J. HYM. RES. Vol. 13(2), 2004, pp. 295-301

The First Gregarious Species of the Agathidinae (Hymenoptera: Braconidae)

C. E. Sarmiento, M. J. Sharkey, and D. H. Janzen

(CES, MJS) S-225 Department of Entomology, Ag. Sci Cen.-North, University of Kentucky, Lexington, KY 40546-0091 USA; (DHJ) Department of Biology, University of Pennsylvania, Philadelphia, PA 19104 USA; email: [email protected]

— Abstract. Coccygidium gregarium Sarmiento & Sharkey, the first known gregarious species of the subfamily Agathidinae (Braconidae), is described. This species was reared from a larva of Euglyphis sp. (Lasiocampidae). The SEM images of its last antennal flagellomere reveal that the characteristic acuminate shape is due to the presence of elongated, presumably sensory, structures. This type of flagellomere, together with its carinate hind trochantellus, are traits present in the genera Coccygidium, Biroia, Dichelosus, Hemichoma and in the Afrotropical genus Hyrtanommatium, suggesting a close phylogenetic relationship. The apex of the ovipositor sheath bears a small pointed process present in other Coccygidium species and also in Biroia, Dichelosus, and Hemichoma but not in Hyrtanommatium; this trait may suggest a close relationship among these genera. SEM images of this structure show that it is covered by ampulliform papillae, here reported for the first time. The pores on the inner apex of the ovipositor sheaths and the ampulliform papillae are either secretory or sensory.

