The identity and recognition of African Tetrastichus species (Hymenoptera:
Eulophidae) associated with fruit flies (Diptera: Tephritidae)
1*
J. LaSalle & R.A. Wharton
2
1
Unit of Parasitoid Systematics, CABI Bioscience U.K. Centre (Ascot), Department of Biology,
Imperial College at Silwood Park, Ascot, Berks, SL5 7PY, U.K.
2
Department of Entomology, Texas A&M University, College Station, Texas, 77843, U.S.A.
The identity of the African fruit fly (Diptera: Tephritidae) parasitoids Tetrastichus giffardii
Silvestri, T. giffardianus Silvestri, T. dacicida Silvestri and T. oxyurus Silvestri (Hymenoptera:
Eulophidae) is discussed. Tetrastichus dacicida is synonymized with T. giffardii. Characters to
recognize and differentiate Tetrastichus giffardii, T. giffardianus, and T. oxyurus are presented.
Lectotypes are designated for all four of these species.
Key words: Eulophidae, Tetrastichinae, Tetrastichus, fruit flies, Tephritidae, parasitoid.
INTRODUCTION
Fruit flies in the family Tephritidae are major
pests in Africa and other parts of the world, and
one of the most serious and widespread pests of
edible fruits, Ceratitis capitata (Wiedemann)
(medfly), is of African origin. African parasitoids,
mostly opiine Braconidae and tetrastichine
Eulophidae, have been used in numerous
tephritid biological control programmes worldwide (Silvestri 1913b; Clausen et al. 1965; Clausen
1978; Steck et al. 1986). Most of these species were
initially introduced from Africa to Hawaii, then
redistributed from Hawaii to other parts of the
world (Clausen 1978; Wharton 1989). At least four
nominal species of Tetrastichus (Eulophidae) have
been shipped to Hawaii since 1914 for tephritid
biological control. Tetrastichus giffardianus Silvestri
has subsequently been sent to at least eight other
countries, and was the focus of a mass-rearing
programme directed primarily against medfly in
Brazil (Fonseca & Autuori 1940; Fonseca 1947). The
status of the other species is largely unknown, in
part because of the lack of adequate information
on how to differentiate the species. Proper identification of parasitoids used in biological control is
imperative, and the purpose of this paper is to
resolve questions regarding the identity of the
African Tetrastichus species attacking fruit flies and
to provide a key to their identification. The ability
to differentiate these species is particularly crucial
to studies attempting to verify apparent differences in patterns of host utilization by the various
eulophids that have been reared from tephritids.
*Present address: CSIRO Entomology, G.P.O. Box 1700, Canberra,
ACT, 2601, Australia.
The only other tetrastichine recorded from fruit
flies in Africa is Aceratoneuromyia indica Silvestri.
This, and possibly other species of Aceratoneuromyia which might be present, are easily distinguishable from Tetrastichus species by the presence
of three or more setae on the submarginal vein as
opposed to a single seta in Tetrastichus (Figs 6, 7).
Tetrastichines are commonly encountered in studies of the parasitoid fauna of tephritids in Africa,
but native tetrastichines appear to be absent from
the parasitoid community attacking New World
tephritids. It is likely that additional species of
Tetrastichus may be found parasitizing fruit flies in
Africa.
TAXONOMIC HISTORY
The genus Tetrastichus as it was traditionally
treated was one of the largest genera in the Chalcidoidea and contained the majority of species in
the subfamily Tetrastichinae. However, this was
not a natural classification and merely reflected
the difficult taxonomy of this group of insects.
Graham (1987) provided a reclassification of the
European Tetrastichinae, in which he divided
Tetrastichus into several smaller and more natural
groups; this classification has since been followed
by Bou…ek (1988), Graham (1991) and LaSalle (1994).
