NOTES ON THE HOST, EGG, AND PUPARIUM OF STYLOGASTER BIANNULATA (SAY) (DIPTERA : CONOPIDAE)

PROC. ENTOMOL. SOC. WASH.
100(4), 1998, pp. 658-664

NOTES ON THE HOST, EGG, AND PUPARIUM OF
STYLOGASTER BIANNULATA (SAY) (DIPTERA: CONOPIDAE)

NORMAN E. WOODLEY AND DARLENE D. JUDD

(NEW) Systematic Entomology Laboratory, PSI, Agricultural Research Service, U.S.
Department of Agriculture, % National Museum of Natural History, MRC-168, Washing-
ton, DC 20560, U.S.A. (e-mail: nwoodley @sel.barc.usda.gov); (DDJ) Department of En-
tomology, Smithsonian Institution, MRC-169, Washington, DC 20560, U.S.A.

Abstract.—The egg and puparium of Stylogaster biannulata (Say) (Diptera: Conopidae)
are described and illustrated in detail based on examination by scanning electron micros-
copy. This species was reared from Gryllus rubens Scudder in Florida, a new host record.
Previous literature is reviewed in light of this new data.

Key Words:

The genus Stylogaster Macquart has
about 85 species distributed primarily in
tropical regions in both hemispheres (Smith
1979: fig. 1). The greatest diversity is in the
New World where 63 species occur (Cam-
ras and Parrillo 1985), two of which are
found in the Nearctic Region. This paper
reports new data on hosts and immature
stages for Stylogaster biannulata (Say)
which occurs from Rhode Island to Ne-
braska, south to Texas, Florida, and Vera-
cruz, Hidalgo, and San Luis Potosi in Mex-
ico (Camras 1965, Camras and Parrillo
1985). The other Nearctic species, S. neg-
lecta Williston, is known from Massachu-
setts to Nebraska, south to Arizona, Geor-
gia, and Sinaloa and Chiapas in Mexico; its
biology remains completely unknown.

HOSTS OF STYLOGASTER

The enigmatic biology of Stylogaster has
been the subject of much speculation ever
since Bates (1863: 365) published one of
the first naural history observations of Styl-
ogaster females hovering over advancing
swarm raids of army ants of the genus Eci-
ton Latreille. Early authors [see Aldrich

Stylogaster biannulata, Conopidae, hosts, egg. puparium, Gryllus rubens

(1930) for a good summary] were of the
opinion that Snlogaster must have been us-
ing army ants as hosts. Lopes (1937) found
eggs of Stylogaster on an unspecified or-
thopteran and a cockroach. Later observa-
tions, particularly detailed ones by Retten-
meyer (1961), showed that the conopids
were ovipositing on insects displaced by the
advancing ants, as well as other insects, es-
pecially tachinid flies of the genera Calod-
exia Wulp and Androeuryops Beneway
looking for hosts displaced by the ants.
However, Rettenmeyer was of the opinion
that cockroaches and possibly other orthop-
teroid insects were the most likely hosts of
Stylogaster, and eggs were inserted acci-
dentally into tachinids utilizing the same
hosts. He did, however, note (1961: 1015)
that one of 17 Stylogaster eggs found on
tachinids had initiated development, so he
did not completely discount tachinids as
hosts. Stuckenberg (1963), Smith (1967,
1969), and Smith and van Someren (1985)
discussed the occurrence of Stylogaster
eggs on various calyptrate Diptera, primar-
ily Muscidae, in the Afrotropical Region.
Some of these flies were associated with

VOLUME 100, NUMBER 4

driver ants while others were associated
with animal dung (and in the fatter case
Stylogaster eggs were found on flies outside
of the geographic distribution of driver
ants). Stuckenberg (1963) was of the opin-
ion that because Stylogaster eggs were
more common on dung-breeding muscids
he studied than was observed by Retten-
meyer (1961) in Panama, it was more likely
that flies were the true Stylogaster hosts in
Africa. Smith (1979) noted that Stylogaster
ligepae Smith was collected while hovering
over a bird nest, and speculated that per-
haps they were looking for flies attracted to
dung or carrion in or near the nest.

All of the above evidence concerning
Stylogaster hosts is circumstantial. It was
not until Smith and van Someren (1985) re-
ported dissecting larvae of Stylogaster var-
ifrons Malloch from cockroach nymphs and
a larva of S. westwoodi Smith from a gryl-
lid cricket that unequivocal host associa-
tions were known. Adults of both species
were seen Ovipositing on their hosts being
displaced by army ants in a garden in Ke-
nya.

