Gephyraulus mangiferae (Felt), N. comb. (Diptera: Cecidomyiidae) : A mango pest from India newly recorded from the Western Hemisphere

2006·5.2 MB·

by  Raymond J Gagné

PROC. ENTOMOL. SOC. WASH.
108(4), 2006, pp. 930-937
GEPHYRAULUS MANGIFERAE (FELT), N. COMB. (DIPTERA:
CECIDOMYIIDAE): A MANGO PEST FROM INDIA NEWLY RECORDED
FROM THE WESTERN HEMISPHERE
RAYMOND J. GAGNE AND JEAN ETIENNE
(RJG) Systematic Entomology Laboratory, PSI, Agricultural Research Service,
U.S. Department of Agriculture, c/o National Museum of National History,
Smithsonian Institution, P.O. Box 37012, MRC 168, Washington, DC 20013-7012,
U.S.A. (e-mail: [email protected]); (JE) Institut National de la Recherche
Agronomique, Centre Antilles Guyane, Domaine de Duclos, F-97170, Petit-Bourg,
Guadeloupe
Abstract.4Dasineura mangiferae Felt (n. comb.) transferred here to the genus
Gephyraulus, is a cecidomyiid native to India that lives in and destroys the flowers of
mango, Mangifera indica (Anacardiaceae). It is reported here from Guadeloupe,
French West Indies, as the first record for the Americas. Adults of both sexes and the
pupa and larva are redescribed with illustrations. This gall midge is discriminated
from its congeners as well as from Procontarinia mangiferae (Felt), a second pest of
mango inflorescences from India already in the West Indies and South America.
Gephyraulus was previously known only in the Palearctic Region from nine species,
all infesting flowers of Brassicaceae. Procystiphora indica Grover and Prasad from
India is also moved to Gephyraulus (n. comb.).
Key Words: Diptera, Cecidomyiidae, gall midges, Guadeloupe, mango pest
In 2004 a cecidomyiid, Dasineura ing further was noted at that time
mangiferae (Felt), was discovered in concerning its biology. Felt recognized
Guadeloupe, French West Indies, among that the species 8<8present[ed] marked
inflorescences of mango, Mangifera in- peculiarities for the genus= and only
dica L. (Anacardiaceae). This is the first tentatively placed it in Dasineura. Grover
notice of this gall midge in the Americas. and Prasad (1966) and Prasad (1967,
Native to India where it is widely 1971) studied the biology and morphol-
distributed, this gall midge is a serious ogy of all stages of this species in India.
pest there (Venkatsubba 1940, Prasad Grover and Prasad (1966) placed it in
1971). It has also been recorded from Procystiphora because of the strongly
Hawaii (Anonymous 1981) where it is modified ovipositor. Procystiphora is
evidently an immigrant. Larvae feed in a Holarctic genus of three species on
developing flowers that become enlarged Cyperaceae and Juncaceae. The particu-
and distorted into conical galls. lar conformation of the modified ovipos-
This insect Was first described as itors of those species is different from
Dasineura mangiferae by Felt (1927) that found in the present species (see
from a series of females reared from below). In our search for a generic home
mango flowers in southern India. Noth- for this species, it was a surprise to find
VOLUME 108, NUMBER 4 931
that D. mangiferae fits satisfactorily into that follows, anatomical terminology of
Gephyraulus. This genus is otherwise the adult stage follows McAlpine et al.
known from nine species from the (1981) and that of the larval stage
western and central Palearctic Region follows Gagné (1989).
