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Gall Inducing Insects Provide Insights I
Gall Inducing Insects Provide Insights I
Field surveys of cynipid gall-inducer occurrences on Quercus species were conducted in Florida, North Carolina, and
Pennsylvania, USA. All cynipids demonstrated strong host species and organ fidelity. One result of this specialization is
effective niche partitioning among cynipids. The host-association patterns of these specialist herbivores should reflect sim-
ilarities among oaks, thus we clustered oak species according to their cynipid distributions. Cynipids distinguished small
differences among their hosts. A dendrogram of oak species based on cynipid distributions was largely congruent with
botanical arrangements. Cynipid occurrences offer information helpful to resolving some aspects of oak systematics. Col-
laborative efforts between taxonomic botanists and entomologists will be useful in resolving a variety of plant and insect
systematic problems.
Key words: classification; Cynipidae; Fagaceae; gall; host–plant association; insect–plant interactions; Quercus; system-
atics.
Many authors (e.g., Felt, 1917, 1940; Mani, 1964) feld, 1994), and Populus (Floate and Whitham, 1995)
have commented on the high level of specificity of gall have demonstrated that gall inducers can partially or al-
inducers to their host plants and to specific plant organs. most completely distinguish hybrid host plants from pa-
Although gall-inducing animals are broadly scattered rental hosts in hybrid zones. Furthermore, Cecidomyiid
across taxonomic lines (i.e., four kingdoms, two phyla, and Tephritid gall inducers were shown to discern sub-
two arthropod classes, and six insect orders), relatively species of the composite Chrysothamnus nauseosus
few plant groups account for most galls. Over 90% of (Floate, Fernandes, and Nilsson, 1996). It is likely that
those occurring in North America attack dicotyledonous the gall inducers respond to subsets of their host plant’s
plants and most of these infest only three families, Ro- genome that may not necessarily be expressed in tradi-
saceae, Compositae, and Fagaceae (Mani, 1964). This tionally utilized plant taxonomic traits. Therefore, the dis-
specificity is in part a consequence of the gall inducer’s tributions of gall inducers on plants may provide inde-
intimate relationship with its host plant (Shorthouse, pendent tests for plant relationships generated from mor-
1982; Raman, 1993). Gall insects must be able to induce phological, chemical, or genetic information. Similarly,
the appropriate host-plant reactions to produce the cell gall occurrences may enable discrimination of morpho-
proliferations that become specific galls (Cornell, 1983; logically similar plant species or hybrids from their pa-
Abrahamson and Weis, 1987). Thus, these insects are rental species (Floate, Fernandes, and Nilsson, 1996).
sensitive to small differences in host-plant physiology, The fidelity of cynipids (tribus Cynipini, Cynipidae:
chemistry, development, and phenology. As a result, gall Hymenoptera) to oaks demonstrates the degree of mo-
inducers may discriminate among closely related species nophagy among gall inducers. In North America, for in-
of host plants (Floate, Fernandes, and Nilsson,1996). In- stance, 87% of all cynipids attack species of Quercus
deed, biologists have used gall identity as a clue to plant (Fagaceae) and the host range of each wasp species is
identity and vice versa (Felt, 1917, 1940; Raman, 1996). generally restricted to one or a few related oak species
For example, studies of hybrids in Quercus (Aguilar and (Abrahamson and Weis, 1987). Burks (1979) listed 485
Boecklen, 1992), Salix (Fritz, Nichols-Orians, and Bruns- species of oak gall-inducing cynipids for North America
north of Mexico and additional species have been de-
1 Manuscript received 11 September 1997; revision accepted 29 De- scribed subsequently. Nearly 300 of these species occur
cember 1997. in the eastern United States. Although the final species
5 Correspondence to WGA at Bucknell University address.
6 Current address: Systematic Parasitoid Laboratory, Kelcz-Adelffy
totals are likely to be somewhat less than these numbers
(because of unpaired alternate generations currently
Str. 6, Koszeg 9730, Hungary.
The authors thank C. Abrahamson, J. Abrahamson, K. Ball, L. Bla- named as separate species), these numbers do suggest the
zure, R. Bowman, M. Chipaloski, T. Craig, D. Cronin, J. Cronin, M. richness of the Cynipini in North America.
