ADAPTIVE DIFFERENCES IN PHENOLOGY IN

30 September 1982 MEM. E NTOMOL. SOC. WASH . 10,1982 , pp. 15-36

ADAPTIVE DIFFERENCES IN PHENOLOGY IN SCIOMYZID FLIES

C. O. BERG, B. A. FOOTE, L. KNUTSON, J . K. BARNES, S. L. ARNOLD, AND K. VALLEY (COB) Department of Entomology, Cornell University, Ithaca, New York 14853; (BAF) Department of Biological Sciences , Kent State University, Kent, Ohio 44242; (LK) Insect Identification and Beneficial Insect Introduction Insti tute, Beltsville Agricultural Research Center, USDA, Beltsville, Maryland 20705; (JKB) Biological Survey, New York State Museum and Science Service, New York State Education Department, Albany, New York 12230; (SLA) Minitab Project, Pennsylvania State Universily. University Park, Pennsylvania 16802; (KV) Bureau of Plant Industry, Pennsylvania Department of Agriculture, Harris burg , Pennsylvania 17110.

Abstract.-Five distinct patterns of seasonality, overwintering, and voltinism in malacophagous Sciomyzidae (Diptera: Acalyptratae) living in cool , temperate latitudes are described. Multivoltine species overwinter as either pupae or adults; univoltine species, as embryonated eggs , partly grown larvae, or pupae. Evolu tion of this phenological diversity has resulted in temporal and spatial partitioning of food resources and consequent reduction of interspecific competition. Species that are active as larvae in fall, winter, or early spring can exploit molluscan populations with relatively little competition from other Sciomyzidae . The sea sonal restriction of need for food by larvae enables univoltine species to colonize emphemeral aquatic habitats that are less favorable for multivoltine species .

Our first indications of phenological diversity in the Sciomyzidae (Diptera: Acalyptratae) were observations that some multivoltine species apparently over winter in the pupal stage; some, as hibernating adults (Berg, 1953). Subsequent studies have shown that multivoltinism with overwintering in the pupal stage is by far the most common, most widespread, and probably the primitive pattern . However, three univoltine patterns also have been found, with univoltine species overwintering as embryonated eggs. as partly grown larvae, or as pupae. These phenological data are dispersed in many papers, each elucidating the biology of a single genus or species group. No summary of seasonality and over wintering in the Sciomyzidae has been published. The only summary of voltinism in this family (Soos , 1958) is based solely on capture records of adults . Without data on rearings and on collections of immature stages, that author could only guess at numbers of generations per year from lengths of observed flight periods. Because collecting efforts had been almost confined to late spring and summer , the entire flight periods of some species had not been observed. This study was made (I) to test and establish the validity of early presumptions of phenological diversity (e.g. to determine whether adult Sciomyzidae can be

16

MEMOIRS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

collected in winter and whether overwintered flies can reproduce), (2) to assemble information on seasonality scattered through the sciomyzid literature and inte grate it into a comprehensive analysis of phenology in this family, and (3) to offer an explanation for the evolution of this phenological diversity in a monophyletic family that is relatively uniform and well integrated in most biological aspects. This explanation focuses on the critical need of all Sciomyzidae to develop through their larval stages when their molluscan food is abundant and accessible, and on the importance of being able to exploit snail populations that are not available to most Sciomyzidae because of their limited seasonal occurrence or their ephemeral habitat. Effective temporal partitioning of food resources has occurred because some species are active as larvae very early in the spring, late in the fall, or during the winter. U nivoltine species whose larvae complete their development during the season when water and snails are present in ephemeral aquatic habitats also isolate themselves spatially. Adaptive differences in phe nology thus have reduced interspecific competition for molluscan food by re source partitioning that is both temporal and spatial. Concerted collecting of Sciomyzidae at all seasons and in all stages of their life cycles began with the discovery that their larvae kill and consume snails (Berg, 1953). Laboratory rearings of about 200 species have demonstrated that almost all sciomyzid larvae feed only on Mollusca (Berg and Knutson, 1978)1. The only reared species of Salticellinae and all known larvae in the Sciomyzinae: Scio myzini are essentially terrestrial, lacking the adaptations for aquatic life possessed by most larvae in the Sciomyzinae: Tetanocerini. All feed as insidious parasitoids, either on terrestrial snails or on aquatic snails that have been stranded or have voluntarily left the water. With few exceptions, they have remained conservative and relatively similar in phenological patterns as well as in habitats and molluscan foods. In contrast, larvae of the Tetanocerini have diversified greatly in their foods, feeding habits, habitats, and phenology. There are greater biological, ecological, and phenological differences within the genus Tetanocera than throughout the Sciomyzini. Larvae of at least some species of Dietya, Elgiva, Eulimnia, Hedria, Knutsonia, Phcrbina, Psaeadina, Renocera, Sepedon, and Tetanoeera are free living predators that are well adapted for life in water. The larvae of other species of Tctanoeera and Sepedon feed as parasitoids on terrestrial snails, and larvae of some species of Tetanocera kill and consume slugs. Most of the aquatic pred ators attack freshwater, pulmonate snails, but Eulimnia phi/potti Tonnoir and Malloch, Kilutsonia lineata (Fallen), and all reared species of Renoeera consume fingernail clams (Sphaeriidae). Larvae of all reared species of Antichaeta burrow into snail egg masses and feed on the eggs, the gelatinous matrix, and the devel oping embryos. Our studies of the Sciomyzidae have been centered at Ithaca, New York Oat. 42.26N). Although they have expanded to other regions of North America and other continents, all species included here except Eulimnia phi/potti inhabit temI We are following Griffiths (1972) and Barnes (1981) in removing from the Sciomyzidae three subfamilies that share very few characters with the Sciomyzinae and probably are no more closely related to them than to Sciomyzoidea in other families. The result is a well unified family composed only of the Sciomyzinae and Salticellinae.

ADVANCES IN DIPTERAN SYSTEMATICS

17

perate latitudes north of the equator. The months specified in Fig. 5 and elsewhere in this paper therefore denote the seasons prevailing during those months in the North Temperate Zone. The use of "vernal " and "autumnal" to delimit temporary ponds and marshes in Fig. 5 and elsewhere follows that of Wiggins et al. (1980). Vernal ponds fill with water from melting snow and rain in March and April, but gradually decline in volume later in the spring and are without surface water by late June or early July. Since they remain dry until the following spring, they have an annual cycle of three to four months wet phase and eight to nine months dry phase . However, the surface water of autumnal ponds and marshes is replenished by autumn rains, usually in October, and maintained throughout the winter and spring, also dis appearing by late June or early JUly. Autumnal bodies of water thus have a wet phase of about nine months and a dry phase of three months. GROUP

1:

MULTIVOLTINE SPECI ES THAT OVERWINTER AS PUPA '

Most species of Sciomyzidae living in cool, temperate latitudes are multivol tine, and most survive the winter in puparia. Species having this phenological pattern (Fig. 5, Group I) can be collected as puparia throughout the year; most species do not occur in nature in any other stage during the winter. (Note ex ceptions u nder Diclya and Atrichom elinll below.) Adults emerge in the spring, and a series of summer generations is produced. Diagonal lines were added across the summer months in Fig. 5 to suggest that no individual egg, larva, or pupa normally persists throughout the summer (as individual pupae do persist through out the fall, winter, and early spring) , and that the average time required for a complete life cycle is about one month. However, summer generations do not remain nearly so discrete as the diagram implies. Because rates of growth and development vary, and especially because adult females may continue to lay a few eggs each day until long after their oldest daughters have begun to oviposit, summer generations overlap in nature . Although five generations are possible as implied , some of the individuals collected in the fall probably represent earlier generations. This common phenological pattern is widespread in the Sciomyzidae and other acalyptrate families. It occurs in the Salticellinae (Knutson et aI., 1970) and in both tribes of the Sciomyzinae, and in species having terrestrial as well as those having aquatic larvae. It characterizes some or all of the reared species of Alri chome/ina (Foote et aI., 1960), Colobaea (Knutson and Bratt, unpublished), Pherhellia (Bratt et aI., 1969), Pteromicra (Rozkosny and Knutson, 1970), and Sciomy za (Foote, 1959) in the Sciomyzini ; and at least some species of Antichaeta (Robinson and Foote, 1978), Diclya (Valley and Berg, 1977), Renocera (Foote, 1976), and Tetanoccra (Foote, 1961) in the Tetanocerini . The developmental stages that survive the winter in species of Group I range from very young pupae through older pupae to pharate adults. Their physiological conditions evidently vary from true diapause to mere quiescence imposed by low temperatures. Species of Tetan ocera illustrate the overwintering conditions typ ical of most species in this group. All 12 puparia of T. fcrruginea Fallen (Holarctic) collected at Ithaca, New York , on 12 December and opened immediately for examination contained very young pupae (Fig. I) . Little pupal development occurred during the winter, and

