BIOLOGY AND LIFE HISTORY OF THE SNAIL-KILLING BELONGING TO THE GENUS SCIOMYZA FALLEN (DIPTERA, )1

BENJAMIN A. FOOTE Department of Entomology and Limnology, Cornell University, Ithaca, N. Y.2

ABSTRACT All known larvae of Sciomyza species are efficient attacks and destroys several individuals of Oxyloma killers of terrestrial snails of the family Succineidae. snails. Some biological-ecological information is pre- Life histories are given in considerable detail for 5. sented for S. dryomyzina Zett., but the exact relation- aristalis (Coq.) and 5. simplex Fallen. The larva of ships with the snail host are unknown for this and for the former is very closely associated in a parasitoid the fourth Nearctie species, 5. varia (Coq.). Keys are manner with Succinea ovalis Say, a common woodland given to the adults, and to eggs, third-instar larvae, and snail of the northeastern states. The larva of 5. simplex puparia of the species for which they are known. Downloaded from https://academic.oup.com/aesa/article/52/1/31/12944 by guest on 02 October 2021 is probably more predaceous in its habits, as it readily

It has been only since the recent publication this genus. S. lucida Hendel and testacea Mac- by Berg (1953) of a paper dealing with the quart are restricted to the Palaearctic Region; habits of the immature stages of the sciomyzid dryomyzina Zetterstedt and simplex Fallen are flies that it has been generally recognized that Holarctic in distribution and aristalis Coquillet the larval stages of this family are killers of and varia Coquillet are apparently limited to the snails. Before that time it was commonly Nearctie Region. Thus four species are known assumed (on no reliable evidence whatsoever) to occur in North America, although dryomyzina that the larvae were consumers of decaying plant has been reported only from Alaska. Biological material or occasionally carnivorous on small information is now available on three of these invertebrates (e.g. Lundberg, 1923). For a more four species. extensive review of the pertinent literature on European workers (Sack, 1939; Verbeke, 194S) the larval habits of the Sciomyzidae the reader continue to use the generic name Bischofia is referred to Berg's paper. It is the purpose of Hendel for the six included species, but it appears the present paper to present a few observations that Sciomyza has distinct priority. Fallen on the life history of three Nearctie species of one (1820) proposed the name Sciomyza to include genus of the family. 12 species of sciomyzid flies. West wood (1840) designated 5. simplex Fallen 1820 as the type ACKNOWLEDGMENTS species of Sciomyza, and his type designations I wish to express my deep appreciation to Dr. were later upheld by Opinion 71 of the Inter- C. (). Berg of Cornell University for his continuing national Rules of Nomenclature. Hendel (1902) support and enthusiasm during the course of the first proposed the name Bischofia and selected present investigation. Without his valuable sug- S. simplex as the generitype of his new genus. gestions and constructive criticisms the life Because this species had already been selected as history studies would have been considerably the generitype of Sciomyza, it seems quite obvious more difficult to undertake. He also made that Bischofia is a junior synonym. Hendel available to me his two reared puparia of S. (1910) recognized that his generic name was a dryomyzina Zetterstedt. Mr. Stuart Neff pro- synonym and stated that Sciomyza should be vided the original material for the rearing of considered as the correct name, but later reversed .V. simplex Fallen and has been a very pleasant himself and reinstated Bischofia without giving companion on many field trips. And finally I any reasons for so doing. wish to tender my thanks to Mr. George C. It is interesting that all the known larvae of Steyskal for his many helpful hints and suggestions this genus are associated with terrestrial snails concerning the and geographic distribu- of the family Succineidae. Repeated attempts tion of the adult flies. to feed the larvae on species of snails belonging to other families were completely unsuccessful. The Genus Sciomyza Fallen The larvae are either predators or parasitoids on According to Steyskal (1954), who presented the living snails and have not been observed to a key to the world species of Sciomyza, there are invade decaying carcasses. In the present paper only six species now recognized as belonging to a predacious larva is considered as being one which normally attacks and kills several snails 'This investigation was supported by a research grant during the course of its larval life. A parasitoid (E-743) from the National Institute of Allergy and larva, on the other hand, is one which invades Infectious Diseases, U. S. Public Health Service. Ac- and eventually kills only one snail during its life. cepted for publication June 23, 1958. The term parasitoid is referable to Reuter (1913) 2Present address: Department of Entomology, Uni- versity of Idaho, Moscow, Idaho. and is in common usage in the literature dealing 31 Annals Entomological Society of America [Vol. with the larval habits of certain groups of KEYS "parasitic" Hymenoptera (Ichneumonidae, Bra- Adults: conidae, Chalcidoidea, etc.). .1. Thoracic dorsum black; mesopleura bare posteriorly: fore femora black, at least on apical one-half.... From the study of the life histories of the S. varia (Coq.) three species an evolutionary development of the Thoracic, dorsum ferrugineous to grayish; meso- -snail relationship can be discerned. Two of pleura with at least a few bristly hairs posteriorly the species, S. dryomyzina and simplex, leave the near suture 2 2. Palpi blackish, at least apically; center of face host snail after completing larval growth to strongly blackened; fore femora wholly yellow. . pupate on or in the ground. The S. aristalis S. aristalis (Coq.) larva, on the other hand, remains with the Palpi wholly yellow; face uniformly yellowish to destroyed snail and eventually forms a puparium reddish-brown 3 within its shell. S. aristalis adult females 3. Mesopleura with at least two strong bristles pos- teriorly in addition to numerous shorter birstly Downloaded from https://academic.oup.com/aesa/article/52/1/31/12944 by guest on 02 October 2021 will not oviposit except directly on the shell hairs; ventral half of pleura pruinose; dorsum of of a living snail while adults of simplex merely mesonotum grayish with four darker longitudinal deposit eggs on vegetation in the immediate stripes; fore femora usually wholly yellow "S. simplex Fall. habitat of its host snail. These two observations Mesopleura with only a very few fine, short hairs clearly indicate that, of the three species, 5. near the posterior suture, without outstanding aristalis is the most intimately related to its host bristles; ventral half of pleura not pruinose; dor- snail. sum of thorax shining reddish-brown; fore femora usually blackened on apical one-half or more.... Sciomyza adults can be distinguished from those S. dryomyzina Zetter. of other sciomyzid