Ceratophyllinae Dampf, 1908

Pilgrim, Robert L. C. & Galloway, Terry D., 2003, Descriptions of flea larvae (Siphonaptera: Ceratophyllidae, Leptopsyllidae) found in nests of the House Martin, Delichon urbica (Aves: Hirundinidae), in Great Britain, Journal of Natural History 37 (4), pp. 473-502 : 475-483

Ceratophyllinae Dampf, 1908 Ceratophyllus (Ceratophyllus) hirundinis (Curtis, 1826) (figures 1–16)

For a general description of Ceratophyllus spp. larvae, refer to Pilgrim and

Galloway (2000).

Description

Head (figures 1–9): Widest posteriorly, slightly wider than long in slide-mounted specimens; dorsal, lateral and ventral surfaces with fine, polygonal reticulation, most obvious over gular region and the antero-dorsal surface of the labrum. Coronal suture short, branching into two frontal sutures that become faint towards the antennal mounds.

Setation: there are normally 17 acicular setae on each side of the head capsule. Parietals (par.): outermost approximately one and a half times as long as innermost, innermost reaching beyond anterior margin of Th.I; middle parietal seta minute, usually slightly anterior to the other parietals. Occipitals: anterior (a.occ.) and posterior (p.occ.) minute; p.occ at or just posterior to margin of head capsule. Frontal (fr.) long, slender, reaching nearly to alveolus of outermost par. Interantennal (i-ant.) very short, fine. Clypeals: medial (m.cl.) stout, length approximately equal to basal diameter of antennal shaft; lateral (l.cl.) nearly the length of antennal shaft. Post-antennal (p-ant.) length approximately that of m.cl. Genals: posterior (p.gen.) long, slender, about equal in length to outermost par.; anterior (a.gen.) short, barely reaching alveolus of p.gen. Sub-genal (s-gen.) long, slender, slightly shorter than p.gen. Post-clypeal (p-cl.) very short, about equal to i-ant. Postmandibular (p-man.) long, slender, reaching at least to alveolus of s-gen. Postmaxillary (p-max.) slender, about as long as m.cl. Para-gular (pa-gul.) long, slender, slightly shorter than s-gen., reaching beyond posterior ventral margin of head. In addition, there are three micro-setae (cervicals, cer.) immediately posterior to the ventro-lateral margin of the head capsule.

Sensillation: there are normally 20 sensilla on each side of the head capsule; positions variable, but typically as in figures 1–3.

Labrum (figures 4, 5): a broadly semicircular disc, projecting antero-ventrally. Dorsal (anterior) face (figure 4) smooth, gradually becoming reticulate in front; each half with one long seta and four short to minute setae; two basiconic sensilla, one campaniform sensillum near the base of the long seta. The anteriormost basiconic sensilla may appear on the ventral surface, especially in isolated mouthparts. There is a single, somewhat larger campaniform sensillum (?) medially. Ventral (oral) face (figure 5) with a broad band of spines, long and thin laterally, short and stout medially; each half with a group of three basiconic sensilla submedially, one basiconic sensillum medially, and two campaniform sensilla among the spines.

Mandible (figure 6): usually with six (range five to seven) distinct teeth on the dorsal margin, distal tooth largest; two setae basally, one long, one minute; two campaniform sensilla above the setae.

Maxilla (figures 8, 9): with a long, slender basal apodeme directed posteriorly. Cardo: ventral surface with one long and one short seta, and a campaniform sensillum near each; one campaniform sensillum on sclerotized ring between cardo and stipes. Stipes: ventral face with one short seta; four basiconic sensilla along and among marginal spines; dorsal face with a dense patch of short, stout spines medially, extending over margin to ventral face; one campaniform sensillum among the spines. A short, blunt antero-lateral lobe. Maxillary palp of two segments: basal segment conical, with one small seta and one campaniform sensillum ventrally; distal segment cylindrical, about two-thirds diameter of basal segment, truncate, with four minute, terminal, basiconic sensilla.

Hypopharynx: an elongated lobe extending anteriorly between the maxillae; tip deflected ventrally, with a pair of minute setae.

Labial palp: very short, cylindrical; with four processes, two short and stout, two about twice as long, slender.

Antenna (figure 7): shaft: cylindrical and elongated, basal third slightly swollen; sense organ near apex, apparently with two internal chambers; a single, long axial seta, slightly less than half the length of the shaft; a corona of four basiconic sensilla. Mound: papillae a, b, a, b and a, together with c and d, subtending approxi-

1 1 2 2 3

mately 150° along lateral aspect; e on medial side of mound; papillae, type B of Bacot and Ridewood (1914); a –a short (# 12 m m), conical, occasionally with

1 3

convex sides and terminal filament, b and b much shorter than a –a.

1 2 1 3

ment (Ab. 1). (12) Ventral view, left half. (13) Dorsal view, left half. (14) Lateral view.

