Colobaea bifasciella (Fallén), 1820

Bratt, Albertus D., Knutson, Lloyd V., Murphy, William L. & Daniels, Anthony A., 2020, Biology, immature stages, and systematics of snail-killing flies of the genus Colobaea (Diptera: Sciomyzidae), with overviews of aspects of the tribe Sciomyzini, Zootaxa 4840 (1), pp. 1-64 : 20-23

Colobaea bifasciella (Fallén), 1820

Map 4

(BNN 6426, 6717, 6763)

Colobaea bifasciella is a distinctive species ( Fig. 1 ; see also the color photo in Williams et al. 2013: 98). The elaborate yellow-and-black color pattern and pictured wings readily distinguish it from all other species of Sciomyzidae .

Type locality. “ In Kjellunge Gothlandiae [ Sweden]” ( Fallén, 1820) . 1♀, NHRS, Stockholm .

Its known geographical distribution—from Counties Mayo and Wexford, Ireland, across northern and central Europe to Hungary (Kalocsa) and Moscow, northward to Vuollerim, Sweden and northernmost Siberia, and east to the South Maritime Territory of Russia—extends farther north and east than that of any other species of Colobaea . Colobaea bifasciella appears to be able to exploit its hosts nearly to the northern, most rigorous limits of their distributions, but C. bifasciella apparently has not expanded significantly into the warmer, southern parts of the host snails’ ranges. Capture records of adult flies range from 10 May (Strachotin, Czech Republic) to 12 September (Gyón, Hungary).

Adult flies of C. bifasciella are found in various macrohabitats, as are those of other species of Sciomyzidae whose immature stages occur only in restricted microhabitats. However, because of their obligatory trophic relationship with G. truncatula and S. palustris , we know that the larval microhabitat must fall somewhere within those occupied by the host snails. The larval microhabitats are further limited to areas in which G. truncatula or S. palustris are stranded, aestivating, foraging out of the water, or otherwise exposed. Submerged snails cannot serve as oviposition sites nor as hosts for larvae of Colobaea .

Where a large, dense population of C. bifasciella was encountered at Frederikslund, near Holte, Denmark, C. bifasciella eggs were found on snails among moist, dead leaves near a small permanent pond in a heavily shaded vernal swamp. Infested snails also were collected from muddy banks bordered by Carex spp. in exposed marshy areas along rivers in northern Sweden. A few puparia were found in shells floating among emergent grasses at the edge of a small, unshaded vernal marsh during spring at Suserup, near Sorø, Denmark.

Laboratory rearings and observations were initiated with many eggs, larvae, pupae, and adult flies collected 7 May–22 August 1964 ( FT 6436 , 6451–6452 , 64100 ) near Sorø and Holte, Zealand, Denmark ; 8–28 July 1967 ( FT 6721–6731 ) at Brattby , near Umeå, Sweden ; and with 1♂ collected 14 June 1967 ( FT 6705 ) and 1♀ collected 8 July 1967 ( FT 6721 ) near Vuollerim , Sweden .

Adult flies mated readily in the laboratory between 27 May and 7 August. Females copulated for the first time 9–12 days after emergence. Females collected on 23 May in Denmark and on 8 July in northern Sweden and then held without males laid viable eggs. The copulatory postures were similar to those of most other species of Sciomyzidae . The male placed his foretarsi on the dorsomesal margins of the female’s compound eyes, grasped the basiventral surfaces of her half-outstretched wings or the sides of her thorax with his midtarsi, and held the sides of her postabdomen with his hind tarsi. Copulation commenced within 10 minutes after males and females had been placed in the same jar.

Preoviposition periods of laboratory-reared females ranged from 12 to 22 days. Females laid eggs from 24 May to 16 August. A female collected on 23 May laid 72 eggs between 24 and 29 May, and a female collected 8 July laid 343 eggs between 9 July and 19 August. Field-collected S. palustris , usually 10 snails of the same sizes as found infested by C. bifasciella in nature, were added to the chamber with the latter female for 24-hour periods during the first half of her oviposition period and for longer periods thereafter. Some snails died in the oviposition chamber; she laid no eggs on them. Daily egg production ranged from 3 to 15 and averaged 8.3 eggs per day. Egg production did not decrease markedly when snails were left in the chamber with the female for several days; under these conditions, she simply laid additional eggs on each snail. One female that emerged in the laboratory laid 55 eggs between 16 and 21 July, and another laid 18 eggs between 9 and 16 August. Unhatched viable eggs were found on snails in the field between 25 May and 23 July. Almost all eggs found in nature, as well as those laid in the laboratory, had been placed across the sutures of living S. palustris ( Figs 2–3 ). However, a viable egg was found on the shell of a living terrestrial snail, Balea perversa (L.), and another was found on an empty shell of S. palustris during a period when the population of C. bifasciella at Frederikslund, Denmark, was very dense. Other species of aquatic and terrestrial snails occurring with the infested S. palustris were offered as hosts to adult female C. bifasciella but seldom were accepted as oviposition sites. On a few occasions, in the laboratory, female C. bifasciella laid eggs on Aplexa hypnorum (L.), young Lymnaea stagnalis (L.) (4.5–5.0 mm in length), and Radix peregra (O.F. Müller) . Lundbeck (1923) stated that all puparia he found were in shells of G. truncatula ; Dr. G. Mandahl-Barth (in litt.) confirmed Lundbeck’s determination of the host snail.