(Gagné 2004) that feed in flowers of
Brassicaceae in the same way as does D. Gephyraulus Rubsaamen 1916
mangiferae on mango. The new addition Diagnosis.4Adult habitus generally
considerably broadens the regional and similar to that of Dasineura: adult
host distribution of Gephyraulus. Procys- extensively covered with scales among
tiphora indica Grover and Prasad (1966), other setation; antennal flagellomeres
another species from mango flowers in sexually dimorphic, those of male (except
India and with a_ generally similar apicalmost) with distinct necks, those
Ovipositor, is also transferred to Gephy- of female without; palpus 4-segmented;
raulus here. wing with Rs vein shorter than wing,
One other Indian gall midge, Procon- joining C definitely anterior to wing
tarinia mangiferae (Felt), is already apex; tarsal claws with strong teeth;
known from mango in the West Indies empodia as long as claws; pulvilli about
and Brazil (Gagné 1994, 2004). It also half length of claws. Third-instar larva
feeds on the inflorescence, where it forms completely covered with verrucae and
swellings on growing tips and buds. This with complete set of larval papillae
species arrived with mango stock, pre- present, the dorsals, pleurals, ventrals,
sumably from India, by the early 20th and terminals with long setae.
century and was named by Felt (1911) Gephyraulus is unique among Dasi-
from specimens from St. Vincent, West neurini for the following combination of
Indies, and named again by Tavares characters: female 7th and 8th tergites
(1918) from Bahia, Brazil. It is one of and 7th sternite (Fig. 4) larger and more
several species of Old World gall midges strongly sclerotized than preceding ter-
that were named first from New World gites and sternites, the 8th tergite addi-
colonizations. tionally with elongate anterior apodemes
that extend beneath the 7th tergite, and
MATERIALS AND METHODS the 7th sternite trapezoid; distal half of
Adults were reared in the laboratory ovipositor stiff, pigmented, becoming
from larvae collected in mango inflor- bilaterally compressed toward apex, cul-
escences. Some larvae and _ resulting minating in narrow, strongly sclerotized,
pupae and adults were killed and stored glabrous, fused cerci (Figs. 546) with
in 70% ethyl alcohol. Specimens for a large pair of sensoria situated dorsally
microscopic study were mounted on just posteriad of a series of short
glass slides in Canada balsam using the dorsoapical setae; female pupa (Fig. 16)
method outlined in Gagne (1989, 1994) with elongate 7th and 8th segments to
and some pupae were critical-point dried accommodate modified postabdomen.
and mounted on stubs for SEM photo- See also Solinas 1982, Sylvén and Solinas
graphs. The syntypes of G. mangiferae 1989, and Sylvén and Tastas-Duque
are part of the Felt Collection on loan to 1993 for illustrations of a range of
the Systematic Entomology Laboratory, species, especially the last for SEM
USDA, from the New York State photographs and authoritative com-
Museum in Albany. The other study ments on the ovipositor of several species
specimens are deposited in the National on Brassicaceae.
Museum of Natural History, Washing- Discussion.4Gephyraulus belongs to
ton, DC (USNM). In the description the cecidomyiine supertribe Lasiopteridi
PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
Figs. 1-9. Gephyraulus mangiferae. 1, Wing. 2, Female third flagellomere (ventral). 3, Male third
flagellomere (ventral). 4, Female postabdomen, seventh segment to end, arrow indicating anterior
apodeme of eighth tergite (dorsolateral). 5, Fused female cerci (enlarged, lateral). 6, Same (dorsal). 7-9,
Male terminalia. 7, Right gonopod not shown (dorsal). 8, Parameres (dorsal). 9, Left gonopod not
shown (ventral).
and the tribe Dasineurini. Except for the Of interest in this context is Dasineura
female postabdomen, the included spe- amaramanjarae Grover (1965) because it
cies could pass for Dasineura and _ pre- is also known from mango inflorescences
sumably descended from an ancestor of in India, but shows no particular re-
some part of the large polyphyletic semblance in either sex to Gephyraulus.
aggregate of 448 described species Its male genitalia in particular are an
(Gagné 2004) now assigned to Dasineura. oddity for Dasineura. Because the gono-
VOLUME 108, NUMBER 4 933
coxites conspicuously bulge out mesally 1.3-1.5 mm in male (m = 7), 1.341.5 mm
near midlength and the gonostyli are in female <(a "4 8)" R= mectine 4C
extremely elongate and narrow, D. amar- appreciably anterior to wing apex; C
amanjarae appears to fit instead in broken at juncture with Rs; Cu forked.
