Rev. Biol. Trop., 39 (1): 87-95. 1991

Evolution of tbe mandibular appendage in figwasps (: )

William Ramírez B. Escuela de Fitotecnia, Universidadde Costa Rica.

(Ree. 20-IX-I990. Acep. 15-X-I990)

Abstract: The phylogenetic value of the conformation of the mandibular appendages, the number of mandibular glands andother head characters in the Agaonidae are examined.The phylogenetic arrangement suggests thatthe pre­ agaonid had a normal bidentate mandible with two glands, and a undistinct facial groove as in sorneDiazi ella (Sycoecinae), Sycophaga (Sycophaginae) and in related chalcidoid non-pollinating fig wasps. lt also had thirteen-seg­ mented antennae;'a long scape, several times ¡onger than wide a long triangular pedicel, two or three anelli andeight flagellomeres withsensilla (as uniquely found in ). The mandibularappendage apparently co-evolved with the development oí the ostiolum of thesyconium andthe firstmandibular appendage was fixed andhad ridges or lameUae. A flexible hinge evolved laterat its base.The polygamous males were wingless with extendible (solenogastrus) abdo­ men and mate inside the galls. These characters are also found in most Sycophaginae.The ancestor of Aganoidae was probably a primary sycophilous wasp, withdorsoventral depressed head, thorax and abdomen, that oviposit through thestylar channel as stiU Sycophaga sycomori does. Sycophaga wasps withits apterousand polyg amous males seem to be the sister group of Agaonidae. The Agaonidae females are characterized by their mandibular appendage and the antennalprocess. They have a prognathous head with gula. Themales are wingless polygamous andsolenogastrous.

Key words: Agaonidae(Hymenoptera), mandibular appendage, evolution, phylogeny.

Ficus is pollinated by small chalcidoid wasps and two or three antennal anelli. The mandibles of the family Agaonidae. The female agaonids were normal bidentate chewing strucrures with have a flat lamellate or denticulate mandibular no special modifications as in Sycophaga syco­ appendage that help them to squeeze between mori, a primary cecidogenous wasp which enters the ostiolar bracts and penetrate the syconia to the syconia of sycomorusL. (Fig. 7) to lay pollinate and oviposit inside of them. The object íts eggs. It is possible to infer that the mandible of this amele is to explain the evolution of the of the pre-agaonid probably had two glands in mandibular appendage in Agaonidae. both sexes as it occurs in many Agaonidae as The pre-agaonid female probably had a prog­ well as in Sycoecinae and Sycophaga, which as nathous subhemispherical or subquadrangular the Agaonidae are primary sycophilous wasps. head, almostas long as broad across the eyes (as (Sycophaginae) females also have in Hg. 1, 2, and 3), with the antennaltoruli situa­ bidentate mandibles with two glands. The scute­ ted elose together in the middle of the face, and llum had lateral grooves (parapsidal furrows) as the facial groove being absent or indistinct as in those found in Sycophaginae (Boucek 1988 a). Diaziella philippinensis (Sycoecinae; see Wiebes The male was apterous solenogastrous with 1974 a, Fig. 22) and Sycophaga (Sycophaginae; extendible abdomen. Grandi 1916). It also had thirteen segmented Once the inflorescence of the pre-Ficus antennae with the scape severaltimeslonger than became completely elosed (a syconium), those wide, and long sensilla on the fourth to eleventh wasps which evolved structures which aided funicular segments, as uníquely found in them in squeezing through the ostiolar scales Tetrapus (Agaonidae; see. Grandi1934, Fig. 1, 2), were probably more successful in entering the 88 REVISTADE BIOLOOIA TROPICAL