The genus Tetrastichus in its current sense is the
third largest genus of Tetrastichinae, and occurs
on all continents. Graham (1991) referred to a
small group of species within Tetrastichus, which
he called the murcia group (= subgenus Musciformia Kostjukov 1977). He stated that although
African Entomology 10(2): 297–304 (2002)
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African Entomology Vol. 10, No. 2, 2002
having a rather characteristic habitus, the group is
difficult to define. Species have relatively long
setae on the vertex (their length 0.7–1.0 that of the
ocellar diameter), and moderately long to very
long setae on the eyes (0.4–0.7 the ocellar diameter). Other characters that help to define this
group (taken from Graham’s key) are: frons with
oblong median area; mouth width at most only
slightly greater (less than 1.3 times) than malar
space; antenna with scape shorter than eye, its
front edge with six or fewer setae; mesosoma with
distinct engraved reticulation; setae on hind
margin of pronotum and adnotaular setae relatively long and suberect; hind coxa more strongly
and coarsely reticulate dorsally than elsewhere,
usually more or less rugulose dorso-basally; gaster
less than twice as long as broad, shorter than head
plus mesosoma, with last tergite less than 1.7 times
longer than broad; ovipositor sheaths reaching
apex of last tergite. Graham (1991) placed five
European species in the murcia group, T. murcia
(Walker), T. dasyops Graham, T. atratulus (Nees),
T. brachyopae Graham, T. solvae Graham, and mentioned that the African T. giffardii Silvestri and
T. giffardianus also belong to this group. All species
in this group appear to be parasitoids of Diptera. It
is not clear that T. oxyurus belongs in this group, as
the setae on its vertex and mesosoma are relatively
short and not semi-erect.
MATERIALS AND METHODS
Lectotypes are designated for four species in this
paper. These were chosen from material originally
collected by Silvestri and stored in alcohol for over
80 years. The poor condition of the material and
similarity of the species involved could lead to
confusion over the identity of these species. In all
cases, lectotypes were designated in order to
maintain stability of usage for the names.
Type material for this study is all from Silvestri
material in the collection of the Dipartimento di
Entomologia e Zoologia Agraria dell’Università,
Portici, Italy (DEZA). In many cases, not all the
type material was found in DEZA. However,
Silvestri routinely exchanged material with other
dipterists and hymenopterists of the era. These
included type specimens, although they were not
always correctly labelled as such. Thus, it is not at
all surprising that only parts of his series are at
Portici. Nonetheless, it was decided to designate
lectotypes in each case from among the original
Silvestri material that was retained in DEZA.
Other material was examined from The Natural
History Museum, London (BMNH), the United
States National Museum, Washington (USNM),
the Bernice P. Bishop Museum, Honolulu (BPBM),
and collections made as part of this study in Texas
A&M University, College Station (TAMU) and the
International Centre for Insect Physiology and
Ecology, Nairobi, Kenya (ICIPE). Not all material
examined is listed under each species, but new
records are indicated.
Terminology is taken from LaSalle 1994.
Genus Tetrastichus Haliday, 1844
Diagnosis. Submarginal vein with one dorsal seta
(with the exception of T. howardi, T. inferens which
have two). Propodeum with a characteristic carina
in the shape of an inverted Y just medial to the
spiracle (Fig. 8); median panels of the propodeum
generally reticulate. Outer surface of hind coxa
usually with strong reticulations. Body usually
black to dark or bright metallic, generally without
light coloration.
Key to female African Tetrastichus species
associated with fruitflies
1. Gaster long, pointed apically, clearly more
than 1.5 times as long as mesosoma (Fig. 2);
hypopygium extending less than half the
length of gaster, ovipositor greater than twothirds the length of gaster, last tergite longer
than wide. Antenna without semi-erect
setae, or with shorter setae (Fig. 3, cf.
Figs 10, 11); antennal segments all distinctly
longer than wide; setae on vertex between
lateral ocellus and eye margin usually
shorter than greatest width of ocellus (Fig. 1)
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . T. oxyurus
— Gaster shorter, rounded apically, clearly less
than 1.5 times as long as mesosoma (Fig. 5);
hypopygium extending half or more the
length of gaster; ovipositor less than twothirds the length of gaster; last tergite wider
than long. Antenna with more distinct
semi-erect setae (Figs 10, 11, cf. Fig. 3); at
least some antennal segments quadrate to
wider than long; setae on vertex between
lateral ocellus and eye margin usually longer than greatest width of ocellus (Fig. 4) . . . 2
2. Speculum large, extending along anterior
margin of wing to base of stigmal vein
LaSalle & Wharton: African Tetrastichus species associated with fruit flies
299
Figs 1–5. Differences of Tetrastichus oxyurus from T. giffardii and T. giffardianus. 1–3. T. oxyurus female: 1, head;
2, mesosoma and metasoma; 3, antenna, showing scape to club only. 4–5. T. giffardii female: 4, head; 5, mesosoma
and metasoma.