Jaapiella Ruibsaamen. Male abdomen: First through fifth
In the key to genera of Neotropical tergites rectangular, with single row of
Lasiopteridi in Gagné 1994, Gephyraulus posterior setae continuous across tergite,
will run to Dasineura. The characters of 1-2 lateral setae each side, 2 trichoid
Gephyraulus that separate it from Dasi- anterior sensilla, and elsewhere covered
neura are: the modified female postabdo- with scales; sixth and seventh tergites
men, including the strongly sclerotized generally similar to preceding except
7th and 8th terga and the bilaterally unsclerotized posteromesally and poste-
flattened ovipositor with its stiff, gla- rior setae present only laterally; eighth
brous, fused cerci (Figs. 4-6); the medi- tergite short, especially posteromesally,
ally angled parameres and the foreshor- without vestiture except for anterior
tened gonostyli of the male genitalia trichoid sensilla; sternites 2-8 with most-
(Figs. 7-9), which presumably serve to ly single row of posterior setae, another
accommodate the shape of the oviposi- single row of setae, not continuous
tor; and the lengthier posterior end of the across sclerite near midlength, and with
female pupa conforming to the robust anterior pair of trichoid sensilla. Genita-
and stiff adult postabdomen inside lia (Figs. 7-9): gonocoxite cylindrical;
gonostylus short, setulose on most of
(Fig. 16).
venter, ridged on most of dorsum;
Gephyraulus mangiferae (Felt), paramere with short, dorsal, long-setu-
new combination lose lobe and long, linear, short setulose
ventral lobe flanking aedeagus, ventral
(Figs. 1-16)
lobe directed mesally; cercus rounded
Adult.4Head: Eyes nearly contiguous
and setose apically; hypoproct divided
at vertex, separated by diameter of | or 2
apically into 2, rounded lobes, each with
facets, facets circular, closely approxi-
long seta; aedeagus shorter than para-
mated except about '% facet diameter
meres, its apex flat.
apart near midheight. Vertex of occiput
Female abdomen (Figs. 4-6): First
rounded. Frons with setae mixed with
through sixth tergites and sternites as in
scales. Labella hemispherical in frontal
male; seventh and eighth tergites and
view, with several setae. Antenna: Scape
seventh sternite longer and more sclero-
and pedicel spheroid, each wider than
tized and more darkly pigmented than
long; 11413 flagellomeres present, first preceding sclerites; seventh tergite trape-
and second connate, distal two in female zoid, widest apically with single, contin-
usually fused; male first through penul- uous row of posterior setae, scattered
timate flagellomeres (Fig. 3) with defi- scales on posterior half, and anterior pair
nite necks; female flagellomeres (Fig. 2) of trichoid sensilla; eighth tergite roughly
without necks. rectangular, slightly longer than seventh,
Thorax: Scutum with 2 lateral and 2 with pair of anterior apodemes extending
dorsocentral rows of setae mixed with beneath seventh tergite, an anterior pair
scales. Scutellum with a group of setae of trichoid sensilla the only vestiture.
and scales on each side. Anepisternum Ovipositor elongate, protrusible, sparse-
with scales on dorsal third, anepimeron ly covered with short setae, distal half
with row of setae, pleura otherwise bilaterally flattened, rigid, with stiffening
lacking vestiture. Wing (Fig. 1): length, ridges, slightly more than twice length of
934 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
: |
ty) 4 Y i ae YU Jove
eu Ly, wy 8L u Ul
Ge Cam i ctl
v 3
L
L
i
AVRO RIAIES SII NINN NANNY vvv~~ +S ais!
