J. H\'\I. RES. Vol. 19(1),2010,pp. 77-83 Plega hagenella (Neuroptera: Mantispidae) Parasitism of Hylaeiis (Hylaeopsis) sp. (Hymenoptera: Colletidae) Reusing Nests of Tn/poxylon manni (Hymenoptera: Crabronidae) in Trinidad All.\x "W. Hook, John D. Oswald, axd Johx L. Xeff (AWTi) Department of Biological Sciences, St Edward's Universin-, Austin, TX 78704-6489, USA; allanh@sted^vards.edu (JDO) Department of Entomolog}-, Texas A&M Universit}-, College Station, TX 77845-2475, USA (JLX) Central Texas Melittological Institute, 7307 Running Rope, Austin, TX 78731, USA — Abstract. Two adultspecimens ofFlega Imgmella were reared from anestofthe crabronid wasp Tryipoxxjlon manni collected in Trinidad in 2008. The mantispids developed by feeding on the immature stages ofacolletidbee,Hylaeiis (Hylaeopsisj sp.,whichhad secondarily occupiedthe cells of the aerial mud nest of T. manni. T^vo dead Hylaeiis pupae were found ^sithin the nest, one of \\'hich had six dead mantispid lar\'ae attached. Numerous insect egg chorions, interpreted as belonging to P. Imgenella, were found in clusters insertedinto small cavities inthe mud ofthe outer surface ofthenest. Five additional adultP. Imgenella ^vere collected inmicrohabitats where other 7. nuinninestswere collected. Thesenewobser\'ationsconfirmthepresenceofP. liagenellainTrinidad, establish the presence of the subgenus Hylaeopsis in Trinidad, and document Flega liagenella as a new parasite ofbees in the genus Hylaeiis. TheinsectorderXeuroptera-lace^vings, records are of considerable interest. The antlions and their relatives - currently S\Tnphrasinae contains three extant genera comprises approximately 5,730valid extant - Anchieta, Trichoscelia and Plega - all of species placed in about 17 families. The which are currently restricted to the Xew family Mantispidae - mantispids or man- World (Penny 1982), and for each ofwhich tis-flies - form a distinctive clade of about few lar\'al host/feeding records are avail- 395 species that is ^vell kno^\Ti for the able. Anchieta includes five species kno^\Ti raptorial forelegs of its predator}' adults, from Brazil and French Guiana, only one of and the larval life histor}^ strategy of ^vhich has a reported host: A. fiimosella species in the subfamily Mantispinae as (West^vood), which has recently been spider egg parasites. Less ^vell kno^\Ti are reared from cocoons of Tn/poxxflon (Tnjpar- the lar\'al strategies of species in the three giliim) aestival Richards in southeastern other extant mantispid subfamilies - the Brazil (Buys 2008). Trichoscelia contains 13 Symphrasinae, Drepanicinae and Calo- species distributed from southern Mexico mantispinae - none of ^vhich are known south to Uruguay, Argentina and southern to be associated with spiders. Brazil (Penny 1982; Ohl 2004). Trichoscelia Of particular interest are lar\'al associa- varia (Walker) has been reared from nests tions of species belonging to the subfamily of the vespid wasps, Polybia ruficeps Symphrasinae, ^vhich is generally consid- Schrottk}' and P. scutellaris (\\lrd\e) (Penny ered to be the sister-group to all other 1982); and Dejean and Canard (1990) mantispid subfamiHes collectively (Penny provide an interesting account of Trichos- and da Costa 1983; Lambkin 1986). The celia santareni (Xavas) invading a colony of biologies of symphrasine species are Polybia digiietana Buysson on the Yucatan poorlyknowTL and, consequently, ne\vhost Peninsula. 78 Journalof Hymenoptera Research: Festschrift Honoring Roy Snelling Table 1. Plega melitomaespecies-group host records. Pkyasp. Hostrecord Location Reference beardii?) Trypoxylon albitarse (Crabronidae) Trinidad Penny 1982 hagenella Hylaeus (Hylaeopsis) sp. (Colletidae), in Trinidad (thiswork) Trypoxylon manninest melitomae Melitoma segnientaria (asM. euglossoides) Mexico (Chiapas) LinsleyandMacSwain1955 (Apidae) sp. near Tn/poxylon sp. Mexico (Veracruz) Parker and Stange 1965 melitomae yucatanae Megachileexaltata (Megachilidae) Mexico (Yucatan) Parker and Stange 1965 Plega includes 14 species distributed manni is a member of the T. fabricator from the southwesternUnited States, south group, in which nest sharing by females is to Bolivia and Brazil (Penny 1982). Two known in at least three species: T.fabricator species groups are generally recognized - Smith (Sakagami et al. 1990), T. maidli the melitomae and signata groups. Members Richards and T. manni (Hook