18


A

B

c

o

ig . 1-3. Fig. I. Overwintering pupa of Telal1oc(!/"a jerrtlKil1ea (the only stage observed). Fig. 2. Overwinteri ng pupa of Dictya sp. (the most adva nced of a ~e ries of stages). Fig. 3. Outdoor screen cage for t e ~li n g winter survival of adults. A. Removable upper section. looki ng in through open bottom. B . Lower section. lined with sheet metal. conta ining sod with vegetation. C, Assembled cage.

puparia collected there on 19 April contained similarly unpigmented , undeveloped pupae. B caus e so much postdiapause development is needed. overwintering puparia do not yield adult flies until more than a week after they are warmed to room tem peratures . Seventy-eight floating puparia of this aquatic predator col


19

lected from marshes in central New York during February, March, and early April produced adults 9-11 days after being brought into the heated laboratory . The uniformity of developmental stages of overwintering pupae suggests a pu pal diapause at a stage that is fixed genetically. This hypothesis is supported by failure of late summer and fall puparia to produce adults when held at room temperatures . Larvae of T. ferruginea and T. rotundieomis Loew (a parasitoid of terrestrial snails) collected near Anchorage, Alaska (Jat. 61 . ION), on 14 August pupariated on 3-10 September, but there was no emergence at laboratory tem peratures during the first four to five weeks after pupariation. Adults of both species emerged after these puparia were refrigerated for seven weeks at 3°C (Berg, 1953). At lower latitudes, an autumn generation usually is produced before pupal diapause intervenes. Active larvae of T. ferruginea are collected into late October in central New York; they have been taken as late as 29 November at Kent, Ohio (Jat. 41.ION). Trelka and Foote (1970) found that pupal diapause of the Nearctic slug-kjlLing species Tetanoeera plebeia Loew, T. valida Loew, and T. clara Loew is facul tative; a few pupae in every generation produced adults in less than three weeks. They attributed an increased frequency of diapause in the later generations pri marily to shortened day lengths . When T. plebeia was reared under constant photoperiods of LD 14: 10, the percentage of diapausing pupae varied from 35% in the first generation to about 46% in the third. However, the proportion of diapausing pupae increased greatly when larvae of any generation were reared under photoperiods of LD 10: 14. Being multivoltine species that overwinter in puparia, species of Dietya are placed in Group I, although the diagram (Fig. 5) does not fully represent their seasonal occurrence. All species commonly found in puparia during the winter in central New York (D . atlantica Steyskal, D. expansa Steyskal. D. pictipes (Loew), and D . texcl1sis Curran) can also be collected there as adults during winter thaws. Insects tend to concentrate their cold-hardiness into a single stage , and winter survival of both pupae and adults seemed unlikely. Furthermore, emergence at laboratory temperatures less than 24 hours after puparia were col lected suggested that it perhaps can also be induced by the slight warming out of-doors on mild, sunny winter days. To find out, some Dietya pupae collected in Berks County, Pennsylvania, (lat. 40.20N) on I January were placed in a growth chamber set to provide the light and temperature conditions that might occur during a winter thaw in the Northeastern States (LD 9.5: 14 .5, at 6-8°C) . Under those conditions, emergence began five days later and continued for 12 days . Collection of 26 floating puparia of these aquatic predators near Han'isburg, Pennsylvania, (Jat. 40.17N) on 21 December, and of 84 in Berks County on 1 January , enabled us to remove the cephalic caps of many puparia and to observe the condition of overwintering Dictya pupae before any appreciable exposure to laboratory warmth. Although more than half had been destroyed by parasitoid Hymenoptera, there were enough uninfested individuals to show remarkable dif ferences in stages of pupal development. Firm, fully pigmented, bristle-covered individuals partially detached from their pupal integument could be called either very late pupae or pharate adults (Fig. 2). At the opposite extreme, there were completely unpigmented, bristle-less, flaccid individuals barely recognizable as

20


very young pupae by the form of the head and the compound eyes (cf. Fig. I). Pupae with various degrees of tissue organization, pigmentation, and bristle de velopment made up a continuum between the two extremes. Unfortunately, all of the most advanced individuals were preserved immediately. A few of the least advanced, placed in a growth chamber set at 21°C and LD 14: 10, emerged as adult flies 9-11 days later. Thus, pupal development in overwintering Dictya is so variable that some held at 6-8°C emerge before others maintained at 21°C. Differences in developmental stages cannot be attributed to specific differences among the species of Diclya included. All species commonly found in puparia during winter could not also occur as adults during winter thaws unless some individuals of all four species survived the winter as very advanced pupae. Indications that winter-collected adults of Diclya may have emerged just a few hours before they were captured suggested that they might not be cold-hardy. To determine cold-hardiness, 13 adults of Diclya spp. collected on 30 January during a spell of mild weather were released in a screen cage (Fig. 3) that afternoon, together with adults of Sepedon juscipennis Loew, Elgiva solicila (Harris), and Pherbellia schoenherri macuiala Cresson that were captured with them 2 • This cage was set outside and left until 4 April (64 days) . Active adults of the three other species appeared in the cage a few hours after it was brought into the laboratory, but no Diclya were seen. Two replications of this experiment, in which six and 26 adults of Diclya spp. were exposed to winter temperatures for only 21 and 23 days, gave similar results. All Dictya died, but some individuals of each of the other species survived. The Diclya recovered by examining the soil and plant material in the cages were D. allantica, D. expansa, D. pictipes, and D. texensis . Less numerous seasonal data on Alrichomelina pubera (Loew) indicate that its phenological pattern is very similar to that of Dictya spp. Foote et al. (1960) obtained adults only four to five days after puparia were brought into the heated laboratory on 26 December, 29 March, and 3 April. More recently, a puparium collected near Ithaca on 5 November yielded an adult only three days later, and two adults were collected during mild spells in January. The female taken with a sweep net on 19 January lived in the laboratory until 15 March and laid several eggs, but none hatched. A year later, another female was collected in a nearby marsh on 30 January. After exposure in an outdoor cage from 30 January to 22 February she did not appear in the cage when it was brought in, nor was she found when cage materials were examined. GROUP

2:

MULTIVOLTINE SPECIES THAT OVERWINTER AS ADULTS

Species in this group breed continuously during spring and summer and produce a series of overlapping generations; then they survive the winter as hibernating adults (Fig. 5, Group 2). Except for the terrestrial, parasitoid larvae of Ph erbellia s. maculata, the larvae of all included species are quick-killing, aquatic predators. The overwintering stage in Group 2 was first suggested by the collection of 2 According to R. Rozkosny (19SI, En\. Scand. 12: 177-ISO), Elgiva solicita (Harris , 17S0) is the prior name for the species identified by authors as E. sundewalli Kloett and Hin cks , 1945, or as E. mJa (Panzer, 179S); Pherbellia schoenherri (Fallen, IS26) is the proper name for P . punCiata (Fa bricius, 1794) , preoccupied.


