Pre-Imaginal Stages of the Blowfly Protocalliphora Falcozi in Nests of the Tree Sparrow (Passer Montanus)

Pre-imaginal stages of the blowfly Protocalliphora falcozi in nests of the tree sparrow (Passer montanus)

Viera Janoskova, Ivan Orszagh, Jan Jamriska & Martin Kopani

Janoskova, V., Orszagh, 1., Jamriska, J. & Kopani, M. 2010: Pre-imaginal stages of the blowfly Protocalliphora falcozi in nests of the tree sparrow (Passer montanus). — Entomol. Fennica 21: 107—116.

This paper offers the initial description ofthe first instar larva ofProtocalliphora falcozi Séguy, 1928 (Diptera: Calliphoridae) and redescription ofthe second and third instar larvae and puparium, as well as distinction between P. falcozi and its relative P. azurea Fallen (Diptera: Calliphoridae). The material was sampled in the National Nature Reserve Sur (SW Slovakia) from nests of the tree sparrow (Passer montanus), which has not previously been classified as a host of P. falcozi. Knowledge of diagnostically relevant characterics to determine bird blowfly larvae and puparia will undoubtedly contribute to the current accepted phylogeny and classification of the genus Protocalliphora.

V. Janoskova, I. Orszaglz &J. Jamriska, Department ofZoology, Faculty ofNat— ural Sciences, Comenius University, Mlynska dolina B], 842 15 Bratislava, Slovakia; E—mails.‘ [email protected], [email protected], [email protected] M. Kopani, Institute ofPathology, School ofMedicine, Sasinkova 4, Comenius University, 811 08 Bratislava, Slovakia; E—mail.‘ [email protected] Received 10 July 2008, accepted I 1 January 2010

1. Introduction including P. rognesi and T. braueri which have Holarctic distribution (Sabrosky et al. 1989, Bird blowflies (Protocalliphora Hough spp.) be- Whitworth 2003a, b). long to the family of Calliphoridae (subfamily Very little data has been published on the Chrysomyinae) together with some other genera identification of pre-imaginal stages of this ge- (Chloroprocta Wulp, Chrysomya Robineau— nus. When third instars are available, they should Desvoidy, Chrysopyrellia Séguy, Cocnliomyia be allowed to pupate for easier identification. Townsend, Compsomyiops Townsend, Hemilu— However, empty puparia are usually the only evi- cilia Brauer, Paralucilia Brauer & Bergenstamn, dence of larvae in birds’ nests. Phormia Robinneau—Desvoidy, Protoplzormiata Various determination keys from the Palae- Grunin, Protoplzormia Townsend and Trypo— arctic region have been published to identify calliplzora Peus). Their larvae are blood sucking Protocalliphora larvae, and these are predomi- parasites on altricial nestlings. 15 species of nantly for third instar larvae, which possess more Protocalliphora and 1 of Trypocalliplzora have diagnostic characters than the first and second been recorded from the Palaearct (Schumann instar larvae: Protocalliphora azurea (Engel 1986, Kurahashi 1993), 10 from Europe (Rognes 1920, Rohdendorf 1957, Iwasa & Hori 1990), P. 2004), and 29 species from the Nearctic region, falcozi (Séguy 1941, Zumpt 1965, Lehrer 1972), 108 Janos/(ova et al. ° ENTOMOL. FENNICA Vol. 21