One of us (NEW) was sent a collection
of Diptera reared from Gryllus spp. by Tho-
mas J. Walker and his associates near
Gainesville, Alachua County, Florida.
While most of the specimens were Tachin-
idae of the genera Ormia Robineau-Des-
voidy and Anisia Wulp, it was surprising to
find some specimens of Stylogaster bian-
nulata in the lot. Most of the Stylogaster
specimens had been reared from Gryllus
rubens Scudder with a couple being reared
from unidentified Gryllus. Susan Wineriter
(personal communication) provided some
details about how these collections were
made. The crickets were collected mostly
in sound traps (Walker 1986) with some
taken in pitfall traps. Crickets were held
alive in the lab individually to check for
parasites for up to 9 d, the main aim being
to study the parasitism level in the crickets
by Ormia ochracea (Bigot). It was estimat-
ed that about 1000 crickets were censused,
and from these only 25-30 puparia of Styl-

659

ogaster biannulata were obtained. Puparia
were obtained from crickets collected in
May, August, September, October, Novem-
ber, and December. Although not observed,
the larvae probably emerged from their
cricket hosts because puparia were found
outside the host. In a few cases more than
one S. biannulata puparium came from a
single cricket, and in at least one case S.
biannulata and the tachinid Anisia gilvipes
(Coquillett) successfully parasitized a single
cricket. In the three cases where data were
recorded, the S. biannulata adults emerged
19-25 days after their puparia were formed.
Nothing is known about how Stylogaster
biannulata locates its host. It certainly is
not dependent on above-ground army ants
as they do not occur in the United States.

THE EGG OF STYLOGASTER BIANNULATA

The eggs of Stylogaster were first de-
scribed by Lopes (1937). Subsequently it
was discovered that the eggs have species-
specific characters which have been illus-
trated for many species (Lopes 1938, Lopes
and Monteiro 1959, Monteiro 1960, Smith
1967, 1979). The end opposite the micro-
pyle is pointed and has subapical] barbs, and
this end is embedded in the insect victim at
the time of oviposition. The actual mecha-
nism of oviposition is unknown (Kotrba
1997, reviews the data on this subject).

We obtained about a dozen eggs from a
female of Stylogaster biannulata that was
collected at Lick Creek Park, Brazos Coun-
ty, Texas. A figure (Smith and Peterson
1987: fig. 54.25) of the egg of this species
has been published but no further descrip-
tive details were given. Because the egg has
not been described in detail, we present in-
formation on its morphology, based on
scanning electron microscope examination.
SEMs have been published only for S. ma-
calpini Smith (Smith 1979: figs. 24-25)
and S. westwoodi (Hinton 1981: plate 119).

Description.—Clavate in shape (Fig. 1),
nonmicropylar end narrow, slightly arcuate
ventrally (Fig. 2), sharply pointed in ventral
view (Fig. 3), blade-like in lateral view

660 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

Photo No.=j}07 LL a 7-Aug-1997

JD ERTS
24-Jun-1996

Figs. 1-8. Egg of Stylogaster biannulata |, Whole egg. ventral view. 2, Whole egg, lateral view. 3, Non-
micropylar end, ventral view. 4, Non-micropylar end, lateral view. 5, Non-micropylar end, posterolateral view,
with inset showing surface sculpture of adjacent area. 6, Whole egg, anterolateral view of micropylar end, with
inset showing surface sculpture of egg body. 7, Surface sculpture of egg body at higher magnitieation. 8,
Micropylar end, showing concentric surface sculpture. Abbreviations: b, barb; es, eversible sac.

VOLUME 100, NUMBER 4

(Fig. +); with a single pair of small, lateral,
subapical barbs (Figs. 3-5, b); small ever-
sible sac present between bases of barbs
(Figs. 3-4, es), when not inflated this re-
gion appearing as a cavity (Fig. 5); entire
surface, except pointed end, with reticulate
surface sculpturing forming irregular cells,
the sculpturing strongest and appearing
scale-like near barbs (Fig. 5), the cells be-
coming more elongate and less strongly in-
dicated on main body (Figs. 6, 7), then
small and roughly concentric around micro-
pylar end (Fig. 8). Length 0.65 mm (n =
1).