Table I.

2I

Adult Sciomyzidae taken in three winter collection s. S ppcdnn fU.H" il'cI/Jlis

E/~ il'(l

Vi rly o

Ph Nhcllia

Collection Dates

.w l/e/ta

spp .

s. maeullil a

1S-19 Jan . 1973 3 March 1973 30 Jan . 1974

37 30 9

9 6 39

8 4 3

4 4 4

2

Totals

76

54

l5

12

3

S('pcdon o rrmpt'S

Atrirhnml'lill a pubera

Totals

59 45 58

I

2

162

adults of Elgiva solicitll, S ep edon fuscipennis, and S. armipes Loew very early in spring and even in late winter (Berg, 1953; Neff and Berg , 1966). Furthermore, winter-collected puparia of these species have never produced an adult fly in our laboratory , although they have yielded many parasitoid Ichneumonidae. Knutson and Berg (1964) reported no emergence from 85 puparia of Elgiva solicita (as Elgiva rufa (Panzer)) collected in a partly frozen pond near Ithaca on 26--27 March . Although the pupae within appeared in excellent condition (some with well developed bristles and pigmentation), all probably were frozen . Laboratory reared larvae and pupae of E . solicita subjected to a constant temperature of 5°e either died or developed through to the adult stage. No diapause of immature stages was observed . After the larvae were reared at 20-25°e, 275 puparia of Sepedon fuscipennis were placed in a growth chamber that maintained a constant temperature of 3°e. Even when these puparia were warmed again to laboratory temperatures, there was no successful emergence from any of the 209 puparia held at 3°e for more than 26 days, and only eight of the 66 puparia refrigerated for 20-25 days produced normal adults. No real effort was made to collect adult Sciomyzidae in winter until this study was undertaken. Then collecting with sweep nets in a marsh near Ithaca resulted in the capture of 59 Sciomyzidae on 18-19 January 1973, 45 on 3 March 1973, and 58 on 30 January 1974 (Table 1). The collection of 18-19 January was made only ten days after the temperature dropped to -20 e; the daily maxima had remained below oDe for eight consecutive days. The collection of 3 March fol lowed the coldest month in 1973, when lows of - 23, - 26, and - 27°e were recorded at the official weather station in Ithaca (Fig . 4). As stated under Dictya above, winter-collected imagoes of E. solicita , S. fus cipennis. and P. s. maculata survived winter exposures in screen-sided cages for 21,23, and 64 days. Temperatures during the 21-day exposure fluctuated around the freezing point and included lows of -19°e (Fig. 4)3. During the 23-day and 64-day exposures the following winter , the temperature dropped to - noe , and daily maxima remained below the freezing point for ten consecutive days. To determine whether any would survive through a whole winter, a cage containing D

" As might have been expected. all flie s included in the ~econd exposure shown in F ig. 4 died. Studies with various insects have demons trate d a rapid loss of glycerol and of cold-hardiness after warming . Bau st and Morris sey ( 1975) stated , " Even the most cold tolerant species resident in the Arctic are irreversibly warm al:c limated within hours at above freezing exposures." Lee ( 1980) re port ed such result s in a species of Coccinellidae and cited sev eral reports of similar observations on various insccts.


22

OF

DAILY TEMPERATURE RANGES THROUGHOUT COLDEST WINTER WEATHER IN 1973

56 52 48 44 40

36 32 28 24 20 '6 12

0

-" ·8 ·12 ·16

JANUARY

FEBRUARY

MARCH

Fig. 4. Daily temperature maxima and minima (upper and lower tracings) during coldest winter weather in 1973 at Ithaca, New York .

27 S . juscipennis, II S. armip es Loew, and 8 E. solicita was set out on 26 October. When this cage was returned to the laboratory on 21 April, four active adults of S.juscipennis and one S. armipes appeared on the screen sides. During all winter exposures , th e cages stood on the ground in a cold upland valley (elevation 326 m) , completely shaded from the winter sun. As final evidence of survival of adults through the winter, mark-release-recap ture studies of S . juscipennis resulted in the recovery on 29 May of a female that was marked and released during the previous August (Arnold, 1978). To determine repr duc tive capacity of flies after winter exposures, females ere held in breeding jars, with and without males, and males were given access LO laboratory-reared virgin females , at laborator y temperatures. Pairs of E. so licita . S _juscipennis , a nd P . s . maculata collected on 18-19 January and on 3 March all produced viable eggs. Previously unmated females of S . juscipennis and E . .'iOlicita laid viable eggs after mating with males collected on 3 March . Pair of E. solicita and S. juscipennis tha t urvived the 64-day exposure during February. Ma r h, and early April al 0 produced viable eggs, as did one of the urviving female of P. s. maculalll in that cage. That female , which had no c ntact with any mal of her species after 30 January , evidently carried viable sperm in her spermathecae throughout the 64-day exposure. Ho wever, wi nter survival of males seems necessary in order to carry viable sperm of . juscipennis and S. armipes through the winter. The three females of S. jllscip el/lzis retrieved from the cage that stood outside from 26 October to 21 April began to oviposit 5-6 days after they were brought into the laboratory . However, the only eggs that hatched were the ones laid by the female paired with

ADVANCE S IN DI PTE RA

23

SYSTEMATICS

the male . He was transferred into the breeding jar of a different female on 3 May and given access to the third female on 17 May. Almost all eggs laid afte r intro duction of the male proved viable. A repetition of this experiment using females and males of S . juscip enn is collected in Berks County, Pennsylvania , on 28 Feb ru ary gave simi lar results. F inall y, a female of S . armipes collected at pond s near Ithaca on 19 F ebruary and kept isolated fro m the male collected with her laid many eggs, bu t none hatched until five days after the pair was united on 2 April. In all of these observations on overwintered S epedon spp., female that had produced only sterile eggs promptly bega n to lay fertile eggs when males were paired with them. Ec kblad and Berg (1972) and Arnold (1978) studied the dynamics of natural population' of S. juscipennis near Ithaca and agreed that this species breeds freely and develops directly throughout the warm season, producing overlapping , nonsynchro nous generations . Arnold added that oviposi tion ceases in September every year, wh en photoperiod is shortening a t the maximum rate. In th is stud y, reproductive diapause was apparent in the S . juscipennis, S. armip s, and E. solicita c Uec ted in Sept mber and held in breeding jars at roo m temperatw'es for a mon th or more before they were set out to test winter survival on 26 October. Although all fl ies fed and remained active, no mating was observed, and no eggs were laid . Only fi ve of the 58 S . juscipennis and two of the 24 S . arm ip es died duri ng that mon th . In sharp co ntrast , th e 17 Tela nocera spp. similarl y maintained at that time (mostiy T. jerruginea and T. loewi Steys kal) mated r peatedI y and laid many eggs; then all died before 3 October. After intensive la boratory studies of S. ji/seipel/nis under controlled conditio ns, Barne (1976) concluded that both temperature and photoperiod influence dia pause induction in the sensitive and r~sp nsive adult stage. His figure s of two dissected fl ies of each sex, showing distinct contrasts between diapallsing and nondiapau sing individuals, demon strate that this diapause is characterized by cessation of ovarian development, cessation of spermatogenesis, and hypert rophy of fa t bodi es. Neff and Berg (1966) reported indications that Sepedofl neili Steyskal (Nearc tic), S. borealis Stey kal (Nearctic) , and S . sphegea (Fabricius) (Pa learctic) also conform to th phenological pattern of Group 2. AlI adults of S. sphegea collected in Mgh nistan on I and 3 Oc tob r, and the eight females that emerged from puparia collected in Afghanistan, were in a reproductive diapause th al ntinued (at laboratory temperatures) un ti l late December. Laboratory-reared adu lts f S. neW emerged during 20-25 Augu st, but they neither mated nor laid egg until the foll owing spli ng , after remai ning active all winter in the laboratory. Fi nally, the collection of adul ts of Psacadina verbekei Rosko ~ny in January and March , and rearing experience with P . zernyi (Mayer) , suggest that species f this Palearctic genus also may conform to thi 'easonal pattern. Two fe males of P. zernyi that e merged on 25 and 27 June after a laboratory generation had been reared in Den mark remai ned in reproductive diapause until th e follo wing spring. Then they laid viable eggs duri ng April and May (Knutson et aI. , 1975). G ROUP

