Table Of ContentHYM. RES.
J.
Vol. 10(2), 2001, pp. 131-137
First Record of Aridehis nifotestaceus Tobias (Hymenoptera:
Braconidae, Euphorinae) Parasitizing Nezara viridula Nymphs
(Heteroptera: Pentatomidae) with Observations on its Immature
Stages and Development
Scott R. Shaw, Gianandrea Salerno, Stefano Colazza, and Ezio Peri
(SRS) Insect Museum, Department of Renewable Resources, University of Wyoming, Laramie,
WY 82071-3354, USA; (GS) Department of Arboriculture and Plant Protection, University of
Perugia, 06122 Perugia, Italy; (SC, EP) Institute of Agricultural Entomology, University of
Palermo, Palermo, Italy
—
Abstract. Aridehis nifotestaceus Tobias is recorded for the first time from Italy as parasitizing
the pentatomid bug Nezara viridula L. This is the first record of the species in southern Europe
and the first host data. The species is re-described and illustrated. New information is provided
on its immature stages, development, and biological control potential.
Species of the euphorinebraconid genus He (1980) describeci a new species from
Aridehis Marshall are cosmopolitan in dis- China, Chou (1987) revised the species of
tributit^n, but most diversified in tropical Taiwan, and, most recently, Chen and van
areas (Shaw 1985). Aridehis species are Achterberg (1997) revised \heArideliis spe-
cjuite distinctive in appearance, and can be cies ofChina. They indicated that about40
easily distinguished from other braconids Arideliis species are now known, of which
by their coarse honey-combed areolate 20 are recorded from China. Shaw (1985)
mesosomal sculpture in combination with estimated that there are at least ten un-
the long, tubular first metasomal segment described Arideliis species in the Neotrop-
and fore wing with a closed second sub- ical region. Despite recent taxonomic
marginal cell (Shaw 1997). Their biology work, until now only one species of Ari-
is not well known but the available re- deliis has been recorcied from Europe (She-
cords indicate that they are solitary koino- nefelt 1969; Papp 1974; Capek and Davi-
biont endoparasitoids of heteropteran dova-Vilimova 1978).
bugs in the families Pentatomidae, Platas- The purpose of this paper is to provide
pidae, Scutelleridae, and Acanthosomati- new host and distribution records for Ar-
dae (Kirkpatrick 1937; Shenefelt 1969; idehis riifotestnceiis Tobias recently discov-
Papp 1974; Capek and Davidova-Vilimova ered in Italy parasitizing the pentatomid
1978; Tobias 1986; Shaw 1988; Maeto and bug Nezara viridula (L.). This is the first re-
Kudo 1992). cord of the species in southern Europeand
Papp (1965) provided a taxonomic the first host data. The host, Nezara viri-
monograph of the world species of Aride- dula, is one of the mostserious agricultural
his, however, six Afrotropical species de- insect pests worldwide, damaging a wide
scribed by De Saeger (1946) were not in- variety of fruit, nut, grain, and vegetable
cluded in Papp's monograph. Later, Papp crops. It is the primary pest of soybean in
(1974) erected the genus Arideloides for a many parts of the world (Todd 1989) and
species from New Guinea, but Shaw it also attacks many wild hosts that serve
(1985) transferred the species to Aridehis. as reservoirs until agricultural crops are
132 Journal of Hymenoptera Research
available (Jones and Sullivan 1988). In It- 515 scanning electron microscope. Adult
aly, annual losses due to this pest fluctu- specimens were preserved in 95% ethanol
ate in relation to changes in population and sent to SRS for description. Preserved
abundance of N. viridiiln (Zandigiacomo adult specimens were transferred to 100%
1990; Colazza and Bin 1990, 1995). Al- ethanol for 24 hours, then into chloroform
though this pest has been the focus of nu- for 30 minutes prior to drying and point-
merous biological control programs, most mounting to prevent shrinkage.
of the recorded biological control agents
attack the egg stage. The only other par- Arideliis rufotestnceus Tobias, 1986
asitoids known to attack the nymphal and (Figs. 1-10) —
adult stages of N. viriduln are Tachinidae Description of adult female. length of
and Encyrtidae. Until now no species of body 4.8 mm; length of fore wing 3.5 mm.