Deyrup, M. Frey, J. Fitzpatrick, R. Hammer, J. Hardin, J. Itami, A. The genus Quercus is distributed worldwide but reach-
Johnson, I. Kralick, J. MacBeth, R. Melika, E. Menges, A. Menke, R. es its greatest species richness in the New World from
Peet, R. Roberts, P. Schmaltzer, A. Schotz, C. Shantz, C. Winegarner, southern Canada to Colombia (Nixon, 1993). The Flora
and M. Winegarner for field assistance and/or technical advice. Support
was provided by NSF grant and supplements BRS-9107150 to WGA,
of North America currently includes 90 species for the
the David Burpee endowment of Bucknell University, the Archbold region north of Mexico (Jensen, 1997; Nixon, 1997; Nix-
Biological Station, and a Smithsonian Institution National Museum of on and Muller, 1997), while Mexico is estimated to har-
Natural History grant to GM. bor 135–150 species (Nixon, 1993). This richness of spe-
1159
1160 AMERICAN JOURNAL OF BOTANY [Vol. 85
Fig. 3. Dendrogram of eastern United States host oaks clustered according to their cynipid gall-inducer communities. The dendrogram illustrates
the results of a hierarchical cluster analysis using between-group linkage and the Jaccard distance measure on binary (presence/absence) data.
very distinct from the other white oaks). The cynipid Q. velutina), but three host species, Q. texana, Q. laevis,
communities on these latter three oaks are very similar and Q. falcata, had positive loadings. White oaks, in con-
and are unique relative to other white oaks. We never trast, showed strong positive (Q. macrocarpa, Q. alba,
found any of the cynipid species that attacked these three Q. bicolor) to negative scores (Q. geminata, Q. virgini-
species on any other oak during our 7 mo of field work ana). Cynipid communities of white oaks varied from
in Florida. strongly positive scores (Q. stellata, Q. margaretta, Q.
In this analysis, ten component axes had eigenvalues chapmanii) to negative scores (Q. prinoides, Q. gemi-
over 1.0, which indicates that many of the cynipid com- nata, Q. virginiana) on axis 4. In contrast, red oak gall
munities on various host oaks are unique and thus not inducers varied from strongly negative (Q. coccinea, Q.
correlated with one another. However only the first five inopina) to weakly positive loadings (Q. texana, Q. lae-
axes individually explained .5% of the variance. The vis, Q. falcata). Finally, the gall communities of white
first three axes explained 17.0, 8.3, and 7.9% of the vari- oaks showed strong segregation on axis 5 with strong
ance, respectively, while axes 4 and 5 explained 6.9, and positive loadings by Q. virginiana, Q. geminata, and Q.
5.4%, respectively (total 45.5%). Eigenvalues for axis 1 minima. The remaining white oaks had weakly positive
5 5.8, axis 2 5 2.8, axis 3 5 2.7, axis 4 5 2.4, and axis to negative scores. In contrast, gall communities of red
5 5 1.8. oaks varied from weakly positive (Q. texana, Q. laevis)
Cynipid communities of red oaks had strongly negative to weakly negative (Q. inopina, Q. coccinea, Q. palus-
(Q. inopina, Q. myrtifolia) to strongly positive loadings tris).
(Q. velutina, Q. rubra, Q. ilicifolia, Q. coccinea) on com- A hierarchical cluster analysis was used to define ‘‘ob-
ponent axis 1. In contrast, all white oak cynipid com- jective’’ groups of cynipid communities according to
munities had negative loadings with the loadings of white their host associations and to reduce the many unique
oaks varying from slightly negative (Q. michauxii, Q. cynipid communities on individual oak species to fewer,
lyrata) to strongly negative (Q. alba, Q. chapmanii). but similar communities. The dendrogram illustrated in
White oaks also had negative loadings on axis 2 with Fig. 3 was formed by an agglomeration of cynipid com-
scores similar to those on axis 1. In contrast, gall com- munities that employed between-group linkage and the
munities of red oaks generally loaded positively on axis Jaccard distance measure on presence/absence data. Each
2 (Q. laurifolia, Q. incana, Q. myrtifolia) with cynipids oak’s cynipid community is shown individually on the
of only three oaks loading negatively (Q. coccinea, Q. left and the most similar communities are gradually
velutina, Q. palustris). On axis 3, red oaks in general had merged toward the right until all cynipid communities
negative scores (most strongly—Q. inopina, Q. palustris, form a single group. As expected, the patterns of cynipid
August 1998] ABRAHAMSON ET AL.—INSECTS OFFER PLANT SYSTEMATIC INSIGHTS 1163
occurrence resulted in red oaks forming a large cluster acorn, bud, woody stem, stem under bark, detachable
(except Q. pumila) and white oaks combining in a second stem, integral leaf, detachable leaf).