P. maruyamensis (Iwasa & Hori 1990) and P. Slovakia on the SE fringe of the Male Karpaty rognesi (Engel 1920). Sabrosky et al. (1989) pro- Mts. (48° 42’ N, 17° 16’ E). The conservatory vided the key for identification ofthird instar lar- area is formed by rare alder wetlands in a flooded vae of 16 species in the Nearctic region. Older terrain depression combined with thermophilous references include descriptions of third instars of oak woods. The collected specimens belong to P. avium (Coutant 1915, Dobroscky 1925) and P. first instar larvae (11), second instar larvae (17), metallica (Hall 1948). third instar larvae (32) and puparia (20), and were Second instar larvae were described for all obtained directly from nestlings or nest mate- Protocalliphora avium (Coutant 1915) from the rial during the 15t—3rel broods of the tree sparrow. Nearctic region and P. azurea (Draber—Monko The material was sampled in the periods of May 2002), P. falcozi (Zumpt 1965), P. maruyamensis 20—June 26, 2006 and May 2—June 27, 2007. (Iwasa & Hori 1990), P. rognesi (Draber—Monko Some of the larvae were kept to develop to 2002) from the Palaearctic region. The only paper puparia and to adults, and this allowed species de- concerning description of the first instar larvae termination according to Draber-Monko (2004). was published by Iwasa & Hori (1990) for P. The pre-imaginal stages were identified from maruyamensis. nests where only specimens of P. falcozz' adults Puparia ofProtocalliphora azurea, P.falcozi, occurred. Mixed infestation by P. falcozz' and P. P. rognesi and Trypocalliphora brauerl' were de- azurea appeared only twice during our research, scribed by Cais et al. (2001), and Whitworth and in these cases the pre-imaginal stages were (2003a) published his key for the determination thus not identified. The puparia of Protocalli— ofpuparia of27 species in the Nearctic region. P. phora azurea were obtained from nests ofParas falcozi has been recorded only from the Palaearct, major in the Botanic Gardens in Bratislava. and mainly as adults (Gregor & Povolny 1959, Larvae were killed by soaking in hot water (to Peus 1960, Lehrer 1972, Mihalyi 1979, Rognes avoid deformation) and they were stored in 76% 1997). P. falcozz' has been reported as a parasite alcohol. Larvae and puparia were mounted in on Paras major (Gregor & Povolny 1959, Lehrer Canada balsam. A digital Leica DFC195 camera 1972), Paruspalustris (Szpila 1999, Wesolowski mounted on a Leica DM 1000 stereomicroscope 2001), Paras caeruleus (Rognes 1997), Ficedula was used for microphotography. Samples for albicollz's (Gregor & Povolny 1959, Lehrer 1972) SEM analysis were dehydrated in graded alcohol, and Phoenicurus phoenicurus (Gregor & subjected to the critical drying point of CO2 Povolny 1959, Lehrer 1972). The tree sparrow (CPD 030, BAL-TEC, BG PRUFZERT). Speci- (Passer montanus) was declared to be an exclu- mens were mounted on carbon stubs and coated sive host of Protocalliphora azurea (Rognes with a layer ofgold in an ion sputtering apparatus 1991) (SCD 050, BALZERS, Lichtenstein). SEM pic- This paper aims to describe the first instar and tures were taken using a JXA 840 A (JEOL, Ja- to re-describe the second and third instar and pan) scanning microscope. puparium ofP. falcozi since all available relevant The study material is deposited at the Depart- published data has been insufficient and too gen- ment of Zoology, Faculty of Natural Sciences, erally diagnostic for the whole genus. Here, we Comenius University. emphasize the characteristics to distinguish the pre-imaginal stages of P. falcozi and P. azurea, since they belong to the most common species 3. Terminology found in nests of cavemicolous nesters in central Europe. With their tapering anterior and truncated posterior ends Protocalliphora larvae generally do not much differ from other genera of Calliphoridae. 2. Material and methods Their body consists of 12 segments, pseudocephalon, 3 thoracic segments (T l—T III), 7 ab- Sampling of the material was conducted in the dominal segments (Al—A VII) and the anal divi- National Nature Reserve Sur situated in SW sion, completely covered with spines. The T I an- ENTOMOL. FENNICA Vol. 21 ° Pre-imaginal Protocallzphomfalcozi 109

' "' '. -' ‘ 5 '-.""' “a; I " I: I. %’ m':ZT' H1125 w meson): SET Woes Fig. 2. SEM of anterior end of body of the first instar of Protoca/Iiphora falcozi, ventral view; a: antenna, as: additional sense organ, 0: cirri, or: oral ridges, pf: prothoracic fringe, mh: mouthhooks, mp: maxillary palpus.

instars. The posterior spiracle region is divided into a hyperspiracular region (above the posterior