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Fig.1: Facial view of head of Diaziella plúUppinensis. (subfamilySYCoeCifUle). after WlCbeS. 1974 a, Fig.22. Fig.2. Facial view ofheadof Sycophagd valentinae. (subfamily Sycopbaginae), afterOrandi, 1952 a, Fig. 1,1. Fig. 3. Facial view ofheadManiella delhiensis. (subfamily Blastopbaginae). Fig. 4. Ventral view of head of Plúlocaenus barbatus. (subfamily Sycoecinae), after Grandi, 1955, Fig. VI. Fig. S, Facial viweofheadof Seres armipes. (subfamily SYCoeCifUle), after Orandi.1952a, Fig.m. 1. Fig. 6. Facialview ofheadof regalis. (Agaonidae.subfamily after Agaoninae), Orandi, 1952 b, Fig.1X, 1. RAMIREZ:·Mandibular appendag� in figwasps 89

figs. The evolution of Agaonidae seems par­ Cladistic relationships oC Agaoeidae based allel to the evolution of the syconium of Ficus, on the conformadon oC the bead: The dado­ especially the ostiolum, syconial size, length gram (Pig. 18) ís especially based on fue num­ of styles of the female flower and number, ber of mandibular glands present in fue female conformation and kind of anthers of the male and male, as well as fue conformation of the flowers. mandibular appendage, the conformationof fue Probably fue first mechanisms that the pre­ head, fue conformation and subdivision of fue agaonids evolved to facilitate fueirentry into fue antennal process (thirdsegment), the conforma­ figs were fue breakage of their antennae and líon of the scape, as well as the presence or wings and fue evolution of structures (e.g. toofu­ absence of maxillar and labial palpus in the like or lamellar structures on the front tibiae and female. The loss of one of the mandibular mandibles) that eased fueir movements in fue glands does not seem to produce any advantage narrow spaces betweenostiolar scales. or disadvantage lO the wasps. lt is assumed fuat Wiebes (1973, 1974 b, 1982 a) divided the subhemispherical or subquadrangular dorso­ Agaonidae into two subfamilies: those with ventraldepressed heads wifuwide facial sulcus lamellate mandibular appendages and short and (as in Blastophaginae) sensilla placoidea in the robust scape(Blastophaginae) and those with second flagellomere, the antennal process with crenulate (with dentides) mandibular appenda­ divisions, the presence of maxillary and labial ges and elongate scapes (Agaoninae). Wiebes palpi, the mandible with fixed appendage, wifu (1973) supposed that the characters of the lamellae and two mandibular glands in both Agaoninae (e.g., fue elongate head, the ventral males andfemales are thepleisomorphous (pri­ crenulations of the mandibular appendages, mitive)states. etc.) represent the pleisomorphous (primitive) state. Wiebes (1982 a) also considered fuat fue wide open facial gro ove (e.g., as in Blasto­ phaginae) is evidently the derived state. Groups oC Ficus, their pollinators aed reJa­ Boucek (1988 a) placed fue Sycophaginae s . tionships: The pollinators of monoecious sub­ str. and Sycoecinae in Agaonidae. While the genus Pharmacosycea (sensu Comer 1969): same author (1988 b) also included in The New World section Pharmacosycea (pig. Agaonidae: Epichrysomallinae, Otitesellinae 18-A) is exdusively poHinated by Tetrapus and Sycoryctinae, the Agaoninae including wasps. Thefemale Tetrapus is primitive becau­ only the fig pollinators. Grandi (1961) sugges­ se the maxilla has distinct galea and stipes, a ted fuat some of fue modífications undergone bacillíform process (palpus), which in some by the agaonid head as inventions seemingly is segmented(e.g., Tetrapus costarica­ meaningless. The Agaonidae, Sycoecinae and nus); fue labium hada palpus(Wiebes 1982 a). Sycophaginae have a gula and not a postgenal Tetrapus is also uniquely characterized among bridge as stated a by Bouc�k (1988a). all Agaonidae by having a normal third seg­ mení wifuout a prominent scale-like process (Grandi 1925) andsensilla in fue frrst funicular Comparison of tbe Agaonidae mandible witb segments, as in the non-agaonid fig wasps. tbat of Sycoecinae snd Sycophaga: The man­ Most female Tetrapus (except the pollinator of diblesof fuefemale andmale Sycophaga syco­ F. tonduzii Stand.)have a headdistinctIy longer mor; (Fig. 7), a wasp which does not have an than wide, less thao one and a half times as appendage, may be similar to fuose in fue pre­ long as broad across the eyes with a narrow agaonids. This type of mandible is still found in facial suleus, long scape, pedicel wifuout axial alI agaonid males (pig. 8). Thebidentate mandi­ spines, reducedunsegmented antennal process bIes (Figs. 10 and 13) of fue Sycoecinae wasps and inandibles with only one gland. Tetrapus (which as the agaonids also penetrate figs to seems to be composed of two well defined oviposit) permit some insight intoearly agaonid groups. In one group fue female mandible has mandibularevolution. Bouc�k (1988 a) alsosta­ two appendages, one large and lamellate (as in ted that the mandible in some genera of Blastophaginae), the ofuer small and wifu teefu Sycoecinae seems to suggest how fuemandibu­ (as in Agaoninae) (pig. 15). The male of this le could have developed. group of Tetrapus haS three pairs of functional 90 REVISTADE BIOLOOIA TROPICAL