3:

U NIVOLTI

E SPECIES THAT O VER W I TE R WITHIN

EGG

M EMBRANES

Repeated observations that eggs of Te tanocera loe wi fail to hatch even when larvae are full y forme d withi n them suggested that this species may normally survive the winter within egg membranes . Further seasonal studies have co n

24

MEMOIRS OF THE ENTOMOLOGICAL SOCIET Y OF WASHINGT ON

vinced us that a larval diapause intervenes in this and at least four other species having aquatic larvae, usually arresting development just before hatching (rarely just after) and prolonging the first larval stadium to a duration of about seven months. The combination of this delay with a reproductive diapause of adults that arrests the life cycle of most species again in late spring and early summer results in univoltinism (Fig. 5, Group 3). Several eggs of T. loewi laid in late summer or early fall were held at laboratory temperatures for 12-31 days without any hatching. When they were then dis sected, living larvae were extracted from all six of the eggs laid on 29 August and from most of the 75 eggs laid in September. However , the sluggish larvae did not feed on small snails , and all died within ten days. A very few eggs hatched normally in the fall, but those larvae behaved similarly and suffered the same fate . A diapause of first-ins tar larvae was suspected , and some eggs laid on 20 Sep tember were refrigerated at 4-6°C to see if diapause development could be com pleted at that temperature. A few larvae hatched in the refrigerator during Jan uary, but most of them died without feeding. Other living larvae were removed from eggs in January . A few of the naturally hatched and manually extracted larvae became active, killed small snails, and began to feed . Although one indi vidual developed through both larval molts , all larvae died without forming pu paria. In this and similar experiments , the percentage of hatching was considerably higher if eggs were refrigerated. However, eclosion occurred sporadically, over a period of two or three winter months. Warming the eggs to room temperature in January did not increase the hatching rate, nor did submerging refrigerated eggs in either cold or warm water. These experiments suggest that a few eggs normally hatch at the low temperatures prevailing in nature in Ja nuary and Feb ruary, then man y more in March (Foote, 1961) . A few first-instar larvae of this Nearctic species were found in vernal ponds and marshes in central New York as early as late February and March. They were numerous on 9 and 17 April, only a few days after the melting of pond ice. Older la rvae were collected in late April and early May . All larvae collected at that season killed aquatic snails quickly and developed directly. Ten of the pu paria formed by larvae collected on 17 April produced adult flies in late May and early June, after pupal periods of 15 to 19 days. Adults were collected commonly from June through September in central New York. Laboratory-reared females and those taken in nature in June and july fed and remained active, but they were clearly in aestival diapause. No mating was observed and no eggs were laid in that season . In contrast , flies collected during August and September mated repeatedly and laid many eggs. Delayed mating a nd oviposition of adults, followed in almost all individuals by a long diapause of unhatched larvae , indicate strongly that three other species of Tetan ocera also conform to the phenological pattern of Group 3. Adults of T. latifibula Frey (Holarctic) , T. soror Melander (Nearctic), and T. punctifrons Ron dani (Palearctic) were collected in June , July , and August, principally or exclu sively in vernal marshes. However, eggs were obtained only in late July and August. Almost all eggs developed so that fully formed larvae were visible through the egg membranes in a few days, but very few hatched when held


25

continuously at laboratory temperatures for 12 to 25 days. Living larvae were removed from eggs of all three species, but all were very sluggish, none fed, and all died in a few days. Refrigeration of these eggs bas demonstrated that diapausing larvae can survive prolonged exposure to cold and that sporadic hatching occurs at temperatures of 5-8°e. Some eggs of T. latifibula were refrigerated on 11 September and left for five months. An egg was removed and dissected on 13 February, and the larva killed and consumed snails in the refrigerator and in the heated laboratory. This larva continued to feed and develop, molting on 24 February and I March, form ing a puparium on 20 March, and producing the only adult obtained from these eggs on 29 March, 44 days after it was removed from its egg. When the remaining 25 eggs were removed on 24 February, 14 had hatched in the refrigerator, but all larvae evidently had died without feeding. Living larvae were removed from two of the 11 unhatched eggs on 24 February, and five of the others hatched on 24 February-2 March. All naturally hatched and manually extracted larvae killed small snails and fed, but all died before their second larval molt (Foote, 1961) . Another N earctic inhabitant of vernal marshes, H edria mixta Steyskal, is placed in Group 3 because it is univoltine and it overwinters within egg mem branes. It lacks an aestival diapause of adults, but its long diapause as unhatched larvae compensates for this by delaying larval development, pupation, and emer gence every spring. The earliest collection record for adults in nature (14 July) is a month to six weeks later than earliest collection dates for other species in Group 3. Although they may start to lay eggs only a week later, their oviposition season then precedes that of other species in Group 3 by only a week or two. Foote (1971) reported that eggs of H . mixta seldom hatched when held at room temperatures for 20 to 135 days. When larvae were excised from the eggs, they were "very sluggish, did not feed, and all died within a few days." There was much better hatching of eggs held at 5-7°C; nine hatched after 81-213 days in the refrigerator. Significantly , the newly hatched larvae became active, attacked snails , and fed when they were warmed to 20°e. Eggs of the central New York population of Tetanocera montana Day (Nearc tic) appear to undergo a diapause before hatching. Only three of 16 eggs held for more than a month at room temperatures in early summer hatched, and more than 22 days always elapsed before hatching occurred. Dissection of unhatched eggs disclosed that six contained living larvae, and all larvae proved listless, did not feed, and died within a few days . However, eggs laid in July by females collected in Bonner County, Idaho, hatched in three to five days, and a generation (clearly the second of that season) was then reared through all immature stages. The Idaho population was breeding in a permanent body of water, where a second generation could develop because aquatic snails persisted throughout the summer. This breeding site thus differed importantly from that of the New York population of T. montana, and from most other breeding sites in which species of Group 3 have been found (Foote, 1961) . GROUP

4:

UNIVOLTINE SPECIES THAT OVERWINTER AS PARTLY GROWN LARVAE

We have collected larvae of Tetanocera vicina Macquart (Nearctic) during every month from November through early May, but not in late spring or summer.

26

MEMOIRS OF TH E E NTOMOLOGICAL SOCIETY OF WASHINGTON

SEPT

OCT

NOV.

DEC.

GROUP 1. M ultl voltin e: ov erwi nt e r as pu pae.

GROUP 2: Mu ltivolt in e: overw inter as adu lt s.

G ROUP 3: Univoill n e: Qve r....Jin l e r wit h' n egg memb rane s.

GROUP 4: Un lvo!Une: ove rwin ter as par tly grown la rvae.

GRO UP 5: Univoltine: overw i nter

as pupae.

W~ t e r

an d Mollusca in verna l marshes. Wate r and Mol lusca aul u m nal marshes,

~n

Fig. 5. Seasonal occurrence in the North Temperate Zone of stages in the life cycles of five phenologica l groups of Sciomyzidae, and of water, s nails, and fingernail clams in temporary ponds and marshes .