large cluster (except the Q. virginiana complex). Fur- The degree of specialization among these gall inducers
thermore, cynipid occurrence patterns produced clusters was particularly evident from the principal components
within each oak section. analysis performed on 127 Florida cynipids. This analysis
Among white oaks, cynipids attacking Q. virginiana showed that cynipids distributed widely across the com-
and Q. geminata formed a tight cluster that overlapped ponent axes with limited overlap occurring even on only
appreciably with cynipids infesting Q. minima. The dis- the first three component axes. Furthermore, the high
tance between Q. minima and the Q. virginiana and Q. number of component axes with eigenvalues above 1
geminata cluster may be exaggerated because of Q. min- demonstrated the high degree of uncorrelated cynipid life
ima’s small stature compared to the other two species. histories. Cynipids appear to have radiated such that in-
Plant architecture influences the oviposition behavior of dividual species use only specific host organs and oak
some cynipid species (W. G. Abrahamson, Bucknell Uni- species. In addition, cynipids attacking the same species
versity and G. Melika, Hungarian Systematic Parasitoid and organ often partition resources by attacking in dif-
Laboratory, unpublished data). This cluster of cynipid ferent seasons. For example, Amphibolips murata and A.
communities on Q. minima, Q. virginiana, and Q. gem- bucknellensis (proposed new species, G. Melika, Hun-
inata is very unique and does not overlap with other garian Systematic Parasitoid Laboratory, and W. G. Abra-
white oaks or red oaks (as indicated by the far right merg- hamson, Bucknell University, unpublished data) both at-
ing of this cluster). A second group of white oaks sharing tack buds of Q. incana, Q. laurifolia, and Q. myrtifolia
cynipids was composed of Q. bicolor and Q. macrocar- as well as several other red oaks. However, A. murata
pa, which was joined by Q. alba and Q. montana. At galls mature in autumn with adult emergence beginning
greater distance to this four-host subunit Q. prinoides and in November and continuing through Florida’s winter. In
Q. muehlenbergii merge. A third cluster of cynipid com- contrast, A. bucknellensis galls develop from early May
munities included those on Q. stellata, Q. margaretta, to June with adult emergence occurring in late May and
and Q. chapmanii. Quercus lyrata merged at a greater June. Such partitioning of resources appears common
distance and at still greater distances with Q. austrina and among cynipids and likely has been driven by selection
Q. michauxii. acting to reduce competition among these gall inducers.
The variation among cynipids attacking red oaks pro-
duced numerous clusters. The tightest cluster included Q. Distinguishing oak relationships via cynipid com-
coccinea, Q. velutina, and Q. rubra. This subunit merged munities—Our analyses of the distributions of 247 east-
with a second subunit composed of Q. ilicifolia and Q. ern United States cynipids on 34 oak species enabled us
imbricaria, and these merged subunits were joined with to generate similarity relationships among the cynipid
Q. marilandica and Q. palustris at greater distances. A communities on these oak species. Our principal com-
second cluster was formed by cynipid species infesting ponents analysis of cynipid distributions clearly distin-
Q. laevis, Q. texana, and Q. falcata, with the greatest guished between members of the red oak and white oak
overlap of cynipids on the first two species. A third large sections. In contrast, many botanical traits (e.g., wood
cluster was formed from cynipids attacking Q. hemi- anatomy, phenolics) are unable to reliably segregate oak
sphaerica and Q. nigra on one hand and those infesting species to their appropriate sections (Tillson and Muller,
Q. laurifolia, Q. myrtifolia, Q. incana, and Q. phellos on 1942; Li and Hsiao, 1973). Furthermore, cynipid distri-
the other. Quercus inopina, a Florida endemic believed butions segregated oaks within sections. The relatively
to be related to Q. myrtifolia (Johnson and Abrahamson, high number of component axes with eigenvalues over 1
1982), has a somewhat unique community of cynipids so indicates the distinctiveness of cynipid communities at-
it joins this third cluster at a still greater distance (cynipid tacking each oak species. These results suggest that cy-
oviposition behavior may be influenced by the shrub nipids can distinguish small differences among oak spe-
growth form of Q. inopina compared to the tree-like habit cies and can offer information helpful to resolving plant
of Q. myrtifolia). Quercus arkansana and the shrub Q. systematic problems. For example, cynipids differentiate
pumila have rather unique cynipid gall communities and between a number of the problematical oak species, in-
consequently merge with other red oaks at larger dis- cluding Q. laurifolia-hemisphaerica, Q. prinoides-mueh-
tances. lenbergii, and Q. virginiana-geminata.