and Starr of the P. melitomae group (P. beardi, pers. obs.). hagenella, melitomae, paraense and yucatanae; MATERIALS see Penny 1982) have been reported as parasites of several bees and aculeate Between 2003 and 2008 the senior author wasps (Table 1). In contrast to the hyme- field collected five specimens of Plega nopteran feeding records of the melitomae hagenella in several places on the island of group, members of the signata group have Trinidad. Three of the specimens were been reared from subterranean insects collected in 2008 under dirt banks harbor- (Parker and Stange 1965). Plega signata ing Trypoxylon manni nests. One female Hagen cocoons have been found inside was taken on 18 July along the Paria Trail, subterranean cocoons of the noctuid moth another female was collected on 23 July up Egira curialis (Grote) (Woglum 1935; as the Maracas Valley in the Northern Range Xylomyges curialis). Werner and Butler and a male was taken on 25 July in the (1965) presented circumstantial evidence Arena Forest Reserve. A fourth specimen of Plega banksi Rehn devouring a scarab (male) was collected on 26July 2003 up the pupa as well as an asilid pupa associated Caura Valley (Northern Range) and a fifth with a scarab pupa in Arizona. They specimen (female) was collected on 25 suggested that the larvae live in soil as August 2005 at U.W.I. Flats (apartments) predators. in St. Augustine (Trypoxylon spp. were The global crabronid genus Trypoxylon, observed nesting around the apartments). which figures prominently in several host InJulyof2008 AWH collected 10 nests of records for the P. melitomae group, contains Trypoxylon manni - seven from along the more than 600 species and is well repre- upper reaches of the Paria Trail (10.746°N sented inthe NewWorld. Trypoxylon manni 61.285°W; connecting the village of Brasso Richards is known from Brazil and Trini- Seco to Paria Bay on the north coast) on 18 dad and commonly attaches its nests to July, two in the Maracas Valley (10.705°N rootlets under dirt banks next to road cuts 61.368°W) on 23 July and one on 25 July in the Northern Range, Trinidad, West along a road entering the Arena Forest Indies (Vesey-FitzGerald 1936). Nests of Reserve (10.562°N 61.256°W). All nests T. manni are often communal and may were collected into and maintained iso- contain up to six females and 64 cells lated in separate plastic bags in order to (Hook and Starr unpubl.). Trypoxylon rear their contents. Two adults of Plega Volume 19, Number 1, 2010 79 hagenella, and numerous presumed eggs reused by Hylaeus, with one to two or and larvae of the same species, were later possibly three Hylaeus cells per T. manni foundtobe associatedwith one ofthenests cell. — collected along the Paria Trail (AWH field Observations on Plega. Two adult Plega note 36-2008). Most of the cells of this nest hagenella, one male and one female, were were subsequentlydissected andexamined subsequently found in the plastic bag for evidence of insect occupation and containing the parasitized Trypoxylon nest, usage. Observations made during the ex- which had been maintained indoors, dry, amination of this nest are summarized and at ambientroom temperatures since its below. collection. The male was discovered nearly dead on 26 July 2008. The nest was RESULTS — subsequently checked irregularly until 18 Observations on Trypoxylon andHylaeus. August. Thenextinspectionwasnotuntil9 The mantispid-parasitized nest had 14 October, when a dead female was discov- cells, of which nine were open when ered. The adult Plega hagenella specimens collected, two were closed with mud and were identified usingthe keys and descrip- three were closed with a tough, transpar- tions of Penny (1982), who noted the ent, membrane indicative of cell reutiliza- existence of previously-collected females tion by a colletid bee, subsequently identi- resembling, but not conclusively identifi- fied asHylaeus (Hylaeopsis) sp. Ofnine cells able as, P. hagenella from Trinidad. The opened by dissection, Hylaeus had reuti- present material confirms the presence P. lized eight, as evidenced by typical Hy- hagenella in Trinidad based on definitively laeus-type transparent cell linings and identifiable male specimens and associated partitions found within the original mud females. cells of the Trypoxylon manni nest. Hylaeus Subsequent examination of the nest reused 11 ofthe 14 cells thisnestcontained. revealed