D, dorsal plate; DL, dorso-lateral plate; VL, ventro-lateral plate; V, ventral plate.

Setae: a –a, anterior row; d –d, dorsal; dl, dorso-lateral; vl, ventro-lateral; v, ventral;

1 6 1 3

v, (outer) ventral; v, (inner) ventral; m, micro-seta. Scale bar: 0.3 mm.

1 2

Thorax (figures 12–14)

Th. I. Dorsal plate, D, covering much of dorsal surface, reaching over sides of segment. Spiracle at an indentation at postero-lateral edge of D.

Setation: anterior row: five slender setae, a –a; a, a, and a very short, fine;

1 5 1 2 3 a short, a nearly twice as long; a, a stouter; a –a on D. Posterior row: D with 5 4 4 5 1 3 three long, slender dorsal setae, d, d and d; ventro-lateral plate, VL, with one

1 2 3 ventro-lateral seta, vl, as long as d; ventral plate, V, with one ventral seta, v, long,

3 nearly three-quarters the length of vl. One ventral micro-seta antero-dorsal to vl, near margin of segment.

Sensillation: D with two sensilla in each of anterior and posterior rows, medially of a, a, and of d, d.

1 2 1 2

Th. II–III. D limited to dorsal surface; dorso-lateral plate, DL, present. No spiracles. Setation: anterior row: five short, slender setae; a longest; a, a on D, a on

4 1 2 3 DL, a between DL and VL, a between VL and V. Posterior row: D with two

4 5 setae, d, d; DL, VL and V each with one seta, respectively dl, vl and v; d, d, dl

1 2 1 2 and vl long and slender, reaching beyond posterior margin of next segment; v shorter but more than half the length of vl, reaching well beyond end of segment. Microsetae: an irregular row of six towards the anterior margin of each segment. Sensillation: D with one sensillum in anterior row, medially of a; two sensilla

1 in posterior row as for Th. I.

Abdomen (figures 12–16)

Ab. 1–7 (figures 12–14). D narrower than on Th. II–III. Spiracle in an indentation of antero-medial margin of DL.

Setation and sensillation: anterior row: six short, slender setae, a –a; similar in

1 6 length; a on D, lateral to sensillum, length more than half the distance to alveolus

1 of d; a antero-ventral to spiracle; a slightly anterior to a and a; a between VL

1 2 3 2 4 5 and V; a slightly medial to V. Posterior row: d very long, reaching beyond next

6 1 segment; d, dl and vl slightly shorter; V with two setae, v slightly shorter than vl;

2 1 v about half the length of v. Micro-setae: an irregular row of five towards the 2 1 anterior margin of each segment. Sensilla as in Th. II–III.

Ab. 8. D as on Ab. 1–7. Spiracle as on Ab. 1–7.

Setation and sensillation: anterior row: a –a slender; relative positions of a and 1 6 1

a –a as on Ab. 1–7, but a antero-dorsal to spiracle. Posterior row: d, d and dl 3 6 2 1 2 somewhat stouter than on previous segments, very long, reaching beyond tips of anal struts; vl long, reaching nearly to posterior margin of Ab. 9. V with v shorter, but reaching alveolus of v on Ab. 9. Note: in common with most known Ceratophyllus spp. larvae (except Ce. styx riparius and Ce. styx freyi Nordberg, 1935 (Pilgrim and Galloway, 2000)), V on Ab. 8 usually carries only one v seta; in Ce. hirundinis two such setae are not infrequent—in 130 larvae (260 intact V plates) among all instars, there were: v + v bilaterally (five larvae), v + v unilaterally (41 larvae), a single v 1 2 1 2

seta (84 larvae). Seta v, where present, is about half the length of v. Micro-setae 2 1

and sensilla as on Ab. 1–7.

Ab. 9. D as on Ab. 1–8. No spiracle.

Setation and sensillation: anterior row: five slender setae, a –a; a, a as on Ab. 1 5 1 2

1–7, a between DL and VL, a between VL and V, a directly anterior to, or 3 4 5

slightly medial of, V. Posterior row: d, d, d and dl thickened and extremely long, 1 2 3

extending well beyond tips of anal struts; vl shorter, extending to nearly the base of anal struts; v shortest, reaching beyond mid-length of Ab. 10. Three micro-setae towards anterior margin of segment; one dorsal, approximately in line with a, two 1 ventral, approximately in line with a, a. Sensilla as on Ab. 1–8.

4 5

Ab. 10 (figures 15, 16). With two weakly sclerotized, dorso-lateral plates which almost meet mid-dorsally, and a single median ventral plate. No spiracle.