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Fig. 7. Mandible of female Sycophaga sycomori with two glands (dottedlines) (subfamily Sycophaginae). Fig. 8. Mandible of maleBla stophaga (Pegoscapus) cumanensis, (subfamily Blastophaginae), Mandibles of Diaziella bicolor with two glands (subfamily Sycoecinae) after Grandi, 1928. Fig. 10. Ventral and dorsal view of the mandibles of Seres armipes, (subfamily Sycoecinae), after Grandi:1952a; Fig. n, 3. Fig. 11. Mandibles of Sycoecus thaumastocnema (subfamily Sycoecinae), after Waterston, 1914, Fig. 3 Fig. 3. Fig. 12. Ventral view of mandible of Philocaenusbarbatus (subfamilySycoecinae) with a fixed carinated appendage, after Grandi, 1952a, Fig. 5.2. Fig. 13. Ventral and dorsal view, of mandible of Phagoblastus barbarus, (subfamily Sycoecinae)after Grandi, 1955, Fig. VIT, 3 & 4. legs (hexapodous). In the second group ("true pollinated by Dolichoris wasps (Fig. 18, Q), tetrapódous"), the female has a single long The ancestor of the pollinators of section mandibular appendage with two lateral rows of Oreosycea and Urostigma (Fig. 18, 2-3), as tooth-like serrations(Fig. 16) and the males are' well as those that inhabit subgenus Ficus and tetrapodous. Sycomorus (Fig. 18,2-18), was probably a The pollinators of the Old World section Blastophaga-like wasp; with two mandibular Oreosycea: Oreosyceafigs are monoecious and glands,segmented maxillary bacillifonn proces- RAMIREZ: Mandibularappen dage in figwasps 91

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15 16 Fig. 14: Mandible of female sp. appendage with lamellae (Agaonidae, Blastopbaginae). Fig. 15. Mandible of Tetrapus sp., thepollinator of F. crassiuscula, subgenus Pharmacosycea, with large lamellatedandsmall carinated appendages (subfamily Agaoninae).Fig. 16. Mandible of Tetrapus costaricanus, thepollinator of F.g/abrata, subgenus Pharmacosycea, with only one mandibular appendage(subfamily Agaoninae).Fig. 17. Mandible of Eli sabethiel la stueckenbergi (Agaoninae) with a single carinatedappendage (subfamily Agaoninae).

ses (as in Dolichoris flabellata), pedicel with whorl of long free free sensilla (Wiebes 1979 c). axial spines, 2- segmented third segment, and In the opinion of Wiebes (1982 b), there is an the four flagellomere without sensilla placodea. undeniable resemblancebetween thewasps from As.in Blastophaga group F (=Dolichoris sensu Pharmacosycea (Tetrapus) and those of Wiebes 1979 c; for Blastophaga groups, see Oreosycea (Dolichoris) but this similarity is Ramírez 1977). For example, in B. nervosae. found in primitivecharacters andas such is not However, Dolichoris vasculosae has a head dis­ indicativeof phylogeneticrelationship. tinctly longer than wide, lacks the maxillary The pollinators of subgenera Ficusand bacilliform process, and has the mandibular Sycomorus: The anceslOr of the pollinators of appendage elongate and loosely attached to the Ficus and Sycomorus (Fig. 18, 2-18) was a mandible. Dolichoris females differ from those Blastophaga-like wasp with distinct unsegmen­ of Tetrapus because they have pockets and cor­ tedbacilliform process. biculae lO carry pollen and do not have sensilla Three sections of Ficus (Ficus, Kalosyce, placodea in thefirst flagellomere. However, D . Rhyzocladus) are pollinated by Blastophaga flabellata female has thefmt flagelomere with a sensu strictu (= B. group A, Ramírez 1978) 92 REVISTA DE BIOLOGIA TROPICAL