genera by the following Eggs: combination of characters: possession of a strong 1. Egg uniformly elongate-ovoid, not flattened or con- propleural bristle; presence of two preapical cave on one side; chorion with all surfaces covered bristles on fore tibia; subbasal arista clothed by a with reticulate pattern; eggs not deposited on snail shells S. simplex black plumosity. The key given below to the Egg flattened or concave on one side; chorion on four Nearctic species is somewhat modified from this flattened surface smooth, without reticulnte Steyskal (1954). pattern; eggs deposited on snail shells. .S. aristalis It is not possible as yet to separate the eggs of Third Instar Larvae: Sciomyza from those of other genera. The eggs 1. Post-oral sternal plate present (fig. 9); spinules in are elongate-oval in shape, white to cream in ventral creeping welts black, conspicuous; ventro- color and have a chorion pattern of reticulated lateral lobes of posterior spiracular disc, well- pits and ridges (fig. 15). The eggs of only two developed (fig. 13); peritreme of posterior spiracles species are known and these can be separated by brown S. simplex Post-oral sternal plate absent or represented by a the accompanying key. very few small spinules; spinules in ventral creep- The following combination of characters will ing welts pale, apices darkened 2 serve to distinguish the larvae of Sciomyza from 2. Peritreme of posterior spiracles densely black; marginal lobe number of anterior spiracles those of other genera: color white to cream; approximately 27 S. aristalis ventral creeping welts with well-defined spinule Spiracular peritreme yellowish to light brown; bands; ventral cornua of pharyngeal sclerite of marginal lobe number of anterior spiracles cephalo-pharyngeal skeleton with conspicuous approximately 25 S. dryomyzina oval window; parastomal bars very poorly Puparia: developed, barely reaching posterior border of the 1. Puparium strongly twisted dorsally and to the left hypostomal sclerite; mouthhooks without acces- on posterior third; strong crease running ob- sory teeth, connected posterodorsally by a liquely across dorsum of posterior four segments; narrow, chitinized bar. Two species are known puparium definitely not barrel-shaped, formed within snail shell (fig. 16) S. aristalis in the larval condition, and the characters of a Puparium basically cylindrical, barrel-shaped, third can be deduced from available puparia. formed away from snail shell (fig. 18) 2 These can be separated by the accompanying key. 2. Anterior spiracles dorsal in position on cephalic. cap (fig. 19), about 32 lobes around margins; Puparia of three species are known, but these spinules in vestiges of larval ventral creeping can be positively distinguished from species welts black, conspicuous; ventral lobes of spi- belonging to other genera only on the basis of the racular disc, closely approximated medially, not larval cephalopharyngeal skeletal characters as divergent, posterior spiracles not visible when mentioned above. The puparium must be opened puparium is viewed ventrally S. simplex Anterior spiracles distinctly lateral in position, on and the cephalopharyngeal skeleton removed and short pedicels (fig. 18), approximately 25 lobes mounted before the definitive characters can be around margins; spinules in ventral creeping determined. Puparia of 5. simplex and dryomy- welts pale with blackened apices; ventral lobes zina are basically barrel-shaped, but those of of spiracular disc divergent, posterior spiracles aristalis are somewhat twisted posteriorly. The visible ventrally S. dryomyzina anterior spiracles are shaped like a cogwheel and have a marginal lobe number varying from 24 Sciomyza aristalis Coquillett to 32. Puparia of the three species are separated An intensive search of the literature failed to by the accompanying key. turn up a single reference dealing with the life Foote: Biology of Snail-Killing Flies 33 history of this uncommon fly. The species is shells containing puparia still have the egg poorly represented in collections and is easily attached (fig. 16). Snails which were unsuccess- overlooked by field collectors. It is apparently fully attacked by the first-instar larvae (11 in all) limited in distribution to the Nearctic Region, remained active for several weeks without and Steyskal (personal communication) reports rubbing off the now empty egg. Usually only adults from the following states and provinces: one egg is attached to a shell, but occasionally a Maine, New Hampshire, Vermont, Massachusetts, snail would be found with two eggs laid end to New York, Michigan, Quebec, Ontario. The end in the suture. In the laboratory up to six species thus seems to be restricted to the north- eggs were deposited on a single living snail placed eastern portion of the country, being replaced in in a breeding jar with a single female fly. Records the mid-west by S. simplex Fallen. maintained on 10 eggs indicate an incubation In ecological distribution the adults show a time of four to five days after which period the distinct preference locally for rather open flood- first instar larva hatches and begins active Downloaded from https://academic.oup.com/aesa/article/52/1/31/12944 by guest on 02 October 2021 plain woods dominated by American elm {Ulmus creeping movements over the surface of the americana L.) and red maple {Acer rubrum L.) snail. Surprisingly, hatching occurs from the and having a luxuriant herbaceous undergrowth. end of the egg farthest from the aperture of the Adults and immature stages were most abundant snail. This was true in every one of the 21 eggs in the vicinity of Ithaca in an open swamp forest held under observation. containing many dead and dying elm and maple Larval habits.—Unless the tiny larva is rubbed trees and having scattered colonies of cattail off the shell it eventually comes in contact with (Typha latijolia L.). The fly habitat preferences the foot of the snail exposed in the aperture. naturally parallel those of the host snail, Succinea Once contact is made the larva attempts to insert ovalis Say, but the snail seems to show greater itself between the mantle covering the flesh and amplitude of habitat selection than does the fly. the outer lip of the snail. If successful the larva The snail, for example, is occasionally common moves dorsally up onto the flesh and soon comes around hillside seepage areas in forested regions, to rest on the mass of the digestive gland. The but I have never taken the fly in such situations. snail flesh is forced down by the larva, forming a Nor has the fly been collected in the fairly dry small depression in which it lies while feeding on margins of open cat-tail marshes even though the gland. Apparently enough oxygen accumu- the snail may occur quite abundantly there. lates in this cavity to support the respiratory needs of the larva. No contact is made by the LIFE HISTORY larva with the oxygen available in the mantle Eggs. Eggs of this species were first discovered cavity of the snail. Feeding activity seems to on September 3, 195G during