Braconidae has been discovered attacking Head: Width of head in ciorsal view 2.1
this host (Jones 1988). times its length; length of first tlagelk^m-
MATERIALS AND METHODS ere 1.5 times length of second flagellom-
ere; length of first and penultimate flagel-
Periodically, during summer and au- lomeres 4.5 and 0.8 times their width, re-
tumn 1998 and 1999, adults and nymphs spectively; median frontal carina weakly
of N. viridula were collected in the fields developed and somewhat obscured by
in Umbria, Lazio and Sicily regions fol- coarse punctate sculpturing; vertex sculp-
lowing the seasonal sequence ofhostplant ture densely punctate; ocellar-ocular dis-
species. Most of the specimens were col- tance 4.5 times ocellar diameter; occipital
lected on maize and various vegetable carina dorsally well-developed and com-
plants. A study colony of the parasitoid plete; length of eye in dorsal view 1.6
was established and maintained in Italy times length of temple; face and clypeus
by GS. Parasitoids were reared in the lab- scultpture densely and coarsely punctate;
oratory at a temperature of 24 plus or mi- intertentorial line 1.6 times length of ten-
nus 1 degree C, relative humidity 65'/o torial-ocular line; malar space 0.33 times
plus or minus 5%, and light/dark condi- height of eye. Mesosoiiia: 1.8 times longer
tions of 16 hours light and 8 hours dark- than wide in dorsal view, densely areo-
ness daily. The insects were kept in plastic late. Wings: Pterostigma 2.0 times longer
boxes and fed with vegetables and sun- than wide at midpoint, anterior margin
flower seeds. Boxes were examined daily distinctly rounded and protruding well
to collect parasitoid cocoons. Also, each beyond anterior margin of wing as delim-
day 5 N. viridula nymphs of the same age ited by vein C-l-SC-(-R; length of marginal
(reared in the laboratory) were exposed to cell 0.85 times pterostigma length; vein r
a parasitoid female in a plastic box (7 X nearly perpendicular to pterostigma and
5.5 X 2.5 cm) for 24 h. The parasitized 2.5 times longer than vein 3RSa bordering
nymphs were removed from the box and second submarginal cell dorsally; vein
kept separately until appearance of para- 3RSb nearly straight basally then curving
sitoid cocoons. towards wing margin apically; vein m-cu
Some nymphs were dissected toobserve slightly antefurcal relative to vein 2RS,
the different developmental stages of the with very short segment of vein (RS+M)b
parasitoid. For SEM analysis theimmature present. Metasoiua: Entirely smooth and
stages were fixed in Karnovsky's medium highly polished; length of first metasomal
(Karnovsky 1965) for one hour at 4 °C, de- segment 7.0 times its width at spiracles;
hydrated in graded ethanol series, critical- metasoma beyond petiole 2.7 times longer
point dried, mounted on stubs, coated than wide in dorsal view; ovipositor
with gold and observed with a Philips EM sheath very short, exposed portion about
Volume 10, Number 2, 2001 133
Figs. 1-5. Aridchi^ nttotc^Uucus. \, Eggs with developingembryos, 200x. Figs. 2-4. First instarlarva. 2, Lar\'a
still partiallysurrounded by trophamnionand teratocytes,ventral view,70x.3, Lateralview, lOOx.4,Ventral
view of head capsule and mouthparts, 170x. 5, Third instar larva, antero-ventral view of head capsule and
mouthparts, 105x.
0.5 times length of hind basitarsus. Color. remainder of mesosoma, and ovipositor
Head, antenna basally, lateral borders of sheath black; wing venation brown, mem-
pronotum, legs, and metasoma orangish brane clear—to slightly dusky medially.
brown; mandible apically, ocellar triangle, Variation. Body position at cieath vary-
134 Journal of Hymenoptera Research
Figs. 6-10. Aridclus rnfotcstaceiis. 6, Third instar larva, ventral view, 11X. Figs. 7-10 Adult. 7, Female near
Neznrn viridiila nymph. 8, Propodeum and metasoma, dorsal view, 42x. 9, Propodeum, dorsal view, 38x. 10,
Head, mesoscutum, and scutellum, dorsal \'iew, 42x.
ing from metasoma fully extended poste- dorsally, hind femur, hind tibia, petiole,
riorly to fully extended anteriorly (ovipo- and dorsum of metasoma posteriorly
sitional stance) with metasomal petiole more or less infused with sn^iokey black
bent under mesosoma and apex of meta- pigmentation. \n all cases dead preserved
soma extending well beyond face. Sonie specimens appear somewhat to have a
individuals appear darker with the head darker mesosoma; while alive some or-
Volume 10, Number 2, 2001 135
angish brown color shows through the than wide. The caudal appendage is lost.
darker black pigmentation. Aside from The third and final iiistar larva is also hy-
genitalic differences, the male is quite sim- menopteriform and apneustic, but thicker
ilar in form and sculpture, but is much and more maggot-like. It is tapering at
lighter in color appearing mostly orange, both ends and thickest medially, being
even over the mesosoma where black pig- about 3x l—onger than wide at maturity.