In rearing jars crowded with adult flies, as many as 29 eggs were laid on each snail, but most shells bore only one or two eggs, whereas with snails collected in nature only one egg (occasionally two eggs) were found on each infested S. palustris . Although Lundbeck (1923) made no mention of eggs of C. bifasciella , many of the snail shells he studied and which ADB and LVK examined at ZMUC still bear one or two collapsed eggshells across the sutures. The incubation period at room temperature was 3–5 days. Eggs usually hatched at the end nearest the aperture of the snail shell.

The feeding behavior of C. bifasciella larvae is one of the most specialized of all Sciomyzidae . It seems to be identical with that of its Nearctic ecological/behavioral equivalent, Sciomyza varia ( Berg 1964, Barnes 1990). According to the definition of Reuter (1913), C. bifasciella should be classified as a parasitoid. That is, the larva feeds carefully within the host in such a way that the host is not killed until the larva is relatively well developed, at which time the larva consumes most of the remaining tissue. Such an insidious manner of feeding during early larval life, with a transition to predaceous habits and finally to saprophagous habits, indicates the evolution of a series of adaptations that are finely adjusted to the activity, defensive reactions, and physiological conditions of the host snail. The occurrence of these three trophic stages (parasitoid, predaceous, and saprophagous) in the development of each larva is reminiscent of the feeding behavior of some individuals of Atrichomelina pubera (Loew) ( Foote et al. 1960) and of some species of Pherbellia ( Bratt et al. 1969) . However, the behavior of larval A. pubera is much more variable than that of C. bifasciella in that larval A. pubera also can develop entirely in a parasitoid/predaceous or saprophagous manner.

A simple but effective technique used during the 1964 and 1967 rearings by ADB and LVK permitted exceptionally close observation of the development of C. bifasciella larvae; see also under Materials and Methods, above, the technique used by Barnes (1990) to study Sciomyza varia . In the laboratory, some snails bearing C. bifasciella eggs were removed from oviposition jars and placed separately in 1x5-cm glass vials containing a wad of damp cotton and plugged with dry cotton. Each snail soon affixed its aperture to the side of the tube. Development of C. bifasciella larvae was then observed through the walls of the tube under 50X magnification by use of a stereoscopic microscope. As soon as the egg hatched, the larva crawled down the side of the shell and penetrated between the mantle and foot until only its posterior spiracles remained exposed. Larvae were very sensitive to sudden movement. When disturbed, they pulled their posterior end below the surface of the snail tissues and remained so for long periods of time. None of the viscous, colorless mucus normally produced by S. palustris when irritated was secreted when the tiny (about 1.0 mm in length) C. bifasciella larvae attacked the snail. When more than one egg had been laid on a snail shell, all larvae that emerged entered the snail, but then all except one of them left the snail within about one day, even though the established larva did not overtly attack the other larvae.

Individual snails remained active for as long as 10 days after larval invasion, but it usually produced an epiphragm within a few hours and thereafter remained motionless. The substance consumed by the newly established larva was not identified during this study, but it seems likely that the youngest larvae feed on mucus and extrapallial fluid. Sometime during the first or second stadium, larvae began consuming nerve tissue between the eye stalks. This subdued the snails but did not kill them immediately. The posterior spiracles of newly molted second-instar C. bifasciella larvae became clearly visible between the retracted foot and the mantle of the still-living snails 7–10 days after the initial attack. The larvae then began to consume all snail tissue within reach. Infested snails usually died and began to decay shortly before the larvae completed the second stadium, but sometimes a pin prick elicited slight muscular movements of the foot and mantle even after a larva had reached the third stadium. Larvae continued to feed on decaying snail tissue for the remaining 1–2 days of the second stadium and for the entire 4–6 days of the third stadium. In the laboratory, the total duration of larval life ranged from 20 to 31 days (first stadium, 10–12; second, 6–13; and third, 4–6). When the host snail of a first- or young second-instar larva died, the larva remained in the dead snail shell but died after a few days.