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which have lost the bacillifonn process. The mandibular crenulate appendages evolved in other sections are pollinated by Blastophaga most of thefemales of this group(as inFig. 17). group B (=Krodibia) Blastophaga groups e and Alfonsiella and Nigeriella (Fig. 18, J and K) D (= Wiebesia?), Ceratosolen and Liporrh0- seem to have the most primitive mandibular palum. Non-long heads or other special modifi­ appendage among the pollinators of cations have evolved in the female pollinators of Galoglychia asthose found in Blastophaginae, die complexFicus-Sy comorus. The Sycomoru s but having ridges with two teeth.or basally wit­ (probablf"riatural) is the only ñg group compri­ hout distinct denticulations (see Wiebes 1974 b). sing both gynodioecious andmonoecious species In Alfonsiella and Elisabethiella the head Is as (Berg 1990,Ramírez 1974, 1977). long as wide across the eyes or distinctly longer The pollinators(Fig. ofsubgenusUrostigma 18, than wide (Wiebes 1974 b, 1982 a). Some fema­ B-p):The subgenushas Urostigma severalsections les of Alfonsiella have twomandibular glands. and pollinatedis several by agaonid genera or COIll­ Agaon, (pig. 18, O) andAllo triozoon (Fig. 18, plexes (Ramfrez 1977). The pollinators ,of section M) have long heads, usually one and half totwo Malvanthera (Ftg. 18, P), evolve<Í very elongaie timeS as long as broads acros the eyes andnarro w heads (except Pleistodontes mandibularis; Wiebes median sulcus. Some Allotriozoon (A. prodigio­ 1982 a) and long crenu1ate mandibularappenda­ sum excepted; Wiebes 1982 a, per8. COlllIJl.) have ges. However in Pleistodontes imperialis andP. elongate heads although not one and a halftimes greenwoodiithe appendagebears lamellae thatare longer than wide. Paragaon (pig. 18, N) has a. scan::ely producedintoteeth. Pleistodontes O and heada little thanlonger broad across the eyes. A11 d baveonemandibular:� Agaon, Allotriozoon andParagaon, (pig: 18, M­ The female ancestor (Fig. 18, 5-6) of the O) have only oneg1and in the mandible in both pollinators oí section Galoglychia: Agaon, sexes anddo.nOt have axialspin.eson thepedicel. Alfonsiella, Allotriozoon, Courtella, Wiebes (1982 a) IÍotecl'thatin the pollinators Elisabethiella, Nigeriella, andParagaon wasa oí Malvanthera and the pollinátors of B�tophaga-like agapnid with Qne gland in the Galoglychia,the maxi11ae do not possess a dis­ .mandibleoftite maleo ·Later, longheads andlong tinct galea, stipes ol'pal pus as in Tetrapus, RAMIREZ: Mandibularappendagein figwasps 93