L
L
L
L
10
2
13
Figs. 10-13. 10, 11, Gephyraulus mangiferae. 10, Larval spatula with associated papillae. 11, Larval
eighth and terminal segments (dorsal). 12-13, Procontarinia mangiferae. 12, Larval spatula. 13, Larval
eighth and terminal segments (dorsal).
eighth tergite, fused cerci high, very capsule. Spatula (Fig. 10) anteriorly di-
narrow, smooth, asetulose, with setae vided into two short, nearly equilateral
only at tapered apex and ventrally, teeth or roughly erose (Fig. 10) and with
a large pair of sensoria situated dorsally long, parallel-sided posterior shaft. Pa-
just posteriad of a _ series of short pillae following pattern basic for super-
dorsoapical setae. Hypoproct soft, line- tribe Lasiopteridi (Gagné 1989, fig. 19).
ar, with two small apical setae. Type series.4Syntypes, four 2, two
Pupa (Figs. 144-16).4Cephalic sclerite on each of two slides, from mango
with two raised bumps, each with 2 flowers, Coimbatore, India, II-8-1924,
papillae, one with elongate seta, the Y..Re |) Raot mcollx: 2Felty +Collection
other without seta. Abdomen evenly No. 3452, deposited in New York State
covered with spicules on all surfaces. Museum, Albany.
Seventh and 8th abdominal segments Other specimens examined.4GUA-
enlarged, longer than preceding seg- DELOUPE: Belair, Vieux-Habitants,
ments. from flowers of mango, IV-14-2004,
Third-instar larva. -Y ellow-orange. An- GR3032,'5 ¢:°5 22isameedatasexcept
tenna about twice as long as wide. V-17-2004, GR3080, 3 6, 3 2, 5 pupae,
Cephalic apodemes as long as_ head 3 larvae; same data except II-17-2005,
VOLUME 108, NUMBER 4
Figs. 14-16. Pupa of Gephyraulus mangiferae. 14, Head and thorax (ventral). 15, Same (lateral). 16,
Female pupa (lateral).
GR3127, 2 36, 3 2. HAWAII: Hilo, I-4- of three species that live in culms of
1981, E. Yoshioka, 5 6,5 2. INDIA: vic. Juncus and Carex (Gagné 2004).
Allahabad, P. Grover, 4 3, 4 &, 6 larvae. Grover and Prasad (1966) and Prasad
Remarks.4Gephyraulus mangiferae dif- (1967, 1971) reported four larval instars
fers in its genitalia from congeners on for G. mangiferae, but they apparently
Brassicaceae. The male gonostyli are took for evidence of different instars the
shorter than those of any other species relative sclerotization of the spatula,
and the ventral lobe of the parameres is whether it was weakly or strongly de-
uniquely inclined mesally. The dorsal veloped. A late second instar may
edge of the female fused cerci as seen in sometimes show the spatula of the de-
lateral view is fairly straight (Fig. 5), veloping third instar inside (Gagne and
whereas it is definitely concave in all Doane 1999); also, an early third instar
other non-mango species. may not have a fully developed and
This species was once placed in Pro- pigmented spatula when newly molted.
cystiphora by Grover and Prasad (1966) Where close observation of actual molts
but the ovipositor of that genus is shaped and/or head capsule measurements have
differently. The 7th and 8th abdominal been made, only three instars can be
tergites of Procystiphora are narrower accounted for in Cecidomyiidae (cf.
than in Gephyraulus, the 8th without Solinas 1965, Wyatt 1967, Parnell 1969,
anterior subdermal apodemes and longi- Gagné and Hatchett 1989, Gagné and
tudinally divided for most of its length, Doane 1999).
and the 7th sternite is elongate and Larvae of both Gephyraulus mangi-
rectangular; the ovipositor is strongly ferae and Procontarinia mangiferae ma-
bilaterally compressed, particularly the ture simultaneously on mango but can be
distal halt9 and the fused9 8cerci <are easily distinguished. Larvae of G. man-
narrow, sharply tapered and pointed, giferae are covered with rough verrucae,
their surface covered with short setae. have a rounded posterior end and mostly
For figures see Gagné 1975 and Meyer long setae (Fig. 11), and the anterior
1984. Procystiphora is a Holarctic genus margin of the spatula is shallowly
936 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
notched (Fig. 10). Larvae of P. mangi- ferae, while their Fig. 9a clearly shows
ferae are smooth, have a quadrate pos- longer gonopods and gonostyli for G.
terior end in dorsoventral view (Fig. 13), indica and parameres that are straighter
setae no longer than wide, and the and not apically inclined towards the
anterior margin of the spatula is deeply aedeagus.
