Live oaks, new hosts for Odontocynips nebulosa Kieffer (Hymenoptera: Cynipidae) in North America

14 Pages·2000·6.9 MB·

by  A D Wilson

PROC. ENTOMOL. SOC. WASH.
102(2), 2000, pp. 360-373
LIVE OAKS, NEW HOSTS FOR ODONTOCYNIPS NEBULOSA KIEFFER
(HYMENOPTERA: CYNIPIDAE) IN NORTH AMERICA
A. D. Wilson, D. G. Lester, and R. E. Edmonson
(ADW, DGL) Forest Insect and Disease Research, U.S. Department of Agriculture,
Forest Service, Southern Research Station, Southern Hardwoods Laboratory, Stoneville,
MS 38776-0227, U.S.A. (e-mail: dwilson/[email protected]); (REE) Texas Forest
Service, Kerrville, TX 78029-3127, U.S.A. (e-mail: [email protected])
—
Abstract. A study of root-feeding insects as potential vectors of the oak wilt fungus
Ceratocystisfagacearum (T. W. Bretz) J. Hunt in live oaks, revealed root galls induced
by the cynipid gall wasp Odontocynips nebulosa Kieffer. The incidence of the wasp on
roots of four oak species and natural live oak hybrids at 14 root excavation sites in 7
counties throughout the Hill Country ofcentral Texas was surveyed. The study was limited
to sites within and adjacent to oak wilt infection centers of the live oak-Ashe juniper
ecotype where oak wilt infected live oaks were being uprooted and rogued for disease
suppression by the Texas Oak Wilt Suppression Project. This is the first report of this
root-galling wasp on live oaks, Q. fusiformis Small and Quercus virginiana Miller X
Quercus fusiformis natural hybrids, in North America. The incidence of root-galling by
the wasp occurred at relatively low levels among trees examined at excavation sites in
each county, indicating a sporadic distribution throughout the region. However, exami-
nations of root-colonization and gall induction by O. nebulosa in uprooted live oaks
showed relatively high levels of root infestations in some trees, including trees exhibiting
symptoms of oak wilt disease. This pattern suggests high population densities in small
localized areas. Examinations of individual gall clusters formed by the wasp on live oak
roots revealed new details of gall morphology and developmental stages of the insect
within galls. The significance of this wasp as a potential vector of the oak wilt fungus is
discussed.
Key Words: host-parasite relationships, Odontocynips nebulosa, Quercus fusiformis,
Quercus virginiana, cynipid gall wasps, Ceratocystisfagacearum, oak wilt
fungus
The cynipid wasps comprise a large from 8 of 37 Nearctic genera listed in the
group ofphytophagous Hymenoptera (Fam- subfamily Cynipinae induce galls on plants
ily Cynipidae) that inhabit angiospermous from at least 35 additional plant genera (see
plants either as gall-makers (subfamily Cy- Burks 1979). Gall induction results from
nipinae) or as inquinones (subfamily Sy- the reactions of host tissues to morphogens
nerginae). Of the more than 800 Nearctic secreted by larvae during feeding (Roh-
species recognized in the Cynipidae, 78% fritsch 1992, Shorthouse and Rohfritsch
induce galls on Quercus species (Burks 1992). The Synerginae, accounting for the
1979, Dreger-Jauffret and Shorthouse remaining 12% of recognized species, de-
1992). Approximately 10% of the species velop as inquinones within galls induced by
VOLUME NUMBER
102. 2 361
Other cynipids, chalcidoids, or dipterous similar multilocular galls induced by this
gall-makers in the family Cecidomyiidae species on post oak and overcup oak (Quer-
(Burks 1979, Ronquist 1994). cus lyrata Walt.). Very little information on
Cynipids are not only highly host-specif- the life cycle, host range, host-parasite re-
ic, but they are remarkably selective in the lationships, and geographical distribution of
types of host tissues that they will colonize. O. nebidosa has been elucidated since the
Most cynipids that induce galls on oak spe- species was described by Kieffer (1910).
cies selectively infest above-ground tissues The genus Odontocynips currently is mono-
of their hosts, including either main stems typic (Burks 1979).
