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Rev. Biol. Trop., 44(3)/45(1): 277-282, 1996-1997

Breathing adaptations of males in tig gall flowers (Hymenoptera: Agaonidae)

Williarn Rarnírez Escuela de Fitotecnia, Universidad de Costa Rica, San José, Costa Rica

(Rec. 6-X-1995. Rev. 14-VI-1995. Acep. 7-11-1996)

Abstract: Apocryptophagus and Sycophaga wasps (Sycophaginae, sensu Boucek 1989) develop in the syconia oC Sycocarpus and Sycomorus figs. The syconia are foil oC a liquid when the males eclose Crom their galIs. The males have terminal abdominal filamentsthat are extensions oC the peritremes. These filament� are used to anchor the poste­ rior part oC the abdomen inside the fig galls, and to maintain the abdominal spirac\es inside them. Earlier authors sus­ pected a breathing fonction. In this position sorne males spend up to 20 minutes probably using the air present inside the galls while they are searching for the dispersed female-containing galls for mating inside. By migrating from gall to gall, the malesare able to breath and displacethemselves along and around all the inundated syconial cavity without drowning. In this paper, new observations and structures associated with breathing are presented and iIlustrated with photographs. Apocryptophagus and Sycophaga males also possess very enlarged longitudinal tracheal truRks which probably function as air or gas reserves. Apocrypta fig wasps (Sycophaginae) also develop in syconia with inundated cavities and the males seem also to use for breathing the air present in the galls. The females oC these genera ec\ose from their galls after mating and after the liquid oC the syconial cavity has been absorbed. Contrary to suggestions by other authors, who supposed the filarnents oC the male Apocryptophagus and Sycophaga were breathing structures or temporary air stores themselves, evidence shows that they help to anchor the end of the gaster inside the galls and that gas exchange occurs thorugh spirac\es in the gaster.

Key words: Male,respiration, adaptations, Hymenoptera Sycophaginae, figwaspS.

The larvae of all sycophilous wasps develop they have "gills", Le., long filaments on the inside modified female fig flowers ("gall flow­ spiracular peritremes. Murray (1990) noted that ers") where, they get the nourishment and air Eukobelea males (=Apocryptophagus) use the for respiration. Several authors have explained forked tip of the abdomens as an anchor, and the functions Oí the large or filamentous per­ that the Apocrypta bakeri male sometimes will itremes of sorne males of the subfamily anchor himself to a gall by lodging the expand­ Sycophaginae. For example, WiIliams (1928) ed tip of the abdomen on the inside of a narrow suggested that the filarnents allowed the males entrance holeo Godfray (1988) noted that of Sycophaga nota (=Apocryptophagus ?) to Apocrytophagus sp. males partially emerged remain submerged [in the liquid of the syconial from the gall after mating, keeping the rear part cavity] for sorne time or were used as f10ating of the body anchored in the original gallo devices. He also noted (without explaining Ramírez (1987) postulated that the large per­ why) that the male had a little difficulty in itremes and protruding breathing structures withdrawing the diverging lamellae [or fila­ found in sorne fig wasps were adaptations to ments] from the galls. Wiebes (1982) noted the humid environments in which they live dur­ that the males of Eukoebelea [probably ing part of their life cycle. Compton and Apocrypaphagus] are arnong the fitst to appear MeLaren (1989) conc\uded that the peritremes in the hurnid interior ofthe receptac\e and that of figwasps studied by them "act as respitatory 278 REVISTA DE BIOLOGIA TROPICAL

