (X2 = 9.12, P = 0.011).
Surprisingly, the frequency of exploitative and interference competition does
not differ significantly between haustellate and mandibulate guilds (X2 = 3.58,
P = 0.167; Table 1). However, the nature of the interference mechanism does
seem to differ. Overt killing and chemically mediated deterrence are more
characteristic of mandibulate herbivores (e.g. 17, 139, 144, 166, 178), while
emigration stimulated by bodily contact and space preemption are more com­
mon for sap feeders (e.g. 41, 88, 100, 114, 123, 124).
=
FACTORS MEDIATING INTERSPECIFIC COMPETITION
Host plant-related factors. natural enemies. physical factors. and intraspecific
competition are all thought to maintain herbivore densities at low levels where
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308
DENNO, McCLURE & OTI
interspecific competition is rare (107). Recent reviews of competition have
also emphasized the importance of plant resources and natural enemies as
significant factors mediating interspecific interactions (34, 48, 49, 83, 1 40). In
this section, we explore how these factors mediate the intensity and outcome
of interspecific competition.
In the assessed studies, host plant factors (immediate, delayed, and textural
effects combined) mediate more interspecific interactions (n = 77) than natural
enemies (n = 24), physical factors (n = 1 5), and intraspecific competition (n
= 29). A comparison between haustellate sap feeders (n = 68) and mandibulate
phytophages (n = 72) shows that mandibulate herbivore interactions are me­
diated by host plant-related factors more frequently than are interactions be­
tween sap feeders (67% vs 38%); natural enemies influence these groups to
approximately the same extent ( 1 5% vs 1 8%), and physical factors (6% vs
1 6%) and intraspecific competition ( 1 2% vs 28%) mediate mandibulate her­
bivore interactions less often than they affect those of haustellate insects (X2
= 1 2.63, P = 0.006). This pattern, however, may in part reflect the current
flurry of research on the effects of induced changes in plant nutrition or
chemistry on the performance of later-feeding mandibulate species (57, 75,
78, 79, 8 1 , 1 36, 1 37, 1 85), a phenomenon seldom studied with sap feeders
(but see 1 14; RF Denno & J Cheng, in preparation).
Host Plants
Many interspecific interactions between phytophagous insects can be intensi­
fied through induced changes in plant nutrition or allelochemistry (75, 8 1 , 1 1 1 ,
1 1 4, 1 45, 1 85). Induced changes may occur immediately and affect the per­
formance of cooccurring species (short-term effect), or they may persist and
adversely alter the fitness of potential competitors in subsequent generations
or seasons (delayed effect).
Abundant evidence indicates that competitive interactions between sap feed­
ers intensify as heavy feeding causes host plants to rapidly deteriorate and
plant nutrition to decrease (4 1 , 1 14). Under such conditions, aphid survival
and population growth decline dramatically (82, 88, 1 75) and emigration
(walking) to neighboring plants increases (9, 43, 88, 175). Large-scale dispersal
also occurs in aphids, when alate forms are selectively produced in interspecific
aggregations ( 1 00). Similarly, for planthoppers interspecific crowing with
Prokelisia dolus triggers the production of migratory forms in Prokelisia
margillata, which results in the selective emigration of P. margillata from
shared habitats (4 1 ) . For both aphids and planthoppers, the triggering of mi­
gratory forms is mediated in part by feeding-induced changes in host-plant
chemistry (37, 39, 4 1 ).
Short-term induced changes in host-plant nutrition and allelochemistry me­
diate interactions between scale insects and adelgids as well. For example,
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COMPETITION IN PHYTOPHAGOUS INSECTS
309
contemporaneous feeding by nymphs of the scale Fiorinia externa significantly
reduces the nitrogen available in young hemlock foliage, which in tum dra­
matically decreases the survival of the scale Nuculaspis tsugae ( 1 1 4). Also,
heavy feeding by the adelgid Pineus boerneri causes resinosis on the bark of
pines, which forces it to feed on needles, where it displaces Pineus coloradensis
( 1 1 6, 1 17 , 1 23).
Short-term induced changes in plant nutrition also mediate interspecific
interactions between mandibulate herbivores. Examples include leaf mining
by the agromyzid Chromatomyia syngenesiae that reduced plant nitrogen and
decreased the growth rate of the root-feeding chafer Phyllopertha horticola
( 1 1 1 ), and plant fertilization that diminished competition between the grass­
hoppers Arphia conspersa and Pardalophora apiculata (145).
Feeding by early-season folivores can also induce long-term changes in plant
quality that can influence the choice of feeding and oviposition sites and hence
the performance of free-living herbivores that feed later during the season. For
example, when fed birch leaves that were artificially damaged to simulate
feeding by the spring defoliator Epirrita autumnata, free-living Lepidoptera
and sawflies exhibited reduced growth rates and/or survival (75, 81, 1 36),
probably as a result of induced phenolics (81). Spring-damaged leaves tended
to adversely affect the performance of mid-season herbivores to a greater extent
than late-season herbi vores (75). Similarly, the growth rate (186), survival
(137), fecundity (78), and density (57) of several other species of free-living
herbivores declined following the damage-induced deterioration of foliage.
Changes in leaf quality can also mediate interactions between free-living
folivores and late-season leaf miners (48, 49). Earl y-season feeding on oaks by
caterpillars of Operophtera brumata and Tortrix viridana (natural and simulated
damage) reduced leaf nitrogen, which adversely affected the survival of Phyl­
{ol1orycter spp. leaf miners (185). Larvae of several species of free-living
Lepidoptera consistently avoided the mined leaves of birch but showed variable
responses to chewed leaves (79). However, larval feeding preferences in this
study were not related in any simple way to induced changes in leaf chemistry.