and branches, twigs, buds, petioles, leaves, The majority of cynipids are considered
flowers, or fruits (e.g., acorns), but rarely of minor economic importance, although a
several of these tissues on the same host. few species such as the gouty oak gall wasp
The greater diversity of somatic, reproduc- Callirhytis quercuspunctata (Bassett), the
tive, and meristematic host tissues serving homed oak gall wasp C. cornigera (Osten
as niches in above-ground plant tissues rel- Sacken), and the oak rough bulletgall wasp
ative to root tissues may account for greater Disholcaspis quercusmamma (Walsh) are
numbers of gall-inducing species and more destructive pests that can cause significant
numerous and varied gall morphology types injury and even mortality to landscape oaks
found on above-ground tissues. Although (Johnson and Lyon 1988, Eckberg and
many oak gall wasp species have sexual Cranshaw 1994). A field study was initiated
and parthenogenic generations that develop in fall of 1993 to survey populations of
different gall types on different oak species root-feeding insects of live oaks that might
or plant organs (Askew 1984), this rarely serve as potential vectors of the oak wilt
occurs in the same generation. fungus, Ceratocystis fagaceariim, in the
Relatively little is known about cynipids Texas Hill Country. This fungus is the most
that cause root galls. Galls produced by serious pathogen causing oak mortality in
most subterranean cynipids form on roots Texas. During initial stages of this study,
that arise near the crown at or just below root systems of live oak trees that had been
the soil surface. Felt (1965) listed only pushed over during oak wilt disease sup-
about 40 cynipid species that form galls on pression activities showed heavy infesta-
plant tissues below ground. More recently, tions of a root-galling insect. Subsequent
Burks (1979) listed approximately 120 spe- investigations showed that the insect re-
cies capable of inducing galls on roots. sponsible for these root galls was O. ne-
Fewer than a dozen species have been de- bidosa. The current research stemmed from
scribed as capable of colonizing and form- the 1993 survey. The objectives were to de-
termine the incidence and severity ofO. ne-
ing galls deeper in the soil profile on small
bidosa infestations of Quercus species in
fibrous and larger true roots. This small
and around the perimeter of oak wilt infec-
group ofsubcoronal species includesBelen-
ocnerna treatae Mayr, Odontocynips nebu- tion centers, elucidate aspects ofits biology
with respect to host specificity, tissue pref-
losa, and Callirhytis species.
erences, and distribution on the host, ex-
Odontocynips nebidosa is distinguished
amine gall morphology and insect devel-
from other subterranean gall wasps by its
opment within root galls on Q. fusiformis
ability to induce the formation of large ir- and Q. virginiana X Q. fusiformis natural
regular multilocular galls on the roots ofits hybrids, and document new hosts of the
hosts. It induces single globose galls and wasp in North America.
larger irregularly-shaped multilocular galls
up to 10 cm in diameter on post oak (Qiier- Materials and Methods —
cus stellata Wangenh.) roots up to 1.3 cm Field survey and root excavations. The
in diameter (Felt 1965). Weld (1959) found root excavations and examinations required
362 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
to conduct most this study were carried out The incidence (frequency of occurrence)
from July through December 1995 in co- of root galling by the wasp was calculated
operation with oak wilt suppressions activ- per tree for each oak species sampled with-
ities of the Texas Oak Wilt Suppression in each county. The number of oak wilt in-
Project, a disease suppression program ad- fection centers that were present within a
m
ministered by the Texas Forest Service. The 500 radial distance of root excavation
oak wilt fungus commonly moves from tree sites also was recorded foreach county. The
to tree through root grafts and common root host parameters measured for individual
systems formed between adjacent trees. trees included tree species, diameter at
Oak trees around the perimeter of actively breast height (dbh), and distance from the
expanding oak wilt infection centers are nearest infected tree within an oak wilt in-
routinely extracted and removed (rogued) fection center. The intensity (severity) and
using backhoes and bulldozers to create a spatial distribution of root colonization on
distance barrier between the advancing trees with galls was recorded as percent
front of the infection center and healthy root flare infestation (proportion ofmajoror
trees in an attempt to prevent root trans- primary roots arising from root flares that
mission ofthe oak wilt fungus. Four species had root galls), total number of galls per
of oaks and natural live oak hybrids, all primary root and per tree, depth of galled
highly susceptible to oak wilt, were pushed roots, and distance of galls from the main
over during this roguing process which pro- stem or bole. Root galls were collected
vided the opportunity to examine and sam- from individual trees at each excavation site
ple the root systems of oaks for root-feed- using lopping shears to cut root segments
ing insects of potential importance as vec- 2-5 cm on each side of individual galls.