Similarly, our hierarchical cluster analysis provided
groups of oaks based on the similarities of their cynipid
DISCUSSION gallers. The grouping patterns evident in the cluster anal-
ysis paralleled those generated by the principal compo-
Specialization and diversification—Our results illus- nents analysis, suggesting that many aspects of these
trate the high degree of specialization and diversification groupings are distinct and represent biological reality.
within the Cynipinae that attack species of Quercus. Pref- Unfortunately no modern comprehensive phylogeny of
erences for host organ and host species were very strong. oak species exists; however, several studies using limited
For example, cynipids that initiated galls on the section numbers of oak taxa are available to compare to our cy-
Quercus (white oaks) were never found infesting oaks in nipid-based clusters of oaks. In general, the groupings of
the section Lobatae (red oaks) and vice versa. Further- oaks generated from similarities of cynipid communities
more, cynipids were constant in their attack of specific are congruent with botanical classification. For example,
host organs such that these gall inducers can be classified botanical treatments (Trelease, 1924; West, 1948; Li and
according to the plant organ attacked (e.g., root, catkin, Hsiao, 1973, 1976a; Solomon, 1983a, b) have clustered
1164 AMERICAN JOURNAL OF BOTANY [Vol. 85
Q. virginiana, Q. geminata, and Q. minima while differ- (see also Li and Hsiao, 1973, 1975, 1976a) of Q. nigra
entiating these oaks from other white oaks. Our classifi- with the cluster of Q. laurifolia, Q. myrtifolia, and Q.
cation generated from cynipid communities agrees with incana but at a distance similar to that of Q. phellos.
this grouping. Cynipid distributions provide support for Li and Hsiao’s
Guttman and Weigt (1989) evaluated the systematic (1975) suggestion to separate Q. imbricaria from this
relationships of 18 Quercus species, including ten red cluster. Cynipids perceive Q. imbricaria as more similar
oaks and eight white oaks using allozyme variation. to Q. ilicifolia. Our findings also agree with the results
Among white oaks, their analysis clustered Q. alba and of an allozyme study (Manos and Fairbrothers, 1987) of
Q. macrocarpa with a second cluster of Q. muehlenbergii red oaks, which suggested that Q. palustris differs con-
and Q. prinus (5 montana). Similarly, the grouping of siderably from the more closely related Q. coccinea, Q.
Q. lyrata and Q. stellata was clustered with Q. virginiana rubra, Q. velutina, and Q. ilicifolia. However, the dis-
and Q. bicolor. Our arrangement has many similarities to tinctiveness of Q. palustris might well disappear if stud-
Guttman and Weigt’s (1989) dendrogram in that cynipid ies proposing the uniqueness of Q. palustris (Manos and
distributions suggest grouping Q. alba, Q. montana, Q. Fairbrothers, 1987; Guttman and Weigt, 1989) had in-
muehlenbergii, and Q. macrocarpa but differed by also cluded additional oaks since other work (Jensen, 1977a)
including Q. bicolor. Furthermore, our clustering sug- suggests that Q. palustris is allied with two unexamined
gested that Q. alba was most similar to Q. montana, not oaks, Q. shumardii and Q. nuttallii.
Q. macrocarpa, which cynipids suggest is most similar Hardin’s (1979a) trichome types also organize a num-
to Q. bicolor. This grouping of Q. macrocarpa and Q. ber of red oaks in a similar way to our cynipid-based
bicolor agrees with Trelease’s (1924) original Macrocar- ordering. Both studies suggested that Q. laurifolia, Q.
pae series but differs from more recent suggestions that myrtifolia, and Q. phellos are related but cynipid distri-
these species be separated (Muller, 1951; Li and Hsiao, butions indicate that Q. pumila and Q. imbricaria should
1973, 1976a, b). Cynipid distributions indicate that Q. be separated from this group. Cynipids perceive Q. nigra
muehlenbergii is more distantly related to other species and Q. hemisphaerica as well as Q. rubra and Q. coc-
in this group than the allozymes examined by Guttman cinea as quite alike, as suggested in Hardin (1979a).
and Weigt (1989). Our clustering of Q. lyrata and Q. Likewise, our arrangement of red oaks using cynipid dis-
stellata agrees with Guttman and Weigt’s (1989) dendro- tributions is congruent with some features of Solomon’s
gram as it does with the proposed more distant relation- (1983b) clustering based on pollen exine traits. The sim-
ship of Q. virginiana. ilarity of (1) Q. falcata and Q. laevis, (2) Q. laurifolia
Comparison of our cynipid-based grouping also can be and Q. phellos, and (3) Q. ilicifolia and Q. velutina is
made with Hardin’s (1979a, b) classification of trichome evident in both orderings.