Survival and development of late-season leaf miners on oak were also
negatively influenced on previously damaged leaves (47-49). Although in­
duced leaf chemistry was implicated in delayed development (46, 49), an
important source of mortality for leaf miners was parasitism, which was sig­
nificantly higher on damaged compared with intact leaves (46-48, 50, 51).
Although parasitoids may be selec tively attracted to damage related changes
in leaf chemistry, structural damage alone affected rates of leaf miner attack
(50). Nonetheless, some leaf miner species avoid ovipositing on previously
damaged leaves, apparently because rates of development, leaf abscission, and
parasitism are elevated (46, 47, 49).
Delayed plant-mediated interspecific interactions also occur for sap feeders,
-
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DENNO, McCLURE & OTT
but these are less well studied. Previous feeding by the scale insect F. externa
dramatically reduced the performance of the next generation of N. tsugae
feeding on the same tree (114). The same result occurred for the planthopper
Prokelisia marginata, whose fitness was diminished when plants were fed
upon by previous generations of Prokelisia dolus (RF Denno & J Cheng, in
preparation). In both of these systems, feeding-related reductions in plant
quality intensified competition.
Interactions between phytophagous insects can also be mediated through
herbivore-produced modifications in plant parts that alter the ability of other
herbivores to utilize those structures. For example, the scolytid beetle Cono­
phthorus resinosae severed the vascular system of pine cones, rendering them
unsuitable for attack by the coneworm Dioryctria disc/usa (112). Flower-bud
feeding by the cecidomyid Arcivena kielmeyerae altered the stamens so as to
preclude subsequent feeding by the weevil Anthonomus biplagiatus (25), and
larvae of the fly Urophora af
f inis
suitable for oviposition by Urophora quadrifasciata (16). Similarly, stem galls
of the sawfly Euura lasiolepis reduced new leaf production, which decreased
the availability of oviposition sites for other sawfly species (63). Foraging by
larvae of O. brumata interfered with the leaf-rolling ability of T. viridana,
which resulted in the latter species' desiccation and death (87).
Plant phenological events can also mediate interactions between phyto­
phagous insects. Synchrony of O. brumata larval eclosion with bud break
drives the population dynamics of this oak-feeding lepidopteran (86). Thus,
despite its superior competitive ability over T. viridalla, stochastic variation
in bud break dictates the intensity of the competitive interaction between these
two species (86, 87). Herbivorous insects feeding in the bracts of Helicollia
spp. plants have a very narrow window of opportunity for oviposition (155,
156). Thus, the extent to which these insects compete is dictated by the
probability of simultaneous colonization (155, 156).
Genetic and environmental variability in plant resistance can also mediate
the intensity and frequency of competitive interactions. For example, the leaf­
galling aphid Hayhurstia atriplicis drastically affected the survival of the
root-feeding aphid Pemphigus betae, but only on susceptible plant genotypes
(135). The intensity of competition among several species of gall-making
sawflies depended on host plant clone (60). The presence of balsam aphids
(Mindarus abietinus) reduced the survival of budworms (Choristoneurafumif­
erana) but only on fir trees susceptible to aphid attack (113). Similarly, the
fecundity of the sawfly Neodiprion edulicolis was reduced in the presence of
the stem worm Dioryctria albovitella, but only on pine genotypes susceptible
to attack from stem worms (134). Only on stressed trees in ornamental plant­
ings (85, 119), and on trees at the edge of their natural range (118), did densities
of several homopterans reach competitive levels.
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COMPETITION IN PHYTOPHAGOUS INSECTS
311
Vegetation texture (plant spacing, patch size, and species composition) can
also dictate interactions between phytophagous insects. Following the removal
of Phyllotreta crucifreae, competitive release of Phyllotreta striolata was
observed, but only in dense plantings in which these collard-feeding flea
beetles could easily move among plants (96). Interactions between two aphid
species (genus Uroleucon) were more intense on small patches of Solidago
altissima than on single stems (43). With the removal of the bug Neacoryphus
bicrucis, several sap-feeding and mandibulate species exhibited a short-term
competitive release, which lasted longer in small than in large patches of
Senecio smal/ii because bugs recolonized small patches more slowly (129).
Finally, the survival of the bug Megalocera recticornis was reduced by another
bug, Notostira elongata, but the competitive effect was removed in the pres­
ence of an alternate host plant species that acted as a refuge for the inferior
competitor (70).
Natural
Enemies
Natural enemies are frequently espoused as maintaining populations of phy­
tophagous insects below competitive levels (9, 106, 107, 148, 173, 174). The
few experimental studies that bear on this hypothesis, however, offer conflict­
ing evidence. Edson (43) experimentally removed invertebrate predators from
patches of S. altissima and found that the densities of two aphid species
(Uroleucon) increased as did interspecific competition. Similarly, the exclu­
sion of parasitoids resulted in increases in normally low-density populations
of hemlock scale insects and in interspecific competition (119). In contrast,
Karban (92-94) showed that populations of three folivores on Erigeron glaucus
were each affected strongly by only one biotic factor: spittlebugs by interspe­
cific competition, plume moths by vertebrate predation, and thrips by clonal
variation. Because the factor that was most important for each herbivore
species did not interact with the other biotic factors, it would be difficult to
conclude that predation mediated competitive interactions (94). Miller (131,
132), by experimentally removing combinations of competitors and natural
enemies, showed that interspecific competition accounted for 5 1 % of the
mortality in bark beetle (Ips calligraphus) populations, whereas enemies ac­
counted for only 38% of mortality. In this instance, foraging by the major
wood-boring cerambicid competitor (Monochamus titillator) also killed the
nonmobile natural enemies of I. calligraphus. Exclusion of natural enemies
did not temper the adverse effect of previous herbivory on the performance of
several birch-feeding herbivores (57). Similarly, predators and parasitoids did
not prevent intense interspecific competition among the insect herbivores
feeding on the flower heads of thistles (188).