In Typha marshes, they occur in open water beneath the ice and within the sheathing bases of Typha leaves. They can be found more easily in small ice-free areas surrounding springs and outfalls of heated waste water . The individuals that overwinter as larvae persist throughout the summer as adults. Like those in Group 3, most species in Group 4 are univoltine because they combine a very long larval stage with an aestival diapause of adults. The major difference from Group 3 is that eggs in Group 4 hatch promptly, and the young larvae begin to feed and grow before the onset of winter (Fig. 5) . To observe the effects of natural conditions, 30 larvae of T. vicino collected near Ithaca in February were refrigerated at 2-4°C and LD 9.5:14.5 on 3 March . They were isolated in wet gravel in small, plastic boxes , and only one snail was supplied each week for each larva. With only one exception, the snails were always dead and largely consumed when checked a week later, and larvae were often found feeding within the shells. There was no larval mortality under those conditions during the following eight weeks. Although there also was no pupar iation, several second-instar larvae molted to the third stadium. Therefore, these

ADVAN C ES IN DIPTERAN SYSTEMATICS

27

larvae were not in a developmental diapause like that attributed by Bradshaw (1972) to the overwintering larvae of Chaoborus americanllS Johannsen . Seventeen larvae were moved on 29 April to a laboratory table , where tem peratures varied from 20 to 30°C , and daily photoperiods equalled or exceeded those in nature. All 17 had formed puparia by 13 May, and emergence from these puparia began on 22 May. Although the 13 larvae that remained under low tem peratures and short days continued to feed regularly, they formed only two pu paria before 7 June, when a malfunction of the refrigerator caused all except one larva to freeze . That larva was removed to the laboratory table on 26 July, where it pupariated on 5 August, and emerged as a normal female on 19 August. Larvae in nature pupate in late April and May, and adults emerge 14 to 20 days later. Adults were collected commonly throughout the summer months in New York, Idaho, and Ohio, the earliest and latest records of the season being 31 May and 29 September in central New York, and 9 June and 1 October in Idaho. Whether reared or wild-caught , the adults observed in June and July apparently mated seldom if at all; almost all of their eggs were retained until late summer or early fall. Adults taken in August and September were sexually active . Within a day after being placed in breeding jars, they began to lay eggs that hatched in 5 14 days. Larvae develop quite rapidly during late summer and early faLl and molt at least once. Then they enter a period of relative inactivity, probably initiated by short photoperiods or low temperatures, in which they feed little even if snails are readily available. Both larvae collected on 6 November near Ithaca, and all five larvae collected on 9 November near Kent, Ohio , remained sluggish, fed spar ingly, and all died within a month. Most larvae collected in the winter killed snails and fed readily. Most were in the third (last) larval stadium, but second-ins tar larvae also were found occasionally from November through March. The developmental delays that control and regulate the univoltinism of T. vicina are not so firmly fixed genetically that they cannot be overridden by very abnor mal environmental conditions. Although most of the larvae warmed to laboratory temperatures in January, February , and March died either as larvae or after forming puparia, a few developed quickly through the pupal stage and emerged as normal adults. Furthermore, larval diapause was once suspended completely. Larvae passed through aJl three stadia in 18-23 days, and an imago (only one from a group of 15 larvae) emerged on 16 November (Foote , 1961). T he phenological plasticity suggested by these rearings recalls similar obser vations of several authors (cf. Bradshaw, 1973) and suggests that T. vicina may produce a second generation where growing seasons are longer. Although we know of no collection of any immature stage in nature between May and Septem ber , a female that emerged in our laboratory in early May began to oviposit in late June . The suggestion of a second generation is based on evidence that the reproductive diapause of adults can be greatly shortened, evidence that the larval diapause can be completely suspended, and the fact that this species ranges southward into North Carolina, Tennessee, and Arizona. Six other species having aquatic larvae have typical Group 4 phenology, Group 4 phenology with minor variations, or facultative Group 4 or Group 3 phenology , depending on local conditions. Collection records for Telan oc era pLumosa Loew

28


and T. abtusi/tbuLa Melander (both Nearctic) indicate that no larvae have been found during late spring and summer; no adults, during fall, winter, or early spring. Larvae collected in the spring were far more active than those taken in the fall. They killed snails readily and fed well, then formed puparia in late April and emerged as adults 16-19 days later. Reared adults and those collected in nature from May to early July were never observed to copulate; those taken later in the summer mated repeatedly (Foote , 1961). One of the most common European species of Sciomyzidae, Pherbina caryLeti (Scopoli), follows the pattern of Group 4 except for adult sexual activity in spring and early summer. Despite the early mating, however, oviposition of most indi viduals is even later in the season than in other species in Group 4. Larvae that we collected in Italy on 7 April formed puparia on 11 and 12 April, and two females emerged on 25 April. These females did not lay eggs until 27 and 30 September, and some flies continued to oviposit until 10 November. Eggs hatched promptly after incubation periods of 9-13 days at 18-22°C, and newly hatched larvae readily attacked and killed snails. However, all larvae lived exceptionally long in both second and third stadia. Larvae refrigerated at 5°C continued to kill and eat snails during the two months they were held at that temperature, and some second-ins tar larvae molted to the third stadium while in the refrigerator. Larvae have been collected in nature only during late September, March, April , and early May; puparia, only during April and early May (Knutson et aI., 1975). A southern hemisphere species known only from the South Island of New Zealand, Eulimnia philpatti Tonnoir and Malloch, illustrates a further modifica tion of the typical pattern of Group 4. Adults mate frequently in spring and early summer, oviposit only six days after eclosion, and the average incubation time is only 7-11 days . Larvae thus are produced long before the adults die off in late summer. As in Hedria mixta in Group 3, however, the larval stage of this species is so prolonged that a single life cycle still requires a whole year. Even when reared at a constant temperature of 15°C and with adequate food always provided, development through the three larval stadia required 5YZ-8YZ months, and the only adult that emerged from a reared puparium appeared 40 days after pupar iation (Barnes, 1980). Larval and pupal stages together could thus require as much as ten months, even under laboratory conditions. Development in nature during winter on the South Island must take considerably longer. In the field, adults have been collected from mid spring to late summer, and Barnes (1980) coLlected second-instar larvae in mid summer, third-instar larvae in winter and early spring , and viable pupae in mid to late spring. Laboratory reared and field-collected larvae attacked their molluscan prey readily in all sea sons observed. Although there was no evident larval diapause, the third larval stadium was more prolonged than any other life stage . Two European species, Knutsonia aLbiseta (Scopoli) and K. Lineata (Fallen), apparently can follow the phenological pattern of either Group 3 or Group 4 (Fig. 5), depending on the availability of water and their molluscan food during the winter. Very few of their eggs hatch in the fall unless they are immersed in water. A larva of K. aLbiseta was found in a marsh in Corfu, Greece , during April, and more than 400 puparia were collected in temporary ponds in Italy in late March, April, and early May. Many of those collected on 30 March were so freshly

ADVANCES IN DIPTERAN SYSTEMATI CS

29

formed that pupation had not occurred within them. The 356 adults that emerged from these puparia in April and early May, and those collected in Greece, En gland , and Belgium in spring and early summer, were inactive sexually. They laid very few eggs, and none hatched. In contrast, adults collected during late summer in Denmark mated frequently , and females laid viable eggs from mid August to mid November. Although eggs appeared well embryonated in only a few days , hatching was delayed until 33 to 76 days after oviposition. Relatively few un wetted eggs hatched even in that length of time. However, about thirty percent of the eggs completely submerged in water hatched within 24 hours after immer sion, some hatching only 14 days after oviposition (Knutson and Berg, 1967) . Knutsonia lineata is far less common than K. albiseta; a puparium taken in a marsh in Denmark on 22 June appears to be the only immature stage ever found in nature. However, the evidence that submersion stimulates hatching is even stronger than for K. albiseta . As in most species in Groups 3 and 4, copulation and oviposition were delayed until late summer and fall. Embryonation was com pleted within four to seven days at laboratory temperatures, but the eggs did not hatch in this situation . Exposure to temperatures of 5°, 0°, and -6°C for periods up to 86 days and subsequent warming to laboratory temperatures did not stim ulate hatching. However , almost 100% hatching was obtained when embryonated eggs were submerged completely in water one to several weeks after they were laid. Most eggs hatched within two to ten days after being submerged (Knutson and Berg, 1967). GROUP