tors ofthe oak wilt fungus. The oak species Measures ofgall morphology and root char-
surveyed for O. nebulosa-'\niQs,\.sA.\ons in- acteristics of galled roots were recorded as
cluded plateau live oak, Q. fusiformis (for- unilocular (single-chambered) or multiloc-
merly Q. virginiana war.fusiformis), Q. vir- ular (multichambered) galls with multiple
giniana X Q. fusiformis natural hybrids of locules, gall dimensions, and corresponding
plateau live oak and coastal live oak, Q. root diameters associated with the galls
virginiana, Lacey oak, Quercus glaucoides found on roots from root excavation sites
Mart. & Gal. (= Q. laceyi Small), Spanish in each county. All data presented are
oak or Texas red oak, Q. texana Buckley (mean ± 1 SE).
(= Q. buckleyi Dorr & Nixon), and black- Gal—l morphology and insect develop-
jack oak, Q. marilandica Miinchh. ment. Representative root galls in various
The exposed root systems of 1,993 ex- stages of development were collected from
cavated oak trees, uprooted along the pe- the root systems oflive oaks near Kerrville,
rimeter of fourteen oak wilt infection cen- TX during root excavations in the fall (18
ters, were examined for root galls of O. ne- November) and early spring (1 1 February).
bulosa. Some trees sampled along the pe- The developmental morphology of root
rimeter and within oak wilt centers were galls (n = 44 for the fall collection, and n
infected with the oak wilt fungus. Oak wilt = 25 for the spring collection) was exam-
infection centers were selected from seven ined by exploratory dissections. The outer
Texas counties throughout the Hill Country layers ofhost tissue forming the wall ofthe
on the Edwards Plateau and Balcones fault galls were removed in sections to reveal hy-
zone. In all cases, research trees were lo- perplastic and hypertrophic tissues forming
cated in scattered stands of mixed hard- within galls during developmental stages of
woods of the live oak-Ashejuniper ecotype the wasp from early larval stages until te-
bounded on the east side by the central Tex- nerals (callow adults) within gall locules
as post oak savannah region. emerged from exit holes chewed through
—
VOLUME 102. NUMBER 2 363
Table 1. Incidence (frequency ofoccurrence) of O. nebiilosa galls on root systems ofoaks surveyed around
the periphery of oak wilt infection centers from seven counties in central Texas.
Q. V. X
CToeuxnatsy OCaenkteWrisl't ExaminQed^fusif^iiniiGias-lled ExaminQe.d:/. Hv'-briGdasl"led ExaQm.inie>dUnicGoailJlesed ExamiQn.edtexaGnaalled ExQiUiiniineadnlaGnadlilcead
— — — —
Bandera 4 —293 —3(1.0) —_18 _— _—35 _— _—_—
Bell 2 —20 —2(10.0) ____ ____
Gillespie 6 1,303 0(0.0) — — ___41 __25_
Kendall 2 23 2(8.7) — —
Kerr 1 37 33(89.2) — —
Mills 2 —28 —3(10.7) — — — — — —
Travis 1 170 2(1.2)
Total 18 1,684 41(2.4) 190 4(2.1) 18 76 25
' Numbers of oak wilt infection centers in the vicinity (500 m) of root excavation sites established in each
county.
-Total numberoftrees examined and number having root galls ofO. nebulosa. Values in parentheses indicate
the percentage of trees with root galls.