Fig. 1. First instar of Protoca/Iiphora falcozi. — a. spiracles), a mesospiracular region (between the Whole body, lateral view. — b. Cephaloskeleton, ven- posterior spiracles) and a hypospiracular region tral view; dc: dorsal cornua, is: intermediate sclerite, (under the posterior spiracles). mh: vc: mouthhooks, pb: parastomal bar, ventral Apart from a well-sclerotized and darkened

— cornua. c. Posterior spiracular region; ao: anal cuticle, the puparium also differs from larvae, opening, ap: anal papillae, p1: dorsal papillae, p3: having a less distinct prothoracic fringe which is supralateral papillae, p4: infralateral papillae, p5: inverted during pupation and also poorly distin- subventral papillae, p6: ventral papillae. guishable papillae. Externally the puparia have varyingly developed cuticular folds (close to the terior spinose band is exceptional, since it is mod- posterior spiracles) and cuticular ridges (dorsally ified to a crown of setae (prothoracic fringe), and ventrally on each segment), and these are not which most likely adheres the larva to the host visible on larval instars. The terminology used for during blood-sucking. Each abdominal segment the description ofpre-imaginal stages was that of has normally three distinct ventral spinal bands — Courtney er a1. (2000) and Whitworth (2003 a). ventral bands bounded by 8 ventral pads (Fig. l). The pseudocephalon has antennae, maxillary palpus and mouthhooks. The cephaloskeleton is 4. Descriptions of larvae composed ofbasal and intermediate sclerites and and puparium mouthhooks. Intermediate sclerite of each instar proceeds to the basal sclerite which consists of 4.1. First instar larva dorsal and ventral comua. Paired labial sclerites are situated between the mouthhooks and the me- The body length is 09—225 m (n: 4). Spines of dian beam of the intermediate sclerite. A labrum each segment are only just visible and lack dis- and accessory sclerite are absent. tinct difference in their shape and size. The pro- The anal division has anal papillae and 7 dis- thoracic fringe is very short compared to that in tinct pairs of papillae (dorsal, subdorsal, supra- other instars (Fig. la), and the ventral pads are lateral, supraventral, infralateral, subventral and clearly distinguishable on each abdominal seg- ventral papillae), but these are not distinct on all ment. Three ventral bands are distinct and unin- llO Jdn0§k0vd et al. ° ENTOMOL. FENNICA Vol. 21

Table 1. Second instar larval characters of Protoca/Iiphora falcozi and F’. azurea.

Reference Length (mm) min—max Number of lobes mean 1r SD. (n) of anterior spiracles (n)

P. falcozi Present study 1.6—5.6* 3.65 i 1.36 (13) 8 (1 0) P. azurea Draber-Monko (1996) 6.0—6.5— 6—7 (occasionally 8)

* Fully developed second instar larvae, the only difference was in length. terrupted. Anterior spiracles are absent. 3a, 3b). The parastomal bar is fused With the in- Each lobe of the pseudocephalon bears an- termediate sclerite (their border is marked by a tenna, maxillary palpus (cluster of several dashed line, Fig. lb). sensilla) and accessory sensillum. On the surface of the pseudocephalon there are numerous cirri and oral ridges, While the labial lobe and ventral organ are absent or indiscernible (Fig. 2). Cephaloskeleton is small, mouthhooks are more strongly sclerotized than the other parts. The intermediate sclerite is elongated (When compared to the second and third instars), and the dorsal comua is longer than the ventral one (Fig.

d‘

fa.“- c

0.01 mm

Fig. 4. Second instar of Protoca/Iiphora falcozi. — a. Whole body, lateral view. — b. Cephaloskeleton, ventral view: dc: dorsal cornua, is: intermediate sclerite, ls: labial sclerites, mh: mouthhooks, pb: parastomal bar, vc: ventral cornua. — c. Posterior spiracular region; ao: anal opening, ap: anal papillae, p1: dorsal papillae, p2: subdorsal papillae, p3: supralateral Fig. 3. Cephaloskeleton of first instar of Protoca/Ii- papillae, p4: infralateral papillae, p5: subventral pa- phora falcozi. — a. Lateral view. — b. Ventral view. pillae, p6: ventral papillae, p7: supraventral papillae. ENTOMOL. FENNICA Vol. 21 - Pre-imaginal Protocalliphorafalcozi l 11

Fig. 5. SEM of anterior end of body of the second instar of Protocalliphora falcozi.