5:

UNIVOLTINE SPECIES THAT OVERWINTER AS PUPAE

U nivoltinism has evolved in phylogenetically and behaviorally diverse genera that survive the winter as pupae. They belong to both Tetanocerini and Scio myzini, live in completely terrestrial as well as seasonally aquatic breeding sites, and feed on dissimilar molluscan foods. The species that breed in vernal ponds and marshes have relatively late larval seasons, with eggs hatching after larvae in Group 4 and most larvae in Group 3 have pupated (Fig . 5, Group 5). Larvae of all species can find their food more readily when ponds are drying, and some species cannot even oviposit until the standing water in their breeding sites has almost disappeared. Females of all reared species of Antichaeta lay their eggs only on the snail egg masses in which their larvae feed a nd develop . Species dependent on eggs of aquatic snails therefore do not oviposit until middle or late May, when receding waters of vernal wetlands begin to expose those snail egg masses. Larvae of Antichaeta melanosoma Melander (Nearctic) form puparia in late June, July, and August, when seasonally wet habitats are drying rapidly. Very few puparia produce adults unless they are held at low temperatures for a few months, then warmed again. Knutson and Abercrombie (1977) got no emergence from several puparia formed in June and July and held for three months at room temperature , although all puparia "appeared to contain living pupae" when opened for examination. Foote (reported by Knutson and Abercrombie) got prompt emergence from only one of eight puparia formed in late August. Five of the other seven puparia yielded adults after they were held at room temperature for 52-62 days , then refrigerated for 117 days, then warmed again . Four Palearctic species of Antichaeta also probably belong, or portions of their

30


populations certainly belong, to Group 5. All occur in temporary ponds or marsh es, all overwinter as pupae, and both of the reared species have a facultative diapause that makes a portion of their populations univoltine. Knutson (1966) collected adults, eggs, and larvae of A. analis (Meigen), all four life stages of A. brevipelll1is (Zetterstedt), and adults of A. atriseta (Loew) and A. obliviosa En derlein in vernal wetlands in Denmark. He found the larvae of A. analis only in exposed egg masses of Lymnaea truncatula (Muller) and concluded that these egg masses are the only oviposition sites used by adult flies. A facultative pupal diapause was indicated by reasonably prompt emergence of only four adults from 12 puparia formed in July, and by emergence from one of the other puparia after it had been held for 323 days at laboratory temperatures. Some puparia of A. brevipennis yielded adults 16 to 20 days after pupariation; other puparia formed by the same group of larvae still contained unpigmented pupae after nine months at laboratory temperatures. Two puparia formed in mid-July were refrigerated at 5°C on 5 December, then warmed to room temperature on 12 June. They produced adults on 25 and 29 June, 346 and 348 days after puparium formation. The species of Renocera that live in vernal ponds have larval seasons similarly delayed, but for a different reason. Larvae that prey on fingernail clams must go down to the bottom to forage for food. This presents no problem while larvae are small enough to obtain their oxygen by cutaneous respiration. Newly hatched larvae descend to the bottom, find and invade a fingernail clam, and often remain in its shell throughout their first stadium (7-10 days). However, larger larvae apparently must keep their posterior spiracles exposed at the surface. Since they do not descend, their feeding is restricted in early spring to shallow pond margins. When ponds are drying, however, microhabitats in which the water is no deeper than the lengths of their bodies are scattered throughout the pond area. Foote (1976) found floating puparia of Renocera amanda Cresson and R. lon gipes (Loew) in vernal ponds and woodland seepage areas during the spring, and collected adults in these habitats in May and June. They mated and laid eggs, from which larvae were reared in June and July. The only larva that survived to pupariation died shortly thereafter, so there is no direct evidence that the July August pupae go into a prolonged diapause. However, the observed flight period of these species in nature terminates so early that a second generation is impos sible. The latest capture record for R. longipes in northeastern Ohio is 28 June; the latest for R. amanda, early July. Instead of becoming more abundant at the season when individuals observed as larvae in June and July might be expected to emerge as adults, adults of both species completely disappear at that time. If adults did emerge and oviposit in late July, August, and September, their larvae could only desiccate and starve in the dust-dry pond basins. Many snail shells containing puparia of Pherbellia simi/is (Cresson) (Nearctic) were found floating in temporary, woodland ponds at Kent, Ohio, during winter thaws and in early spring. A few days after they were brought into the laboratory, adults emerged, mated, and laid eggs. The larvae that resulted were reared to pupation, but only 16 flies emerged from the 117 puparia in the first 60 days they were held at room temperature. After eight of the remaining puparia were refrig erated at 5°C for the next 254 days, then returned to room temperature, all yielded adult flies. In three other experimental treatments of puparia, adults emerged more than a year after pupariation, sometimes only after a second period of

ADY ANCES IN DIPTERAN SYSTEMATICS

31

refrigeration. These data indicate that about 85% of the individuals reared from the eggs of overwintered flies go into a pupal diapause that is broken only by long, and in some cases repeated, exposure to low temperatures (Bratt et al., 1969). A pupal diapause also results in univoltinism in six species of Sciomyzini whose pheno'logy has no direct relationship to the seasonal filling and drying of tempo rary aquatic habitats . Pherbellia albovaria (Coquillet) (Nearctic), P. albocostata (Fallen) (Holarctic), P. annulipes (Zetterstedt) (Palearctic), P. dubia (Fallen) (Palearctic), Tetanura pallidiventris (Fallen) (Palearctic), and Oidematops jer ruginells Cresson (Nearctic) all attack land snails, and all breed in strictly ter restrial situations. No laboratory-reared puparium of any of these species has yielded an adult in less than 50 days, even in heated laboratories. In P. albocos tata, the only species in which we have seen pupal development proceed that rapidly, prolongation of the third larval stadium results in observed developmental periods totalling 137-211 days. Since even the shortest of these exceeds the long est known flight period (19 May to 20 September, in Great Britain), a second generation seems impossible. The shortest observed pupal period for the other five species varies from 120 to more than 200 days. Oldham (1912) obtained adults of P. dubia in April from puparia in snail shells collected in February, but it must be presumed that these puparia were formed the prev,i ous autumn if not the previous summer. We have not gotten an adult from a laboratory-reared puparium of P. duhia in less than four months. All laboratory-reared puparia of P. a/bovaria required at least 200 days before emergence, and the known flight period of this species spans only 50 days (Bratt et aI., 1969). Knutson (1970) obtained an adult of Tetanura pallidi ventris on 10 June from a puparium in a snail shell collected on 15 December. Foote (1977) got no emergence from 19 laboratory-reared puparia of Oidema tops jerruginf!us that were exposed to laboratory temperatures for 26--106 days, then refrigerated at 5-7°C for 90-150 days. However, the pupae in all puparia still appeared viable and healthy . An observation on field-collected puparia led Foote to suggest that a few pupae in each generation may require at least two lengthy exposures to low temperatures before they will break diapause. Although two of the eight puparia collected on 23 March had not produced adults by 8 September, both still contained apparently viable pupae. DISCUSSION

To seek assurance before writing this paper that it would be appropriate for this Festschrift , I (COB) visited the USDA and Smithsonian entomologists in April 1981. I discussed the paper with both editors, then (without mentioning where it would be submitted) with Curt Sabrosky. I was delighted to find that he is quite interested in phenology. He matched our findings with unpublished ob servations of his own on Protocalliphora (Diptera: Calliphoridae). Just as Scio myzidae that breed in temporary ponds are univoltine, so also are species of Protocalliphora that parasitize birds that produce only one brood of young per year. Perhaps his enthusiastic response tempted me to talk too long about prob able evolutionary histories. That familiar twinkle in his eye warned me of an imminent Sabroskyan wisecrack, but it was already too late. Something I had said evidently had given him all the ammunition he needed. He hesitated only to