Each larva developed through all three stadia in a single snail. Additional snails placed in the rearing containers never were attacked, even when the first host snail was very small. The range in width/length measurements of 19 S. palustris attacked in nature was 2.2–3.8 mm wide and 4.8–11.0 mm long; the range for seven hosts attacked in the laboratory was 3.4–5.5 mm wide and 4.8–10.1 mm long. Adult flies that emerged from puparia in small shells were, in some instances, only half as large as those that developed in larger hosts.

Larvae consumed all or almost all of the mostly decayed snail tissues before pupariating, at which time they pushed any remaining tissues and debris out of the snail shell. Often the muscular anterior part of the foot, the mantle, and the ovotestis could be seen among this material. Such emptying of the shell seems to have two advantages: it reduces the danger of mold growth that might kill the pupa or attract enemies, and it makes the shell somewhat more buoyant. No septum material such as that excreted by pupariating larvae of C. americana and by several species of Pherbellia was produced by any pupariating C. bifasciella larvae. The anterior portion of the puparium was characteristically expanded to close off the shell whorl ( Fig. 4 ).

Lundbeck (1923) reported obtaining adult flies during spring from puparia found in flood debris. A puparium that ADB and LVK collected on 7 May 1964 at Suserup Skov , near Sorø , Denmark, produced a female on 16 May. In the laboratory, 81 puparia were formed by field-collected larvae, from larvae that had developed from field-collected eggs, or from larvae that had developed from eggs laid in the laboratory. Fourteen adult flies emerged between 10 January and 12 February 1968 from the 57 puparia formed between 26 July and 21 August 1967 from the rearing ( BNN 6763 ) initiated with a female collected 8 June 1967 at Brattby , near Vuollerim , Sweden. Twenty-four puparia formed between 14 June and 28 August 1964 were held at 76% relative humidity at room temperature; 18 adult flies emerged between 2 July and 19 December. The puparial periods for 10 of these adult flies (7♀, 3♂) were not of exceptional duration, ranging from 14 to 21 days (average 17.4 days), in contrast to the duration of six other puparia formed at the same time by both laboratory-reared and field-collected larvae; these required 114–154 days (average 131.8 days) to produce adult flies (1♀, 5♂). Also recorded were two puparial periods of intermediate (63 and 81 days) duration .

In this initial study of the basic life cycle of C. bifasciella, ADB and LVK were able to show only that the duration of the puparial period is variable; it may be very short and similar to summer generational periods of other species of Sciomyzidae , or it may be as much as 10X longer than those and include a quiescent stage. Because both quiescent and nonquiescent pupae were obtained from the same group of eggs laid in the laboratory and held at the same temperature and humidity, it seems likely that the occurrence of puparial periods of two distinctly different durations is controlled genetically and is not solely a function of environmental conditions. Similar behavior was observed during rearings of Pherbellia similis (Cresson) ( Bratt et al. 1969) .

Regarding longevity, in the laboratory, four field-collected adult flies lived 4, 7, 42, and 50 days, and six laboratory-reared adult flies lived 6–32 days.

The fact that adult flies emerge soon after puparia are collected in the spring, that eggs in nature are laid as early as 25 May, and that puparia formed in late summer and held at room temperature may require as long as 154 days before emergence of adult flies indicates that C. bifasciella overwinters in the puparium.

Regarding natural enemies, Lundbeck (1923) obtained “a Cryptine and a Chalcidid” from puparia collected during spring; although thought to be deposited in the ZMUC, Thomas Pape informed LVK (in litt. March 2015) that these two parasitoids could not be located there. A puparium collected at Sorø, Denmark on 9 June 1964 and held continuously at room temperature and 76% relative humidity produced an ichneumonid wasp on 10 July 1965.

Figures

FIGURE 1. Colobaea bifasciella (Fallén), ♂. Original drawing by Greta Lyneborg, Copenhagen, Denmark. Body length: 2.47 mm.

MAP 4. Geographic range of Colobaea bifasciella (Fallén).

FIGURES 2–4. Eggs and puparium of Colobaea bifasciella (Fallén): 2, 3, eggs on shell of Stagnicola palustris; 4, puparium of C. bifasciella in shell of Stagnicola sp.