They have anal papillae and only 5 pairs of tiny papillae (dorsal, supralateral, infralateral, subventral and ventral) developed on the anal division, With the supralateral, infralateral, subventral, ventral and anal papillae clearly distinguishable. The anal papillae are rounded and the anal opening is situated slightly anterior to the anal papillae. The posterior spiracles are small and bilobed (Without a gap between two forming slits) and they are poorly sclerotized. The peritreme is incomplete, With an absent spiracular Fig. 6. Cephaloskeleton of second instar of Protocalli— scar (button). Spines in the mesospiracular region phora falcozi. — a. Lateral view. — b. Ventral view. are also absent (Fig. 1c).

sensillum indiscernible or absent. Numerous cirri 4.2. Second instar larva and oral ridges occur on the surface of the pseudocephalon. The labial lobe and ventral or- The body length is given in Table l. Spines of gan are absent or indiscernible (Fig. 5). each segment and prothoracic fringe are distinct The cephaloskeleton is stout, mouthhooks are (Fig. 4a). On T II—A VII the central spines are more strongly sclerotized than the other parts. slightly longer than the marginal ones. Ventral The parastomal bar is not fused With intermediate pads are easily distinguishable on each abdomi- sclerite, and the dorsal cornua is longer than the nal segment, and there are three distinct and unin- ventral one (Fig. 4b, 6a, 6b). terrupted ventral bands. Anterior spiracles are Anal papillae and all 7 pairs ofpapillae are de- present, number of developed lobes is given in veloped on the anal division, including distinct Table 1. supralateral, infralateral, subventral and ventral Each lobe of the pseudocephalon bears an- papillae. The subdorsal papilla is poorly devel- tenna and maxillary palpus, with an accessory oped, and anal papillae are rounded, While the ll2 Jdn0§k0vd er al. a

Table 2. Third instar larval characters of Protocalliphora faicozi and P azurea

Reference Length (mm) min-“max Number of lobes mean i 8.0. (n) of anterior spiracles (n)

P. faicozi This study 11.3404" 7.98 i 1.91 (15) SW11 (15) Zumpt (1965) 1243“- 5;; (occasionally 10) P. azurea Draberw Monko (2004) 13~15~ 8 lwasa & Horl (1990) 1345“- 5-40

* Fully developed second instar larvae, the only difference was in length. anal opening is situated slightly anterior to the anal papillae. Posterior spiracles have 2 slits with a distinct gap between them. The peritreme is in:- complete but more sclerotized in comparison with the first instar. A spiracular scar (button) is developed although it is not clearly distinguishable. and. spines are developed in the meson- spiracular region (Fig. 4c).

4.3. n mm larva

The body length is given in Table 2. Spines of each. segment and prothoracic fringe are distinct

T HmA are '- On VH central "'F (Fig. 7a). spines I" V! i “H'; (H ”'s'f’rba'l, ”ha ; ,9 - 's. :x‘lu’lf‘r 'i ‘ irlffifff‘!"'11:fdff F ffi",‘.flf} fi 5 19 I‘l‘1fiiprrflfl"?if I f :Ell d’ ones. { I! ‘ f l' than I the Ventral I «4’: ‘ll I. 10,: ,fi?f Iri’fc'g slightly longer marginal \h ‘o 1' 3!!! ”I; J 'r ‘l‘l f 73f .p g “(M g In}! dug in fl r \ .r , 5 3 12‘“‘ _n Hg; 9‘ 3:9 {115‘ I 1’ are on each abdomi_—- 1i «a fig W hi5“ pads easily distinguishable I? l' n?

'."H g, i 'p I‘M d 1.! 3 ‘0 J -’ {‘1‘ I; / . nal and there are three distinct and. uninu ‘9' “II-r, segment. a'.

' A. b r-I. p3 tempted ventral bands. Anterior spiracles are “I; /- I; “I.