a collecting trip consist of a series of rasping movements of the to an open flood-plain woods bordering the larval mouthhooks over the flesh of the snail. outlet stream of Cayuta Lake, Schuyler Co., N. Y. After the first two days the larva increases in where the host snail occurs abundantly. During size very rapidly and soon becomes readily visible the examination of a few snails that were attached as an elongate, translucent maggot contrasting to leaves of cattail, one specimen was noticed quite strongly with the darker body of the snail. which had a small, white, reticulate egg attached After being invaded by the larva the snail to the shell. Further collecting resulted in the remains active for three or four days without discovery of 21 living snails with attached eggs, much visible sign of distress. It continues to out of a total of 220 snails examined. All 21 feed and move about normally. At the end snails were taken a few feet above the ground on of four days, however, the snail becomes highly the leaves of cattail. All were definitely alive inactive, retracts somewhat into its shell and when collected and were later transported to the frequently attaches itself by a mucous secretion laboratory where they were placed individually to the substrate (usually a Typha leaf in nature). in small, dry stender dishes. After still another day it shows signs of life only The egg is deposited longitudinally in the by the waves of fine tremblings that pass over suture separating the last two whorls of the shell the now completely retracted foot. At the end and is typically placed only a few millimeters of seven or eight days death of the snail occurs away from the shell aperture (fig. 14). Measure- and decay of the remaining flesh begins. Appar- ment of the distance from the lower end of the ently death occurs at about the time the larva egg to the aperture of the shell gave a range of molts into the third instar. 0.2 to 5.() mm. in the 21 eggs examined. Placed Even after the snail dies the larva continues as it is in a suture between two convex surfaces, to feed on the decaying flesh and quickly reduces the egg is admirably protected from being it to a black, highly odoriferous liquid. However, rubbed off the shell as the snail moves about in the relationship of the larva to the snail host is its normal activities. An additional insurance that of a parasitoid even though the larva com- is provided by the glue-like substance cementing pletes its larval life as a saprophagous form. the egg firmly to the shell. Actual evidence for Only a single snail is normally consumed by a the permanence of the egg on the snail is that larva during the course of its development. In Annals Entomological Society of America [Vol. 52 the laboratory a snail frequently died before the left there until Dec. 28, 1950, (35 days) when feeding larva's posterior spiracles became exposed they were again removed to room temperature. to the air in the aperture. In all such cases the No emergence had occurred by Feb. 7, 1957, larva also succumbed. Probably larval death when the puparia were re-examined. Two were was ultimately caused by the accumulation of definitely dead as evidenced by an abundance poisonous decomposition products within the of mold enveloping the puparia. The remaining snail shell. The larva apparently did not make five still appeared good and were then placed any attempt to reach the air in the aperture and outdoors in a renewed attempt to break diapause. was never observed to leave the decomposing Air temperatures during late February and snail completely. However, if death of the March dropped as low as 10° F. for several days snail occurs after exposure of the larval posterior at a time. On April 1, 1957, all five puparia spiracles to the air in the aperture the larva were returned to room temperatures. On April 24, is little affected, usually completes its develop- 1957, a single female aristalis emerged. No Downloaded from https://academic.oup.com/aesa/article/52/1/31/12944 by guest on 02 October 2021 ment and pupates in the shell. If an egg is laid further emergence was obtained and the remaining on a small specimen of snail the larva either four puparia were eventually preserved. The forms an undersized puparium or succumbs to environmental factors responsible for the initiation lack of food. In no cases did a larva leave one of diapause remain unknown. The eight diapaus- snail and attack another although several living ing puparia were all reared from eggs collected snails were placed together in the same small dish. (Sept. 3, 1956) in nature and their subsequent Pupation.—Approximately 11 days after inva- larval development was under the relatively sion of the snail, larval development is completed stable conditions of the laboratory. If a physical and the fully grown larva prepares to pupate. It environmental factor such as temperature or first eliminates from the gut the remaining food photoperiodism is the cause of the initiation of material and then reverses itself in the shell so diapause it must be operative either on the egg that now the posterior spiracles are directed or on the adult which deposits the egg. towards the apex and the anterior spiracles are The diapause problem is somewhat further exposed to the air in the shell's aperture. The complicated by the fact that a female collected larval integument loosens from the underlying in nature during mid-August laid eggs which flesh, rapidly hardens and soon assumes the eventually gave rise to non-diapausing pupae. reddish color of the puparium. The belief that Much more penetrating experimentation will be pupation within the host snail shell is the normal necessary before an understanding of the diapause situation is supported by the discovery in nature phenomenon in this species can be gained. It of two shells containing well-developed puparia. would seem that two, three or, perhaps, even Another bit of evidence is that one larva which more generations a year are possible in the did pupate away from the snail formed a puparium vicinity of Ithaca since the egg to egg period is nearly shaped to fit within the aperture of the approximately 35 days under laboratory condi- shell. This observation also indicates that the tions. In nature this developmental period shape of the puparium may have become partially could be considerably lengthened or shortened, fixed genetically and may not be completely according to weather conditions. determined only by the peculiar configuration of Adult behaviour.