(Fig. 7). Basal vein mostly without setae,
base of cubital vein mostly without setae, so
that speculum is largely open behind. Paraspiracular carina usually not as distinct as in
giffardii, with outer branch poorly defined
(Fig. 9, cf. Fig. 8) . . . . . . . . . . . . . . T. giffardianus
— Speculum small, extending along anterior
margin of wing much less than half the distance to the base of stigmal vein (Fig. 6).
Basal and cubital veins complete; speculum
completely closed behind. Paraspiracular
carina distinct, with outer branch well defined (Fig. 8, cf. Fig. 9) . . . . . . . . . . . . T. giffardii
Tetrastichus giffardii Silvestri, Figs 4–6, 8,
10–15
Tetrastichus giffardii Silvestri, 1913a: 205–206.
Lectotype 9 [present designation] Nigeria,
Olokemeji, 27.xi.1912, F. Silvestri, ex Ceratitis
antisticta (DEZA). 49, 58 paralectotypes,
same data as lectotype (DEZA).
Tetrastichus dacicida Silvestri, 1915: 375–377.
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African Entomology Vol. 10, No. 2, 2002
Figs 6–9. Differences between Tetrastichus giffardii and T. giffardianus. 6–7. Forewings: 6, T. giffardii; 7, T. giffardianus. 8–9. Scutellum and propodeum: 8, T. giffardii; 9, T. giffardianus.
Lectotype 9 [present designation] Cameroon, Victoria, i.1913, F. Silvestri, ex. Dacus
bipartitus [= Dacus bivittatus] (DEZA). 28
paralectotypes, same data as lectotype
(DEZA). Syn. n.
Biology. From the following hosts (all Tephritidae): Bactrocera cucurbitae (Coquillett), Bactrocera
dorsalis (Hendel), Ceratitis anonae Graham, Ceratitis
antisticta Bezzi, Ceratitis capitata (Wiedemann),
Ceratitis colae Silvestri, Ceratitis ditissima (Munro),
Ceratitis giffardi Bezzi (probably a synonym of C.
cosyrae: DeMeyer 1998), Ceratitis punctata
(Wiedemann), Ceratitis rosa Karsch var. fasciventris,
Ceratitis simi (Munro), Dacus bivittatus (Bigot),
Trirhithrum coffeae Bezzi. Host information mainly
taken from Noyes (1998, as either T. giffardii or T.
dacicida), although nomenclature has been updated using Norrbom et al. (1998). Although both
T. giffardii and T. giffardianus are widely polyphagous, one major pest species listed above,
Ceratitis rosa and its variety fasciventris, is a definite
host for T. giffardii, whereas we have not yet confirmed it as a host for T. giffardianus.
Greathead (1972) reported that T. giffardii attacked fruit flies in Ugandan coffee, but did not act
in a density dependent manner, and only reached
detectable levels when host populations were
high. The present study shows that this species
can be fairly common in Kenyan squash.
Tetrastichus giffardii is a gregarious, koinobiont
endoparasitoid. Silvestri (1913b) stated that T.
giffardii oviposited in the eggs or young larvae of
their hosts. This is different from T. giffardianus,
which prefers older larvae (4–7 days) for oviposition (Purcell et al. 1996). Several adults will
emerge from each host puparium. Silvestri also
LaSalle & Wharton: African Tetrastichus species associated with fruit flies
301
Figs 10–15. Variation in Tetrastichus giffardii. 10–11, female antenna (note difference in relative size of first two funicular segments); 12–13, male antenna (note difference in relative size of first two funicular segments); 14–15, ventral
sensory plaque on male scape.
noted (1915) that the biology of T. dacicida was
similar to that of T. giffardii.