Introduced herbivores are often deficient of natural enemies as are pest
species in managed habitats as a result of control practices (28, 72). Thus, a
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DENNO, McCLURE & orr
higher incidence of competition between introduced species or species in
managed habitats may provide indirect support for the hypothesis that natural
enemies diminish competitive interactions. In support of this hypothesis, we
detected interspecific competition more frequently in introduced systems (91 %
of 45 interactions) than in systems comprised of native herbivores (77% of
136 interactions) (X2 = 3.88, P = 0.049). Interactions between scale insects and
adelgids on hemlock ( 1 14, 1 1 5, 1 19, 1 22) and pine ( 1 20, 1 2 1 , 1 24), studied
in their native Japan and in eastern North America where they have been
introduced, provide a striking example of the mediating role of natural enemies.
In Japan, natural enemies usually maintain densities below competitive levels.
In contrast, in North America where specialized natural enemies are largely
ineffective, these insects fiercely compete to the point of competitive exclusion
in regions of overlap. Similarly, severe competitive interactions often take
place between herbivorous insects that have been serially introduced without
natural enemies to control noxious weeds (84). Competition, however, was no
more frequent in managed (90% of 42 interactions) than in natural habitats
(78% of 1 39 ihteractions) (X2 = 3 . 1 7, P = 0.075).
Alternatively, novel host plant associations for introduced herbivores may
foster increased densities and competitive interactions. For example, intro­
duced homopterans attain high densities and compete on new hosts but rarely
compete on native hosts with which they have had a long-standing association
( 1 19, 1 24).
Also, mandibulate herbivores in concealed feeding niches experience a
higher incidence of interspecific competition than free-living herbivores in
exposed niches (X2 = 1 1 .90, P = 0.00 1 ; Table 1 ) with presumably more
enemy-related mortality (73). This observation is consistent with the view that
natural enemies can moderate interactions between some phytophagous in­
sects.
Besides influencing the intensity of interspecific competition, natural ene­
mies may also alter the outcome of competition between two species. Whether
enemies promote coexistence or accelerate exclusion appears to depend on
which herbivore suffers most from attack. Increased enemy attack on the
inferior competitor may hasten its reduction or exclusion. For instance, the
shift of a bivoltine shared parasitoid to the second generation of the scale insect
N. tsugae accelerated its exclusion by the univoltine and competitively superior
F. externa ( 1 1 5 , 1 22). Likewise, elevated attack of yellow scale Aonidiella
citrina by shared parasitoids hastened its exclusion from citrus orchards by
California red scale Aonidiella aurantii, �hich is the better competitor (35).
A shared parasitoid also tipped the competitive balance between two leafhop­
per species with similar competitive abilities (158). The replacement of Eu­
rythroneura elegantula by Eurythroneura variabilis in the vineyards of
California resulted from selective attack on E. elegantula eggs, which were
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COMPETITION IN PHYTOPHAGOUS INSECTS
313
inserted closer to the leaf surface and consequently experienced greater para­
sitism ( 158). Furthermore, the aphid Panaphisjug/andis experienced dramatic
density increases in commercial walnut orchards following suppression of the
competitive dominant Chromaphis juglandicola by a parasitoid ( 1 30).
When the bark beetles Dendroctonus ponderosae and Ips pini were experi­
mentally forced to simultaneously colonize pine trees, D. ponderosae suffered
directly from competition for phloem resources but also incurred greater mor­
tality from parasitoids and predators, some of which were normally associated
with and attracted by the pheromones of I. pini (15). In this case, interspecific
competition and enemies acted in concert.
Natural enemies also indirectly intensify interactions between eady season
folivores and late season leaf miners. For example, rates of leaf miner para­
sitism were higher on chewed leaves than on intact ones (46, 47, 50, 51), which
resulted from parasitoid attraction to physical damage (50) and perhaps leaf
chemical cues as well (49).
Evidence also suggests that some aphids compete for the services of tending
ants, which increase aphid persistence by deterring invertebrate predators (3,
4, 32). Thus, mutualistic ants can have a positive effect on aphid population
size, thereby increasing the potential for interspecific competition (4).
Physical Factors
Weather-related factors mediate competitive interactions more frequently be­
tween sap feeders ( 16% of 68 interactions) than between mandibulate herbi­
vores (6% of 72 interactions). The disproportionate susceptibility of sap feeders
to physical factors may be related to their relatively small size and exposed
feeding niches. For instance, heavy rain and wind reduced the densities of
Eurythroneura leafhoppers on sycamore below competitive levels ( 1 26, 1 27).
Sap feeders may also be more sensitive to plant stress reSUlting from adverse
weather ( 1 0 1 ).
Differential temperature tolerance can also dictate competitive outcome.
Tropical species of rice-feeding Nephotettix leafhoppers out-competed tem­
perate species under warm rearing conditions, but the reverse occurred when
they were raised under cooler conditions ( 1 80). The psyUjd Arytaina spartii
undergoes egg diapause and is more cold tolerant than its competitively supe­
rior congener A. genistae ( 1 83). However, the early hatch of A. spartii eggs
in spring allows nymphs to preempt buds before the superior competitor is
active.
For mandibulate herbivores, subtle changes in physical conditions can also
shift the competitive result. Because developmental optima differ, the bruchid
Callosobruchus chinensis excludes Callosobruchus maculatus at 30oe, but a
2°e increase completely reverses the outcome (64). The subtropical fruit fly
Dacus dorsalis readily out-competed the subtemperate Dacus capitata in cooc-
314
DENNO, McCLURE & OTT
cupied fruits at low elevations in Hawaii, but D. capitata dominated at higher
elevations (97). Similarly, the buprestid Agrilus hyperici persisted in only
shaded habitats where the chrysomelid Chrysolina quadrigemina, the superior
competitor in sunny sites, was at a developmental disadvantage (84).