The Agathidinae are comprised of ap- geti, Hemichoma Enderlein and Dichelosus proximately 52 genera worldwide, with 20 Szepligeti are derived clades within Coc- occurring in the New World. Nearly 1000 cygidium. species have been described, mostly from All agathidines for which there are re- tropical areas. The subfamily has been re- liable rearing records are reported as sol- vised at the tribal level by Sharkey (1992), itary koinobiont endoparasitoids of lepi- and there have been several faunal treat- dopteran larvae. Members of Bassus and ments and generic revisions (Muesebeck Agathis (Microdini and Agathidini respec- 1927, Marsh 1961, Nixon 1986, Sharkey tively) oviposit in the host, placing the egg 1983, 1986, 1988, 1990, Simbolotti and van inside a ganglion of the ventral nervous Achterberg 1999, van Achterberg 1990, system or attaching it to the lateral lobe of and Briceno 2003). The genus Coccygidium the protocerebrum; the larva remains as a de Saussure, 1892 (in this paper we follow first instar, floating in the haemocoel, dur- the generic concept of Chou and Sharkey ing the feeding period of the host, and 1989; including Zelomorpha Ashmead) is then quickly develops in the final larval probably the most species-rich genus of and prepupal stage of the host; the final- the tribe Disophrini. This genus includes instar parasitoid emerges after the host about 35 described species distributed has spun its cocoon and completes its worldwide but more than 100 Neotropical feeding externally (Shaw and Huddleston species are awaiting description. Although 1991, Sharkey 1997). Coccygidium species, Coccygidium has never been revised, cur- as with all the members of the tribe Di- rent studies (by C.S. and M.J.S.) suggest sophrini, possess short strong ovipositors that the Neotropical genera Biroia Szepli- and parasitize free-living caterpillars in 296 Journal of Hymenoptera Research their late instars. Host records of Coccygi- rounded, flanged and with a few irregular dium include noctuids, arctiids, notodon- rugae basad of eye (Fig. 4). Ratio of length = tids, and lasiocampids (http://janzen.sas. of malar space to eye height 0.3. upenn.edu, Shenefelt 1970). Most species Mesosoma. Epicnemial carina complete of Disophrini are diurnal and brightly col- and with distinct angle. Groove of epic- ored, but some are nocturnal and have the nemial carina wide and flat, with about 10 characteristic pale coloration and enlarged robust transverse ridges, strongest at mid- ocelli of nocturnal hymenoptera (Sharkey length, absent in ventral third (Fig. 9). Me- 1997). In this paper we describe a new sopleuron uniformly punctured. Precoxal species of Coccygidium that represents the sulcus indicated ventrally by one crenula, first record of agathidine larvae living gre- otherwise barely depressed and smooth. gariously within a single host individual. Posterior margin of mesopleuron with 7-8 robust carinae. Suture between meta Coccygidium gregarium n. sp. Sarmiento and & episternum metepimeron complete, Sharkey smooth, transversed by carinae of sube- Holotype Female (The variation ob- qual size (Fig. 10). Convex flange on pos- served in the paratypes is included in terodorsal border of mesopleuron absent. square brackets in italics) Dorsal apex of meta episternum with two Size. Mesosoma length 2.7 mm (Fig. 1). carinae. Flange at the anteroventral area of Forewing length 6.9 mm (Fig. 2). metepimeron (i.e., juxtacoxal flange) wide, Color. Mostly black except as follows: with a transverse carina (Fig. 10). Area an- basal fourth of fore and mid-tarsi yellow terior to subpronope not modified into with brown markings; wings infumate; flange or disk. Posterolateral margin of metasoma orange. pronotum smooth. Notaulus indicated by Head. Medial ridge or convexity of face weak depression. Median longitudinal present (Fig. 3) [or absent]. Face convex mesoscutal groove absent. Scutellar sulcus medially, flat laterally, lacking striations, deep, subquadrate, with 1 [or 3] longitu- with small, sparse punctures laterally, and dinal carina [e]. Scuto-scutellar articulation dense foveolate punctures medially (Fig. absent. Posterior border of mesoscutal sul- 3). Penultimate labial palpomere 25% cus carinate. Scutellum rounded laterally, shorter than apical palpomere. Eyes not rugose. Transverse groove of scutellum emarginate; eyes not converging ventrally deep, with crenulae extending anteriorly (Fig. 3). Posterior orbit not bordered by but not reaching midway to scutellar sul- groove (Fig. 4). Lateral carina of frons in- cus. Median areola of metanotum without complete posteriorly, composed of rugae median longitudinal carinae (Fig. 12). Pos- and fovea. Frontal depression smooth. terior border of median areola of metan- Distance between antennal insertions sub- otum acute with acute longitudinal crest. to their diameter. equal Number of anten- Surface of propodeum with irregular stri- nal 35 flagellomeres [36-37]. Apical flagel- ations (Fig. 12); median, lateral, and pleu- lomere acuminate (Figs 5-6). Ratio of dis- ral areolae present; anteromedial and pos- tance between inner margins of eyes to teromedial areolae together forming spin- distance between lateral margins of lateral dle-shaped area with several transverse ocelli : 1.6. Depression laterad of lateral carinae; anterolateral areola divided by ocellus absent. Area of vertex posterior to several ridges converging anterolaterally; ocelli smooth. Longitudinal depression posteromedial areola with a transverse ca- posterior to ocelli weak, not indicated by rina; posteromedial keels weak, converg- distinct at groove. Gena, mid-height, pos- ing; transverse keel distinctly curved and ! erior to eye, barely projecting posteriorly complete to pleural carina, dividing pro- ^^—^^^-^^^ l IT*-^.-*'* ' __•"** 7"/"»f\ 1„ ~~,-i. Volume 13, Number 2, 2004 297 tooth of fore-tarsal claw truncate. Tibial Guanacaste, Sector Cacao, Estacion Cacao, spur of fore-leg 0.58 times as long as bas- 1150 meters, Lambert coordinates: North itarsomere. Longest tibial spur of mid-leg 323104 East 375725, (Lat 10.92691, Long 0.68 times as long as basitarsomere. Hind -85.46822), jul/15/1999, Mariano Pereira femur and lat- rugoso-punctate dorsally collector, voucher 99-SRNP-1161 http:// erally, areolate-rugose ventrally. Longest janzen.sas.upenn.edu (label 2) Ex Eugly- of hind 0.53 times as spur leg long as bas- phis sp Janzenl4, (Lasiocampidae), feeding itarsomere. Carina of hind trochantellus on Beilschmiedia costaricensis (Lauraceae), indicated of hind weakly (Fig. 11). Apex (D. Janzen's database 99-SRNP-1161 http: tibia with 2 or 3 spines arising directly //janzen.sas. upenn.edu). Caterpillar pre- from Basal tooth of apical margin. hind pupal date 3 August 1999, 19 tightly tarsal claw truncate. packed, elongate, large, white/gray co- vein of fore Wings. (Fig. 2) 3M wing coons completely filling the host cocoon, straight. 3RSa vein of fore wing shortly not silked together. Eclosed on 22 August developed. RS2a vein of fore wing longer 1999. Deposited in the Instituto Nacional than r-m cross vein. RS2b vein of forewing de Biodiversidad, Costa Rica (INBIO). absent. CUb vein of hind nebulous. 4 14 data wing Paratypes: 6 6 , 9 9, same as ho- Metasoma. Tl weakly convex. Apex of lotype and from same brood; 1 9, MEX: ovipositor sheath lacking transparent la- Veracruz, Fortin de las Flores, XII-22-63/ mella, curved dorsally with a small acute Blacklight L. R. O'Brien collector, Insect process (Fig. 13). Apex of the ovipositor Collection Los Angeles County Museum sheath covered with ampulliform papillae of Natural History. Paratypes deposited at (Figs 14-15). INBIO, Instituto de Ciencias Naturales of Male. Does not differ from the female the Universidad Nacional de Colombia, in non-sexual characters. American Entomological Institute, Hyme- Etymology: The specific name refers to noptera Institute, University of Kentucky the gregarious behavior in the larval stage. Insect Collection, and Los Angeles County This is the first known case of gregarious- Museum of Natural History, ness for the genus Coccygidium and for the Morphology. The acuminate apex of the subfamily Agathidinae. last antennal flagellomere is composed of Distribution: Known from northwest- six tubular projections (Fig. 5) and, al- ern Costa Rica and from Fortin de las Flo- though their shape strongly suggests a res, Veracruz, Mexico, but probably wide- sensorial function, high resolution images spread in Central America and southern (Figs. 6) indicate that these processes are Mexico. Elevation range: 975-1150 meters, devoid of any appreciable sensory struc- C. gregarium can be distinguished from ture for chemical reception such as the all other species of the genus by its unique placoid sensillae or the pores present in color pattern and by the following com- other parts of the antenna (Figs. 5, 7). The bination of morphological characteristics: surface of these tubular projections in- poorly developed lateral carina of frons; stead is completely smooth and solid (Fig. gena at mid-height, posterior to eye, with- 6). These structures may be sensory or- characteristics such out acute posterior projection; postero- gans to test physical ventral area of the gena round and evenly as surface vibrations. last antennal flanged; notauli weakly impressed; pro- This shape of the flagello- all of the podeum strongly carina te. mere is characteristic of species genus, and of the nominal Neotropical Material examined genera Biroia Szepligeti, Hemichoma Ender- Dichclosus have Holotype female: 1 9, (label 1) COSTA lein, and Szepligeti. We RICA, Guanacaste, Area de Conservacion also observed this trait in the Afrotropical Research 298 Journal of Hymenoptera