—As is the case with many the shell. During the summer months under sciomyzids, there seems to exist in this species a laboratory conditions the pupal stage lasts short period of time between emergence of about 20 days. At the end of this period the adults and the occurrence of mating. However, emerging fly pushes apart the dorsal and ventral no conclusive evidence is available to support cephalic caps of the anterior end of the puparium this assumption. While mating was never ob- and escapes. If, however, eggs or early instar served until the second day after emergence, no larvae are collected in late summer and fall continuous observation on the adults was main- (Sept. 3, 1956), development proceeds up to the tained and it is possible that mating occurred puparium stage at which time a diapause may the first night after emergence. Mating of this become operative causing some of the to pass the winter as young pupae within puparia in the snail shells. With the return of warm weather in the following spring the diapause is broken and development of the pupae continues EXPLANATION OF PLATE I until eventually the adult flies emerge, mate and Third instar larval structures of 5. aristalis. start the cycle over again. From the eggs found (All measurements in mm.) FIG. 1.—Lateral view of larva. on living snails collected (Sept. 3, 1956) in nature FIG. 2.—Cephalopharyngeal skeleton; PS—pharyngeal a total of seven puparia were eventually obtained. sclerite, DC—dorsal cornu, VC—ventral cornu, HS— No adult flies emerged from these puparia even hypostomal sclerite, ES—epistomal sclerite, MH— after 30 days of exposure to room temperatures mouthhook, V—ventral bar. (65°-75°F.). On Nov. 12, 1956, all seven FIG. 3.—Anterior spiracle. FIG. 4.—Ventral spinule band pattern on abdominal puparia were placed in a refrigerator (45° F.) and segments two through seven. FIG. 5.—Posterior spiracular disc. Biology of Snail-Killing Plies PLATK I Benjamin A. Foote

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35 36 A nnals Entomological Society of A merica [Vol. 52 species was observed several times in the rearing Nothing is known concerning the food of the jars, but I have never observed any sort of a adults in nature. In the laboratory they feed prenuptial courtship behaviour on the part of the readily on a moistened mixture of honey and male as has been reported for many other species brewer's yeast. They are very susceptible to of Diptera. In all observed cases, the male low moisture content in their immediate environ- assumes a dorsal position astride the female with ment and, in the laboratory, it was necessary to both partners facing in the same direction. The water the breeding jars daily. Very little is anterior tarsi of the male are placed along the known about the adult longevity in nature. inner margin of the eyes of the female just Adults can be found at practically any time exterior to the fronto-orbital bristles. The male's during the summer, but this could merely indicate middle legs are widely spread and come down emergence of successive generations. In the over the leading edge of the slightly spread breeding jars, the adults lived up to 63 days, but wings of the female. The male's hind tarsi are most died within a month after emergence from Downloaded from https://academic.oup.com/aesa/article/52/1/31/12944 by guest on 02 October 2021 loosely placed against the sides of the female's puparia. posterior abdominal segments. These hind tarsi, Remarks.—It is, of course, quite possible that however, are frequently moved forward and the larvae can develop in species of snails other backward and may even be completely freed than Succinea ovalis, especially those species from contact with the female. The duration of closely related to the "normal" host. On one copulation is quite variable lasting anywhere occasion, a single living specimen of Oxyloma from a few seconds to over an hour in length. decampi (Tryon) (family Succineidae) was found Copulation is repeated frequently throughout with an egg of S. aristalis attached to the shell the life of the male: in the usual manner. This snail is very closely There seems to be a definite egg maturation related to 5. ovalis and frequently occurs together period existing between the first observed mating with it in the same habitat. It possesses the of the adults and the actual deposition of eggs. same habit of crawling up on vegetation to This interval varied from 2 to 4 days in the 5 escape an overly wet substrate. It is, however, females kept under observation. After this a much smaller snail and it is doubtful if a single apparent maturation period, the female deposits specimen could satisfy the nutritional needs of eggs more or less continuously over considerable the larva. In the case mentioned, the first instar periods of time. One reared female remained larva failed to invade the snail successfully. alive for over 2 months in the rearing container, Living specimens of both Succinea avara Say and and deposited from 1 to 6 eggs daily for the Oxyloma decampi were placed together with first 10 days after oviposition commenced. After adult females of aristalis in a breeding jar and that, her egg-laying activities were more spas- eggs were deposited on the shells of both species. modic, with considerable lapses of time occurring Hatching occurred, but all larvae died without between periods of oviposition (intervals of 2 successfully invading the snails. Some egg deposi- to 10 days). Records maintained on this reared tion was also obtained on specimens of Lymnaea female showed that she laid a total of 36 eggs palustris (Lymnaeidae), but once again the over the two-month period. Two wild-caught larvae failed to penetrate the snail flesh. No females deposited 32 and 39 eggs over a 16 day eggs were deposited on living snails belonging to period. the families Polygyridae and Endodontidae. Egg-laying was observed several times in the It seems logical to expect that one snail could laboratory and a definite behaviour pattern support only a single larva and, in nature, two could be discerned. The adult female, upon eggs were rarely found together on the same contacting the shell of a living Succinea, taps it snail. In the single instance in which two larvae a few times with her fore tarsi while moving were found feeding together within a snail, only slowly about on the shell surface. Occasionally one larva managed to complete its development she undergoes a spinning motion, revolving and pupate. The second larva was found dead several times in place on the body whorl of the shell while gradually moving back to the suture separating the last two whorls. This spinning activity ceases shortly, with the female coming EXPLANATION OF PLATE II Third instar larval structures of 5. simplex. to rest facing away from the apex of the shell. (All measurements in mm.) Probing movements with the tip of the abdomen FIG. 6.—Anterior spiracle. then occur in the immediate vicinity of the FIG. 7.—Ventral view of'eighth abdominal segment. suture. This lasts only a few seconds, then the FIG. 8.—Posterior spiracular plate. ovipositor is exerted and an egg quickly deposited FIG. 9.—Sternal plate and spinule patch on venter of first thoracic segment. in the suture. The fly then leaves the shell or, FIG. 10.—Ventral spinule band on third thoracic at least, she has not been observed to immediately segment. lay another egg on the same shell. Several eggs FIG. 11.—Ventral spinule band pattern on first ab- may be deposited in the suture but, apparently, dominal segment. FIG. 12.—Ventral spinule band pattern on abdominal only as a result of repeated visits by the ovi- segments two through seven. positing female. FIG. 13.—Posterior spiracular disc. Biology of Snail-Killing Flies PLATK 11 Boni'amin A. Foote Downloaded from https://academic.oup.com/aesa/article/52/1/31/12944 by guest on 02 October 2021 0.0 5