which he considers to be primitive states. Blastophaga-like ancestor witbout maxillary Unlike Tetrapus; they havesensilla placodea in bacilliformprocess. the last seven flagellomeres only. Corner The pollinators of subgenus Pharma­ (1985) botanically associates section cosycea: Tetrapus andDolichoris do not seem 10 Stilpnophyllum (pollinated by Blastophaga be related.Tretrapus is the pollinatorof the New group G) with section Malvanthera (pollinated World sectionPharmacosycea and belong10 the by Pleistodontes) while Wiebes (1979 a) in bis subfami1y Agaoninae (sensu Wiebes 1973). revised cladogram, fits the pollinators of Dolichoris (Fig. 18, Q), the pollinators of Stilpnophyllum in the midst of section Oreosycea, belong to the subfami1y Conosycea (with several Blastophaga-like Blastophaginae (sensu Wiebes 1973). In groups) and according to Comer (1985), this Dolichoris (except D. vasculosae) andTetrapus has geograpbical and botanicalsupp ort. there still are maxillary bacilliform processes on The pollinators of sections Americana, the maxillae. Wiebes(1982 a) supposes "all this Conosycea, Leucogyne, Stilpnophyllum and to be a primitive condition dating from theagao­ Urostigma (Fig. 18 B-I) belong to the subfa­ nid ancestor". Wiebes (1973) stated that in bis mily Blastophaginae sensu (Wiebes 1973). opinion the wasps Oreosycea (Dolichoris) from , Their ancestor (Fig. 18, 5-11) was a share so many apomorphous("derived' ) charac­ Blastophaga-like wasp with two mandibular ter states with Blastophaga from subgenus glands in both sexes. This type of mandible Ficus, that aclose relationsbip seems likely. is still found in Eupristina (Fig. 18, C), Wiebes(1973 and 1982 b) luniped Tetrapus while in Parapristina and Waterstoniella (the pollinators of New World section (Fig. 18, D and E) the males have only one Pharmacosycea subgenus Pharmacosycea), mandibular gland. In Deilagaon the females Pleistodontes (the pollinators of Malvanthera), have one or two glands. The male of D . and Agaon, Allotriozoon, Alfonsiella, annulatae has two glands (Wiebes 1977 a). Elisabethiella andNigeriella (thepollinators of Deilagaon, Eupristina, Parapristina and Galoglychia) in subfamily Agaoninae. Uolike Waterstoniella are the pollinators of section Tetrapus the pollinators of Galoglychia and Conosycea. Malvanthera do not possess maxillary palps In Pegoscapus (the pollinator of section nor sensilla· in the first funicular segment and Americana), Blastophaga clavigera break the antennae and wings when entering (=Blastophaga group G), the pollinator of sec­ thesyconia. The pollinators of the Urostigma tion Stilpnophyllum (with one species), sections Americana, Conosycea, Leucogyne, Manie/la (pollinators of sections Leucogyne) Stilpnophyllum and Urostigma (Fig. 18 B-I) and Blastophaga group E (=Platyscapa, the seem to form a holophyletic group thatbelongs pollinator of section Urostigma) themales have to Blastophaginae (sensu Wiebes 1973). one mandibular gland (Fig. 18 F-I). AH the The subfamily Agaoninae (sensu Wiebes pollinators of these sections of Urostigma have 1973) does not seem to form an holophyletic lameHate mandibular appendages; however, group as suggested by Wiebes (1973, 1974 b, Waterstoniella williamsii has small teeth on the and 1982 a). Long heads and crenulate mandi­ appendage(Wiebes 1982 a). bular appendages seem to have evolved inde­ pendentIy in three agaonid groups, that is, 1) Pleistodontes (Fig. 18, P), the pollinator of the. Mandibular relationships among Asian section Malvanthera, 2) the pollinators Agaonidae: The pollinators of subgenera of the African fig section Galoglychia (Agaon, Ficus and Sycomorus: Blastophaga sensu Alfonsiella, Courtella, Allotriozoon, Elisa­ strictu .. (=Blastophaga group A) group B bethiella, Paragaon and Nigeriella (Fig. 18, J­ (=Kradibia), Blastophaga groups C and D O), and 3) most species of New World genus (Wibesia), Ceratosolen and Liporrhopalum, Tetrapus (Fig. 18, A). Long heads have also belong to the Old World and form a related evolved in Ceratosolen inmanis and

group (Fig. 18, R-Y). They belong 10 subfamily Dolichoris vasculosae .. two Blastophaginae Blastophaginae (sensu Wiebes 1973). The (Wiebes 1982 a), and in Seres armipes pollinators of subgenus Urostigma (Fig 18 B-P) (Sycoecinae). According to Bouc�k (1988 b), form a related group with a common thepresence of denticulate cross laminae on the_ 94 REVISTA DE BIOLOGIATROPIC AL