siphons and perhaps also as temporary gas Observations were made using a dissecting stores" for the insects. microscope while the males of Apocryptophagus According to Compton and MeLaren nota, (Baker) Sycophaga cyclostigma Waterston (1989), the hydrofuge hairs on the peritremes and Apocrypta sp. (probably A. guineensis of sorne fig wasps are associated with syconia Grandi) were eclosing from the galls and mat­ having liquid-filled lumens. These hairs were ing. The males did not appear to be disturbed by found to be capable of repelling liquids and the microscope light and manipulations after the perhaps also serving as temporary air stores. syconia were opened and they continued search­ Both the male and female syconia of the ing and mating. Meomorphe, Sycocarpus and subgenus Sycomorus figs, where Old World Sycophaginae wasps develop, are pollinated by RESULTS Ceratosolen wasps (Wiebes 1963) and become filled with a transparent liquid or "liquour" The terminal filaments of Apocryptophagus after being oviposited or pollinated and Sycophaga (Figs. b-c, Fil) are extensions of (Cunningham 1889, Baker 1913, Williams the peritremes of the two abdominal spiracles 1928, Murray 1987). This phenomenon has with the small spiracles located at their bases. also been observed by the author for several They are covered with small bristles (Fig. C) or other species of the subgenus Sycomorus hairs as noted by Ansari (1967). The hairs are (sensu RamÍrez 1977), for Ficus minahassae bent over at their tips (Compton & MeLaren (Teysm. et Vr.) Miq. (sect. Sycidium, ser. 1989). Apocrypta males have wide plate-like Phaeopilosae) and Ficus pseudopa lma Blanco (not prong-like) large and conspicuous spiracu­ (sect. Pseudopalmeae) of subgenus Ficus lar peritremes covered with bristles or sensilla which are also pollinated by Ceratosolen (Ulemberg 1985). wasps. Compton and MeLaren (1989) also When early male phase syconia of both mentioned the presence of liquid in the lumens species of fig studied were opened, the of Sycomorus and Sycocarpus figs. Apocryptophagus and Sycophaga males had This article rather proposes the indirect cut, with their mandibles, a narrow slit from associated respiratory functions of the tail-like inside the gall flowers where they developed. appendages on sorne Sycophagini males, as They partially emerged, head frrst, leaving the well as of the large peritremes of Apocryptini end of the abdomen with the filaments and males (Sycophaginae). spiracles inside the gall (Fig. a). While still Material and Methods: Gall syconia from a anchored with the rear part of the abdomen and single tree in early male phase of a gyno-dioe­ filaments inside the galls, the males stretched cious F. nota (Blanco) Merr., (for developmen­ out the abdomen (like an elastic ribbon) inside tal phases, see Galil and Eisikowitch 1968) were the inundated syconial cavity and appeared to collected on the campus of the University of searchin the liquid for galls containing females Philippines at Los Baños (UPBL) in November, of their own species. Abdomen stretching 1989. The syconia were found to have emerging allowed the males to find female-containing males of Apocryptophagus nota (Baker). galls a distance of about six galls. Once the The syconia of F. sur Forssk. (monoecious) anchored males of both genera found a gall were also obtained from a single tree in early containing a female, with the mandibles they male phase at the Botanical Garden of Rhodes cut a narrow slit in the upper surface of the University, Grahamstown, South Africa gall, introducing the narrow flat head and tho­ (November, 1990), when the Sycophaga rax. Inmediately they liberated the end of the cyclostigma and Apocrypta sp. males were abdomen and the filaments from the gall in eclosing from thegalls. The liquid of the syco­ which they developed, contracted the body nial cavity in both species had not been rapidly and penetrated completely into the gall, absorbed and the cavity was completely inun­ probably mating there. Shortly after the dated. The syconia were transversely cut near abdomen disappeared, the male head started the ostiolum to preserve the maximum volume emerging through the exit (see also Williams of fluid. Many nematodes were swimming in 1928), suggesting that mating was brief, as the liquid at the time the syconia were opened. noted by Godfray 19.88 for Apocrypta sp., W. Rrunírez: Adaptations of male figwasps 279

Fig. l. Males of Apocryptophagus sI'. from Ficus nota in Luzon, Phillippines: (al maJe atlached to a female-contam­ ing gall flower; (b) lateral view of male notiee the abdomi­ nal filaments; (e) end of abdomen with filaments; (d) dor­ sal view of maje showing the ¡arge longitudinal traehea and filaments. G=gall: Plm = filament; Tra = trachea. 280 REVISTA DE BIOLOGIA TROPICAL

