THE WASMANN JOURNAL OF BIOLOGY

Vor.. n. No. 2 FALL, 1960

The Life Cycle of Clythia agarici (Willard) (Diptera: Platypezidae)

EDWARD L. KESSEL, University ot San FTCmcisco and CalifoTnia Acaclemy of Sciences.

Ulyfh1:a agctrici (\Villard), unlike most of its , is often ahnndant in the spring of the year. An excellent oppor­ tunit:· tu make observations on its life history was afforded me during ~lpril and lVIay of 1960 at my home in Novato, California. Se\·eral mushrooms of the genus f1gar·icus, probably belonging to the 'ipecies A. CH'1Jensis, matured simultaneously. It was on the morning- of April16, soon after the veils had broken to reveal the gills on the ·e specimens, that the female began visiting the fungi. They started arriving about 10 A.M. and all during the warm part of the day they were ovipositing, as many as six at a time on one mushroom. It was possible to observe them at close range b.'· excavating a "head hole" so that one could look up at the undersurfaces of the fungi. The flies came in slowly for landings on the tops of the mush­ rooms. ~ome of them came directly from a distance. Others alighte

263 264 THE WASMANN JOURNAL OF BIOLOGY, VuL. 1, , 1960

serve a "snowshoes" for the female in walking on the mushy surfaces of decomposing fungi. The fact that the tarsi an' more obviously flattened in the female (fig. 1) than in the male 1 fig. 2) lends credence to this suggestion becau.·e it is the fe mal e that must visit the mushl'oom to lay her eo·o· . However, from the ob­ servations described below, it is evident that the female.· Yisit the mushrooms only during the time that they provide firm footinO', which fact explode the "snowshoe" theory. Nevertheless. the fact

...... -- FmunE 1. F emale of Clythia agctrici, showing flattened seg·ments or posterior tarsi.

FIGl'l!E 2. Male of Clythia aga?"ici. showing posterior tarsi less flat­ tened than in female. LIFE CYCLE OF CLYTHIA AGARICI-KESSEL 265 remains that it is onl:· the females that have business with the fungus as adult , and that business pertains to oviposition. Possihl.'- the heavier and more flattened hind tarsi of the female are adapted to some function in connection with egg laying·. It occnned to me that possibly the female inserts her hind tarsi into the cleft between two gills and thereby forces a wider open­ ing fol' her abdomen. But this attractive theory was soon shown to be incorrect. The flies were not easily disturbed and this fact allowed their activities to be closely watched as the whole under­ surface of the mu hroom was brought into focus through a read­ ing glass. The magnificatio n was adequate to reveal clearly what happened during oviposition. TIH• flie-.; backed into the egg-laying position, sometimes with head directed toward the periphery of the pileus, sometimes to­ ward the stipe. Ordinarily they would take a few steps forward and then back up into the slit between two gills, sinking so deeply that the abdomen was out of sight and t he was up to her wing· bases. The wings were in fact flattened out over the surface of the pileus, but the hind legs were not thrust down between the gills as t>xpected. In tead, the:v were directed outward under the wings. mostl:· sideways and only a little toward the rear, the fiattenetl tar:i braced acros two or three gills on each side. The remained in this seemingly awkward position for about eight or te11 s('(·onls, and then, apparently by stiffenino· the segments of hel' flattened tarsi, eased herself neatly out of the slot. The egg. are like little wiener· in relative length and thickness as well as in the much elongated, slightly curved hape. Later examination showed that each is attached along its full length to the lateral urface of a single gill, about halfway up to the ba e of the gill where it originates on the underside of the pileus. 'l'he eggs are not glued in place; they stay in position merely by adhering to the moist surface of the gill, and so are easy to re­ move for observation. They are creamy white in color. The follo,,·ing day, April 17, I again took my position in the obsenation "head hole,'' expecting to observe more egg laying, but at no time during the entire day was a female seen to visit the under ·ide of the fungus. ow and then one of the flies (the females were still quite numerous in the vicinity, running about in typical stop-and-go fashion or just sitting on nearby foliage) would happen onto the upper surface of one of the mushrooms, 266 THE WASMANN JOURNAL OF BIOLOGY, VoL. l c, 1960 but such flies never tarried long. The gill surface of the fungus had completely lost its attraction for them. In this connection it should be noted that mushrooms found infested with the lalTae of platypezids on previous occasions had always had larvae of ap­ proximately one size. This is under tandable when one has dis­ covered that, for a particular fungus plant, oviposition b.'· platy­ pezid flies seems to be confined to a period of a single da:·. Hatching of the eggs began on the evening of Aprill7. g-iving an incubation period of approximately 36 hours. Hatching was completed by the morning of the next day, indicating that all the embryos had developed at about the same rate. Ob ervations made on the activities of the young larYae (fig. 3) both macroscopically and under the microscope, reYealetl that they do not burrow into the gill tissues. Instead, during the first several days they seem to feed only along the surface of a gill,