mentation is limited to smokey pigmen- Biology. Aridelus rufotestnceus was
tation along the borders of the a—reolation. found for the first time in October 1998
Description of iuunaturc stages. The egg near the Umbria region of Perugia, Italy
is alecithal (with no visible yolk), oval, (parasitism rate4.3%). During the summer
with a clear chorion through which the of 1999 we found the parasitoid in the La-
white enibryo and developing tropham- zio region (parasitism rate 21.7%) and in
nion are visible. The developing embryo Sicily (parasitism rate 12.5%). The mature
has a large oval head capsule, followed by egg is usually lemon-shaped, with a ped-
12 similar undifferentiated body seg- icel. When the first instar larva hatches
ments. The thoracic segments are not vis- from the egg, the teratocytes dissociate
ibly different from the abdominal seg- into the hemolymph and increase in size.
ments. The trophamnion forms a large In laboratory conditions the period from
mass of spongy white teratocytes below egg deposition to emergence ofthe mature
the embryo, enveloping the embryo pos- larva was 23.18 plus or minus 2.77 days
teriorly. The mature embryo has a thick (n = 37). The mature larva emerges from
round head capsule with no trace of eyes the host through a hole in the interseg-
or antenna, deep anterior tentorial pits, mental membrane between the ultimate
long sickle-like mandibles, simple mouth and penultimate segments, crawls away,
opening, 11 undifferentiated similar body and spins an oval white silk cocoon. After
segments, and 12"' segment longerbearing emergence of the parasitoid larva the host
anus ventrally and a long tapering caudal may survive for several days (although
appendage. The first instar larva is of the clearly not in healthy condition). Adults
caudate form, similar to the mature em- emerged from the cocoon in 22.27 plus or
bryo with a thick round head capsule with minus 1.45 days (n = 37). The adult life
no trace of eyes or antenna, deep anterior span was, in mean, 212.08 plus or minus
tentorial pits, long sickle-like mandibles, 8.18 days (n = 106) with a range from 6
simple mouth opening, 11 undifferentiat- to 43 days. Reproduction is parthenoge-
ed similar body segments, and 12* seg- netic (thelyotokous, or sometimes deuter-
nient k^nger bearing anus ventrally and a otokous). In the lab only 3 males were ob-
long tapering caudal appendage densely tained relative to 200 females. Prior to ovi-
covered with short, thick, flexible setae. position females approach potential hosts
The first instar has an apneustic respira- on foot and inspect them, both visually
tory system, with no visible spiracles. The and via antennation. Oviposition is typi-
body becomes much thicker as the young cally very rapid, lasting a few seconds at
larva feeds and grows. The second instar most, during which the female rapidly ap-
larva becomes hymenopteriform remains proaches the host on foot, throws back the
apneustic. The sclerotized head capsule is antennae, flexes the metasoma under the
much smaller, with short mandibles, and mesosoma while both exserting the ovi-
becomes enveloped by the fleshy first tho- positor and telescoping posterior metaso-
racic segment as the larva grows. The sec- mal segments. Eggs are inserted into the
ond instar larva is yellowish white with membranous cervical region between the
undifferentiated segments, less distinct head and thorax or into the intersegmental
than in the first instar, and about 5x longer areas of the posterior abdominal region of
136 Journalof Hymenoptera Research
the host. Supernumerary eggs of larvae the observed color forms are related to
were dissected from hosts collected in the patterns of host use.
field and in hosts parasitized in the labo- The study of Capek and Davidova-Vi-
ratory, but in all cases only one larva de- limova (1978) suggested that there are
veloped per host, hi the laboratory Aride- four larval instars in A. cgrcgius, but our
liis nifotestnccus was able to parasitize 2"'\ observations suggest only three larval in-
3"-\ and 4* instar host nymphs, as well as stars in A. rufotcstnccus. Capek and Davi-
adults. Younger instars were more suit- dova-Vilimova defined their instars 1 and
able for parasitoid development with 95% 2 as morphologically similar, but differing
of 3'^' instars parasitized and 85.7% of 2"^^ only in slight differences in the length of
instars parasitized permitting complete the mandible. In fact, since their firstinstar
parasitoid development. The highest mor- was arbitrarily defined as comprising the
tality rate recorded for parasitized adults smallest individuals, and was based only
was 80.0%. on 2 individuals (N = 2), their sample size
Discussion.—Terminology used in the was simply too small to demonstrate a sta-
description follows that of Sharkey and tistically significant difference between
Wharton (1997). This species is a typical their instars 1 and 2. Another possible ex-
member of the genus and can be keyed to planation is that all their individuals with
genus without difficulty using the key long, fighter-type mandibles and caudal
provided by Shaw (1997). This species can appendage belong to the same instar (1)
be identified using the key to Chinese Ar- and there are only 3 instars.