probably A. mega Ulemberg and their galls while the syconial cavíty was still Apocryptophagus sp. males inhabiting F. his­ filled wíth liquido They cut narrow slits to eelose pidiodes S. Moore. Then, the male pushed out from their galls, and stayed for a short time the anterior part of the body, leaving again only anehored to the slit by the swollen rear of the the end of the abdomen and filaments inside abdomen. Next they pulled the abdomen from the gall, and the process was repeated. By the gall, carrying two airbubbles in the abdomi­ sequentially using the gaIl of the last mated nal peritremata, swam and "searehed" between female as an stationary "respiratory tank" eaeh the galIs until they found one containing a male eould eover all the cavity. Less frequent­ female, where they cut a narrow slit, penetrated ¡y, the galls left empty by other males, (e.g., an and apparentIy mated, for a few seeonds. empty gall of a Ceratosolen male, as noted by Godfray 1988), galls with mated females, or those with males of its own species, were also DISCUSSION used. Sycophaga cyclostigma males have an abdominal morphology similar to The males of Apocryptophagus, Apocrypta Apocryptophagus males, they also become and Sycophaga emerge from the gall where they anehored with the filaments, and probably use developed before the males of other species (e.g. the gases present in the galls of F. sur for respi­ Ceratosolen, Philotrypesis, Sycoryctes and oth­ ration; one male seemed to aetively search for ers). This probably prevents overerowding and 22 min while anchored from one gallo Both avoids damage by males of fighting speeies Apocryptophagus and Sycophaga males pos­ ("soldier males" of Murray 1989 and 1990). sess very enlarged tracheal trunks along their These observartions support the hypothesis that, bodies (Fig. d, Tra.), as also illustrated by in order to breath inside the inundated syconial Compton and MeLaren (1989, Fig. 1) whieh cavitíes, the Sycophagini males and probably probably funetion as air sacs or air reserves. Apocrypta, use the oxygen present inside the Other syeophilous wasps do not have enlarged gall flowers which contrary to the syconial cavi­ traehea; e.g., PhilotrypesiS caricae (L.) as illus­ ty do not have liquido The ribbon-like extensible trated by Joseph (1958, Figs. 15-17). abdomens of Apocryptophagus and Sycophaga Several Apocrytophagus males (N=12) were males allow them to seareh and to find the experimentally dislodged from the galls and female-eontaining galls, which are dispersed left in the fig eavity. They would reaeh an open inside the syconíal cavity while they are still gall and enter it; otherwise, they beeame inac­ anchored to a gallo The large non-projeeting tive or died. Males (N=12) anehored to their broad concave peritremes of Apocrypta males galls (as in Fig. a) and extraeted from the syeo­ probably allow them to breath inside the female­ nial eavity, were introduced into a 70% alcohol containing galls, as well as to obtain air bubbles solution and survived for �8 min, while those from the gall which are carried on the per­ (N=12) that were introduced without contac itremes, while freely traveling along the inundat­ with galls (as in Fig. d) died almost immediate­ ed syeonial cavity. ly. These observations provide indireet evi­ The function of the liquid found in the syco­ dence that anchored males used gall oxygen nial lumen is uneertain (Comptom & MeLaren and that they used only the spiracles of the 1989). Janzen (1979) suggested (with no sup­ eight abdominal segmento When an anchored porting evidence) a defensive function, stating maJe met a conspecific maJe in the syconial "that the liquid without doubt eontains antibiot­ cavity, it pushed him aside and no biting or ic eompounds". MeLaren and Compton (ín fighting was observed. However, Godfray preparation) have faíled to confirm that the liq­ (1988) noted fighting for an Apocrytophagus uid of F. sur has either anti-fungal or anti-bac­ sp. The Apocryptophagus and Sycophaga terial properties. The liquid of the syeonial cav­ males studied did not guard females after mat­ ity is secreted by the figs after the primary ing or spend much time within female galls, in sycophilous wasps have oviposited or fertilized constrast with Murray's observations (1990) on the fig flowers and this probably avoids the Apocrypta bakeri (Joseph). penetration of supernumerary pollinators, as The Apocrypta males (probably A. guineen­ suggested by Baker (1913), and of supernumer­ sis) of about 10 syeonia of F. sur, eelosed from ay Sycophaga colonizers. W. Ramírez: Adaptations of maJe fig wasps 281

ACKNOWLEDGMENTS machos usan el aire de las agallas para respirar aunque no poseen filamentos terminales. Las The author is indebted to the University of hembras de los géneros mencionados son fertil­ Costa Rica (UCR) and to the University of izadas dentro de las agallas y eclosionan de Philippines at Los Baños (UPLB) for providing éstas cuando el líquido del sicono ha sido financial support and other facilities for travel­ absorbido. Contrariamente a las sugerencias de ing to the Philippines. To Blass Hernaez, otros autores que creyeron que los filamentos Systematic Laboratory, for the identification of de los machos Apocryptophagus y Sycophaga F. nota. To Ludwig Naegel and Heriberto eran estructuras respiratorias o reservas de aire, Flores of Farming Systems and Soil Resource la evidencia demuestra que los filamentos Institute and Raymond Lucero, Department of abdominales sirven para anclar la parte caudal Entomology, Forest Science (UPLB) for the del abdomen dentro de las agallas y que inter­ use of the laboratory and transportation facili­ cambio de gas ocurre a través de los espirácu­ ties. To R.H. Hepburn and other personel of the los abdominales. Department of Zoology and Entomology (Rhodes University Grahamstown), for their financial, laboratory and transportation facili­ REFERENCES ties in South Africa. J. Monge Nájera of the Biology School, University of Costa Rica made Ansari, M.O. 1967. A new species of fig inseets (ChaJcidoidea: Hymenoptera fromIndia. Indian 1. Ent. suggestions to improve the manuscript. . 28: 74-83.

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