two mantispid pupal exuviae, Trypoxylon species do not line their nest one protruding from each oftwo nest cells, cells with secretions, but this is a charac- both of which were marked by the char- teristic feature of colletid bee cells (Al- acteristic cellophane-like lining of Hylaeus. meida 2008). Two dead Hylaeus pupae A loose double-walled cocoon of typical were found in these lined exterior cells. neuropteran form was extracted from one Of these, one pupa was unparasitized but of these cells. In another cell, six neurop- the other had six dead mantispid larvae teran larvae of at least two sizes were attached to its thorax and abdomen (the found attached to a dead Hylaeus pupa. head was missing). Further inspection of the partially dis- Identification of the bee species as sected nest revealed the existence of Hylaeus (Hylaeopsis) sp. is based on the numerous, small, whitish, insect egg cho- dead pupae found in the nest and on bee rions associatedwithits outerlayers. While rearings from 46 additional Trypoxylon some of the eggs may have been deposited manni nests collected previously in 1996 on the exposed outer surface of the nest, and 1999 (primarily along the Blanchis- most appear to have been inserted into seuse Road in the Northern Range of small cavities in the nest's irregular mud Trinidad). Interestingly, a diversity of surface, often in small groups of 3-6 per cleptoparasites was reared from 19 of the cavity. The small cavities are natural earlier 46 nests, but no mantispids. Six features ofthe original mud nest, the result (13%) of the 46 nests collected during this of incomplete joining or smoothing of earlier period had some level of Hylaeus adjacent, rounded, mud boluses used in cell reutilization. Those six nests contained its construction. At least 29 empty egg a total of 93 cells, of which 16 (17%) were chorions were found in or on the nest, but 80 Journalof Hymenoptera Research: Festschrift Honoring Roy Snelling it seems likely that additional eggs were tified P. hagenella adults from the Trypox- lost during the dissection of the nest, or ylon nest renders plausible the discovery of were inserted so deeply into crevices that immature P. hagenella stages in the same they were hidden from view. The eggs nest. The general morphology of the were narrowly lacrimiform in shape (with recovered larvae is consistent with their the micropylar process terminating the determination as first-instar mantispid mm narrowed end), ca. 0.7 long, simple larvae. The larvae are morphologically (i.e., stalkless), and marked externally with similar to the first-instar larvae of both a networkofraisedpolygonal ridges. All of Plega yucatanae (described by Parker and the eggs appeared tobe empty, their larvae Stange 1965) and other described first- having emerged through longitudinal slits instar mantispids (e.g., Climaciella brunnea located near the micropylar ends of each [as Mantispa brunnea], Dicromantispa inter- egg. rupta [asMantispa interrupta], Dicromantispa sayi [as Mantispa sayi], Leptomantispa pul- DISCUSSION chella [asMantispa pulchella] and Zeugoman- — Hylaeus (Hylaeopsis). This Neotropical tispa virescens [as Mantispa viridis], see subgenus of 15 species has been reported Hoffman and Brushwein 1992; Tuberonotha from Mexico south to Paraguay and south- strenua [as Climaciella magna] and Mantispa em Brazil, but it has not previously been japonica, see Kuroko 1961). reported from Trinidad, the neighboring The eggs noted above, in addition to Guyanas, or Venezuela (Urban and Moure being physically associated with the man- 2007). Ten or more undescribed Hylaeopsis tispid-parasitized nest, are also consistent species are suspected to be present in the both morphologically and behaviorally Neotropical fauna (Michener 2007). Adults with a mantispid identification. Their size ofthe Trinidad Hylaeopsis are much smaller is appropriate to that of the smaller than adult Plega hagenella, suggesting that mantispid larvae observed in the nest. Plega larvae must consume multiple bee The deep insertion of many of the eggs larvae and/or pupae to reach adulthood. If into fine crevices in the mud surface of the this is true, the pattern of multiple bee nest is consistent with oviposition via a cells per wasp cell and gregarious nesting slender, elongate, ovipositor, the presence (also reported in H. (Hylaeopsis) tricolor ofwhich is, within