"I I ..-§E; (“‘1' .. number of lobes is in ,: l. P.B present. u developed given J' 3' A. I! n "’ J c. ‘ jar-it, 'leg:;" ([3: ‘i‘ .. “In auntie-w. ,I 3 .yw: v; r' an“: ‘ ...--’ 2;. o, ’1',”l t 5‘4”,“ ut‘t“~“ Table (I f'1 '7 .r «‘5?! {3' if ntffivhfm t”q.“ a a4 Hflw‘u’my f “via“: #91,; “4“}t .. 31"“il‘afis' 1;...1' fl ,(flwv’gfly;fillyauagjl19"};f'I {9;} 1;“ $kh 3 \ 2 W“ "mil.»di’;"¢,”‘ll§lft".11l‘ Hi Each lobe of the bears arr- w“ INN" ‘ 1mm“ r filr’rf’fw «1,1I'1'5‘ pseudocephalon ‘ wiflo.f'/II‘ fif’JJj ’l’313‘i5’3‘31‘s“ ‘thr f ,3 J 9' - Ir; “1‘1. . “y”! ,rj ‘4' i V d a" I. "J t ,l" {(1J 1“ * f or 4",! g If f a," 1“ " i’rV’I’J'1fif'r’rf" a ll terma and with the if“ " w .v I ##313 a i 1 4 maxillary palpus. accessory ’r;,' 1110'...” 4 Mew-”p r i 9',“ ‘ 4) . f I “I r sensfllum indiscemible or absent. On the surface I, of the pseudocephalon there are numerous cirri and. oral ridges. and. the labial lobe and. ventral 0r- gan are also indiscemible or absent (Fig. 8}. The cephaloskeleton is thick. with the mouthhooks more sclerotized than other parts. The parastomal bar is not sted with the intermediate sclerite and the dorsal comma is longer than the ventral one (Fig. 7b. 9a. 9b). Fig. 7. Third instar of Protocaliiphora falcozi -—- a. Whole body, lateral View. --—- b. Cephaloskeleton, venm The anal papillae and all 7 pairs ofpapillae are tral View; dc: dorsal comma, is: intermediate sclerite, developed on the anal division. including distinct ls: labial sclerltes, mh: mouthhooks, vc: ventral subventral and ventral supralateral. infralateral. --- comma. c. Posterior spiracular region; a0: anal The subdorsal is devel- papillae. papilla poorly opening, ap: anal papillae, p1: dorsal papillae, p2: oped. While the anal papillae are rounded with the subdorsal papillae, p3: supralateral papillae, p4: anal opening situated slightly anterior to the anal infralateral papillae, p5: subventral papillae, p6: ventral papillae. There are posterior spiracles with 3 slits. papillae, p7: supraventral papillae. ENTOMOL. FENNICA Vol. 21 - Pre-imaginal Protocalliphorafalcozi 113

Fig. 8. SEM of anterior end of the third instar of Protocalliphora falcozi.

with a distinct gap between them. The peritreme is complete and a spiracular scar (button) is developed but seldom easily distinguishable. There are also mesospiracular spines (Fig. 7c).

4.4. Puparium

The body length is 7.11— 8.34 mm (mean in SD. = 7.95 i 0.42, n = 9), with all 3 ventral spine bands easily distinguishable. There are cuticular folds in the hypospiracular and mesospiracular region. However, there are small ones in the ' only - .. if .n {é . hyperspiracular region. Additionally, the cuticu- Fig. 9. Cephaloskeleton of third instar of Protocalli— lar ridges are as distinct as the cuticular folds. The phor‘a falcozi. — a. Lateral view. — b. Ventral view. puparia found in nests were sometimes covered by nest material. to complete their development successfully (Ben- net & Whitworth 1991). Additionally, enough 5. Discussion host nests with nestlings are required in order to collect sufficient material of larvae and puparia. Identification of pre-imaginal stages of bird We have not yet acquired an approach to keep lar- blowflies according to their morphological char- vae artificially, due to an alternative host used to acteristics appears indisputably more difficult nourish bird blowfiy larval instars (larvae pre- than for adults. In some cases this seems almost sumably cannot complete their development on impossible. presocial nestlings). Another problem occurs in Lack of available data on determination of obtaining eggs since females kept under artificial Protocalliphora larvae demands arduous samp- conditions cannot lay their eggs despite apparent ling since these obligate bird parasites are neces- mating (Bennet & Whitworth 1991). Such inade- sarily connected to their host, and this is essential quate material results in insufficient opportunity 114 Jdn0§kovd et al. ° ENTOMOL. FENNICA Vol. 21