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Intraspecific Competition
Evidence supporting the view that intraspecific competition diminishes the
intensity of interspecific competition is mixed (44, 1 26). For example, in only
40% of the 70 species for which data were available was intraspecific greater
than interspecific competition. Interspecific competition equaled or exceeded
intraspecific competition for 8 ( 1 1 %) and 35 (50%) species, respectively.
However, there was a slight tendency for intraspecific competition to be greater
than or equal to interspecific competition more frequently for sap feeders (60%
of 42 interactions) than for mandibulate species (39% of 28 interactions) (X2
= 2.7 1 , P = 0.099). In some sap feeders, intense intraspecific competition seems
able to moderate interspecific interactions. The best evidence comes from
Eurythroneura leafhoppers on sycamore and Eupteryx leafhoppers on nettles,
in which strong intraspecific competition diminished but did not preclude
interspecific interactions ( 1 26, 1 65). Additional evidence indicates that intra­
specific compctition is a more important mortality source for leaf miners than
interspecific competition ( 1 9, 5 1 ).
However, in the Homoptera (4 1 , 1 14, 123, 124, 1 83) and chewing insects
(3 1 , 87) strong intraspecific competition in the competitive dominant often
does not deter extreme adverse affects on the competitive subordinate. For
instance, 1 4 of the 1 5 species we were able to evaluate experienced a higher
degree of intraspecific competition than interspecific competition, yet the
adverse effects of each species were greater on its competitor than on itself.
Perhaps the extent to which intraspecific competition tempers interspecific
interactions depends on the symmetry of the interspecific interaction. If the
interactions are symmetric, as was the case for the two leafhopper systems
( 126, 1 65), then strong intraspecific effects may dampen interspecific ones.
However, if interspecific interactions are very asymmetric, as is the case for
most phytophagous insects (Table 1), then strong intraspecific effects in the
superior competitor may not preclude a significant interspecific impact on the
inferior competitor.
It has often been assumed that intraspecific competition is a prerequisite for
interspecific competition (see 174). In one instance, however, spittlebugs ac­
tually benefited from conspecifics, but suffered badly in the presence of plume
moth competitors (94). Furthermore, in our analysis, interspecific competition
was far more important than intraspecific competition for 27 of 28 species for
which data were available. In fact, 1 4 of these species experienced regional
or local competitive exclusion (8, 1 8, 7 1 , 84, 97, 1 1 4, 123-125). Also, for
COMPETITION IN PHYTOPHAGOUS INSECTS
315
herbivores that compete via interference mechanisms (aggression or deterrent
chemicals), interspecific competition may occur despite abundant food re­
sources and diminished intraspecific competition ( 1 7 , 54, 55, 7 1 , 109, 1 10,
143, 166, 1 78). These examples cast doubt on the premise that intraspecific
competition is a necessary requirement for interspecific competition.
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Interplay of Factors Mediating Interspecific Competition
Given the experimental information available, it is difficult to champion one
particular factor as mediating competitive interactions or inflicting the most
mortality on phytophagous insects, even within a given system. For example,
in the community of insect herbivores feeding on E. glaucus, no single factor
(interspecific competition, natural enemies, or host plant clones) explained the
organization of this community because each factor was most important for a
different herbivore species (94). For two aphid species on goldenrod, abun­
dance was dictated by the dynamic interaction of interspecific competition,
predation, and dispersal in response to induced changes in plant quality (43).
Several two-factor studies also show that interspecific competition can be the
most important source of mortality as often as natural enemies and host plants.
Of the 1 3 natural systems in which the relative importance of these factors
was reported, interspecific competition was most influential in 6 (9, 57, 13 1 ,
183, 185, 188), natural enemies were most important in 5 ( 1 9, 46, 47, 1 19,
173), and host plant factors were most consequential in 2 (63, 87).
Although the evidence that host plants, natural enemies, and physical factors
mediate certain competitive interactions is compelling, sweeping generalities
concerning their impact are often unjustified. Herbivore life histories can vary
widely (e.g. mobility, aggregation, body size, feeding niche), and these differ­
ences may be equally important in arbitrating competitive interactions (see
94).
LIFE HISTORIES AND FEEDING STYLES THAT
INFLUENCE COMPETITION
Certain life history traits (mobility or aggregation) and feeding styles (feeding
niche, diet breadth, and host plant growth form) may influence the probability
for competition in phytophagous insects. Herbivores that are immobile and
have little ability to switch host plants may be more likely to experience
competition (94). Our analysis supported this hypothesis. Sessile herbivores
competed in 89% of 71 interactions, whereas mobile herbivores competed in
only 76% of 111 interactions (X2 4.54, P = 0.033). This pattern was strongest
for mandibulate herbivores, in which competition was detected in 89% of 56
interactions involving sessile species (e.g. leaf miners, wood borers, root feed­
ers), but in only 69% of 68 interactions involving mobile herbivores such as
=
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316
DENNO, McCLURE & OTI
free-living grasshoppers and caterpillars (X2 = 6.76, P = 0.009). Similarly, for
mandibulate species that develop within a discrete resource (fruit, seed, cone,
inflorescence, stem, gall, or leaf), competition was detected more frequently
(86% of 43 interactions) than it was for their less confined counterparts (free­
living folivores and wood borers; 68% of 65 interactions) (X2 = 4.4 1 , P =
0.036).