Setation and sensillation: each side with three stout ventro-lateral setae, v-l: two on dorso-lateral plate, upper seta reaching or surpassing tip of anal strut, lower seta reaching about mid-length of strut; one on ventral plate not surpassing mid-length of strut; one micro-seta near anterior margin of dorso-lateral plate; antero-ventral seta, a-v, variable in length, often reaching to at least v-l row; post-ctenidial seta, pct, very short, slender, just behind lateral portion of anal comb. Anal comb of two discrete rows: anterior row usually of two (rarely one or three) short setae on each side; posterior row of five or six (rarely seven) short setae on each side, in a single, slightly irregular row. One sensillum anterior to a-v.

Anal strut and anal mound: strut finger-like, tip bluntly rounded, slightly curved ventrally; a lightly sclerotized strip on dorsal surface, extending forward on to anal mound; one sensillum on ventral surface of each strut; each mound with five (rarely three, four or six) short setae in a single row.

First instar larva

As L except as follows. Egg burster (figures 10, 11): approximately one-third II-III

the length of the head capsule, rear end at posterior margin of the head capsule; sole-shaped, a distinct, blunt egg tooth at about anterior fourth. Antenna: shaft uniform in diameter, shorter than in later instars, but axial seta more than half the shaft length.

Material examined

UK. Scotland, Grampian: Collieston, NK 0328, 28 September 1987, ex D. urbica nests on sea cliff, D. K. Mardon and R. W. Marriott, 1 L (+1 X; also adults and

II-III larvae Ce. rusticus , adults Ce. f. farreni , adult and larvae Ca. waterstoni ; adults and larvae F. laeta ). England, Leicestershire: Queniborough, SK6412, October 1977, ex D. urbica nest, F. Clark and D. A. C. McNeil, 7 L (+55 WW, 78 XX; also adults

II-III

Ce. f. farreni , see Clark and McNeil, 1981: 17); Birstall, SK5908, October 1984, ex D. urbica nest on building, F. Clark and D. A. C. McNeil, 1 L, 10 L (+25 WW, I II-III

56 XX; also larva Ce. rusticus , adults Ce. f. farreni ). Lincolnshire: Stoke Rochford, SK9127, 7 November 1990, ex D. urbica nest on building, F. Clark, 2 L, 12 L II-III III exuviae ex cocoons containing 5 WW, 7 XX Ce. hirundinis (+26 WW, 32 XX; also adults and larvae Ce. rusticus ); November 1991, ex D. urbica artificial nest, F. Clark, 6 L III exuviae ex cocoons containing 4 WW, 2 XX Ce. hirundinis (+1 X; also adult Ce. f. farreni , adult Ceratophyllus (Emmareus) garei Rothschild ). Buckinghamshire: Slough, SU 9779, 14 September 1964, ex D. urbica nest, ‘D. G.’ per M. J. Cotton, 4 L, 1 L (+12 WW, 16 XX; also adults Ce. rusticus , adults Ce. f. farreni ). Cornwall: I II-III

Hayle, SW5637, autumn 1979, ex D. urbica nest on building, F. Clark and D. A. C. McNeil, 3 L, 5 L (+44 WW, 50 XX; also adults Ce. f. farreni , see Clark and I II-III

McNeil, 1984: 60). Essex: Little Maplestead, TL 8233, 2 mi. NNE of Halstead , 10 September 1990, ex D. urbica nest on building, R. S. George, 10 L, 5 L

I II-III (+85 WW, 165 XX; also adults and larvae Ce. f. farreni ). Norway, Hedmark: Kongsvinger , 17 June 1967, ex D. urbica nest , R. Mehl, 1 L, 3 L (also adults I II-III

Ce. hirundinis , adults Ce. rusticus , adults Ce. f. farreni ). Spain, Badajoz, June 1997, ex D. urbica nests on building, S. Merino, 5 L, 7 L, and 4 L exuviae ex cocoons I II-III III

(+6 WW, 5 XX). France, Savoie: Valloire, 12 July 1910, ex Hirundo rustica nest, K. Jordan, 3 L (+2 WW, 3 XX; also adults Ce. rusticus, BMNH 1923 –615). Haute- II-III

Alpes: Freissinières , Cirque de Dormillouse, ‘sur voûte rocheuse’, ca 1500 m, 6 September 1966, ex D. urbica nest, J.-C. Beaucournu, 1 L (+ 16 adults, many II-III

larvae; also adults Ce. rusticus ); 29 August 1979, ex D. urbica nest, 7 L (+26 II-III adults; also adults and larvae Ce. rusticus , adults F. laeta ). Lozère: Meyrueis, Gorges de la Jonte, ‘sur paroi rocheuse’, ca 750 m, August 1973, ex D. urbica nest, J.-C. Beaucournu, 1 L (+ ca 100 adults; also adults Ce. rusticus ). Meurthe-et-Moselle: III