the order Neuroptera, a (Schrottky) by Sakagami and Zucchi 1978) synapomorphy of the mantispid subfamily maycontributetomakingthisbee species a Symphrasinae, to which Plega hagenella suitable host for Plega hagenella. Not all belongs. Although at least two Plega Hylaeopsis species nest gregariously, how- species have been reared from egg to adult ever, and the hyperdispersed, single-celled (P. dactylota and P. signata; see MacLeod nests of H. (Hylaeopsis) grossus (Cresson) and Redborg 1982), no published descrip- (Michener and Brooks 2003) may be adap- tions or illustrations of Symphrasine man- tive in helping to avoid attacks by larger tispid eggs exist. Interestingly, however, nest parasites like Plega. the eggs noted here bear a strong resem- — Plega. Although definitive, reared, lar- blance to, though are somewhat more vae and eggs of P. hagenella have yet to be slender and elongate than, those illustrated described, detailed observations derived by Minter (1990, fig. 1) for Mucroberotha from the parasitized Trypoxylon nest re- vesicaria - a species belonging to a group of ported here, together with existing knowl- several genera of uncertain phylogenetic edge of mantispid immatures, present a placement that have in recent years been strong circumstantial case that the eggs placed in either the family Mantispidae or and larvae noted above are those of P. Berothidae (as Rhachiberothinae), or as a hagenella. The rearing of definitively iden- separate family (as Rhachiberothidae). The Volume 19, Number 1, 2010 81 presence of sessile eggs in both rhachiber- into question the accuracy ofprevious host othines/ids and symphrasine mantispids records of Trypoxylon species for other P. has potentially interesting implications for melitomae group species (Table 1). The the interpretation ofthe stalked eggs found discovery of a mantispid-parasitized bee in both mantispine mantispids and ber- in a reutilized aculeate wasp nest makes it othine berothids (both of which are rela- apparent that accurate host records for P. tively derived subfamilies within their melitomae group mantispids cannot be families). If sessile eggs are found to be inferred from published associations un- symplesiomorphic in rhachiberothines/ids lessthepossibilityofnestreuseis explicitly and symphrasine mantispids, the stalked addressed. eggs found in berothines and mantispines The observation that P. hagenella adults are likely to be independent, derived can be collected in sheltered, exposed-soil, innovations. situations favorable for Trypoxylon nesting — Parasite Biology. Because the Plega ha- provides a new focal point for field genella adults emerged from the mud nest collecting Plega adults, which are rather of Trypoxylon manni, it was initially as- rarely collected in tropical regions. It sumed that P. hagenella was a parasite of T. remains to be determined, however, manni. However, several observations and whether these Plega individuals are pref- lines of evidence suggest that, at least in erentiallytargetingbeesreusing Trypoxylon this case, P. hagenella was parasitizing the nests in such microhabitats, or whether Hylaeus (Hylaeopsis) sp., not T. manni. First, they are attracted to such areas for general no remnants of Trypoxylon immatures were shelter and/or for access to a potentially found in the nest, suggesting that the larger array of subterranean-, surface- and original nest builders had vacated the nest aerial-nesting aculeate Hymenoptera that prior to its occupation by Hylaeus and would likely be attracted to the same Plega. Second, all evidence of P. hagenella sites because of their suitability for nest- cell occupation (i.e.,pupalexuviae, cocoon, building. presumed larvae) was found in nest cells Because of the paucity of available host with membranous linings, indicating an records, the degree of host-specificity of association with the cells reused by Hy- individual Plega species is currently un- laeus, rather than the uncoated cells of clear, though the possible division of wild Trypoxylon. Third, the presumed larvae of hostsproposedbyParker & Stange (1965) - P. hagenella were clearly found in associa- i.e., P. melitomae group species on aculeate tion with a Hylaeus pupa in the nest. Hymenoptera and P. signata group species Several of the larvae appeared to have on a larger array of subterranean insects their jaws successfully inserted into the (e.g., larvae and/or pupae of Coleoptera, cuticle of the bee pupa, and differences in Lepidoptera and Diptera) - still appears as the sizes of some of the larvae suggest that a broad generalization. It should be noted, at least some had fed successfully. What however, that this generalization may not actually killed the discovered bee pupae apply to captive individuals reared under and mantispid larvae is unknown. Finally, artificial conditions (MacLeod and Red- abee host for P. hagenella is consistentwith borg 1982). the known bee hosts of at least two other All Mantispinae with known biologies members of the Plega melitomae species have spider-associated larvae, and adults group (P. melitomae and yucatanae; see with highly r-selected reproductive strate- Table 1). In fact, the three-species interac- gies, each female producing hundreds to tion documented here - Plega hagenella thousands ofminute, stalked, eggs that are parasitizing a Hylaeus (Hylaeopsis) species deposited in the environment with appar- reutilizing a Trypoxylon manni nest - calls entlylittle or no attemptto ovipositin sites 82 Journalof Hymenoptera Research: Festschrift Honoring RoySnelling that might increase the probability of Kuroko,H. 1961.Ontheeggsandfirst-instarlarvaeof emerging larvae encountering suitable two species of Mantispidae. Esakia. Occasional hosts. The finding of Plega hagenella eggs LambPkaipne,rsKo.ftheH19i8k6o.sanABiroelvoigsiicoalnLoafbortahteorAyu3s:tr2a5l-i3a2.n directly deposited on a nest containing the MantispidJa.e (Insecta: Neuroptera) with a con- immature stages of its host suggests that P. tribution to the classification of the family. I. hagenella, and possibly other symphrasine General and Drepanicinae. Australian Journal of mantispids, employs a different, more Zoology, Supplementary Series 116: 1-142. targeted, oviposition strategy that actively Linsley, E. G. and J. W. MacSwain. 1955. Two new speciesofPlegafromMexico.Pan-PacificEntomol- places eggs in closer proximity to potential ogist 31: 15-19. hosts. Strategies such as this suggest MacLeod, E. G. and K. E. Redborg. 1982. Larval the existence of more complex adult Platymantispine mantispids (Neuroptera: Plani- behaviors, particularly higher levels of pennia): possibly a subfamily of generalist pred- host-searching ability in females. Within ators. Neuroptera International 2: 37-41. Michener,C. D.2007. BeesoftheWorld.JohnsHopkins the Mantispidae, extraordinary intraspeci- University Press, Baltimore, xvi + 557pp. fic and oviposition behaviors are also andR.W.Brooks.2003.Dispersalofbroodcells found in the symphrasine species Trichos- in a Mesoamerican hylaeine bee: a probable risk- celia santareni, whose males and females spreadingbehavior(Hymenoptera,Colletidae).Pp. engage in lekking behavior, followed by 151-152in:Melo,G.A.R.,andI.A.dosSantoseds. Apoidea Neotropica: homenagem aos 90 anos deJesus the females flying to, entering and ovipos- SantiagoMoure.EditoraUNESC,Criucuma, Brazil. iting within active vespid nests (Dejean Minter,L.R. 1990.Acomparisonoftheeggsandfirst- and Canard 1990). instarlarvae ofMucroberotha vesicaria Tjederwith those of other species in the families Berothidae ACKNOWLEDGMENTS and Mantispidae (Insecta: Neuroptera). Pp. 115-129 in: Mansell, M. W. and H. Aspock eds. This paper is dedicated to the memory of Roy AdvancesinNeuropterology. ProceedingsoftheThird Snelling. Chris Starr and Carl Fitz-James graciously International Symposium on Neuropterology (3-4 made their homes available during my stay in February 1988, Berg en Dal, Kruger National Trinidad, and the Department of Life Sciences, The Park,SouthAfrica).SouthAfricanDepartmentof University of the West Indies provided office and Agricultural Development, Pretoria. 298pp. laboratory facilities. The Wildlife Section of the Ohl,M.2004.AnnotatedcatalogoftheMantispidaeof Forestry Division, St. Joseph, Trinidad issued collect- theWorld(Neuroptera).ContributionsonEntomol- ing and export permits. Voucher specimens are ogy, International. 5: 131-262. deposited in the University of Texas and Texas Parker, F. D. and L. A. Stange. 1965. Systematics and A&M University insectcollections. biological notes on the tribe Platymantispini (Neuroptera: Mantispidae) and the description LITERATURE CITED of a new species of Plega from Mexico. Canadian Entomologist 97: 604-612. 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