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37 38 A nnals Entomological Society of A merica [Vol. 52 within the decaying flesh of the snail, but if it disc, also a few spinules dorsad to spiracular was killed by the other larva could not be plates. determined. Anterior spiracles circular, shaped more or less Nothing is yet known about the parasites, like a cog wheel with 25 to 28 lobes around parasitoids, predators and other enemies of the margins (fig. 3), color slightly yellowish. Posterior immature stages of the fly. A single egg was spiracles with well-developed, densely black found which had a round hole in the chorion peritremes, spiracular slits narrow, straight, reminiscent of the emergence hole of certain egg elongate; stigmatic scar circular, included in parasitoids of the wasp family Trichogram- peritreme, but appearing slightly darker in color, matidae. I have observed that the eggs of other marginal scars absent. Spiracular disc (fig. 5) species of sciomyzid flies are attacked by these more or less flattened with two strong, bluntly tiny wasps. rounded ventral lobes, ventro-lateral lobes shorter; lateral, dorso-lateral and dorsal lobes reduced to Downloaded from https://academic.oup.com/aesa/article/52/1/31/12944 by guest on 02 October 2021 DESCRIPTIONS OF IMMATURE STAGES mere tubercules. Anal plate bilobed, colorless. Egg (fig. 15).—Elongate-ovoid, flattened to Cephalopharyngeal skeleton (fig. 2) well- slightly concave on side attached to shell, bluntly developed, strongly pigmented with black. rounded at both ends; 1.15-1.50 (average 1.29) x Pharyngeal sclerite with dorsal and ventral 0.35-0.41 (0.39) mm. (21 eggs examined); chorion cornua separated posteriorly by deep sinus opaque, light cream color to faintly yellow; extending forward three-fourths distance to chorion finely sculptured with reticulate pattern anterior margin of sclerite; each ventral cornu of tiny pits and ridges except on the smooth, containing oval, unpigmented window postero- unmarked ends and on the side attached to the dorsally; window also present in each dorsal shell. cornu, but considerably narrower and partially Third larval instar (fig. 1).—Length 12.0 to obscured by pigment; dorsal cornua connected 14.5 mm., width 2.8 to 3.2 mm. Color white to dorsally by antero-dorsal bridge; parastomal cream throughout except on blackened posterior bars very poorly developed, each consisting of spiracular plates. Body more or less elongate, short prolongation from shallow sinus on anterior subcylindrical, tapering anteriorly, obliquely border of pharyngeal sclerite, this prolongation truncate posteriorly with spiracular disc margined barely reaching posterior margin of hypostomal with several rather distinct lobes. Cephalic sclerite. Hypostomal sclerite free anteriorly and segment with two pairs of one-segmented sensory posteriorly from adjacent sclerites, somewhat papillae on anterior margin above oral opening, "H"-shaped, but with anterior arms about twice these not surrounded basally by blackened length of posterior arms, crossbar solidly pig- sclerotized rings. mented, without window. Epistomal sclerite Spinule bands mostly restricted to ventral weakly pigmented, immediately dorsad to and creeping welts, no bands completely encircling in close contact with hypostomal sclerite, consist- body; spinules in creeping welts small, pale with ing of central arch indented on each side anteriorly blackened apices; post oral band with well- and with projection extending posteriorly on developed spinules, broad ventrally, narrowing either side, these flattened rods reaching crossbar laterally, absent dorsally, a few small, pale of hypostomal sclerite. Mouthhooks well-devel- spinules lining lateral margins of atrium; first oped, strongly pigmented, bridged postero-dorsally by narrow bar; basal piece without teeth on thoracic segment without distinct sternal plate anterior margin, with small oval foramen anteri- ventrally, but with small patch of four to eight orly. Ventral bar present below antero-ventral spinules; second thoracic ventral creeping welt margin of basal piece, free laterally from mouth- without well-defined spinule band, only with a hooks, consisting of flattened arch extending few widely scattered spinules; third thoracic ventrally across space between mouthhooks and creeping welt with single undivided spinule band long narrow rod projecting posteriorly from each ventrally, spinules directed posteriorly; first side of bar; teeth present along anterior margin abdominal welt with single spinule band laterally, of bar, fading out laterally. dividing ventrally to form two distinct bands, spinules in both bands with apices directed Puparium (fig. 17).—Length 5.2 to 0.9 mm., posteriorly; second through seventh abdominal width 2.8 to 4.2 mm. Color shining reddish- creeping welts with three spinule bands ventrally, brown, darker brown to black on dorsum of these bands less separated from each other than anterior half, fading to light reddish-yellow in 5. simplex with spinule-free areas between or brown posteriorly; venter mostly reddish- bands narrow (fig. 4), spinules in most anterior yellow, dark reddish-brown to nearly black band of each segment with apices directed anteriorly. Shape somewhat affected by position anteriorly, those of two other bands directed in snail shell; posterior three or four segments posteriorly, eighth abdominal segment with usual strongly twisted dorsally and to the left, strong three bands anteriorly on segment plus narrow crease extending obliquely across dorsum of band just before anal plate. Numerous spinules posterior two to four segments where puparium on ventral and ventro-lateral lobes of spiracular was in close contact with shell columella; puparium Biology of Snail-Killing Flies PLATK 1 r I Benjamin A. Foote Downloaded from https://academic.oup.com/aesa/article/52/1/31/12944 by guest on 02 October 2021