Although aggregation in the superior competitor is thought to promote
coexistence by providing refuges for the inferior competitor ( 1 0), aggregation
in the same niche for reasons related to plant quality may facilitate interspecific
interactions (41 , 1 14, 1 24). Under these circumstances, contact among indi­
viduals is frequent and the group may modify plant nutrition or induce plant
chemistry in ways that intensify plant-mediated interactions (41, 1 14). Indeed,
we found that competition occurred more frequently for pair-wise interactions
involving aggregated herbivores (89% of 83 interactions) than it did for inter­
actions involving only solitary species (74% of 35 cases) (X2 = 3.99, P = 0.046),
a pattern documented previously (34). The aggregated distributions of sap
feeders and wood borers contributed heavily to this result.
Phenotypic trade-offs between life history traits such as dispersal and fe­
cundity (40) may preclude an herbivore from being both a successful disperser
and a superior competitor if competitive ability depends on fecundity and rapid
population growth. Thus, phytophagous insects exploiting ephemeral habitats
may be destined to competitive inferiority. Evidence from the free-living
Homoptera and Hemiptera supports this hypothesis. In 10 of 13 interactions
that could be assessed, the relative loser was a better disperser than was the
winner ( 1, 4 1, 43, 69, 70, 88, 1 14, 124, 129, 175), and dispersal ability was
equivalent in the remaining 3 species pairs. A balance between dispersal and
competitive ability among species exploiting ephemeral and patchy resources
is thought to promote coexistence ( 1 0, 1 60). Coexistence occurs because the
inferior competitor can emigrate to unoccupied habitats, a phenomenon well
demonstrated for several homopterans (41, 43, 88, 175). High fecundity, how­
ever, was not associated with competitive ability. Across all herbivore guilds,
the winner tended to be no more fecund than the loser (winner > loser in 1 6
cases, and winner < loser i n 20 interactions).
Body size does appear to influence competitive outcome. Across all guilds, the
superior competitor was larger than the inferior competitor in 4 1 interactions,
equal in size in 17 interactions, and smaller in size in 20 interactions. This trend
was particularly strong for mandibulate herbivores (winner > loser in 32 cases,
winner = loser in 5 cases, winner < loser in 10 cases), whereas in sap feeders, size
did not appear as important in dictating competitive superiority (winner > loser
in 6 cases, winner = loser in 12 cases, winner < loser in 7 cases) (X2 = 1 3 .7 1 , P =
0.00 l ). In many direct interactions involving mandibulate herbivores, particu­
larly stem borers, seed feeders, and root feeders, the competitive success oflarger
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COMPETITION IN PHYTOPHAGOUS INSECTS
317
individuals was achieved by overt overpowering and killing of opponents via
aggressive biting behavior (24, 1 43, 1 48, 1 66, 1 78), or by inadvertent killing
while foraging ( 1 39, 1 68). Such behavior is less possible for sap feeders, which
may explain the poor association between large body size and competitive
success in this guild. Nevertheless, there are a few hemipterans and homopterans
in which large body size and/or aggressiveness confers competitive superiority
in direct interactions (6, 70, 1 29).
One might hypothesize that multivoltinism (independent of body size) could
contribute to rapid population growth and competitive superiority, especially
for species that interact exploitatively. We found no overall support for this
hypothesis. The superior competitor underwent more generations per year than
did the inferior competitor in 9 cases, fewer generations in 1 2 cases, and their
voltinism was the same in 82 instances. Several examples illustrate why having
more broods per year is not necessarily a competitive advantage. Any advan­
tage the bivoltine psyllid A rytaina genistae gains in autumn is offset in spring
because the univoltine Arytaina spartii appears first and preempts most feeding
sites ( 1 83). Additionally, the numerical advantage of bivoltinism in the scale
insect N. tsugae is offset by increased parasitism from a parasitoid shared with
its univoltine competitor F. externa. When the latter scale insect becomes rare
in fall, the parasitoid shifts to N. tsugae. Furthermore, the high rate of para­
sitism accelerates the exclusion of the bivoltine scale from cohabited forests
( 1 1 5 , 1 22). In some cases, however, a second generation may provide a refuge
for the inferior competitor and promote coexistence ( 1 6, 69). Finally, although
having a shorter life cycle and producing more broods per year than one's
competitor confers an advantage under constant conditions, this advantage is
less likely to be realized in temperate habitats because life cycles are resyn­
chronized every winter ( 1 3) .
Arriving at a resource first allows some species to gain the numerical, and
consequently, the competitive edge (43, 54, 84, 1 1 0, 1 1 2, 1 14, 1 83). Early
arrival can result either from advanced seasonal emergence (84, 1 14, 123, 1 83)
or rapid colonization (54, 1 10). Early arrival tends to confer competitive
superiority when coupled with rapid population growth and/or the preemption
of resources that results from physical exclusion ( 1 1 4, 1 83) or chemical de­
terrence (54, 1 1 0). When the advantage of early arrival was experimentally
removed, the scale insect F. externa lost its competitive superiority ( 1 1 4).
The Homoptera possess many life history traits that promote competitive
interactions, including rapid population growth (41 , 88, 1 75), aggregation
(reviewed in 4 1 ), sessile behavior throughout much of their life cycle (6, 35,
92, 1 1 4, 123, 1 24, 1 26), and feeding on a common phloem resource ( 1 35).
The frequent combination of these traits in the Homoptera may partly explain
their over-representation in studies demonstrating competition (4 1 , 92, 1 35,
1 74) (Table 1 ) .