to compare more species in their pre-imaginal of nestlings and spend their period in hosts, so stages. Therefore, some authors described Proto— that they do not have segments completely cov- calliphora larvae entirely according to character- ered with spines, and this can play a defensive istics distinctive of additional or even all genus role in a host’s body (also e.g. Auchmeromyia species (e.g. Zumpt, 1965: descriptions of the Brauer and Bergenstamm and the third instar of second and third instars ofP. falcozi). Cordylobia Gruenberg). Since larvae ofthe same instar can have vary- The main features ofP. falcozi larvae include ing nutrition their characteristics can vary, and enlarged antennae, numerous cirri and oral ridges this makes identification more complicated (e.g. on the pseudocephalon. Enlargement ofantennae distance between spines, prothoracic fringe di- and maxillary palpi in the first instars ofparasitic ameter and the distance between posterior spira- or predatory species from the genera Bellardia cles). Also, during food deficiency, the body Robineau-Desvoidy, Onesia Robineau—Desvoi- length of a more advanced instar may be shorter dy and Pollem'a Robineau—Desvoidy was also ob- than that of a younger one. Moreover, length of- served (Szpila 2003, 2004). This phenomenon is ten varies within the same instar due to differing possibly associated with a necessity for better ori- food sources and conditions. Certain body parts entation in nature. Females of Calliphora Robi- such as the cephaloskeleton and posterior spira- neau-Desvoidy, Phormia Robineau-Desvoidy cles also have a surprising degree ofvariability in and Lucilia Robineau—Desvoidy, which do not their sclerotization in the same instar. have enlarged antennae and maxillary palpi, lay In comparison with the Nearctic region, re- their eggs directly onto a suitable food source, cent research on bird blow flies in the Palaearctic whereas parasitoids do so when actively search- area has not been intensive enough. Larvae of ing for their host in soil (Szpila et al. 2008). Fe- Protocalliphora distincta, P. isochroa, P. Iii, P. males of Protocalliphora spp. lay their eggs di- peusi, P. nuortevai and P. proxima, all Palaearc- rectly on nestlings or on nearby nest material. tic species, have not been described. Most data al- Even though they can lay on a suitable food ready distinguishes only Trypocalliphora larvae source (nestlings), larvae are intermittent feeders, from Protocalliphora and Protocalliphora leaving their hosts facultatively after sucking rognesi from P. azurea and P. falcozi. enough blood, but they soon search for this Larvae ofP. azurea and P. falcozz' often inter- source again. act with the same host and their hosts build simi- There is a lack of detailed information con- lar nests or remain in nests for approximately the cerning the anal pad ofProtocalliphom larval in- same period, therefore identification of their lar- stars. The anal pad, which has been described in val instars still seems doubtful. Original morpho- the second instar of P. rognesi (Draber—Monko metric analysis supported by other references 2002 ) is similar to that ofP. falcozi. The position showed shorter second and third larval instars for of the anal opening ofthe first instar ofP. falcozi P. falcozi than for P. azurea. The number ofante- corresponds with that of Phormia regina rior spiracle lobes may be the same in both spe- (Meigen, 1826) and Lucilia illustris (Meigen, cies, and hence this does not represent a reliable 1826) and this was described by Szpila et al. characteristic for identification (Tables 1 and 2). (2008). Differences in the shape of cephaloskeletons in There are morphological differences for iden- these 2 species appear also insignificant (Draber— tification in puparia and adults between P. falcozi Monko 2004). However, there is some degree of and P. azurea (Cais et al. 2001, Draber—Monko discrepancy in the intermediate sclerite region, 2004). In our analyses, some additional charac- including the parastomal bar. Detailed synthesis teristics used in determination ofNearctic species of cephaloskeletons requires additional material (Whitworth 2003 a) have also been taken into ac- for analysis. count. The cuticle surface of fully developed Segments of Protocalliphora species, which puparia ofP. falcozi is distinctly different than in are completely covered with spines, exhibit rela- P. azurea. On the surface they are wrapped in a tively rare features for dipteran larvae. The Try— hair cocoon, and this is usually absent in P. pocalliphora larvae burrow directly into the flesh azurea. ENTOMOL. FENNICA Vol. 21 ° Pre—imaginal Protocalliphorafalcozi 115