(All measurements in mm.) FIG. U Living Succinea ovalis snail showing egg of 5. aristalis attached to shell. FIG. 15 Enlarged view of aristalis egg. FIG. 10 Puparium of aristalis within 5. ovalis shell. FIG. 17 Dorsal view of puparium of 5. aristalis. FIG. IS Puparium of S. dryomyzina. FIG. IS) Puparium of .S\ simplex. 39 40 A nnals Entomological Society of A merica [Vol. 52 strongly flattened dorso-ventrally on anterior in marginal lobing; 24 to 2(5 marginal lobes. four or five segments, swollen ventrally. Anterior Lobing around spiracular disc reduced; ventral spiracles dorsal, well removed from anterior lobes most noticeable, these not closely approxi- margin of first segment; circular; light reddish- mated medially, but divergent; ventro-lateral brown in color, darker centrally with numerous lobes subequal to ventrals, narrower; remaining small black spots; narrow gap in marginal lobing lobes barely perceptible; spiracular disc not posteriorly; spiracular disc with only ventral subtended ventrally by shelf formed by ventral lobes conspicuous, these appressed to puparium lobing, spiracles thus visible when puparium is and not strongly protruding; other lobes barely viewed ventrally; spiracular peritremes yellowish, perceptible. Spiracular plate solidly black except interslit areas black, slits and stigmatic scars for yellowish spiracular slits, stigmatic scars not more yellowish. Ventral spinule band pattern appearing lighter. Ventral spinule band pattern as described for 6". aristalis, spinules pale with as described for larva, spinules pale with darker blackened apices; ventral sternal plate and Downloaded from https://academic.oup.com/aesa/article/52/1/31/12944 by guest on 02 October 2021 apices. No sternal plate or blackened tubercle blackened tubercle patch absent. Anal plate patch on first segment ventrally. Anal plate blackish. reddish-brown to blackish, slightly sunken below general surface of puparium. Sciomyza simplex Fallen There is a single reference in the literature Sciomyza dryomyzina Zetterstedt concerned with the biology of this species. A search of the literature produced a single Lundbeck (1923) published a short description reference dealing with the life history of this of the discovery of the puparium of Bischofia species. Berg (1953) discovered that the larvae (equals Sciomyza) simplex during the spring attack and destroy living snails belonging to the months in flood refuse bordering lakes and genus Oxyloma. He collected approximately 300 marshes in Denmark. He also collected a single living Oxyloma decampi gouldi Pilsbry from an puparium in October which produced an adult Equisetum marsh located in the Matanuska fly in a heated room 24 days later. The puparium Valley of Alaska. These were set up in clean, is very briefly described as being somewhat dry finger bowls. A few days later he noticed cylindrical, slightly attenuated at each end and that a few of snails were dead, and closer examina- blackish-brown in color. The puparia were tion of the containers revealed the presence of two completely free of any snail. fly puparia. One of these puparia eventually This species shows a Holarctic distribution produced an adult of S. dryomyzina. Unfortu- being found throughout northern Europe and nately Dr. Berg was unable to carry out further northwestern North America. In this continent, investigations into the biology of the species, and it is known from the following states and life history data remain quite meagre. It is provinces: Michigan, Wisconsin, Iowa, North apparent from Berg's rearing that the larvae Dakota, Montana, Oregon, Washington, Alberta, invade and eventually consume living snails, but Manitoba, Alaska (Steyskal, personal communica- whether the relationship to the snail is a parasitoid tion). It is thus seen to be mainly western and or a predacious one remains unknown. Berg northern in distribution and has not been recorded informs me tljat the Oxyloma snails were very east of Michigan. 5. aristalis apparently replaces abundant in the marsh and had the usual habit it in the northeastern portion of the country. of crawling up onto vegetation. I have never collected this species in the field S. dryomyzina is widespread in the Palaearctic and must, therefore, depend on the observations Region, but is known only from Alaska in North of other collectors concerning the ecological America. Both dryomyzina and simplex occur distribution of the flies. Berg informs me that it together in the same habitats in Alaska (Berg, was a fairly common species in an Equisetum personal communication) and both are now marsh in the Matanuska Valley of Alaska. Later known to attack living Oxyloma snails. he collected adults on July 2, 1957, near Ft. Puparium (fig. 18).—Length 5.2 mm., width Yates, North Dakota. These flies were swept 2.0 mm. Color dull to subshining light reddish- from a marshy situation bordering a sluggish brown, slightly darker on spiracular disc. Shape stream margined with a lush growth of water- basically cylindrical, not distinctly truncate loving grasses and sedges. Mr. Stuart E. NefF posteriorly, but with spiracular disc somewhat also collected this species recently (July 4, 1957) elongate; puparium narrowed anteriorly and by sweeping the margins of a shallow lake somewhat flattened dorsoventrally to form lateral bordered by a fairly wide band of Scirpus spp. ridges on cephalic caps. Anterior spiracles dis- growing in a few inches of water. This lake tinctly lateral in position on ridge of first apparent (Lake Emma) is located near Prince Albert segment, on short peduncles, narrowed antero- National Park, Saskatchewan, Canada. These posteriorly giving somewhat rectangular appear- three collecting records, all from widely scattered ance to spiracle; color more or less uniform localities, definitely indicate that S. simplex is a reddish-yellow, darker centrally, with numerous dweller in the more open marshes containing small black spots; narrow gap present posteriorly herbaceous vegetation. This is in distinct con- Foote: Biology of Snail-Killing Flies 41

trust to >S\ aristalis which prefers well-shaded remain long with a dead snail once decay had floodplain woods. It is now known that simplex progressed to any extent and, therefore, did larvae attack and destroy living snails of the comparatively little saprophagous feeding. genus Oxyloma, and both Dr. Berg and Mr. Neff Some information is available concerning the inform me that specimens of Oxyloma were so length of time spent in the three larval instars. abundant in the marshes where the adult flies Larvae which hatched on July Hi were in the were collected that while sweeping for flies they second instar by July 18, giving a first larval frequently would pick up several snails in the net. stadium lasting only 2 to 3 days. Some of these second instar larvae molted into the third instar LIFE HISTORY on July 20 and the remainder on July 21, thus Eggs. Eggs of this species were first obtained giving a second instar stadium lasting from on July Hi, 1957 when Neff returned to Ithaca 2 to 4 days. Only three puparia were obtained. from western Canada. He collected adult flies One was formed on July 25, another on July 2(i, Downloaded from https://academic.oup.com/aesa/article/52/1/31/12944 by guest on 02 October 2021 on July 4, 19.17, and confined them in a jar for and the third on July 27. This would indicate transportation back to Ithaca. A single male that the third larval stadium lasts about (i days. fly was still alive when Ithaca was finally reached, The total time spent as a larva did not exceed but on the stems and leaves of a moss placed 12 days. in the bottom of the jar were 10 eggs and two The snail, when first attacked by the larvae, very recently-hatched larvae. The eggs were gives off copious amounts of mucus and throws loosely attached to the moss and were easily its foot around violently. Usually these defensive removed to small stender dishes. They were measures on the