Phalacrotophora beuki ( Diptera : Phoridae ) , a parasitoid of ladybird pupae ( Coleoptera : Coccinellidae )

In the years 1998-2000, parasitization of the pupae of various ladybird species by scuttle flies of the genus Phalacroto­ phora was studied in central Poland. Altogether, 12 ladybird species were found to be parasitized by these flies, and one of them, Anatis ocellata (L.), proved to be a host of P. beuki Disney, a species whose biology had not previously been described. Our studies showed that P. beuki can limit the numbers ofA. ocellata. In its typical habitat, i.e. Scots pine forests, 35-40% of this ladybird were parasitized by P. beuki. In other habitats, however, where A. ocellata occurred sporadically, P. beuki was not recorded from A. ocel­ lata or other ladybird pupae. P. beuki was described from a single female collected in Holland. The present paper describes the hith­ erto unknown male, which is very similar to the males of P. berolinensis Schmitz and P. delageae Disney. The feature that reliably separates the males of these three species (a detail of the hypopygium) is described. This feature enabled the recognition in the col­ lection of the Cambridge University Museum of Zoology of a male of P. beuki from Germany, previously assigned to P. berolinensis.


Seven species of Phalacrotophora
Enderlein are reported from Europe.While the biology of most of them is unknown, the three species, P. fasciata (Fallén), P. berolinensis Schmitz and P. delageae Disney, are parasitoids of ladybird pupae (Disney & Beuk, ]997).Most is known about the life cycles of P. fasciata and P. berolinensis.Mating in these species occurs on, or nearby, ladybird prepupa.After copulation the male moves away from the female, which remains with the prepupa, and parasitizes it when it begins to pupate.Usually several eggs are laid on the ventral thoracic region of the pupa.Egg-Iarval development of the parasitoid lasts 7-] 2 days and then the larvae leave the dead host pupa and pupate in the soil.Adult flies may emerge after 15-25 days or overwinter and emerge next season (Disney et al., 1994;Ceryngier & Hodek, ]996).P. fasciata and P. berolinensis overwinter as fully formed adults within the puparia (Disney, 1994).
In this paper the life cycle of Phalacrotophora beuki Disney, a species only recently described from a single female caught in Holland (Disney & Beuk, 1997), is described.The hitherto unknown male is described and the character distinguishing it from the morphologically very similar males of P. berolinensis and P. delageae is illustrated.

MATERIAL AND METHODS
Most of material for this study was obtained in 1998-2000 in central Poland (around the village Dziekanów Lesny, some 15 km NW of Warsaw) during investigations of the parasitoids of ladybird juvenile stages (Ceryngier & Durska, in prep.).Pupae of various ladybird species were collected in various habitats and transferred to the laboratory, where they we re kept singly in Petri dishes until adult or parasitoid emergence.Larvae of scuttle flies th at emerged from host pupae we re left in the dishes, where their further development (pupariation, pupation, emergence of adults) took place.The puparia, from which flies did not emerge af ter at least one year, we re dissected.Adults found within the puparia we re gently removed.Additionally, several Phalacrotophora females were observed attending ladybird prepupae or pupae in the field.These flies we re collected together wi th their hosts.
Male specimens obtained in this study and assigned to P. beuki are very similar to those of P. berolinensis and P. delageae.The males of these three species are reliably separated by details ofthe hypopygium (see Results).]ndeed males ofthis species group previously not collected with their distinctive females need to be checked in the light of this newly discovered feature.Phalacrotophora males from the collection of the Cambridge University Museum of Zoology we re re-examined and one male P. beuki found.