Remarks.—Unfortunately the eggs we
examined were embedded in glue on a point
with the specimen from which they came,
and we were unable to clean them com-
pletely. In hydrated specimens, the eversi-
ble sac appears regularly rounded, as in
Smith and Peterson (1987: fig. 54.25), not
irregular as in the SEMs. Lopes (1937) con-
cluded that the larva enters the host through
this structure. Rettenmeyer (1961) postulat-
ed that this sac was inflated when the egg
was inserted into a host and helped hold the
egg in place and possibly also absorbed nu-
trients from the host. Based on osmotic ma-
nipulations, Stuckenberg (1963) was of the
opinion that the eversible sac functioned at
least in part in erecting the lateral barbs.
Hinton (1981) was skeptical of this theory
as he thought the barbs were more or less
immovable. We found some evidence to
support Stuckenberg’s idea. In Fig. 5, an
egg in which the sac is not everted, the
barbs are more closely appressed to the sur-
face of the egg, while in Fig. 3, where the
sac is everted, the barbs are more erect.

How the larva hatches from the egg is
still uncertain. Rettenmeyer (1961: fig. 1)
illustrated an egg found on a tachinid with
a larva just emerging from the micropylar
end, and therefore discounted Lopes’
(1937) theory that the larva emerged
through the eversible sac. Smith and van
Someren (1985) also reported observing
eggs that had embryoes visible inside that
were facing the micropyle. However, the

661

empty eggs of S. varifrons present on cock-
roach nymphs from which they dissected
larvae were intact, indicating that the larvae
had entered the host from near or through
the sac.

THE PUPARIUM OF STYLOGASTER BIANNULATA

We examined 29 or 30 puparia obtained
from the rearings of S. biannulata from
Gryllus already discussed in the section on
hosts. All specimens are now housed at the
National Museum of Natural History,
Smithsonian Institution, Washington, D.C.
As this life stage is unknown for any Styl-
ogaster, we are describing it here.

Description.—Reddish brown to dark
brown; ovoid (Fig. 9), surface finely wrin-
kled with crisscrossing network of slightly
raised bands (Figs. 10, 11, rb), at higher
magnification the surface appears more
deeply wrinkled (Fig. 11); posterior end
with lateral raised areas that are bilobed
(nearly c-shaped: Figs. 12, 13), with nu-
merous raised, cone-shaped tubercles that
end in a pore (Figs. 14, 15; peg-like exudate
present in many pores is apparently a result
of drying); posterior end near apex with
deep cavity with ovoid opening (Fig. 16);
inner surface of cavity finely wrinkled
(Figs. 17, 18), with larger wrinkles more or
less radiating from slightly depressed
points. Length 4.3-5.9 mm.

Remarks.—The structure of the pupar-
ium closely reflects the larval description
provided by Smith and van Someren
(1985). The bilobed, laterally raised areas
on the posterior end presumably correspond
to the tracheal system, and the sunken cav-
ity on the posterior end was also noted in
the larval description. We were not able to
describe the larval cephalopharyngeal skel-
eton that is present inside the anterior end
of the puparium. It is extremely small, and
we were not successful in several attempts
in removing it from the tissue in which it
was embedded. What we could see corre-
sponds with the larval mouthparts described
by Smith and van Someren (1985: figs. 10,
11).

662 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

JD

14-Aug-1997 M

Figs. 9-14, Puparium of Srvlogaster biannulata. 9, Whole puparium, lateral view. 10, Surface sculpture of
main body of pupanum. 11, Higher magnification view of surface sculpture of main body of puparium. 12.
Posterior end of puparium, lateral view. 13, Posterior end of puparium, posterior view. 14, Conical tubercles of
tracheal tissue on posterior end of puparium. Abbreviation: rb, raised band.

VOLUME (00, NUMBER 4

663

Figs. t5-18.
t6, Posterior cavity of puparium. (7, Inner surface of internal cavity of purparium. 18, (nner surface of internal
cavity of puparium, higher magnification.

We consider it doubtful that the second
instar larvae that Rettenmeyer (1961: 1016)
speculated might be Stylogaster are this ge-
nus. The large mouthparts and simple pos-
terior spiracles Rettenmeyer described are
not at all Tike those of the larvae described
by Smith and van Someren (1985) and the
puparia we examined.

ACKNOWLEDGMENTS

We thank Thomas J. Walker and Susan
A. Wineriter (University of Florida, Gaines-
ville) for providing the Stylogaster adults

Stylogaster biannulata. 15, Conical tubercles of tracheal tissue on posterior end of puparium.

and puparia as well as information on how
they were collected and reared. Robert A.
Wharton (Texas A & M University, College
Station) provided the specimen with eggs
for our study. Walter R. Brown and Susann
G. Braden (Electron Microscopy Labora-
tory Smithsonian Institution) assisted ma-
terially with SEM work. Steven W. Linga-
felter (Systematic Entomology Laboratory)
helped with scanning some of the SEM im-
ages into a more usable format. Wayne N.
Mathis (Smithsonian Institution), Andrew
V. Z. Brower (Smithsonian Institution).