lobed (Fig. 12). Adults of the two are According to Grover and Prasad
also distinct: the R; wing vein of G. (1966), eggs of G. indica are laid in
mangiferae is fairly straight and joins C young buds and larvae feed on the
noticeably anterior to the wing apex internal organs of the flower and prevent
(Fig. 1) while that of P. mangiferae 1s fruiting, which is essentially the same
definitely curved apically and joins C far damage as for G. mangiferae. A bi-
behind the wing apex. ological difference given for the two
Biology.4According to Venkatsubba species is that the larvae of G. mangiferae
(1940) and Prasad (1967, 1971) females appear usually to pupate in the flowers
lay one or more eggs among sepals and while those of G. indica drop to the soil
petals of unopened flower buds. In India to pupate. The larva of G. indica was not
eggs hatch in less than two days and the described in detail in Prasad (1971). The
larvae begin to feed on the developing ranges of the two species appear to be at
reproductive parts of the flower. The least partly contiguous in India.
attacked flower bud becomes enlarged
and conical and no fruit is produced (fig. ACKNOWLEDGMENTS
P-2, p. 43, Prasad 1971). Larvae are fully We are grateful to: David Herzog
developed in about 8 days and usually (CIRAD-Guadeloupe) for collecting the
pupate in situ, although some full-grown samples of G. mangiferae in Guadeloupe;
larvae left the flowers and dropped to the Nit Malikul for preparing the slides,
soil; the pupal stage lasts four to five Lucrecia H. Rodriguez for assistance
days (Prasad 1967). See Solinas and with preparing the plates of illustrations;
Bucci (1982) for a detailed study of the and Netta Dorchin, Keith M. Harris,
development of Gephyraulus diplotaxis Peter Kolesik, Allen L. Norrbom, and
(Solinas) and the progress of apparently Ronald Ochoa for their helpful com-
similar damage in Italy to flowers of ments on the manuscript.
Diplotaxis muralis (L.) D.C. (Brassica-
ceae)-
LITERATURE CITED
Gephyraulus indica (Grover and Prasad), Anonymous. 1981. Serious mango pest established
new combination in Hawaii. Plant Pest News, U.S. Department
of Agriculture, Animal and Plant Health
We have not seen type specimens of
Inspection Service, Plant Protection and Quar-
this species and rely for this determina- antine 1(3): 1.
tion on Grover and Prasad 1966. The Felt, E. P. 1911. Four new gall midges (Dipt.).
descriptions and drawings of that paper Entomological News 22: 3014305.
44, 1927. Four new Indian gall midges.
indicate that the ovipositor of G. indica is
Memoirs of the Department of Agriculture in
longer, more gradually attenuate, less
India, Agriculture Research Institute, Pusa 10:
stiff and less pigmented than that of G. 1-4.
mangiferae and its fused cerci are longer, Gagne, R. J. 1975. A review of the Nearctic genera
more tapered, and more setose. Grover of Oligotrophidi with piercing Ovipositors
(Diptera: Cecidomyiidae). Entomological News
and Prasad (1966) offered also dorsal
86: 5-12.
and ventral views of the male genitalia of
. 1989. The Plant-Feeding Gall Midges of
G. indica but the dorsal view (Fig. 9b)
North America. Cornell University Press,
appears to fit the genitalia of G. mangi- Ithaca, New York. xi + 356 pp.
VOLUME 108, NUMBER 4 O8y/
. 1994. The Gall Midges of the Neotropical . 1971. The Mango Midge Pests. Cecidolo-
Region. Cornell University Press, Ithaca, New gical Society of India, Allahabad. vii + 172 pp.