32


select wording for maximum thrust, then told me, "I can see you're getting old, Cliff. You don't want to work anymore-you just want to speculate." Knowing our honored colleague's limited appreciation for this sort of thing, we will keep this section brief. Considering its obvious advantages, the widespread occurrence of the pheno logical pattern of Group 1 throughout the Cyclorrhapha seems understandable. Multivoltinism provides high potential rates of population increase and enables insects to compensate for a cold, wet spring, for example, by reproducing later. Overwintering in the pupal stage provides the Cyclorrhapha with excellent winter protection inside their tough, semi-rigid, and drought-resistant puparia from me chanical injury and dessication. In this stage only, individuals have remained in diapause when rewarmed after exposure to low temperatures, then emerged as normal adults more than a year after pupariation, following a second period of refrigeration (cf. Pherbellia similis and Oidematops ferrugineus). If some indi viduals in natural populations thus continue in prolonged pupal diapause through out a growing season, then emerge as adults in the second or even the third season after pupariation, the capacity to do this may be of paramount importance in "rescuing" a species after a catastrophic season has eliminated all of its active individuals locally. Since the pattern that combines multivoltinism with overwin tering within puparia has so many advantages for the Cyclorrhapha, why have four alternative patterns evolved in the Sciomyzidae? Those patterns must pres ent compensatory advantages, perhaps peculiar to the Sciomyzidae. If not, they would not persist. While subsisting entirely on molluscan food, sciomyzid larvae also show higher rates of survival and production when such food is abundant in their habitat (Eckblad and Berg, 1972). Thus it is clearly advantageous for any species to advance its larval season so as to exploit an abundant snail population in early spring, before the eggs of other Sciomyzidae have hatched. For the Sciomyzidae, overwintering in the pupal stage has the disadvantage that postdiapause devel opment, emergence, mating, oviposition, incubation, and hatching must all occur before their larvae can utilize this food. By overwintering as adults, species in Group 2 eliminate the delays for postdiapause development and emergence. As a result, their larvae get started, on the average, about two weeks ahead of those of Group 1 (Fig. 5). They probably suffer higher winter mortality rates than species in Group I, but the trade-off of some winter survival for the earlier beginning of their larval season evidently is advantageous. By overwintering as fully formed larvae in diapause within their egg mem branes, species in Group 3 eliminate the delays for mating, oviposition, and in cubation, thus advancing their larval seasons significantly ahead of those of Group 2. They have also become univoltine, thereby restricting their demand for larval food to the season when water and snails are present in vernal ponds and marshes (Fig. 5). This enables them to segregate themselves from potential competitors spatially as well as temporally. The ephemeral aquatic habitats that they colonize are characteristically rich in molluscan fauna, but not desirable for multivoltine species whose successive generations demand larval food throughout the sum mer. The seasonal patterns of Groups 3 and 4 also provide an important advantage unrelated to larval food. Although the Sciomyzidae are so heavily attacked by parasitoid Hymenoptera that collections of puparia formed in late spring, summer,

A VANCES IN D IPTERA

SYSTEMA TICS

33

and fall often yield more Hymenoptera than flies we have never reared a para itoid wasp from any puparium of pecies in these groups. The phenological pattern of species in Group 4 involve further trade-offs in evolu ti on. Because hatching OCCUI in the falI, they cannot live in vernaJ pond . However, they do reduce compet.ition from muItivoltine specie by olonizing autumnal ponds and marshes. The larvae sacrifice wha tever winter protection the egg membranes could have given them, but they grow and develop throughou t the winter feeding (withou t competition from larvae of any other group) on the snails that remain activ in that season . Although the eggs of Group 3 start to halch before the melting of pond ice in earl y spring the well matured larvae of Group 4 are incomparably more efficient than the newly hatched larvae of Group 3 in exploiting the first nail that emerge from hibernation. The precise timing of larval production in the fi r t generation of the season thu re uJts in a c1as ic xample oftemporaJ partitioning offood re ource . Heavy demands for snail food in the spring are made sequentially by larvae of Group 4, Group 3, Group 2, and, fi nally, Group I (Fig. 5). Larvae of Group 1 have a unique advantage in the faJI that may largely compen ate for their late start in the spring. They are then relieved fro m competition from all other Sciomyzidae; larvae of aU univoltine pecies have pupariated , and reproductive diapause has terminated production of larvae by pe i s in Group 2. Group 5 includes a h lerogeneous a semblage of pecies that apparently have become univoltine in r spon e to quite different evolutionary pres ure . The univoltinism of pecies whose Larvae attack aquatic Mollusca, like that of species in Groups 3 and 4, enable them to reduce inter pecific competition by colonizing ephemeral aquatic habitats . However, the habitat of the strictly terrestrial species in Group 5 do not become uninhabitable every summer as ephemeraJ pond do. These species attack a wide variety of terrestrial nails living in and around rotting wood. The microhabitats of the snails and their predator, in forest litter and beneath rotting logs, retain moisture remarkably well even in very dry ummer . We uspect tbat the univoltini m of the e terrestrial Sciomyzidae. like that of Sabro ky' Protocalliphora, is related in tead to ' ea onally limited growth tages of their ho t or prey. Many terrestrial snail have one-year life cycles. Life cycles of the parasitoid Sciomyzidae mu t be synchronized with tho e of thei.r prey so that snail are large enough when attacked to survive until the larvae are well grown. When snails die prematurely in the laboratory, as when attacked by too many larvae, the larvae also die. An attack of even a single larva on a small, young snail wouJd probably have this resul t. However, attacks on snails that are too weU matured probably would result in more nails destroying larvae either by swallowing them (see Bratt et aI., I%9 under Pherbe llia dorsala (Zetterstedt) and P. dubia) or by encapsulating them (see Moor, 1980). The fi nel y tuned syn chronization required for the ucce s of the e in ti mate, parasitoid relationsbips is possible only with univoltine species. Development of ciomyzid larvae depends on extremely variabl conditions of weather, surface water, and availability of molluscan food . SurvivaJ and repro du ction therefore de mand sy nchron iza tion of periods of development with periods of favorable environmental conditions. The ability to delay or advance periods of development, commonl y termed ' 'phenological plasticity, " is accomplished in

34


part by appropriate responses to environmental cues. Larvae of Knutsonia in dry habitats retain the protection of their egg membranes throughout the winter; in wet habitats, the aquatic larvae hatch in the fall and utilize the winter season for larval growth and development. In many situations, however, more precise synchronization is demonstrably achieved through a two-step process. After responding to environmental cues, the resulting population is further adjusted phenologically by rigorous natural selection . Responses to environmental cues often cause species of Dictya to emerge from overwintering puparia before the arrival of permanently warm spring weather. Much mortality undoubtedly results. However, their gradual, asyn chronous emergence ensures the emergence of some individuals during the first spring weather that remains above their limit of cold tolerance. This early emer gence enables their larvae to start exploiting the spring snail populations about a week ahead of other larvae in Group 1. Species in Group 3 get a similar ad vantage from early, asynchronous eclosion of larvae overwintering within egg membranes. Here too, mortality of the earliest individuals is more than compen sated by the advantage of getting others started just as soon as local weather conditions permit. Our moral responsibility to encourage the continued productive output of a cherished colleague in dipterology compels us to append a challenge in this per sonal note to Curt Sabrosky : inasmuch as your original observations on season ality in ProtoclIlliphora would be of considerable interest to dipterists, ecologists, and students of evolu·tion ; and inasmuch as your responsibility to the scientific community includes the release of such significant findings for the edification and use of fellow scientists; and inasmuch as you have always accepted and dis charged all responsibilities with exemplary zeal; and inasmuch as papers like this don't require any work-just speculation, really; and inasmuch as all of us old men love to speculate; then why don't you sit down some Saturday afternoon and write a paper on seasonality in Protocalliphora? ACKNOWLEDGMENTS