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DENNO, McCLURE & OTT
Dietary specialists may incur increased competition because they do not
have the option of switching to alternative host plant species. In contrast, the
metabolic costs and foraging styles associated with feeding on a chemically
diverse array of plants may influence the competitive ability of polyphagous
species. Regardless, we found no evidence to suggest that the frequency of
competition differed between monophages (83% of 1 1 7 interactions) and
polyphages (74% of 65 interactions) (X2 = 2.09, P = 0. 1 48). However, for most
interactions involving polyphages, competition was tested with only one host
plant species present. This caveat is noteworthy because the presence of an
alternate host plant species reduced competition between the two hemipterans
N. elongata and Megaloeera reetieornis (70). Also, competitive interactions
between polyphagous grasshoppers resulted in shifts in the proportion of mono­
cots and dicots in their diets ( 1 45). These examples suggest that polyphagy
may provide feeding options that diminish competitive interactions for some
species.
Competitive interactions may be less intense on large, more architecturally
diverse plants on which herbivores may be able to escape from one another
(see 34). We found that the growth form of the host plant did affect the
likelihood of competition. Interspecific competition occurs less frequently on
trees and shrubs (74% of 1 00 interactions) than on forbs and grasses (87% of
82 interactions) (X2 = 4.27, P = 0.039).
TAXONOMIC RELATEDNESS AND INTERSPECIFIC
COMPETITION
Competition may be more likely to occur between closely related taxa because
of similarity in feeding niche ( 1 33). In support of this hypothesis, interspecific
competition was detected in 1 00% of 44 interactions involving congeneric
species pairs. In contrast, competition occurred in only 74% of 1 37 noncongen­
eric interactions (X2 = 7 .07, P 0.008). However, even though closely related
taxa competed more frequently, competition was still common between non­
congeneric pairs, 41 of which were interordinal interactions.
=
LINK B ETWEEN RESOURCE PARTITIONING, NICHE
SHIFTING, AND INTERSPECIFIC COMPETITION
Sharing the same feeding niche is thought to intensify competition between
two species. Conversely, spatial and temporal differences in the use of re­
sources may diminish competitive interactions ( 1 5 1 , 1 52). In support of this
classical view, severe competition between phytophagous insects often occurs
when they share an identical niche (4 1 , 43, 92, 1 66, 1 83). For example, several
competitive exclusions involving sap feeders have occurred in species that
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COMPETITION IN PHYTOPHAGOUS INSECTS
319
prefer to feed in the same microhabitat on the plant ( 1 14, 1 23, 1 24). Also, of
four species of aphids on bean plants, the two species sharing the same feeding
site competed more intensively than those exhibiting microhabitat segregation
(82). Regarding the moderating effects of resource partitioning on interspecific
interactions, we found substantial evidence that temporal and spatial differ­
ences in resource use can dampen, although not necessarily preclude, compe­
tition. Here we explore experimental evidence for an association between
resource partitioning and reduced competition, and the use of shared resources
and niche shifting.
The widespread evidence for competitive interactions between early-season
and mid- to late-season feeders via altered plant chemistry (57, 75, 78, 79, 8 1 ,
1 36, 1 37, 1 85) suggests that temporal displacement does not necessarily pre­
vent competition. However, several manipulative experiments suggest that
temporal partitioning may reduce interspecific competition for some species.
Leaf miners normally feed later in the season than do many free-living leaf
chewers (49, 1 85). By experimentally forcing a generation of the miner Phyl­
lonorycter spp. to emerge in the spring and thereby cooccur with leaf chewers,
the miner' s fitness was much lower than it was in the naturally occurring
summer generations ( 1 85). Despite a more nutritious plant resource in spring,
miner survival was adversely affected by leaf damage-related interactions with
chewers.
Similarly, the bark beetle D. ponderosae attacks living pines, while I. pini
usually follows by exploiting dying trees ( 1 42). Experimentally forced syn­
chrony of these beetles resulted in drastic reductions in the survival of D.
ponderosae, which was attributable to direct competition with I. pini as well
as increased mortality from the predators and parasitoids normally associated
with I. pin; ( 1 5, 1 42). The observation that enemy pressure can be reduced by
the temporal partitioning of resources is consistent with the view that herbi­
vores compete for enemy-free space ( 1 2, 1 40).
Reciprocal avoidance of aggregation pheromones in bark beetles deters
colonization and contributes to their spatial segregation both within and among
trees ( 1 7 , 20, 22, 55, 1 09, 1 1 0, 1 38, 1 82). Furthermore, in the absence of a
competitor, bark beetles occupy broader niches than they do in mixed species
populations (30, 1 38, 1 42). Notably, when beetles that normally partition
resources are forced to interact experimentally, severe competition can ensue
( 1 1 0, 142).
During oviposition, females of Callosobruchus maculatus beetles mark
beans with a chemical that inhibits oviposition by Callosobruchus rhodesien­
sis, forcing them to place eggs elsewhere (7 1 ) . When these two bruchid species
are confined together in mixed culture, C. maculatus excludes C. rhodesiensis
(7 1). Similarly, on large-sized beans, Callosobruchus anaUs feeds in the center
of the bean and Callosobruchus phaseoli feeds near the outside surface; this
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DENNO, McCLURE & orr
microhabitat segregation allows these bruchids to coexist ( 1 78). When these
species are reared together on small beans, partitioning of the bean is precluded,
and C. analis excludes C. phaseoli ( 1 77, 1 78).
In contrast, the spatial segregation of the host plant by many sap-feeding
insects does not appear to preclude interspecific competition ( 1 , 82, 88, 1 23,
1 75). In these cases, competition may result from the sharing of a common
phloem resource, because even foliar-feeding and root-feeding sap feeders can
compete intensively ( 1 35). Similarly, mandibulate folivores may induce chemi­
cal changes in plants that adversely impact other species, especially immobile
ones, elsewhere on the plant (34).