iiiclus species provided by Chen and van It is worth stressing that in Italy no
braconid has ever been recorded as para-
Achterberg (1997). In the key to world
species of Papp (1965) this species keys to sitoid of Pentatomidae. Moreover, since
1989, the Department of Arboriculture
couplet 23, A. iiigritliornx Muesebeck, but
and Plant Protection of the University of
A. nifotestnccus can be distinguished from
Perugia periodically collected N. viriduln
that species by its lighter colored antenna
from the field to assess the parasitization
(flagellum entirely black in A. nigrithoriix),
more coarsely sculptured head (head only level of tachinid flies, and the presence of
any braconid was never observed. In con-
finely punctate in A. iiigrithonix), and sideration of this, we can hypothesize a re-
weakly developed median frontal carina
cent fortuitous introduction of A. iicznrn-
(strongly developed in A. )iigritliomx). A. plingus in Italy, as happened in the past for
rufotcstnccus can be distinguished from A.
the tachinid Triciiopodn pcniiipcs F. (Colaz-
egrcgrius Schmiedeknecht, the only other za ct nl. 1996). Since the parasitoid was al-
European species, by its more coarsely ready recorded from China and Russia,
sculptured head and lighter body (head this may be a natural range extension
mostly smooth and body black in A. cgrc- from eastern areas. Another possibility is
gius). The three described North America that the parasitoid may have previously
species, A. fishcri (Viereck), A. uiclaudcri been present but niade a recent host-
(Brues), and A. iiigrithonix Muesebeck, are switch from other hosts. However, no al-
identical morphologically but differ only ternate hosts have yet been found in Italy,
in color (entirely orange, black head, or although the following pentatomids have
black mesosoma, respectively). Given the been examined for the presence ofthe par-
wide range of color variations seen in A. asitoid: Eiirydciun olcrnccum (L.), Eurydciiin
rufotcstnccus, it would seem questionable vcntrnlc (Kit.), Eurygnstcr sp., Grnpliosoiiin
to separate Aridclus species based on color lincntuiii (L). and G. scmipuiictntuiii (F.).
alone. Careful field studies are needed for Mntc—rinI cxnniiiicd for rc-dcscriptioii of
the North American species to examine if ndiilt. 3 females: Italy, Palermo, lab
Volume 10, Number 2, 2001 137
reared ex. Nezara viridiila, December 1999; (Heteroptera: Pentatomidae). Annals ofthe Ento-
5 females, 1 male, same data except Pe- mological Societi/ofAmerica 81(2): 262-273.
rugia, October 1998; 21 females, same data Jones, W. A. and M. J. Sullivan. 1982. Role of host
plants in populationdynamicsofstinkbugpests
except Perugia, August 1999. Specimens of soybean in South Carolina. Environmental En-
deposited in University of Wyoming In- tomology 11: 867-875
sect Museum, Laramie; Nationaal Natu- Karnovsky, M. S. 1965. A formaldehyde glutaralde-
urhistorisch Museum, Leiden, The Neth- hyde fixative of high osmolarity for use in elec-
erlands; and Natural History Museum, tron microscopy, journal ofCell Biology 27: 137-
138.
Budapest, Hungary. Kirkpatric, T. W. 1937. Studies on the ecology ofcof-
ACKNOWLEDGMENTS fee plantations in East Africa. The Transactionsof
the Roi/al Entomological Societi/ of London 86(14):
We are very grateful to Prof. Ferdinando Bin, De- 247-343.
partment of Arboriculture and Plant Protection,Uni- Maeto, K. and S. Kudo. 1992. A new euphorine spe-
versity of Perugia, Italy for his helpful cooperation. cies of Aridelus (Hymenoptera: Braconidae) as-
We also wish to thank Dr. C. van Achterberg of the sociated with a subsocial bug Elasmucha putoni
Nationaal Natuurhistorisch Museum, Leiden, The (Heteroptera, Acanthosomatidae). Japanese jour-
Netherlands,forhishelpfulcooperationinborrowing nal ofEntomology60(1): 77-84.
the holotype of A. nifotcstacciis and confirming the Papp, J. 1965. A monograph of the genus Aridelus
Marsh. (Hymenoptera, Braconidae: Euphorinae).
identity of this species.
Acta Zoologica Academiae Scientarum Hu)igaricae
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