variation among 42 species of eastern United States oaks. However, our cynipid-based arrangement of red oaks
Overall, Hardin’s scheme for variation among white oaks disagrees with botanical character-based arrangements in
largely parallels our grouping of white oaks. Species several ways. For example, cynipid distributions do not
within several of our clusters shared trichome features support the clustering of Q. arkansana with Q. marilan-
including (1) Q. stellata, Q. margaretta, and Q. chap- dica and Q. laevis (Trelease, 1924; Li and Hsiao, 1973,
manii, (2) Q. macrocarpa and Q. bicolor, and (3) Quer- 1976a; Hardin, 1979a). These gallers view Q. marilan-
cus montana, Q. muehlenbergii, and Q. prinoides. How- dica as more similar to Q. imbricaria and Q. ilicifolia,
ever, our arrangement of Q. michauxii did not predict its and Q. arkansana is seen as a rather distinctive species.
shared trichome features with Q. montana, Q. muehlen- Guttman and Weigt’s (1989) arrangement differs from
bergii, and Q. prinoides. It is possible that such disagree- ours by grouping Q. falcata with Q. rubra as well as Q.
ments stem from the conservation of trichome character velutina with Q. nigra.
states in spite of alterations to numerous other characters. It is likely that some of the differences in arrangements
Cynipids probably evaluate a suite of host-plant traits and result from the inclusion and exclusion of various spe-
react to the composite of character states rather than to cies. If the evolutionarily closest species to an included
individual characteristics. Consequently, the dendrogram species have been excluded with the analysis, more dis-
generated from cynipid distributions likely assesses oak tantly related species will be clustered. For example, cy-
relationships using many traits, many of which may not nipid distributions suggested similarities among Q. fal-
be expressed in traditionally utilized plant taxonomic cata, Q. laevis, and Q. texana, however, these latter two
traits. species were not included in studies such as Guttman and
Trelease’s (1924) and Li and Hsiao’s (1973, 1975, Weigt’s (1989).
1976a, b) arrangements of red oaks share many features Geographic distribution factors also confound any ar-
with our cynipid-based arrangement. For example, all ar- rangement based on herbivores such as gall inducers. Be-
rangements recognize the similarities of Q. laurifolia, Q. cause oak and cynipid species vary in their geographic
myrtifolia, and Q. incana in addition to the affinities of distributions, not all combinations of host association are
Q. rubra and Q. coccinea. Furthermore, cynipid distri- possible. This problem limits our ability to use insect
butions support the suggestion that Q. ilicifolia (Li and herbivores to provide plant systematic insights across
Hsiao, 1976b) and Q. velutina (Li and Hsiao, 1976a, b) geographic areas the size of North America.
are not as distinct as Trelease (1924) proposed. Indeed, We must add the cautionary note that the arrangement
community similarities of oak-galling cynipids support of oak species based on cynipid distributions is phenetic
Muller’s (1951) and Jensen’s (1977a, b) proposals that Q. and thus cannot be interpreted as a definitive indication
velutina has affinities with Q. coccinea and Q. rubra. Our of evolutionary relationships. Nevertheless, because the
arrangement also conforms to Muller’s (1951) placement cynipids are responding to a suite of biological traits that
August 1998] ABRAHAMSON ET AL.—INSECTS OFFER PLANT SYSTEMATIC INSIGHTS 1165
vary across their host plants, the patterns of phenetic vari- species to be recognized from south-central Florida. Bulletin of the
ation in host associations must reflect in part phylogenetic Torrey Botanical Club 109: 392–395.
LI, H. L., AND J. Y. HSIAO. 1973. A preliminary study of the chemo-
relationships and species distinctiveness. This study and systematics of American oaks: phenolic characters of leaves. Bar-
others (Aguilar and Boecklen, 1992; Fritz, Nichols-Ori- tonia 42: 5–13.
ans, and Brunsfeld, 1994; Floate and Whitham, 1995; , AND . 1975. A chemosystematic study of the series
Floate, Fernandes, and Nilsson, 1996) suggest that col- Laurifoliae of the red oaks: phenolics of leaves. Bartonia 43: 25–
laborative efforts between taxonomic botanists and en- 28.
tomologists will aid the resolution of a variety of plant , AND . 1976a. A preliminary study of the chemosystem-
atics of American oaks: phenolic characters of young twigs. Bar-
and insect systematic problems. tonia 44: 14–21.
, AND . 1976b. A preliminary study of the chemosystem-
atics of American oaks: phenolic characters of staminate catkins.
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