We found numerous cases of niche shifting in the presence of a competitor
(or previous damage), whereby a species was relegated to a poor feeding site
( 1 1 4, 1 23, 1 24, 1 34, 1 57), a different feeding or oviposition site ( 17, 20, 46,
47, 52, 54, 7 1 , 79, 9 1 , 99, 1 09, 1 12, 1 38, 144, 1 63), a different host plant
species (70, 1 45), or a different portion of the habitat (35, 4 1 , 97, 1 00, 1 30)
.
In one case, the presence of a competing bruchid species promoted the rapid
adaptation of another bruchid species to a novel host plant species (176). In
several of the above cases, niche shifting was mediated by chemicals (inter­
ference mechanism) produced by one herbivore that deterred colonization ( 1 7 ,
20, 1 09, 1 38), feeding ( 1 44), o r oviposition b y another (52, 54, 7 1 , 9 1 , 99).
Another common response to interspecific crowding is emigration to nearby
plants (9, 43, 69, 82, 88, 1 29, 1 63) or distant habitats (41 , 1 00). Emigration
triggered by heterospecifics is better documented for sap feeders ( 1 3 cases)
than it is for mandibulate herbivores (1 case). Emigration deters local exclusion
in aphids because as mixed species aggregations contribute to the rapid demise
of the current plant, the inferior competitor colonizes neighboring healthy
plants (88). Although emigration allows an insect to escape the effects of
interspecific crowding, enemy-related risks may be associated with movement
(146).
Even though interspecific competition results in niche constriction or shift­
ing for some phytophagous insects, for others the niche does not change in the
absence of competitors. For instance, the distribution of Mordellistena splen­
dens within stems did not differ between populations with and without an
important competitor ( 1 66). Similarly, the distribution of Eriosoma spp. gall
aphids on the leaves of elm did not differ between regions of allopatry and
sympatry with a major competitor (6). Such observations have been used to
suggest that niche divergence does not necessarily result from interspecific
competition (6).
We have presented substantial evidence that supports the classical view that
species sharing the same niche compete most severely, and that resource
partitioning can often moderate, but not necessarily preclude, interspecific
competition. Several studies have demonstrated that when normally displaced
COMPETITION IN PHYTOPHAGOUS INSECTS
32 1
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herbivores are experimentally forced to cooccur, intense competition results.
However, our analysis also suggests that traditional views of the relationship
between resource partitioning and competition must be modified to include
cases in which spatially segregated sap feeders compete via a shared phloem
resource, and cases in which temporally or spatially displaced folivores com­
pete through herbivore-induced changes in plant physiology.
INTERSPECIFIC COMPETITION AND REPULSED
DISTRIBUTIONS
Repulsed distributions of herbivores in the field have been used as evidence
for interspecific competition (36, 1 27, 1 84). Conversely, positive associations
have been called on to challenge the importance of competition ( 1 02, 1 70,
1 7 1). Here we present data for and against the relationship between interspe­
cific competition and herbivore distribution.
On the interplant scale, 25 of the species pairs we studied were negatively
associated. Of these, 10 were sap feeders (2, 35, 43, 1 14, 1 23, 1 24, 1 28, 1 30,
1 35, 1 58); 7 were stem borers ( 143, 1 66); 2 were wood borers ( 1 1 0, 1 42); 2
were fruit/cone feeders (97, 1 1 2); and 4 were involved interguild interactions
(3 1 , 94, 1 28). For 1 3 of these species pairs, strong experimental evidence
linked interspecific competition to repulsed distribution (3 1 , 43, 94, 1 10, 1 14,
1 23, 1 24, 1 28, 1 35, 1 42, 1 66).
In contrast, competition was not demonstrated between thrips and plume
moths, yet they showed a negative association in the field; differences in habitat
selection caused their lack of cooccurrence (93). Other species were positively
associated despite the occurrence of interspecific competition (43, 6 1 , 1 38,
1 82). Positive associations between potential competitors may result from both
species responding similarly to host plant variation (e.g. nutrition) for feeding
or oviposition ( 1 9, 6 1 ) . For some phytophagous insects, evidence also suggests
that feeding and oviposition sites are not chosen on the basis of competitor
presence or absence (9, 1 39). Together, these observations emphasize the
weakness inherent in inferring interspecific competition from insect distribu­
tional data (see 27, 80, 1 50).
FACILITATIVE INTERACTIONS BETWEEN
PHYTOPHAGOUS INS ECTS
We found 1 1 interactions between phytophagous insects that were facilitative
(Table 1). Four of these cases involved aphid species that showed increased
survival, development rate, or body size when in close proximity to another
herbivore species (56, 67, 98, 1 59). In three of these instances, one aphid
species selected the most nutritious feeding site on the plant, which happened
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322
DENNO, McCLURE
& OTT
to be adjacent to the nutrient sink created by an aggregation of a previously
established aphid species (56, 98, 1 59).
Also, feeding by one folivore (Lepidoptera) may stimulate plant regrowth,
which benefits other herbivores that feed later in the season (33, 1 86). How­
ever, an increase in the intensity of herbivory may change the herbivore
interaction from facilitation to competition. For instance, moderate herbivory
by the western tent caterpillar, Malacosoma californica, had positive effects
on the fall webworm Hyphantria cunea, but heavy defoliation conferred ad­
verse effects on performance ( 1 86). Similarly, Ips avulsus is attracted to trees
under attack by other bark beetle species, and the mixed species attack can
increase the probability of all the species securing oviposition sites as they
mutually defeat resin-based tree defenses (55, 1 38, 1 82). However, this initial
benefit does not preclude intense competitive interactions among species for
the best development sites (55, 1 38, 1 82). Thus, for some cases of facilitation,
positive effects are transient and give way later to competitive situations.