664

Douglass R. Miller, and Allen L. Norrbom
(Systematic Entomology Laboratory) re-
viewed the manuscript.

LITERATURE CITED

Aldrich, J. M. 1930. American two-winged flies of the
genus Stylogaster Macquart. Proceedings of the
United States National Museum 78: 1-27.

Bates, H. W. 1863. The naturalist on the Amazons: A
record of adventures, habits of animals, sketches
of Brazilian and Indian life, and aspects of nature
under the Equator during eleven years of travel.
G. Routledge & Sons, London. x + 518 pp.

Camras, S. 1965. Family Stratiomyidae, pp. 625-632
In Stone, A. et al. eds., A catalog of the Diptera
of America north of Mexico. U.S.D.A. Agricul-
ture Handbook 276. United States Department of
Agriculture, Washington, D.C. iv + 1696 pp.

Camras. S. and P P Parrillo. 1985. Review of New
World Stylogaster (Diptera: Conopidae). Annals
ot the Entomotogical Society of America 78:1 11—
126:

Hinton, H. E. 1981. Biology of insect eggs in three
volumes. Volume | Pergamon Press, Oxford, New
York, Toronto, Sydney, Paris, Frankfurt. xxiv +
473 pp.

Kotrba, M 1997. Shoot or stab? Morphological evi-
dence on the unresolved oviposition techniqué in
Stylogaster Macquart (Diptera: Conopidae), in-
cluding discussion of behavioral observations.
Proceedings of the Entomological Society of
Washington 99: 614-622.

Lopes. H de S. 1937. Contnbnição ao conhecimento
do genero “Stvlogaster” Macquart. 1835, (Dipt.
Conopidae). Archivos do Instituto de Biologia
Vegetal 3: 257-293.

. 1938. Sobre uma nova especie do genro Styl-
ogaster Macquart, do Brasil (Dipt.: Conopidae).
Memórias do Instituto Oswaldo Cruz 33: 403-
405.

Lopes, H. de S. and L. Monteiro. 1959. Sébre algumas

PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

espécies brasileiras de Stylogaster Macq., com a
descrição de quatro espécies novas (Dipt., Cono-
pidae). Studia Entomologia 2: 1—24.

Monteiro, L. 1960. Insecta Amapaensia. Diptera: Con-
opidae: espécies do gênero Stylogaster Macquart,
1835. Memórias do Instituto Oswaldo Cruz 58:
103-114.

Rettenmeyer, C. W. 1961. Observations on the biology
and taxonomy of flies found over swarm raids of
army ants (Diptera: Tachinidae, Conopidae). Uni-
versity of Kansas Science Bulletin 42: 993-1066.

Smith, K. G. V. 1967. The biology and taxonomy of
the genus Stylugaster Macquart, 1835 (Diptera:
Conopidae, Stylogasterinae) in the Ethiopian and
Malagasy regions. Transactions of the Royal En-
tomological Society of London 119: 47-69.

. 1969. Further data on the oviposition by the
genus Siviogaster Macquart (Diptera: Conopidae,
Stylogasterinae) upon adult calyptrate Diptera as-
sociated with ants and animal dung. Proceedings
of the Royal Entomological Society of London

(A) 44: 35-37.

. 1979. The genus Stvlogaster (Diptera: Cono-
pidae, Stylogasterinae) in the Australian Region.
Australian Journal of Zoology 27: 303-310.

Smith, K. G. V. and B. V. Peterson. 1987. Conopidae,
Chapter 54, pp. 749-756 In McAlpine, J. F, ed.
Manual of Nearctic Diptera. Volume 2. Agricul-
ture Canada, Ottawa. i-vi: 675-1332.

Smith, K. G. V. and G. R. Cunningham-van Someren.
1985. The larva of Stylogaster varifrons Malloch
(Dipt., Stylogastridae). Entomologist’s Monthly
Magazine 121: 81-85.

Stuckenberg, B. R. 1963. A study on the hiology of
the genus Stylogaster, with the description of a
new species from Madagascar (Diptera: Conopi-
dae). Revue de Zoologie et de Botanique Aftricai-
nes 68: 251-275.

Walker, T. J. 1986. Monitoring the flights of field erick-
ets (Gryllus spp.) and a tachinid fly (Euphasiop-
tervx ochracea) in north Florida. The Florida En-
tomologist 69: 678-685.