FrouRJ> 3. Young larvae of Clythia aga?'ici exposed by removing the gills of their mushroom host. LIFE CYCLE OF CLYTHIA AGARICI- KESSEL 267

working where there is a concentration of pores. Mycetophilid maggots may be found in the same fungu , but these cylindrical larvae with their prominent dark heads not only present a very different appearance but also behave very differently within the host. While the young, conspicuously flattened larvae of this platypezicl species feed by scraping· away on the gill surface , the fungu ·-gnat maggots burrow through the mushroom tissues. To look for the younger larvae of Clythia aga1·ici, one needs only to look bet~een the gills, whereas to check for mycetophilicls, one must pull the mu hroom tissues apart. By the fourth clay the larvae of Clythia agarici had the sur­ faces of the gills, especially along their bases, engraved with a series of wormlike trails. By the sixth clay the mushroom tissues had softened and the rim of the disc had flopped. Most of the lar­ vae had by this time deserted the gills and moved toward the cen­ tral axis of the fungus. Many of them had congregated above the stipe and under the disc at its center. On the seventh clay the larvae had completely disappeared from the gill area. ot only was there a concentration of them above the stipe, but others had penetrated its apex and crowded into it interior. Many had even pa sed down to the subterranean area of the tipe prepar~tory to entering the ground to pupate. It eemed prudent at this stage to remove the ftmgi as intact as possible, along with the soil around and below their ba e . From previous observations on undisturbed fungi it was evident that althoug-h there is often a concentration of pupae under the col­ lapsed fungus and in the interior of the decomposing stipe, there may a Iso be considerable dispersal of the mature larvae prior to pupation. Therefore, in order to lose track of as few pupae a possible, the mushrooms with their full-grown larvae were dug up and transferred to rearing cage·. These were gallon-size card­ board cylinders such as are commonly used for packino· ice cream. The fungi wore placed on a one-inch layer of damp river sand which covered the bottom of the rearino· cage. The mouth of a small o- Jass jar was inserted into the upper wall of the containers so that the jar would serve as a lighted verandah when the posi­ tively phototropic adults were ready to emerge and show them­ solves. It is a well-known fact that when such rearing cages are placed in an uncontrolled laboratory environment which does not dupli- 268 THE WAS!VIANN JOURNAL OF BIOLOGY, Vor.. 18, 1960

TABLE I 1.'e mpe1·atm·e anclp1·eC'ipitation figM·es• to1· the 1Je?'iocl /1'0?n A.tJril JG to May 2 ancl inclicating to1· each clay the clevelotJmental stage ot the insec ts in this life-1t1 sf01·y stucly ot Clythia agarici.

T emperature ( degrees F.) PrecipitatiotJ Date .l1ax. Min. in i,cJr es Developmental stage A~,ril 16 72 40 Oviposition 17 68 41 Incubation (hatching began in evening 1 18 67 50 Trace 1-day larvae 19 69 47 2-day larvae 20 73 43 3-day larvae 21 66 45 Trace 4-day larvae 22 58 40 5-day larvae 23 53 39 .08 6-day larvae 24 61 36 7 -day larvae 25 65 45 8-day larvae 26 59 41 .88 9-day larvae 27 61 46 .04 10-day larvae 28 61 42 11-day larvae 29 70 42 12-day larvae 30 68 40 13-day larvae (pupation began) M~;Y 1 69 45 T race 14-day larvae 2 63 43 1-day pupae 3 58 47 .16 2-day pupae 4 65 46 Trace 3-day pupae 5 70 41 4-day pupae 6 78 45 5-day pupae 7 74 47 6-day pupae 8 68 46 7-day pupae 9 76 42 8-day pupae 10 77 51 9-day pupae 11 75 50 10-day pupae 12 69 52 11-day pupae 13 72 48 12-day pupae 14 72 46 13-day pupae 15 66 46 14-day pupae (emergen ce began) 16 71 47 15-day pupae; day 2 of emergence 17 69 45 16-day pupae; day 3 of emergence 18 70 49 17 -day pupae; day 4 of emergence 19 82 50 18-day pupae; day 5 of emergence 20 66 49 19-day pupae; day 6 of emergence 21 63 46 20-day pupae; day 7 of emergence 22 63 41 21-day pupae; day 8 of emergence 23 57 47 .42 22-day pupae; day 9 of emergence 24 62 49 .21 23-day pupae; day 10 of emergence 25 70 54 Trace 24-day pupae; day 11 of emergence 26 75 50 25-day pupae; day 12 of emergence 27 77 51 26-day pupae; day 13 of emergence 28 73 50 Emergence completed

• I wish to express my appreciation to Donald L. Eberly, a neighbor of min e and meteo rolo­ gist with the Pacifi c Gas and Elect ric Company, for supply in g the temperature and precipita tion

LITERATURE CITED

KESSEL, E. L., and BERTA B. KESSEL 1939. Diptera associated with fungi. Wasmann Collector, 3:72-92. Wn,LARO, FRANKIE 1914. Two new species of found at Stanford Unive1·sity. Psyche, 21: 166- 168.