mandibular appendages of sornePleistodontes mandibular appendage in the agaonid female seems to raise questions about the subdivision and solenogastry in the male reinforces their of Agaoninae and Blastophaginae by Wiebes. monophylous origino The conformation of the mandibular appen­ dage alone and the long head in Agaonidae do not seem to be a good discriminatory subfamily RESUMEN character since Dolichoris vasculosae and three species of Tetrapus have mandibular appenda­ Se examinaronel valor filogenético de la con­ ges intermediate between those of subfamily formación de los apéndices mandibulares, el Blastophaginae (with lamellae) and número de glándulasmandibulares y otras carac­ Agaoninae(with spines or crenulations). terísticasde la cabezade la familiaAgaonidae. El Furthermore, Waterstoniella williamsi, arreglo filogenético sugiere que el pre-agaónido (Blastophaginae) (sensu Wiebes 1973) has a tenía una mandíbula nonnal bidentada, con dos mandibular appendage with ventral lamellae glándulas y una hendidura facial defInida como which are shaped so as to forro small teeth (as en algunas especies de Diazella (Sycoecinae), in Agaoninae). This mandibular appendage is Sycophaga (Sycophaginae) Y" en otros cálcidos quite similar to that of sorne species of Elisa­ que habitan los siconios y no son polinizadores. bethiella (Agaoninae). Thus, long mandibular El preagaónido tenía una antena con trece seg­ appendages with crenulate mandibular appen­ mentos; escapolargo, variasveces más largo que dage seem to have evolved independently in ancho; un pedicelo largo y triangular; dos o tres several groups of Agaonidae. These groups anillos ("anelli") y ocho flagelomeros con sensi­ develop in unrelated groups of Ficus and in dif­ las (como se encuentra únicamente en Tetrapus). ferent geographical areas and inhabit groups of El apéndice mandibular aparentemente coevolu­ figs (sections Galoglychia, Malvanthera and cionó con el desarrollo del ostiolodel siconio, era Pharmacosycea) with ostiolar bracts bending fIja y contenía rebordes o láminas. Un punto de down to form a a tunnel-shaped or crateriform movimiento (o bisagra) evolucionó más tarde en passage. Comer (1985) concluded that the la base del apéndice. El ancestrode los agaónidos resemblance of sect Malvanthera with sect. fue probablemente una avispa sicofIla primaria Galoglychia resulted from índependent parallel con cabezaaplanada, prognata con gulay tórax y evolution. The same thing could have happen­ abdomen aplastados dorsoventralmente, que ovi­ ned to their pollinators. However, according to positaba a lo largo del canal del estilo. Las avis­ Berg (1986), the sections Galoglychia and pas sicofilas Sycophaginae con sus machos ápte­ Malvanthera may be closely related, but sec­ ros y polígamos parecen serel grupoh ermano de tíon Pharmacosycea is no! related to these two los Agaonidae. Los agaónidos están representa­ Urostigma sections. He also states that section dos, por los polinizadoressimbióticos del género Pharmacosycea is probably the most primitive Ficus y se caracterizan porel apéndice mandibu­ of the the subgenus Pharmacosycea and lar y el proceso antenal. Los machos son ápteros probably of the whole Pharmacosycea­ y solenogastros. Urostigma group. It is also possible that the three groups of Agaoninae represent convergent evolution. It REFERENCES is not difficult to find such a degree of conver­ gence in agaonids that penetrate syconia with Berg, C.C. 1986. Subdivision of Ficus subg. Urostigma very similar ostiola, through which the wasps sect. Galoglychia (Moraceae). Proc. Kon. Ned. Akad. must entero Thus, the subfami1y Agaoninae Wet. (e) 89:121-127. (sensu Wiebes 1973) does not seem to form a Berg, C.C. 1990. Reproduction and evolution of Ficus holophyletic group. According to Wiebes (Moraceae) traits connected with the adequate rea­ (1973) the elongate head does pose the ques­ ring of pollinators. Mem. N.Y. Bot. Gard. 55: 169- tíon as to monophyly of the Agoninae. The 185. unique presence of sensilla on the fourth seg­ Boucé'k, Z. 1988 a. Australian Chalcidoidea ment of the female Tetrapus not only ques­ (I:Iymenoptera). A biosystematic revision of genera of tions the monophyUy of Agaoninae but also fourteen families, with a reclassification oC species. that of Agaonidae. However,the presence of C.A.B. Intemational, Wallinford,U.K. 832 p. RAMIREZ: Mandibular appendage in figwasps 95