5 mm

in in lateral Figs. 1-8. Coccygidium gregarium n. sp.: 1, habitus; 2, wings; 3, head anterior view; 4, head view; 5, terminal or last antennal flagellomere; 6, close up of the apex of the last flagellomere; 7, detail of the surface of the antenna far from the apex, note the evenly distributed multiple pores; 8, Habitus of Euglyphis Janzen 14, host larva of C. gregarium n. sp.

genus Hyrtanommatium Enderlein. This listed above, but not in the Afrotropical character, in conjunction with the carinate genus Hyrtanommatium. SEM images re- hind trochantellus, suggests a monophy- veal that this process and most of the letic clade comprised of these genera (Sar- sheath apex are covered by ampulliform miento & Sharkey, in prep). papillae (Figs. 14-15). In addition, the in- The process on the ovipositor sheath is ternal side of the sheath is covered with present on most species of Coccygidium pores which may indicate the presence of mH in rhp nominal Npntroniral cenera a secretorv svstem. Previous studies have Volume 13, Number 2, 2004 299

9-15. arrow to Figs. Coccygidium gregarium n. sp.: 9, epicnemial carina; 10, meta-epimeron (the points the juxtacoxal carina); 11, carina of hind trochantellus; 12, dorsal view of metanotum and propodeum (AP \ = = = = anteropleural areola, ALA anterolateral areola, AMA anteromedial areola, TK transverse keel, PPA = = posteropleural areola, PLA posterolateral areola, PMA posteromedial areola); 13, ovipositor sheath (the arrow points to the apical process); 14, apex of ovipositor sheath, medial (internal) view showing the ampul- liform papillae (see text); 15, apex of ovipositor sheath, lateral (external) view.