Distribution. Congo, Cameroon, Benin, Ghana,
Kenya, Nigeria, Uganda (Noyes 1998). Imported
into Hawaii against Bactrocera dorsalis, but without
major impact (Clausen 1978). All recent records
from Hawaii are of T. giffardianus, suggesting that
T. giffardii may never have established there.
Remarks. T. giffardii: Silvestri (1913a) did not
mention how many specimens he used in the description of T. giffardii. However, he did state that
between 15 and 34 individuals emerged from each
Ceratitis or Dacus pupa, indicating that he had seen
many specimens. The lectotype was selected from
10 specimens (59, 58) in the DEZA collection, so
some type specimens are missing.
T. dacicida: Silvestri (1915) made no mention of
how many specimens he had when describing
T. dacicida. The lectotype was selected from three
specimens (19, 28) in the DEZA collection.
The decision to synonymize T. dacicida with T.
giffardii was not a simple one. Table 1 lists characters given by Silvestri (1915) to separate the
two species, with comments on each character.
Basically, none of the characters proved to be
consistent and without variation. Examination of
type material did not show characters that could
be used, or even that were always consistent
with Silvestri’s observations on the difference;
and field collected material could not be divided
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Table 1. Characters provided by Silvestri (1915) to distinguish Tetrastichus dacicida from T. giffardii.
Sex
T. dacicida
T. giffardii
Comments
Female Funicular segments 2 and 3 longer Funicular segments shorter than Subjective and variable. It is not clear just what
than in T. giffardii.
in T. dacicida.
Silvestri meant by shorter and longer as he did not
give actual range measurements. Certainly this is
variable in the material examined (Figs 10–11).
Female Mesoscutum with more lateral
setae [from the description seven
short setae on each side].
Mesoscutum with fewer lateral Most T. giffardii examined have 3–4 adnotaular
setae [from the redescription
setae. None have seven, including the T. dacicida
(Silvestri 1913b) three setae on types.
each side].
Female A seta situated in base of wing
near the base of the basal vein.
This apparently refers to a basal
seta in the cubital vein which is
placed basal to junction of cubital
vein and basal vein.
Seta absent
We have seen some series where this seta is
generally present, and these specimens also tend
to have F2 and F3 longer. However, the mesoscutum still has only 3–4 adnotaular setae, the
male antenna does not display the ‘T. dacicida
characters’, and the character is not consistent in
the entire series.
Male
Scape with ventral plaque longer,
more or less divided.
Scape with ventral plaque
shorter, not divided.
It is again not clear just what Silvestri meant by
shorter and longer as he did not give actual range
measurements. As to the division, this plaque is
mostly undivided in all T. giffardii specimens
(including the only male dacicida paralectotype
which has antennae). A few specimens were
examined in which this plaque is malformed and
apparently in two parts. This appears to be just an
occasional aberration, and not a valid species
level character (Figs 14–15).
Male
The first funicular segment shorter The first funicular segment
than the second.
longer than the second.
into groups, which would be indicative of species
differences. Thus, we are synonymizing T. dacicida
with T. giffardii.
Tetrastichus giffardianus Silvestri, Figs 7, 9
Tetrastichus giffardianus Silvestri, 1915: 372–375.
Lectotype 9 [present designation] Benin
(Dahomey), Cotonou, ii.1913, F. Silvestri, ex
Ceratitis giffardi (DEZA). 29, 28 paralectotypes, same data as lectotype (DEZA).
Biology. From the following hosts (all Tephritidae): Bactrocera cucurbitae (Coquillett), Bactrocera
dorsalis (Hendel), Bactrocera latifrons (Hendel),
Bactrocera passiflorae (Froggatt), Bactrocera tryoni
(Froggatt), Bactrocera xanthodes (Broun), Ceratitis
anonae Graham, Ceratitis capitata (Wiedemann),
Ceratitis giffardi Bezzi (probably a synonym of
C. cosyrae: DeMeyer 1998), Ceratitis punctata
(Wiedemann), Dacus bivittatus (Bigot), Dacus
ciliatus (Loew), Dacus demmerezi (Bezzi), Neoceratitis cyanescens (Bezzi), Trirhithrum nigrum
(Graham). Host information mainly taken from
Noyes (1998), although nomenclature has been
This is variable, even in the series of five male
T. giffardii paralectotypes, as at least one of them
has F1 distinctly shorter than F2 (Figs 12–13).
updated using Norrbom et al. (1998).