part of the snail are unsuccessful, scattered over the surface of the moss and no and the larvae quickly begin feeding on the distinct clusters could be discerned. A few living exposed flesh. After about (i hours, the snail snails of the genus Lymnaea were also in the jar, becomes inactive, retracts somewhat into its but no eggs were found attached to their shells. I shell, and may attach itself to the substrate by a feel that in nature the female merely deposits her mucous secretion. Death of the snail follows eggs in the immediate neighborhood of the snail within 24 hours or less depending, in part, on the host and that the larvae then must seek out and number of larvae present. The snail flesh invade the snail. decays quite rapidly, once death has occurred, No information is available as to the length and soon reduces to a highly odoriferous liquid. of the incubation period except that it must be However, the larvae leave the carcass before this less than 14 days as all eggs had hatched by stage is reached. July 18, 1957 (they were laid between July 4 and Pupation.—Approximately 11 to 12 days after July Hi). The newly emerged first instar larva hatching, the larva is fully grown and prepares is quite active and moves about in an apparent to pupate. It leaves the snail upon which it is search for food. Hatching occurs through one feeding, empties the remaining gut contents and, end of the egg. in the rearing dishes, at least, moves down into Larval habits. -Because larvae of S. aristalis the moist sphagnum moss used as a substrate. and dryomyzina were known to attack living The larva becomes shortened in length, thickens snails of the family Succineidae, it was decided and loses the typical appearance of a dipterous to present to the recently hatched larvae living maggot. The integument loosens from the under- snails belonging to the genera Succinea and lying flesh, quickly hardens and assumes the deep Oxyloma. Two larvae were placed on the shell reddish-brown color of the puparium. In all of Succinea ovalis Say, but these failed to invade three cases where pupation was obtained, the the snail and were eventually lost. In two other puparium was formed away from the snail host. rearing dishes larvae were placed with specimens The puparium is basically barrel-shaped and of Oxyloma decampi (Tryon), and these snails definitely not adapted to fit within the aperture were quickly attacked and overcome by the of an Oxyloma snail. The posterior spiracles are larvae. The larvae do not move up onto the not directed dorsally, indicating that the puparium flesh under the shell as is the case with aristalis is not adapted to float at the water's surface. If larvae, but merely remain at the shell aperature a puparium is placed in water, the posterior feeding on the exposed flesh. As many as four spiracles are submerged. In nature pupation larvae were seen feeding on a single snail. probably takes place in the moist soil bordering Frequently a larva would insert its body into the the marsh. flesh of the snail, but always remained with at Only a single adult emerged from the three least the posterior spiracles exposed to the air puparia. A male emerged on August 5, 1957, in the aperture. From the rearing, it seems that from a puparium formed on July 25, 1957, thus the relationship of the larva to the snail is more giving a pupal period of about 10 days. Emergence or less of a predacious nature. Certainly, in the of the adult occurs in the usual manner, with the rearing dishes, the larvae moved readily from a dorsal and ventral caps of the anterior end of the dead and decaying snail to an active, living one. puparium being split apart along a line of It was also observed that the larvae did not weakness. 42 A nnals Entomological Society of A merica [Vol. 52

No emergence was obtained from the remaining black tubercles (fig. 9); second thoracic ventral two puparia even after 40 days of exposure to creeping welt without distinct band of spinules, room temperature conditions. These puparia a few scattered spinules may be present; third were examined on September 15, 1957, and showed thoracic segment with single, undivided spinule no mold or other evidences of death. It was band ventrally (fig. 10); first abdominal segment believed that a diapause had become operative with single band laterally which divides ventrally and, in an attempt to break the possible diapause, into two distinct bands separated by narrow, the two puparia were placed under refrigeration spinule-free area as in 6". aristalis (fig. 11); second at a temperature of 45° F. for 66 days. They through seventh abdominal creeping welts with were again removed to room temperatures (65° to three bands ventrally (fig. 12), these separated 75° F.) on November 21, 1957. No emergence from each other by distinct, spinule-free areas had occurred by December 20, 1957, and the which are somewhat wider than in 5. aristalis, experiment was terminated when a heavy growth spinules in each anterior band with apices directed Downloaded from https://academic.oup.com/aesa/article/52/1/31/12944 by guest on 02 October 2021 of mold enveloped the puparia, indicating that anteriorly, those of following two bands directed death of the pupae had occurred. posteriorly, second through seventh segment also Adult behaviour.—Practically nothing is known with small patch of spinules on sides of body just about the activities of the adult flies in nature. anterior to spinule band, this patch fading out The single male collected in western Canada by on seventh segment; eighth abdominal segment Mr. Neff remained alive in the breeding jar with usual three bands anteriorly plus narrow, only 18 days. No information is available undivided band just before anal plate (fig. 7). concerning mating habits and egg-laying behav- Numerous spinules on ventral and posterior iour. The adults fed readily in the laboratory surfaces of ventral lobes of spiracular disc, on a mixture of brewer's yeast and honey. spinules smaller, less heavily pigmented on Remarks.—The natural food of the larvae dorsal surfaces and on other lobes surrounding remains unknown, although it is confidently felt disc, small group of darker spinules dorsad to that it is one or more species of Oxyloma snails. posterior spiracles. The discovery by Lundbeck (1923) of puparia Anterior spiracles (fig. 6) yellowish, shaped during the early spring indicates that in Europe, like a cog wheel with approximately 32 marginal at least, the winter is passed as a quiescent or lobes. Posterior spiracles (fig. 8) surrounded by diapausing pupa within the puparium. The fairly wide, brown peritremes; spiracular slits puparium has not been collected in the field in as in 5. aristalis, stigmatic scar circular, lighter this country. No information is yet available in color, marginal, circular scars present on concerning the possible predatory and parasitoid either side of spiracular slits. Posterior spiracles, enemies of the immature stages. on the whole, considerably lighter in color than those of 5. aristalis. Spiracular disc flattened DESCRIPTION OF IMMATURE STAGES with ten marginal lobes (fig. 13); ventral lobes Eggs.