reported the presence of several types of pillae. Their function is unknown but pos- sensory organs on both the ovipositor and sibly they are used to mark hosts with the ovipositor sheath of the Hymenoptera chemical secretions, or they may be sen- (Quicke et al. 1999, Vilhelmsen 2003), but sory structures to test host suitability, this is the first report of ampulliform pa- Biology: This is the first gregarious spe- 300 Journal of Hymenoptera Research cies reported for the subfamily Agathidi- quently by the inventory, it is either a very nae. Nineteen adult wasps emerged on 19 rare species or one that normally lives in August 1999 from a cocoon of Euglyphis the crowns of tall trees. These traits may sp. Janzenl4 (Lasiocampidae) (Fig. 8). The apply to Coccygidium gregarium as well. lasiocampid cocoon was filled with 19 ACKNOWLEDGMENTS elongate tightly packed large white/gray silk cocoons that were, however, not We thank P. Southgate (U. of Kentucky) for the SEM Debra of and the silked, glued, or otherwise attached to images. Murray (U. Kentucky) two reviewers for their comments. This re- each other. The wasp larvae emerged from insightful search was supported by NSF grants DEB 9972024 the of the host as is for all prepupa typical and 0205982 to M. Sharkey and B. Brown (L. A. of known species Agathidinae. The lepi- County Natural History Museum), and by NSF dopteran larva (Fig. 8, and also images at grants 8307887, 8610149, 9024700, 9306296, 9400829, and 0072730 to We thank the http://janzen.sas.upenn.edu, voucher 9705072, D.H.J. para- taxonomists in the ACG for and code 99-SRNP-1161) was collected as a collecting, rearing, by entering the information about these larvae and instar on 15 1999, and penultimate July their parasitoids in the data base. This is paper 04-08- on 3 in the full spun August 1999, rainy 059 of the Kentucky Agricultural Experiment Station. season. Its food Beilscfnniedia costar- plant, LITERATURE CITED icensis Mez & Pittier, is among the many lauraceous trees fed on by at least 10 spe- Achterberg, C. van. 1990. Revision of the subtribe Me- socoelina Viereck cies of Euglyphis Huebner in this rainfo- (Hymenoptera: Braconidae). — Zoologische Mededelingen, Leiden 64: 31-57. rest cloud forest intergrade located on Briceho, G. 2003. Taxonomic revision of the genus Se- the western slope of Volcan Cacao, Area sioctonus (Hymenoptera: Braconidae: Agathidi- de Conservacidn Guanacaste (ACG), nae). Journal of Hymenoptera Research 12: 238-271. northwestern Costa Rica. The two locali- Burns, J. M. and D. H. Janzen 2001. Biodiversity of ties where specimens of C. gregarium have pyrrhopygine skipper butterflies (Hesperiidae) in the Area de Conservacion Costa been collected, Estacion Cacao and Fortin Guanacaste, Rica. Journal the 55: 15- de las Flores are sim- of Lepidopterists' Society (Mexico), extremely 43. ilar in their climate and in their L. Y. original Chou, and M. J. Sharkey. 1989. The Braconidae vegetation /ecosystem (personal observa- (Hymenoptera) of Taiwan. 1. Agathidinae. Jour- nal the Taiwan Museum 42: 147-223. tion, D.H.J. ), despite being respectively on of D. M. and M. Burns. 1998. the Pacific and Atlantic coasts of Central Janzen, H., J. Sharkey, J. Parasitization biology of a new species of Bra- America and being separated by several conidae (Hymenoptera) feeding on larvae of thousand kilometers. Costa Rican dry forest skippers (Lepidoptera: the Through 2002, 24-year-old ongoing Hesperiidae: Pyrginae). Tropical Lepidoptera 9 lepidopteran larvae inventory of the ACG (suppl.): 33-11. Janzen, D. H. 2003. How are Costa Ri- (e.g., Burns and Janzen 2001, Janzen 2003, polyphagous can dry forest saturniid caterpillars? Pp. 369-379 Janzen et al. 1998, 2003, Schauff and Jan- in: Basset, Y., V. S. E. and R. zen Novotnyh, Miller, 2001, Sharkey and Janzen 1995) has L. Kitching, eds., Arthropods of tropical forests. Spa- reared lar- 1,452 wild-caught lasiocampid tio-temporal dynamics and resource use in the cano- vae, 98% of which are members of 20 + py. Cambridge University Press, Cambridge. Janzen, D. H., A. K. Walker, B. G. Del- species of Eugh/phis, without any other J. Whitfield, vare, and I. D. Gauld. 2003. Host-specificity and rearings of C. gregarium. Indeed, these lar- hyperparasitoids of three new Costa Rican spe- vae only produced 21 other hymenopter- cies of Microplitis Foerster (Hymenoptera: Bra- ous all of which are parasitoids, represen- conidae: Microgastrinae), parasitoids of sphingid tatives of a single undescribed species of caterpillars, journal of Hymenoptera Research 12: 42-76. Microgastrinae (Parapautcles "par22", Bra- Marsh, P. 1961. A taxonomic revision of the genus conidae, det. Alejandro Valerio). Since this Cremnops in America north of Mexico (Hyme- species of Eugli/phis (Janzenl4) has not noptera, Braconidae). Annals of the Entomological n found either previously or subse- Society of America 54: 851-861. Volume 13, Number 2, 2004 301

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