During the course of the present study, and
through examination of the literature, this species
has often been reared from collections of fruits
from which several species of fruit flies have also
emerged. Under these circumstances, precise host
relationships could not be determined. Although
several additional species of hosts have been
implicated in this fashion, they were not included
in the host lists.
This species is a gregarious, koinobiont, larval–
pupal endoparasitoid (Clausen 1978; Ramadan &
Wong 1990; Purcell et al. 1996). The parasitoid oviposits into mature host larvae, and the adults
emerge from young pupae after the puparium is
formed.
Tetrastichus giffardianus has been used as a biological control agent against a variety of fruit flies
in several countries (Clausen 1978; Purcell 1998).
Because of its wide host range, it has recently been
studied to see if it has a non-target effect on other
fruit fly species. It was found not to parasitize any
non-frugivorus tephritids in Hawaii (Purcell et al.
LaSalle & Wharton: African Tetrastichus species associated with fruit flies
1997; Duan & Messing 1998).
Distribution. Benin, Cameroon, Egypt, Kenya,
Nigeria, Sierra Leone, Tanzania. Introduced into
the Réunion Islands; in the New World into
Argentina, Brazil, Puerto Rico, U.S.A. (California);
and in the Australia/Pacific region into Australia,
Fiji, Hawaii, New Caledonia, Samoa, Vanuatu
(Noyes 1998; Clausen 1978). Establishment was
never documented in some of the areas of introduction (e.g. California), and its current status in
all but Hawaii is unknown.
Remarks. Silvestri (1915) made no mention of
how many specimens he had when describing
T. giffardianus; however, he did mention that this
species was known from Nigeria and Benin
(Dahomey). The lectotype was selected from five
specimens (39, 28) from Benin in the DEZA collection, so some type material is missing.
Tetrastichus oxyurus Silvestri, Figs 1–3
Tetrastichus oxyurus Silvestri, 1913b: 138–139.
Lectotype 9 [present designation] Nigeria,
Olokemeji, F. Silvestri, ex Carpophthoromyia
(as Ceratitis) tritea (DEZA). 29 paralecto-
303
types, same data as lectotype (DEZA).
Biology. This species was described from 10 specimens that emerged from a puparium of Carpophthoromyia tritea (Walker).
Distribution. Kenya (new record), Nigeria.
Remarks. Silvestri (1913b) described this species
from 10 female specimens. The lectotype was
selected from three female specimens in the DEZA
collection, so some type specimens are missing.
ACKNOWLEDGEMENTS
We thank G. Viggiani and E. Guerrieri for kindly
locating and loaning the Silvestri types. M. Purcell
provided recently collected material from Hawaii
and S. Kimani allowed us the opportunity to
examine material acquired under ICIPE’s African
fruit fly initiative. Other curators who have loaned
material or given access to their collections are:
K. Arakaki (BPBM), J. Noyes (BMNH), M. Schauff
(USNM). M. De Meyer and I. White supplied
information on the tephritid host names. This
work was supported in part by USDA/NRI grant
No. 9703184 and the Texas Agricultural Experiment Station.
REFERENCES
BOU„EK, Z. 1988. Australasian Chalcidoidea (Hymenoptera). A Biosystematic Revision of Genera of Fourteen
Families, with a Reclassification of Species. CAB International, Wallingford, U.K.
CLAUSEN, C.P. (Ed.). 1978. Introduced Parasites and Predators of Arthropod Pests and Weeds: a World Review. Agricultural Handbook No. 480. U.S. Department of
Agriculture, Washington, D.C.
CLAUSEN, C.P., CLANCY, D.W. & CHOCK, Q.C. 1965.
Biological control of the Oriental fruit fly (Dacus
dorsalis Hendel) and other fruit flies in Hawaii. United
States Department of Agriculture, Technical Bulletin
1322: 1–103.
DE MEYER, M. 1998. Revision of the subgenus Ceratitis
(Ceratalaspis) Hancock (Diptera: Tephritidae). Bulletin
of Entomological Research 88: 257–290.
DUAN, J.J. & MESSING, R.H. 1998. Effect of Tetrastichus
giffardianus (Hymenoptera: Eulophidae) on nontarget flowerhead-feeding tephritids (Diptera:
Tephritidae). Environmental Entomology 27: 1022–
1028.