'Natural hybrids ofcoastal live oak and plateau live oak, Q. virgiiiiana X Q.fusiformis.
the walls. Adults used forexamination were pal, and teneral developmental stages with-
reared from additional galls (n = 23) placed in galls, percent emergence from gall cham-
in 7-10 X 6.5 cm plastic insect cages with bers, and percent insect viability and
screened lids held at 24 C for 50 days fol- mortality within galls. Means of all mea-
lowing the fall gall collection. In the last surements were expressed as (mean ± 1
stages of pupation, tenerals were exposed SE).
within gall locules by dissection. Represen-
Results
tative adult voucher specimens of O. ne-
bulosa were deposited 17 February 1994 in Field survey and root excavations.
the National Museum of Natural History, Root galls induced by O. nebulosa were
Smithsonian Institution, Washington, DC found only on live oaks, Q. fusiformis and
(Ref.: TSU Lot no. 94-1040). the natural hybrids Q. virginiana X Q. fu-
Galls (n = 69) examined from the fall siformis, encountered at the periphery of
and spring collections were placed into surveyed oak wilt infection centers (Table
three developmental categories including 1). Some live oaks (<5%) within the infec-
previous-year mature galls, current-year tion center that were infested with the wasp
mature galls, and current-year immature exhibited diagnostic symptoms of oak wilt.
galls. Previous-year mature galls were old Other oak wilt infection centers were found
black weathered galls from which a prior in the vicinity of surveyed areas as well.
generation had emerged the previous year. The infestation rates of individual root sys-
Current-year mature galls were light brown tems among all live oak trees at the periph-
and contained locules with larvae, pupae, or ery of oak wilt centers were less than 11%
tenerals of the next generation to emerge. (range 1.0-10.7%) at all but one survey
Current-year immature galls were small, site. At the single site in Kerr County, 89%
tan-colored galls containing white internal ofsurveyed trees exhibiting galled root sys-
tissue bearing predominantly larval stages. tems. This high level of incidence was as-
Galls in each developmental category were sociated with an oak wilt infection center at
characterized by measurements of the gall a rural residence where all ofthe trees with-
and insect including mean number ofcham- in the center had to be rogued to contain
bers per gall, gall chamber size (internal di- the spread of the disease.
ameter), percentage of insects in larval, pu- The live oaks rogued and pushed into
364 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
Table 2. Host parameters, root infestations, and location ofgalls on roots of live oaks species in the Texas
Hill Country.
Texas
County'
VOLUME NUMBER
102, 2 365
Table 3. Gall morphology and root diameters associated with O. nebulosa galls collected from roots of
Quercusfusifonnis and Q. virginiana X Q.fusifonnis hybrid trees.
366 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
Fig. I. Host-parasite relationships associated with O. nebulosa-'induced galls collected from roots of live
oaks, a, Veinal necrosis leaf symptom of oak wilt-infected tree, b. Location of galled root segments collected
on feederroots in the main root ball nearthe bole, c. Shallow subterranean rootgalls withrootsprouts,collected
before emergence, d, Multilocular (multichambered) gall with exit holes collected after emergence, e, Closeup
of unilocular (single-chambered) gall with dead (pruned) distal root section and root sprout, f, Multilocular
mature galls on root segments comparing the light-colored, current-year living galls (top segment) with black,
necrotic previous-yeargalls (bottom segment).
surrounding the larva began aberrant cell nins and tannins) often formed within the
division and expansion resulting in the for- swollen tissues immediately around the lar-
mation of localized tissue swellings (Fig. va. The localized aberrant tissue was con-
2a). Dark brown necrotic tissues with oxi- sumed during feeding by the developing
dized phenolic compounds (presumably lig- larva to form hollowed-out cells or locular
VOLUME 102, NUMBER 2 367
Fig. 2. Developmental morphology of gall formation and insect development in O. nebulosa-\niQ?,\.ed live
oak roots, a. Initial stage of gall development with the formation of localized tissue swellings around larva
(arrow) surrounded by brown necrotic areas in response to larval feeding, b. Development of locular initial
(arrow) in gall tissue resulting from tissue consumption by larva, c. Pupae within two adjacent locules of a
multilocular gall, d. Pupa with wing cases during late stages of pupation, e. Opaque pupa with separating
exoskeleton, removed from gall chamber immediately prior to molt to teneral (callow adult) stage, f, Adult
female with expanded wings ready for flight. Scale bars = 1.0 mm.