York. xv + 352 pp. Rubsaamen, E. H. 1916 (1915). Cecidomyidenstu-
. 2004. A catalog of the Cecidomyiidae dien IV. Revision der deutschen Oligotrophar-
(Diptera) of the world. Memoirs of the ien und Lasiopterarien nebst Beschreibung
Entomological Society of Washington, No. neuer Arten. Sitzungsberichte der Gesellschaft
25. 408 pp. Naturforschender Freunde zu Berlin 1915:
Gagné, R. J. and J. F. Doane. 1999. The larval 485-567.
instars of the wheat midge, Sitodiplosis mosel- Solinas, M. 1965. Studi sui Ditteri Cecidomiidi. I.
lana (Diptera: Cecidomyiidae). Proceedings of Contarinia medicaginis Kieffer. Bollettino del-
the Entomological Society of Washington 101: PIstituto di Entomologia della Universita di
57-63. Bologna 27: 249-300.
Gagné, R. J. and J. H. Hatchett. 1989. Instars of 1982. Studi sui Ditteri Cecidomiidi. IV.
the Hessian fly (Diptera: Cecidomyiidae). Paragephyraulus diplotaxis n. gen., n. sp.
Annals of the Entomological Society of Amer- Memorie della Societa Entomologica Italiana
ica 82: 73-79. 60: 315-334.
Solinas, M. and M. Bucci. 1982. An ecological
Grover, P. 1965. Studies on Indian gall midges
investigation into flower galls on Diplotaxis
(Diptera: Cecidomyidae) XII. The mango
muralis D.C. caused by the gall midge Para-
blossom midge, Dasyneura amaramanjarae, n.
gephyraulus diplotaxis Solinas. Entomologica
sp. Annals of the Entomological Society of
17: 5-22.
America 58: 202-206.
Sylven, E. and M. Solinas. 1989. Structural and
Grover, P. and S. N. Prasad. 1966. Studies on
systematic review of Gephyraulus Ribsaamen
Indian gall midges XVI: Four species of gall
(Diptera, Cecidomyiidae, Oligotrophini) with
midges (Cecidomyiidae: Diptera) affecting in-
description of G. moricandiae sp. n. from
florescence of mango. Cecidologia Indica 1:
Tunisia. Entomologica 22: 15434.
1-13, pls. I-VI.
Sylven, E. and R. Tastas-Duque. 1993. Adaptive,
McAlpine, J. F., B. V. Peterson, G. E. Shewell, H.
taxonomic, and phylogenetic aspects of female
J. Teskey, J. R. Vockeroth, and D. M. Wood,
abdominal features in Oligotrophini (Diptera,
eds. 1981. Manual of Nearctic Diptera, Vol. 1.
Cecidomyiidae), and four new Dasineura spe-
Research Branch, Agriculture. Canada Mono-
cies from the western Palearctic. Zoologica
graph No 27. vi + 674 pp.
Scripta 22: 277-298.
Meyer, H. 1984. Experimentell-6kologische Un-
Tavares, J. S. 1918. Cecidologia brazileira: Cecidias
tersuchungen an Gallmticken (Cecidomyiidae4 que se criam em plantas das familias das Ver-
Diptera) in Salzwiesenbereichen Nordwest- benaceae, Euphorbiaceae, Malvaceae, Anacar-
deutschlands. Faunistisch-Okologische Mittei- diaceae, Labiatae, Rosaceae, Anonaceae, Am-
lungen, Supplement 5: 14124. pelidaceae, Bignoniaceae, Aristolochiaceae e
Parnell, J. R. 1969. The biology and morphology of Solanaceae. Brotéria, Série Zoologica 16(1):
all stages of Toxomyia fungicola Felt (Diptera: 21-48.
Cecidomyiidae) in Jamaica. Proceedings of the Venkatsubba, I. C. S. 1940. The mango cecidomyid
Royal Entomological Society of London (A) Dasyneura mangiferae Felt, in Cochin. Indian
44: 113-122. Journal of Entomology 2: 98.
Prasad, S. N. 1967. Gall-midges of economic Wyatt, I. J. 1967. Pupal paedogenesis in the
importance XI: On a study of biology of Cecidomyiidae (Diptera) 34A reclassification
Procystiphora mangiferae (Felt) with special of the Heteropezini. Transactions of the Royal
reference to extent of infestation. Cecidologia Entomological Society of London 119(3):
Indica 2: 61-73 & pls. I-II. 71-98.