Field studies in Poland
In a study of the parasitoids of ladybird juvenile stages (Ceryngier & Durska, in prep.), pupae of ]2 ladybird species were found to be hosts of parasitic scuttle flies.For 11 host species, their scuttle fly parasitoids were easily obtained because most of their larvae !eft these hosts, pupated and subsequently emerged as adults.All 11 ladybird species were parasitized by Phalacrotophora fasciata, 5 by P. berolinensis and 4 by P. delageae.However, after the first year of the study it was realised that the specific status of the scuttle flies parasitizing the twelfth ladybird, Anatis ocelIata (L.), was uncertain.Although in its typical habitat, pine forests, A. ocelIata was frequently parasitized, not one adult fly emerged from the relatively large, thick-walled puparia formed by larvae after leaving the pupae of this ladybird (Tabie I).In contrast, scuttle fly larvae emerging from the pupae of other ladybirds collected from pines [Myzia oblongoguttata (L.), Harmonia quadripunctata (Pontoppidan), CoccinelIa magnifica (Redtenbacher), Exochomus quadripustu-latus (L.)] usually developed into adults of either P. fasciata or P. berolinensis.
To obtain adults of the species parasitizing A. ocellata the flies attending prepupae or pupae of this ladybird in the field we re collected and the unhatched fly puparia th at came from A. ocellata pupae were checked for adult flies.
Altogether, in 1999 and 2000, 5 female flies th at had either just laid eggs on freshly moulted A. ocellata pupae, or were attending A. ocellata prepupae waiting for them to pupate, were collected.These females were put with their hosts in the labora-T ABLE 3. Parasitization of Anatis ocellata pupae from plants other than Scots pine.'Iarva or pupa within puparium tory.From each of these hosts parasitoid larvae emerged and subsequently pupated but failed to give ri se to adult flies.However, all the adult flies so collected proved to be Phalacrotophora beuki.
Dissections of the puparia from parasitized A. ocellata in 1998 and 2000 (material from 1999 was lost) showed that they mostly contained early developmental stages (larvae or pupae) of the flies.However, in 64 puparia from 24 hosts adult flies were present.All females found in these puparia we re P. beuki and the males were assumed to be males of this species (TabIe 2).
Dissections of unhatched puparia obtained from other ladybirds revealed adults of P. fasciata, P. delageae and P. berolinensis, but not P. beuki.
So P. beuki was only recorded as a parasitoid of A. ocellata in pine forests.A. ocellata pupae collected from untypical habitats for this species: deciduous trees and shrubs, we re not parasitized by P. beuki or any other scuttle flies (TabIe 3).Data presented in Table 3 should be treated with caution as the numbers of pupae collected were low due to the rarity of A. ocellata on deciduous plants.It should be mentioned, however, that the pupae of other ladybirds [Adalia bipunctata (L.), A. decempunctata (L.), Calvia quatuordecimguttata (L.)] collected in these habitats at the same time we re frequently parasitized by P. fasciata and P. delageae., 1994;Ceryngier & Hodek, 1996).P. fasciata is even reported to parasitize a non-ladybird host, the chrysomelid Oulerna gallaeciana (Heyden) (Miczulski, 1978).
Our studies in central Poland seem to indicate that, in contrast to P. fasciata and P. berolinensis, P. beuki is restricted to one host, the largest European ladybird, Anatis ocelIata.However, the previous record of P. beuki may suggest a broader host range for this species.Dr Mattias Buck (in litt.)reports that in June 1992 he collected a female of P. beuki sitting on a pupa of Coccinella septernpunctata in Germany.This does not prove that this encounter would have resulted in parasitization.
There are many reports in the literature of A. ocelIata parasitized by P. fasciata (Marriner, 1932;van Emden, 1950;Parmenter, 1965;Filatova, ]974; Kuznetsov, ]987; Majerus & Kearns, 1989) and P. berolinensis (Klausnitzer, 1969(Klausnitzer, , 1976;;Majerus & Kearns, 1989).In our survey A. ocelIata was not parasitized by these species, although in the habitats where the pupae of A. ocelIata were collected both fly species frequently parasitized other ladybirds.During this study A. ocelIata was only parasitized by P. beuki.The identity of scuttle flies bred from A. ocelIata ought to be checked, especially where the identification was based only on males.P. beuki seems to be an uncommon species.It was described in 1997 from a single female, but material in collections from before this date need checking for misidentifications, especially as our study suggests that P. beuki could be a quite frequent parasitoid of ladybirds in coniferous forests, a habitat widespread in Europe.Why did P. beuki remain undiscovered for

Re-examination of Phalacrotophora males in an insect collection
Comparison of Phalacrotophora males from the collection in the Cam bridge University Museum of Zoology with the P. beuki males from Poland revealed that one male in the Cam bridge collection, which had been assigned to P. berolinensis, belonged to P. beuki.This specimen was collected in Germany (N.Bavaria, nr Schweinfurt, 19 June 1983, W. Büchs).As the males from Poland are all teneral, this German specimen was used to obtain the colours and wing measurements for the description of the male of P. beuki.

Male
Frons similar to female but not obviously narrowing below (anteriorly).Supra-antennal bristles more strongly differentiated from the more numerous adjacent frontal hairs than in female.Antennae and palps similar to those in female.Labrum pale straw yellow and only about 0.8x as broad as postpedicel (third antennal segment).LabelIa a little broader than in female.Abdominal tergites 1, 2 and 6 entirely, or largely, orange yellow.T5 with at least anterolateral brown patches.T3 and T4 largely brown in outer thirds but variably orange yellow in middle thirds.Venter straw yellow with hairs restricted to segment 6. Hypopygium as in Fig. 1, with the epandrium orange brown and the anal tube light brown.The left lobe ofthe hypandrium as in Fig. 4, with the microsetae restricted to a patch on the posterolateral extremity.The right lobe is as in P. berolinensis (see Fig. 6

Affinities
In the key to European species in Disney & Beuk (1997) the male of P. beuki runs to couplet 5, to P. berolinensis and P. delageae, whose separation from each other is far from satisfactory.However, in the present study a better character was found to distinguish all three species.The left lobe of the hypandrium is entirely covered in dense microsetae in P. berolinensis (Fig. 2).In P. delageae the microsetae only occur on the outer half along the entire length and only extend onto the inner half at the tip (Fig. 3).In P. beuki the microsetae are restricted to a patch on the posterolateral extrèmity (Fig. 4).
Parasitic Phalacrotophora, especially P. fasciata and P. berolinensis, are rather catholic in their choice of host species.They can parasitize many species of ladybirds belonging to the subfamilies Coccinellinae and Chilocorinae (Disney, 1994; Disney I l such a long time? A. ocelIata, the main host species of this scuttle fly, is widely distributed in Europe and other parts of the Palearctic Region (Iablokoff-Khnzorian, 1982).Maybe, the "cryptic nature" of P. beuki can be partly explained by the specific requirement~for its development.The laboratory conditions used by us, and perhaps other workers, for rearing scuttle flies are suitable for some species but not P. beuki.In natural conditions, the larvae ofthis species probably pupate in the soil, i.e. in a humid environment.Thus for the successful development of P. beuki pupae it is important they are kept at a relatively high humidity.In our study the humidity was not controlled but fluctuated with the external conditions.Some other physical factors, however, might also be involved.For example, the flies might require particular temperature conditions for diapause completion.
The premature mortality of P. beuki mayalso be related to the unsuitability of A. ocel/ata as a host, although, in our opinion, this is unlikely.It is known that parasitoids sometimes parasitize unsuitab!e hosts (e.g.Vinson, 1976), but the regular parasitization of more than one third of quite an abundant but unsuitable ladybird is highly maladaptive.

T
ABLE 1. Parasitization by scuttle flies of Anatis ocellata pupae collected on Scots pine (pinus sylvestris L.) T ABLE 2. Scuttle flies found in the puparia that originated from Anatis ocellata pupae.