initials (Fig. 2b). Larvae continued to feed nerals while still in the galls. Tenerals
within developing galls throughout the emerge from the galls on warm days in late
summerand early fall months, enlarging the winter to early spring (usually early Feb-
locular cavities to form chambers. None of ruary in Texas) by chewing through the
the chambers appeared to contain more than wall of their chamber and escaping through
one larva. Larvae began pupating within the exit hole or chewing into the locule of
chambers of the galls in the fall (Fig. 2c). an adjacent chamber with an exit hole to
Pupae (Figs. 2d-e) began molting, breaking escape. Large numbers of adults were ob-
free from their wing cases to become te- served emerging from the soil above sub-
368 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
Table 4. Gall and insect development, insect viability, and emergence associated with root galls of O. ne-
bulosa on infested Querciisfusiformis and Q. virginiana X Q.fusifonnis hybrid trees.
VOLUME 102, NUMBER 2 369
a higher percentage of larvae and pupae, brids {Q. virginiana X Q. fusiformis) that
but had a lower percentage of tenerals and form between coastal and plateau live oaks
total emergence than current-year mature occurs abundantly in the region between
galls from the spring collection. However, eastern parts ofthe Edwards Plateau and the
immature galls contained a much higher Brazos River to the east (Nixon 1984).
percentage of larvae than mature galls Consequently, the current study has dou-
among current-year galls from both collec- bled the host range to include semiever-
tions. Mature previous-year galls from both green oaks and expanded the known habitat
collections lacked insect developmental of O. nebulosa to xeric savannah-wood-
stages since all living tenerals had already lands of the southwestern United States.
emerged prior to collection. Insect emer- Lyon (1996) recently described seven new
gence was highest in previous-year mature cynipid species on leaves and twigs of
galls and lowest in current-year immature white oaks from this region. Weld (1960)
galls for both collections. The majority of listed 130 species ofphytophagous cynipids
tenerals emerging from previous-year and from the southwestern United States with
current-yearmature galls in both collections an additional 1 17 gall types that were never
came from the same chambers within which associated with a specific cynipid. The
they developed while the remaining portion specificity with which O. nebulosa coloniz-
emerged from an adjacent or more distant es and forms galls on the roots of its hosts
chamber from which they developed. This may be a survival advantage to the species
latter type ofemergence was achieve by te- in avoiding dessication in xeric habitats
nerals chewing their way into an adjacent (see Femandes and Price 1992).
chamber from which the occupant had al- This survey indicates that the incidence
ready emerged and created an escape route of live oak root-galling by O. nebulosa
to the outside of the gall. Insect viability around oak wilt infection centers is rela-
within galls was highest in immature galls tively low (1.0-10.7%) within most of the
and higher in current-year mature galls than areas surveyed. However, the small per-
in previous-year mature galls. centage of trees that were infested tended
to have relatively high infestations of their
Discussion
root systems based on the percentage of
The limited occurrence ofO. nebulosa on major roots that were galled on individual
two live oak species and its absence on the trees. These data suggest that the occur-
red oaks (subgenus Erythrobalamis), in- rence of this wasp is sporadic in the Ed-
cluding blackjack oak, Lacey oak, and wards Plateau region, but that it tends to
Spanish oak in this survey, suggests host occasionally form relatively high popula-
specificity to certain oaks in the white oak tions in small localized areas or in individ-
group (subgenus Leucobalanus). Hitherto, ual clumped stands (motts) of live oaks.
O. nebulosa has been reported from Geor- The occurrence and incidence of the wasp
gia and Arkansas only on post oak {Q. stel- does not appear to be influenced by the in-
lata) and overcup oak {Q. lyrata) by Weld fection-status of trees since root-galling did
(1959), both white oak species. The live not occur at significantly higher frequency
oaks are intermediate species having sap- in infected than in healthy live oaks. There-
wood anatomical characteristics ofboth the fore, oak wilt infection of live oaks proba-
white oak and red oak groups. However, bly does not predispose live oaks to O. ne-
live oaks are generally classified as white bulosa-'miQsidLiion. Since the wasp occurs in
oaks based on leaf and acorn characters. both oak wilt infected and uninfected live
Quercus fusiformis is well established oaks, the presence of C. fagacearum in the
throughout the Edwards Plateau region of root system does not appear to be a nutri-
central Texas. The natural continuum ofhy- tional requirement for larval development.