Most facilitative interactions were very asymmetric, with only one species
gaining an advantage. In one unusual interaction between the leaf miner C.
syngenesiae and the root-feeding chafer P. horticola, the leaf miner benefited
from root feeding whereas the root feeder was disadvantaged by foliar feeding
( 1 1 1).
Few if any of the aforementioned facilitative interactions represent tightly
coevolved relationships. However, some ant-tended lycaenid butterflies ensure
protection of their offspring by specifically ovipositing on plants with ants
already tending homopterans ( 1 1 , 1 62).
Finally, some studies demonstrating facilitation between herbivores and
detritivores have been incorrectly included in assessments of interspecific
interaction between "phytophagous insects" (26, 1 07). For example, the elegant
experimental studies of Seifert & Seifert ( 1 56) on the insect inhabitants of
Heliconia bracts actually involved several species that are detritivores (155,
1 56). All cases of facilitation reported in this community represented interac­
tions between an herbivore and a detritivore, which is not surprising when one
species increases food resources for another. The only two herbivore-herbivore
interactions studied were both weakly competitive.
SUMMARY AND PROSPECTUS
This review has reexamined the importance of interspecific competition in the
population biology of phytophagous insects. Our analysis of a greatly expanded
database, selected from all feeding guilds, demonstrates widespread evidence
for interspecific competition between phytophagous insects (76% of 1 93 pair­
wise interactions). Of all the guilds examined, competition was most frequently
detected among sap feeders, stem borers, wood borers, and seed and fruit
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COMPETITION IN PHYTOPHAGOUS INSECTS
323
feeders. Interspecific competition was least likely to occur between free-living,
mandibulate folivores. Most interspecific competitive interactions were mark­
edly asymmetric. This asymmetry may explain the lack of a general tendency
for intraspecific competition to diminish interspecific interactions.
Host plant factors mediated far more interspecific interactions than did
natural enemies, physical factors, and intraspecific competition combined. An
important consequence of variation in host plant chemistry may be the con­
centration of herbivores at optimal feeding sites, thereby predisposing them to
competitive interactions. The extent to which natural enemies direct competi­
tive interactions depends on which competitor is attacked. Selective attack of
the inferior competitor can promote competitive exclusion; concentrated attack
on the superior competitor may promote coexistence; and heavy attack on both
herbivore species may deter competition altogether.
Exploitative and interference mechanisms were equally frequent when all
herbivore species were considered as a whole. However, interference compe­
tition was more common in mandibulate herbivores living in concealed niches
(e.g. stem borers and seed feeders) compared with free-living species. For
mandibulate herbivores, but not sap feeders, competitive superiority was very
strongly associated with large body size and aggressive behavior.
Phytophagous insects were more likely to compete if they were closely
related (congeners), introduced, sessile, aggregative, and fed internally on a
discrete resource (e.g. seed, fruit, or stem) or fed on forbs or grasses as opposed
to trees or shrubs. Interspecific competition between herbivores occurred with
similar frequencies in managed and natural habitats.
Despite the widespread evidence for interspecific competition presented
here, a demonstration of the overall importance of interspecific competition
in the population and community ecology of phytophagous insects remains a
challenge. Several experimental studies in natural systems have specifically
addressed the relative importance of interspecific competition, natural enemies,
and host plant factors. The results of these studies indicate that competition
was as important as natural enemies and host plant factors in structuring the
community of herbivores (92-94), or that herbivore abundance was dictated
by the dynamic interaction of interspecific competition, predation, and disper­
sal in response to induced changes in plant quality (43). Two-factor compari­
sons in natural systems have also shown that interspecific competition can be
the most important source of mortality (9, 57, 1 3 1 , 1 83, 1 85, 1 88), as often as
natural enemies ( 1 9, 46, 47, 1 19, 1 73) and host plants (63, 87). These com­
parative studies, coupled with the paucity of experimental evidence against
interspecific competition (only 1 8% of 1 93 interactions), provide little support
for the claim that competition is a weak and infrequent force in phytophagous
insect communities. To the contrary, the existing experimental evidence for
this assertion is itself weak and infrequent.
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324
DENNO,
McCLURE & orr
Given the experimental data currently available, we conclude that there is
far more justification for retaining competition as a potentially important factor
than for dismissing it. Other recent assessments have drawn similar conclusions
regarding the potential importance of interspecific competition in phyto­
phagous insect communities (34, 48, 49, 94, 1 69). We argue, as have others
(34, 48, 49, 94), for the collective assessment of both intra- and intertrophic­
level factors in studies investigating the distribution and abundance of phyto­
phagous insects. Toward this end, sufficient evidence exists to call for the
resurrection of interspecific competition as a viable hypothesis warranting
serious consideration in future investigations of the structure of phytophagous
insect communities.
ACKNOWLEDGMENTS
Hans Damman, John Losey, Charles Mitter, Susan Mopper, and Merrill Pe­
terson critiqued an earlier draft of this review and provided many helpful
suggestions. Tim Paine, Douglas Ferguson, Tom Henry, Ronald Hodges, and
David Smith confirmed the diet breadth and various life ' history traits for
several species of Hemiptera, Coleoptera, Lepidoptera, and Hymenoptera. John
McAllister and Andie Huberty assisted with the monumental literature chase.
Ches Zeeb helped condense and catalogue host plant data and offered constant
direction. We are most appreciative to all of these colleagues for their assis­
tance and support. This research was supported in part by National Science
Foundation Grants BSR-86 14561 to RFD and DEB-9209693 to RFD and JRO.
This is Scientific Article Number A-6564, Contribution Number 8776 of the
Maryland Agricultural Experiment Station, Department of Entomology.
Any Annual Review chapter, as well as any article cited In an Annual Review chapter,
may be purchased from the Annual Reviews Preprlnts and Reprints service.
1-800-347-8007; 415-259-5017; email: [email protected]
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