FONSECA, J.P. 1947. Criação da vespinha africana no
Instituto Biológico. O Biológico 13: 147–156.
FONSECA, J.P. & AUTUORI, M. 1940. Processos de
criação da ‘Vespinha africana’ parasita da ‘mosca do
Mediterraneo.’ O Biológico 6: 345–351.
GRAHAM, M.W.R. DE V. 1987. A reclassification of the
European Tetrastichinae (Hymenoptera: Eulophidae), with a revision of certain genera. Bulletin of the
British Museum (Natural History). Entomology Series
55: 1–392.
GRAHAM, M.W.R. DE V. 1991. A reclassification of the
European Tetrastichinae (Hymenoptera: Eulophidae): revision of the remaining genera. Memoirs of the
American Entomological Institute 49: 1–322.
GREATHEAD, D.J. 1972. Notes on coffee fruit-flies and
their parasites at Kawanda (Uganda). Technical Bulletin of the Commonwealth Institute of Biological Control
No. 15: 11–18.
LaSALLE, J. 1994. North American genera of Tetrastichinae (Hymenoptera: Eulophidae). Journal of
Natural History 28: 109–236.
NORRBOM, A.L., CARROLL, L.E., THOMPSON, F.C.,
WHITE, I.M. & FREIDBERG, A. 1998. Systematic
database of names. Myia 9: 65–251.
NOYES, J.S. 1998. Catalogue of the Chalcidoidea of the World.
Biodiversity Catalogue Database and Image Library
CD-ROM Series. Expert Center for Taxonomic Identification, University of Amsterdam, Amsterdam.
PURCELL, M.F. 1998. Contribution of biological control
to integrated pest management of tephritid fruit flies
in the tropics and subtropics. Integrated Pest Management Reviews 3: 63–83.
PURCELL, M.F., DUAN, J.J. & MESSING, R.H. 1997.
Response of three hymenopteran parasitoids introduced for fruit fly control to a gall-forming tephritid,
Procecidochares alani (Diptera: Tephritidae). Biological
Control 9: 193–200.
PURCELL, M.F., VAN NIEUWENHOVEN, A. &
BATCHELOR, M.A. 1996. Bionomics of Tetrastichus
304
African Entomology Vol. 10, No. 2, 2002
giffardianus (Hymenoptera: Eulophidae): an endoparasitoid of tephritid fruit flies. Environmental
Entomology 25: 198–206.
RAMADAN, M.M. & WONG, T.T.Y. 1990. Biological observations on Tetrastichus giffardianus (Hymenoptera:
Eulophidae), a gregarious endoparasitoid of the
Mediterranean fruit fly and the Oriental fruit fly
(Diptera: Tephritidae). Proceedings, Hawaiian Entomological Society 30: 59–62.
SILVESTRI, F. 1913a. Notizia preliminare di un Tetrastichus (Immenottero Calcidide) parassita di specie di
Ceratitis e Dacus nell’Africa occidentale. Reale
Accademia dei Lincei 22: 205–206.
SILVESTRI, F. 1913b. Viaggio in Africa par cercare
parassiti di mosche dei frutti. Bollettino del Laboratorio
di Zoologia Generale e Agraria della R. Scuola Superiore
d’Agricoltura in Portici 8: 1–164.
SILVESTRI, F. 1915. Descrizione di nuovi imenotteri
calcididi africani. Bollettino del Laboratorio di Zoologia
Generale e Agraria della R. Scuola Superiore d’Agricoltura
in Portici 9: 337–377.
STECK, G.J., GILSTRAP, F.E., WHARTON, R.A. & HART,
W.G. 1986. Braconid parasitoids of Tephritidae
[Diptera] infesting coffee and other fruits in westcentral Africa. Entomophaga 31: 59–67.
WHARTON, R.A. 1989 Classical biological control of
fruit-infesting Tephritidae. In: Robinson, A.S. &
Hooper, G. (Eds) Fruit Flies, Their Biology, Natural
Enemies and Control. 303–313. World Crop Pests 3B.
Elsevier, Amsterdam.
Accepted 20 November 2001