Boucék, Z. 1988 b. An overview of me higher classifica­ Grandi, G. 1%1. The Hyrnenopterousmsects of the super­ tion of me Chalcidoidea (parasitic Hymenoptera)., p. family Chalcidoídea developing within me receptacles 11-23. In V. K. Gupta (ed.). "Advances in parasitic of Figs. Theirlífe history, syrnbiosis andmorphological Hymenoptera Research, Proceedings of the II adaptations.Boll. 1st. Ent.Univ. Bologna25: 1-13. Conference on me and Biology of Parasitic Hymenoptera held at the University of Florida, RamírezB., W. 1974. Coevolution of Ficus andAgaonidae. Gainesville, Florida". Ann. Missouri Bol. Gard.61: 770-780.

Ramírez B., W.1978.-A new classification of Ficus. Ann. Comer, EJ.H. 1969. Taxonomic notes of Ficus Linn. Asia Missouri Bot. Gard. 296-310. and Australasia. 1. Subgen. Urostigma (Gasp) Miq. Gdns.Bull. Singapore 17: 208-304. Waterston, J. 1914. Notes on AfricanChalcidoidea. l. Bull. Entom. Res. 5: 249-258. Comer, EJ.H. 1985. Ficus (Moraceae) and Hymenoptera (Chalcidoidea): Figs and their pollinatorfo. Biol. J. Wiehes, J.T. 1973. Phylogenetic specificity of figs and fig Linnean Soco25:187-195. wasps. p. 21-29 In M.B.M. Brantjes (ed.). and dispersal. Dept. of Bot. Mijmegen: 21-29. Grandi, G. 1916. Gli Agaonini (Hymenoptera Chalcididae) raccolti nell'Africa occidentale dal Prof. F. Silvestri. Wiehes, J.T. 1974a. The genus Diaziella Grandi Boll. Lab. Zool. Portici 10:121-186. (Hymenoptera Chalcidoidea, Torymidae Sycoecini). Proc.K. Ned. Akad. Wet. 77(3):295-300. Grandi, G. 1925. Morfologia del gen. Tetrapus Mayr e des­ crizione di una nuove specie della Costa Rica. Boll. Wiebes, J.T. 1974b. Nígeriella, a new genus of West Soco Ent. Ita!. 57:1-13. African fig wasps allied 10 Elisabethiella Grandi (Hymenoptera Chalcidoidea, Agaonidae) Zool. Meded. Grandi, G. 1928. Un nuovo genere e quattro nuove specie Leiden 48: 29-47. di Imenotteri sicofili di Sumatra. Boll. Lab. En!. Bologna 1:71-89. Wiebes, J.T. 1977. Deilagaon, a new genus of Indo­ Malayan and Papuan fig wasps (Hymenoptera Grandi, G. 1934. Nuovi Agaonidi '(Hymenoptera Chalcidoidea, Agaonidae). BijdrgenKierk. 46:291-298. Chalcididae) della fauna neotropica. Boll. Lab. Ent. Bologna 7:186-197. Wiebes, J.T. 1979. The fig wasps genus Dolichoris Hill (HyrnenopteraChalcidoidea, Agaonidae)Proc. K. Ned. Grandi, G. 1952a. Insettti dei fichi senegalesi. Boll. 1st. Akad. Wet. 82:181-196. Ent. Univ. Bologna 1: 186-191. Wiebes, J.T. 1982a. The phylogeny of the Agaonidae Grandi, G. 1952b. Insetti dei fichi messicani, maJe si (Hymenoptera, Chalcidoidea) Netherlands J. Zool. ed australiani. Boll. 1st. Ent. Univ. Bologna. 19:47- 32:395-411. 67. Wiehes, J.T. 1982b. Fig wasps (Hymenoptera) p. 735-755 Grandi, G. 1955. Insetti dei fichi (Hymenoptera­ In: J.L. Gressit (ed.) Biogeography and Ecology of Chalcididae) dell'Africa australe. BolI. 1st. Ent. Univ. New Guinea. Monographie Biologicae 42, W. Junk, Bologna 21: 85-106. The Hage.