—Elongate ovoid, rounded at both ends; strong, bluntly rounded; ventro-lateral lobes 1.1-1.3 x 0.31-0.36 mm. (three eggs examined); narrower; lateral lobes shorter, but distinct, chorion opaque, white in color; chorion uniformly slightly turned apically towards ventro-laterals; finery reticulate, pits shallow, elongate, sub- dorso-laterals short, rounded; dorsals reduced to rectangular, reticulations absent on extreme slight protuberences. apices of egg. Cephalopharyngeal skeleton very similar to Third larval instar.—Length 7.5 to 8.0 mm., that of S. aristalis, but with following differences: width 1.2 to 1.4 mm. Color white to cream hypostomal sclerite with posterior arms very except for darkened post spiracular plates and short, projecting only slightly from crossbar; ventral spinule bands. Body elongate, sub- mouthhook without oval foramen, but with two cylindrical, tapering anteriorly, truncate poste- or three very small fenestrae anteriorly; ventral riorly with terminal segment margined with ten bar without flattened rods projecting posteriorly. more or less distinct lobes. Cephalic segment Puparium (fig. 19).—Length 5.4 to 6.3 mm., with two pairs of one-segmented sensory papillae width 2.4 to 2.6 mm. Color shining reddish- dorsad to atrium, both pairs surrounded basally brown, darker on posterior spiracular disc. by blackened sclerotized rings; ventral papillae Shape basically cylindrical, more or less truncate with basal rings incomplete on antero-dorsal posteriorly, spiracular disc not elongate and not side; dorsal papillae with rings complete. turned dorsally; puparium narrowed anteriorly Spinules mostly restricted to ventral creeping and somewhat flattened dorso-ventrally to form welts, spinules black, conspicuous, post-oral lateral ridges on cephalic caps. Anterior spiracles spinule band broad ventrally, narrowing laterally, dorsal in position, very close to anterior margin fading out dorso-laterally, narrow row of pale of first apparent segment; nearly circular in spinules border lateral margins of atrium; first shape; color reddish-brown, marginal lobes more thoracic segment with distinct sternal plate, yellowish, numerous black spots centrally; mar- brown to black in color, preceeded anteriorly by ginal lobing absent posteriorly leaving narrow conspicuous patch of very heavy, stubby, densely gap; 30-33 marginal lobes. Lobing around Foote: Biology of Snail-Killing Flies

spiraeular disc reduced over that of larva; Saskatchewan. Unfortunately no habitat data ventral lobes blunt and broad, closelv approxi- was recorded on any of the locality labels pinned mated medially; ventro-laterals most prominent, with the specimens. narrow; remaining lobes greatlv reduced; spi- raeular disc subtended vcntrally by shelf formed REFERENCES CITED by ventral and ventro-lateral lobes, spiracles Berg, C. O. 1953. Sciomyzid larvae (Diptera) that thus not visible when puparium is viewed feed on snails. Jour. Parasitol. 39: 630-36. Fallen, C. F. 1820. Diptera sueciae. Rciomyzides: 11. ventrally; spiraeular peritremes brownish, slits Hendel, F. 1902. Revision der palaarktischen Scio- and stigmatie scars more yellowish. Ventral myziden. Abh. Zool.-Bot. Ges. Wien, Bd. II, Heft spinule band pattern as described for third instar 1. 92 pp. larva, spinules strong, black in color; sternal 1910. tlber die Nomenklatur der Acalyptratengat- plate present on venter of first apparent segment, tungen nach Th. Beckers Katalog der palaarktischen Dipteren, Bd. 4. Wiener Ent. Zeitung 29:307-13. Downloaded from https://academic.oup.com/aesa/article/52/1/31/12944 by guest on 02 October 2021 brown to black in color, proceeded by blackened Lundbeck, W. 1923. Some remarks on the biology of tubercle patch. Anal plate blackish. the Sciomyzidae, together with the description of a new species of Ctenulus from Denmark. Vidensk. Medel. Dansk Naturhist. For. Kobenhavn 7b: 101- Sciomyza varia (Coquillet) 109, 4 figs. Of the four Nearetic species of the genus Reuter, O. M. 1913. Lebensgewohnheiten und Instinkte der Ineskten. Berlin: R. Friedlander & Sohn. 488 Sciomyza, varia is the least known biologically. pp. It is a very rare species and is poorly represented Sack, P. 1938. in: Linder, Die Fliegen der palaeark- in museum collections. No reference to any tischen Region. 37. Sciomyzidae. Stuttgart: E. phase of its biology could be discovered in the Schweizerbart. 87 pp., 23 figs., 1 pi. Steyskal, G. C. 1954. The Sciomyzidae of Alaska literature. It is apparently restricted in distribu- (Diptera). Proc. Ent. Soc. Washington 56(2): 54-71. tion to the Nearetic Region and Stevskal (personal Verbeke, J. 1948. Contribution h l'etude des Scio- communication) reports it from the following myzidae de Belgique (Diptera). Bull. Mus. Roy. vStates and provinces: Michigan, Ontario, Quebec. Hist. Nat. Belgique 24(3): 1-31. Westwood, J. O. 1840. An introduction to the modern Two specimens in the Canadian National classification of insects. Vol. 2. London: Long- Museum were collected in the province of man, Orme Brown, Green and Longmans.

THE CLASSIFICATION OF THE EPHEMEROPTERA I. EPHEMEROIDEA: BEHNINGIIDAE1

GEORGE F. EDMUNDS, JR.2 AND JAY R. TRAVER3

ABSTRACT The two previously known Old-World species of representative of the family, Dolania americana, is de- Behningia are reviewed. B. ulmeri Lestage is known from scribed from four nymphs from the Savannah River and 2 nymphs from the Volga River of Russia, B. lestagei its tributaries in South Carolina. All these nymphs have Motas and Becesco from 1 nymph from the Dniester remarkable adaptive features for burrowing in sand. The River in Moldavian S.S.R. and 3 from the Warta River Behningiidae seem derived from potamanthid-like ances- in Poland. The 2 adult males, 1 nymph, and 4 nymphal tors, and pertain to the superfamily Ephemeroidea. A exuviae from the lower Amur River of Eastern Siberia, new subfamily, Anepeorinae, is erected for the heptageniid which Tshernova earlier referred doubtfully to B. ulmeri, genus Anepeorus whose nymphs, like those of Behningiidae, are placed in B. tshernovae, n. sp. The first American have truly ventral gills.

The mayfly family Behningiidae is one of the mature nymphs (one male, one female) col- rarest and least known families of mayflies. The lected June, 1922, in the Volga River by A. first known representative of the group was Behning. The mayfly was not named. Figures described by Georg Ulmer (1924) from two were given of the dorsal view of the whole nymph, antenna, developing genitalia of the male nymph, lThis study was supported in part by grants-in-aid mouthparts, gills one and two, legs, and venation to the senior author by the National Science Foundation of the nymphal wing pad. Principally because of (NSF-G 2514) and the University of Utah Research the incipient wing venation, Ulmer thought the Fund. Accepted for publication May 5, 1958. "University of Utah. nymph might be allied to the Oligoneuriidac, 'University of Massachusetts. although he noted that the developing male