M. J. Tauber, Cornell University, and A. G. Wheeler, Jr., Pennsylvania De partment of Agriculture, kindly reviewed this paper and made helpful suggestions for its improvement. Steven C. Horn made the illustration reproduced as Fig. 5. LITERATURE CITED

Arnold, S. L. 1978. Sciomyzidae (Diptera) population parameters estimated by the capture-recapture method. Proc. Entomol. Soc. Ont. 107(for 1976): 3-9. Barnes, J. K. '1976. Effect of temperature on development , survival, oviposition, and diapause in laboratory populations of Sepedon juscipenllis (Diptera: Sciomyzidae). Environ. Entomol. 5: 1089-1098. - - . 1980. Taxonomy of the New Zealand genus ELilimllia , and biology and immature stages of E. phi/pulli (Diptera: Sciomyzidae) . N .Z. J. Zool. 7: 91-103. - --- . 1981. Revision of the Helosciomyzidae (Diptera) . J. R. Soc. N .Z. 11(1): 45-72. Baust, J. G. and R. E. Morrissey. 1975. Supercooling phenomenon and water content independence in the overwintering beetle, Coleumegilla maC/tiata . J. Insect Physiol. 21: 1751-1754. Berg , C. O. 1953. Sciomyzid larvae (Diptera) that feed on snails. J. Parasitol. 39: 630-636. Berg, C. O. and L. Knutson. 1978. Biology and systematics of the Sciomyzidae . Annu. Rev. Entomol. 23: 239-258.


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Bradshaw . W. E. 1972. Photoperiodic control in the initiation of diapause by Chaoborus americanus (Diptera: Culicidae) . Ann. Entomol. Soc. Am. 65: 755-756. --- . 1973. Homeostasis and polymorphism in vernal development of Chaoborus americallus. Ecology 54: 1253-1259. Bratt, A. D., L. V. Knutson. B. A. Foote, and C. O. Berg. 1969. Biology of Pherbellia (Diptera: Sciomyzidae). N. Y. Agric. Exp. Stn. Ithaca Mem. 404: 1-246. Eckblad, J. W. and C. O. Berg. t972. Population dynamics of Sepedoll fuscip ennis (Diptera: Scio myzidae). Can. EntomoL 104: ·1735-1742. Foote, B. A. 1959. Biology and life history of the snail-killing flies belonging to the genus Sciomyza Fallen (Diptera: Sciomyzidae). Ann. Entomol. Soc. Am. 52: 31-43. - - - . 1961. Biology and immature stages of the snail-killing flies belonging to the genus Telanocera (Diptera: Sciomyzidae). Ph.D. T hesis, Cornell Univ. 190 pp. - - - . 1971. Biology of Hedria mixfa (Diptera: Sciomyzidae). Ann. Entomol. Soc. Am. 64: 931 941. - - - . 1976. Biology and larval feeding habits of three species of Renocera (Diptera: Sciomyzidae) that prey on fingernail clams .(Mollusca: Sphaeriidae). Ann. Entomol. Soc. Am. 69: 121-133. - - -. 1977. Biology of Uidemalops ferrugineus (Diptera: Sciomyzidae), a parasitoid enemy of the land snail Slenoirema hirsulum (Mollusca: Polygyridae). Proc . Entomol. Soc. Wash. 79: 609 619. Foote. B. A .. S . E . Neff, and C. O. Berg. 1960. Biology and immature stages of Africhom elina pl/b era (Diptera: Sciomyzidae). Ann. Entomol. Soc. Am. 53: 192-199. Griffiths, G . C. D. 1972. The Phylogenetic Classification of Diptera Cyclorrhapha with Special Ref erence to the Structure of the Male Postabdomen. Junk, The Hague. 340 pp. Knutson. L. V. 1966. Biology and immature stages of malacophagous flies: Anlicha('/(I analis, A. alrisela, A. brevipennis, and A. obliviosa (Diptera: Sciomyzidae). Trans. Am. Entomol. Soc. 92: 67-101. - - - . 1970. Biology and immature stages of Telanura pa/lidivenlris , a parasitoid of terrestria l snails (Diptera: Sciomyzidae). Entomol. Scand. I: 81-89. Knutson. L. and J. Abercrombie . 1977. Biology of AllIichaefa melanosoma (Diptera: Sciomyzidae), with notes on parasitoid Braconidae and Ichneumonidae (Hymenoptera). Proc. cntomol. Soc. Wash. 79: 111-125. Knutson , L. V. and C. O. Berg. 1964. Biology and immature stages of snail-killing flies: The genus Eigiva (Diptera: Sciomyzidae). Ann. Entomol. Soc. Am. 57: 173-192. - - - . 1967. Biology and immature stages of malacophagous Diptera of the genus Knuisonia Ver beke (Sciomyzidae). Bull. Inst. R. Sci . Nat. Belg. 43(7): 1-60. Knutson , L. V .. R. Rozkosny, and C. O. Berg. 1975. Biology and immature stages of Pherbina and Psacadinu (Diptera: Sciomyzidae). Acta Sci. Nat. Acad. Sci. Bohemoslov. Brno 9(1): 1-38. Knutson. L. V., J . W. Stephenson, and C. O. Berg. '1970. Biosystematic studies of Sallicell(/ fasciala (Meigen), a snail- killing fly (Diptera: Sciomyzidae). Trans. R. Entomol. Soc. Lond. 122(3): 81 100. Lee, R. E., Jr. 1980. Physiological adaptations of Coccinellidae to supranivean and subnivean hi bern acula. J. Insect Physiol. 26: 135-138. Moor , B. 1980. Zur Biologie der Beziehung zwischen Pherbellia punclafa (Diptera, Sciomyzidae) und ihrem Wirt Sueril/ca pUlris (Pulmonata, Sty10mmatophora). Rev. Suisse Zoo I. 87: 941 953. Neff, S . E. and C. O. Berg. 1966. Biology and immature stages of malacophagous Diptera of the genus Sepedon (Sciomyzidae). Va. Agric. Exp. Stn. Bull. 566, 113 pp. Oldham , C. 1912. Report on the land a nd freshwater Mullusca observed in Hertfordshire in 1910. Trans. Hertfordshire Nat. Hist. Soc. Field Club 14: 288. Robinson, W. H. and B. A . Foote. 1978. Biology and immature stages of Anlichaela borealis (Dip tera: Sciomyzidae), a predato r of snail eggs. Proc. Entomol. Soc. Wash. 80: 388-3%. Rozko sny , R. 1981. A new name and some new synonyms of Palaearctic Sciomyzidae (Diptera). Entomol. Scand. 12: 177-IRO. Rozkosny, R. and L. V. Knutson. 1970. Taxonomy, biology and immature stages of Palearctic Plerolllicra, snuil-kiljling Diplera (Sciomyzidae). Ann. Entomol. Soc. Am. 63: 1434-1459. S06s, A. 1958. 1st dus Insektenmalerial der Musecn fiirethologische und iikologische Untersuchungen verwandbar? Acta Entomol. Mus. Nall. Pragae 32: 101-150.

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TreLka, D. G. and B. A. Foote. 1970. Biology of slug-killing Tetanocera (Diptera: Sciomyzidae). Ann . Entomol. Soc. Am. 63: 887-895. Valley, K. and C. O. Berg. 1977. Biology, immature stages, and new species of snail-killing Diptera of the genus Dictya (Sciomyzidae). Search Agric. (Ithaca. N.Y.) 7(2): 1-44. Wiggins . G. B., R. J. Mackay, and 1. M. Smith. 1980. Evolutionary and ecological strategies of animals in annual temporary pools. Arch. Hydrobiol. Suppl'. 58: 97-206.