Longuyon, Buré d’Orval, 10 August 1932, ex D. urbica nest, Heim de Balsac, 4 L II-III (+many adults). Germany, Mark (now= Brandenburg): Cablow (=Kablow), 30 August 1936, ex Chelidon (= Delichon ) urbica nest, E. Otten, 1 L, 2 L (+adults, I II-III

BMNH 1923–615 ) and 6 L (+1 W, 1 X, DEI) ; Eberswalde, 24 July 1989, ex D. II-III

urbica nest, C. Kutzscher, 1 L (+7 WW, 2 XX, DEI); 29 July 1990, ex D. urbica nest, III

C. Kutzscher, 1 L (+3 XX, DEI). Switzerland, Vaud: Commugny , 19 July 1964, ex III

D. urbica nest, J. Steffen, 1 L, 4 L ( BMNH 1964–753). Italy, Basilicata: Potenza, I II-III

Viggiano, 22 July 1969, ex ‘ Hirundo rustica (?)’ nest (suspected lapsus calami for D. urbica , see Mei, 1996: 546), V. Vomero, 5 L (+6 WW, 10 XX). Poland, Kuźnice, II-III

near Zakopane, 20 September 1969, ex D. urbica nest, K. Bartkowska, 2 L, 6 L; I II-III Resko, 9 October 1990, ex H. rustica nest, S. Kaczmarek, 2 L. Slovakia, Trnava , II-III

27 June 1985, ex D. urbica nest ND 315/85, D. Cyprich and M. Krumpál, 1 L, 3 I

L (also adults Ce. rusticus ); 25 August 1985, ex D. urbica nest ND 404/85, D. II-III

Cyprich and M. Krumpál, 4 L (+adults); Opatová, near Váhom, 24 September II-III

1985, ex D. urbica nest ND 218/85, D. Cyprich and M. Krumpál, 5 L (also adults II-III

Ce. rusticus ); Staré Hory, 17 September 1989, ex D. urbica nest ND 245/89, D. Cyprich and M. Krumpál, 2 L (also larvae Ce. rusticus ). Russia, Caucasus , no II-III

data, 2 L, 3 L.

I II-III

Remarks

Ceratophyllus hirundinis is a widespread and commonly collected parasite of the House Martin in Great Britain and Ireland (George, 1974; Clark and McNeil, 1981, 1984) and in much of Europe and parts of central Asia (Haddow et al., 1983). It has considerable tolerance for different habitats, artificial and natural, and may be found in nests on buildings and cliffs (Smit, 1957) from sea coasts to inland sites up to 2500 m (Beaucournu and Launay, 1990). Collections of larval exuviae in association with adults in cocoons from Lincolnshire (Stoke Rochford) provided absolute confidence in the identification of this species. The distinctive anal comb and arrangement of anal mound setae separate Ce. hirundinis from other species associated with House Martins in Great Britain. We include specimens from a variety of locations outside of Great Britain under Material examined, where adult Ce. hirundinis were present in the same nests, and where no species other than those considered in this paper are expected to occur. We include the specimens from Caucasus with some reservation; these five larvae were remounted from a single slide provided by the Anti-plague Institute of the Caucasus and Transcaucasus in Stavropol’, Russia. The only other information on the slide is ‘ Ceratophyllus hirundinis ’. We believe these specimens may be some of those reported by Karandina (1964), and which would have been reared from eggs obtained from identified adults (Karandina, 1964: 476–477, 485).

Karandina (1964) was the first to provide details of the larva of Ce. hirundinis . The numbers of setae she reported in the anal comb and on the anal mound agree with those found here. She also provided data on the relative lengths of some setae on the head and abdomen, but did not include illustrations of any aspect of Ce. hirundinis .

Kir’yakova (1965: 221) reported differences between larvae of Ce. gallinae and larvae taken from D. urbica nests in Ryazan Province, Russia, in which associated adults were Ce. delichoni and Ce. hirundinis . She distinguished two species of larvae, designating as ‘ Ceratophyllus (s. str.) hirundinis (?) Sam., 1819’ the one with two pairs of setae in the anterior comb row, and five or six setae on each anal mound. This clearly agrees with our findings, and we support her suggested identification. We have not seen larvae of Ce. delichoni , but the characters she gives for her ‘ Ceratophyllus (s. str.) delichoni (?) Nordb, 1935’ larvae cannot be construed as those of Ce. hirundinis .

Ye (1990: figures 26a.36, 26b.15) illustrated the egg burster of what she believed to be Ce. hirundinis , but indicated that it was possibly that of Ceratophyllus caliotes Jordan, 1937 . We have not seen the first instar larva of Ce. caliotes , but in our material of Ce. hirundinis the shape of the egg burster was variable. In dorsal view, there was often a weakly stained area anteriorly, extending forward, so that the anterior margin of the plate was not always easily determined. At the posterior end, the margin of the plate was usually faintly distinguishable.