tic on birds in Poland. 7 Annales We propose that data obtained in our analyses Zoologici (Warsza- 52: 3337337. will be useful in complex phylogenetic simula- wa) Draber-Monko, A. 2004: Calliphoridae. Plujki (lnsecta: tions. Iwasa and Hori declared that some (1990) Diptera). Fauna Polski. Tom 23. 7 Muzeum i lnstitut which are absent in other characteristics, Chryso- Zoologii PAN, Warszawa. 662 pp. myinae genera, presumably corresponded with Dobroscky, I. D. 1925: External parasites ofbirds and the specialized blood sucking habit such as in Proto— fauna of bird nests. 7 Biological Bulletin 48: 2747 phormia, Phormia and Chrysomya. For example, 281. E. O. 1920: die nicht als these include tubercles at abdomi- Engel, Dipteren, Pupiparen sind,

undeveloped 7 Vogelparasiten. Zeitschrift fiir Wissen—schaftlich nal segment VIII, prothoracic fringe, relatively Insektenbiologie 15: 2497258. small small with mouthhooks, posterior spiracles Gregor, F. & Povolny, D. 1959: Kritischer Beitrag zur a long distance between them. Except in Kenntniss der Tribus Phormiini (Diptera, Calli- Protocalliphora, obligatory haematophagy is phoridae). 7 Acta societatis entomologicae Cecho— sloveniae 56: 26750. seen only in rare forms of parasitism of Calli- Hall, D. G. 1948: The blowflies of North America.7 phoridae larvae. Morphology ofbird blowfly lar- Thomas Say Foundation, Washington. 477 pp. vae be beneficial to the evolu- may comprehend Iwasa, M. & Hori, J. 1990: The calliphorid larvae parasitic tion of Calliphoridae when larval haematophagy on birds in Japan (Diptera: Calliphoridae). 7 Medical originating in saprophagy is considered. How- and Veterinary Entomology 4: 1417146. H. 1993: of the Ornitho— ever, the data offered in this paper is proposed to Kurahashi, Japanese Species parasitic Blow Flies: Protocalliphora and T73490- become essential for syn- complex phylogenetic 7 calliphora (Diptera: Calliphoridae). New Entomol- theses. ogist 42: 8715. Further should lead to analysis undisputedly Lehrer, A. Z. 1972: Diptera. Familia Calliphoridae. Fauna the elaboration of a key to identify all bird blow- Republicii Socialiste Romania, Vol. ll (12). 7 fly larval instars. Morphometric characteristics of Editura Academiei RSR, Bucuresti. 247 pp. F. 1979: 7 the cephaloskeleton will most likely present a de- Mihalyi, Fe'meslegyek Huslegyek. Calliphori- dae 7 Sarcophagidae. 7 Fauna Hungariae 135. 7 flnitive challenge in diagnostics, whereas the Akadémiai Kiado, Budapest. 152 pp. number of anterior lobes and their spiracle shape Peus, F. 1960: Zur Kenntnis der ornithoparasitischen and size will become secondary in species identi- Phormiinen (Diptera, Calliphoridae). 7 Deutsche fication. Entomologische Zeitschrift 7: 1937235. Rognes, K. 1991: Blowflies (Diptera, Calliphoridae) of Fennoscandia and Denmark. Fauna Acknowledgements. This research was supported by Vega Entomologica No. 1/4333/07 and UK/172/2008 projects. Scandinavica. Vol. 24. 7 E.J. Brill, Leiden. 272 pp. Rognes, K. 1997: Additions to the Swiss fauna of blow— flies. with an analysis of the systematic position of Calliphora stylifera (Pokorny, 1889) including de— References scription of the female (Diptera, Calliphoridae). 7 Mitteilungen der schweizerischen entomologischen Bennet, G. F. & Whitworth, T. L. 1991: Studies on life his— Gesellschaft 70: 63776. tory of some species Protocalliphora (Diptera: Calli— Rognes, K. 2004: Protocalliphora. 7 In: Pape T. (ed.), phoridae). 7 Canadian Journal ofZoology 69: 20487 Fauna Europea: Calliphoridae. Version 1.1. [w 2058. document]. URL http://www.faunaeur.org/. (Site vis— Cais, L., Draber-Monko, A. & Szpila, K. 2001: Bird blow— ited on 19 April, 2007). flies (Calliphoridae: Protocalliphora, Trypocallipho- Rohdendorf, E. B. 1957: On the parasite flies, injurious to

7 m) in Poland. Polish Journal of Entomology 70: nestling singing birds. 7 Entomologicheskoe 2777291. obozrenie 36: 1167124. Courtney, G. W., Sinclair, B. J. & Meier, R. 2000: Mor— Sabrosky, C. W., Bennett G. F. & Whitworth T. L. 1989: phology and terminology of Diptera larvae. 7 In: Bird blow flies (Protocalliphora) in North America Papp, L. & Darvas, B. (eds.), Contributions to Manual (Diptera: Calliphoridae), with notes on Palearctic spe— of Palaearctic Diptera. Vol. 1: 857161. Science He— cies. 7 Smithsonian Institute Press, Wash. DC. 312 rald, Budapest. 994 pp. PP- Coutant, A. F. 1915: The habits, life history, and structure Séguy, E. 1941: Etudes sur les mouches parasites. II. of a blood—sucking muscid larva (Protocalliphora Calliphorides. Calliphorines (Suite), Sarcophagines et azurea). 7 Journal of Parasitology 1: 1357150. Rhinophorines de l’Europe occidentale me'ridionale. Draber-Monko, A. 2002: The larvae ofthe genus Protocal— Encyclopédie Entomologique, (Sér. A 21). 7 Paul liphora Hough, 1899 (Diptera: Calliphoridae) parasi- Lechevalier, Paris. 436 pp. 116 Jdnoskovd et al. ° ENTOMOL. FENNICA Vol. 21

Schumann, H. 1986: Family Calliphoridae. 7 In: Soos, A. Journal of Medical and Veterinary Entomology 22: & Papp, L. (eds), Catalogue of Palaearctic Diptera. 1 6725. Vol. 12: 1 1758. Akademiai Kiado, Budapest. 265 pp. Wesolowski, T. 2001: Host-parasite interactions in natural Szpila, K. 1999: Muchowki z rodziny Calliphoridae (Dip— holes: Marsh tits (Paruspalustris) and blow flies (Pro- tera) Puszczy Bialowieskiej. 7 Parki Narodowe i Re— tocallzphorafalcozi). 7 Journal ofZoology 255: 4957 zerwaty Przyrody, BialowieZa 18.1: 43751. 503. Szpila, K. 2003: First instar larvae of nine West-Palaearc- Whitworth, T. L. 2003 a: A key to the puparia of27 species tic species of Pollenia Robineau—Desvoidy, 1830 of North American Protocalliphora Hough (Diptera: (Diptera: Calliphoridae). 7 Entomologica Fennica Calliphoridae) from bird nests and two new puparial 14: 1937210. descriptions. 7 Proceedings Entomological Society Szpila, K. 2004: First instar larvae offive West Palaearctic of Washington 105: 99571033. species of Bellardia Robineau—Desvoidy, 1863 and Whitworth, T. L. 2003b: A new species ofNorth American Onesia Robineau—Desvoidy, 1830 (Diptera: Callipho— Protocalliphora (Diptera: Calliphoridae) from bird ridae). 7 Studia Dipterologica 11: 3017112. nests. 7 Proceedings Entomological Society of Szpila, K., Pape, T. & Rusinek, A. 2008: Morphology of Washington 105: 6647673. the first instar larva of Calliphora vicina, Phormia re- Zumpt, F. 1965: Myiasis in Man and Animals in the Old gina and Lucilia illustris (Diptera, Calliphoridae). 7 World. 7 Butterworths, London. 267 pp.