Amphipsyllinae Ioff, 1936

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 : 493-499

Amphipsyllinae Ioff, 1936 Frontopsylla (Orfrontia) laeta (Jordan and Rothschild, 1920) (figures 18, 25, 26, 30–41)

Description

Head (figures 30–32): Widest posteriorly, slightly longer than wide in slidemounted specimens; head capsule covered with fine, polygonal reticulation, most obvious over gular regions. Coronal suture relatively long, ca one-third the length of head behind the antennal mounds.

Setation: there are normally 17 acicular setae on each side of the head capsule. Parietals (par.): outermost long, near front end of coronal suture; innermost very short, between outermost and coronal suture; one minute, well anteriorly along frontal suture. Occipitals: anterior (a.occ.) on the posterior margin of the head capsule; posterior (p.occ.) minute, postero-laterally of a.occ. Frontal (fr.) slender, not reaching half way to alveolus of outermost par. Inter-antennal (i-ant.) very short, fine. Clypeals: medial (m.cl.) slightly longer than basal diameter of antennal shaft; lateral (l.cl.) less than half the length of antennal shaft. Post-antennal (p-ant.) length greater than diameter of antennal shaft. Genals: posterior (p.gen.) long, slender, about as long as outermost par.; anterior (a.gen.) short, surpassing alveolus of p.gen. Sub-genal (s-gen.) long, slender, about half the length of p.gen. Post-clypeal (p-cl.) about equal to m.cl. Post-mandibular (p-man.) long, slender, reaching almost to alveolus of s-gen. Post-maxillary (p-max.) very short, about equal to m.cl. Paragular (pa-gul.) long, slender, reaching beyond postero-ventral margin of head capsule. In addition, there are three cervical setae (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 30–32.

Labrum (figures 33, 34): a short, broad disc, projecting antero-ventrally, basal sclerite a well-developed broad band. Dorsal (anterior) face (figure 33) lightly reticulate; each half with one long seta, one short seta basally and one minute seta anteromedially; four basiconic sensilla distally, of which the antero-medial and anterolateral are distinctly pointed, remainder blunt; one campaniform sensillum medial to the long seta. There is a single campaniform sensillum (?) medially. Ventral (oral) face (figure 34) covered with short, fine and rather sparse spines medially and posteriorly, and with long, coarse and very dense spines laterally; each half with one basiconic sensillum medially and two campaniform sensilla.

Mandible (figure 35): with three to six distinct, blunt teeth, apical and second prominent, larger than remainder, basal tooth smallest, sometimes no more than a small bump; two setae basally, ventral seta at least twice the length of dorsal; two campaniform sensilla above setae.

Maxilla (figures 37, 38): with a long, slender basal apodeme directed posteriorly. Cardo: dorsal surface with a dense patch of short, stout spines medially, extending on to stipes and over to ventral surface; one campaniform sensillum dorsally among the spines; ventral surface with one long and one short seta, a campaniform sensillum near each; one campaniform sensillum on sclerotized ring between cardo and stipes. Stipes: shorter than cardo; ventral surface with one short seta, four basiconic sensilla along and among marginal spines. Antero-lateral lobe not conspicuous. Maxillary palp of two cylindrical segments; basal segment with one small seta and one campaniform sensillum ventrally; distal segment slightly more than half 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 36): shaft: cylindrical, elongated, basal third slightly swollen; sense organ near apex, apparently with two inner chambers; a single, long axial seta, 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 approximately 150° 1 1 2 2 3

along lateral aspect; e on medial side of mound; papillae, type B of Bacot and Ridewood (1914), a –a short (# 12 m m), conical, straight-sided or lightly convex, 1 3

with faint markings and occasionally with a terminal filament; b and b much 1 2 shorter than a –a.

1 3

Thorax (figures 39–41)

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

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

1 2 3 4 nearly twice as long as a –a; a short; a –a on D. Posterior row: D with three

1 3 5 1 3 long, slender setae, d, d and d; VL with one seta, vl, slender, shorter than d; V

1 2 3 3 with one short seta, v, less than one-quarter the length of vl. One ventral micro-seta antero-dorsal to vl, near margin of the 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; DL present. No spiracles. Setation: anterior row of five slender setae, a –a, mostly longer than on Th. I;

1 5 a longest. Posterior row: d, d, dl and vl long and slender; v very short, less than 4 1 2 one-quarter the length of vl. Micro-setae: 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 on Th. I.

Abdomen (figures 39–41)

Ab. 1–7. D narrower than on Th. II–III. Spiracle in an indentation of anteromedial margin of DL.

Setation and sensillation: anterior row of six short, slender setae, a –a, similar 1 6

in length; a on D, lateral to sensillum; a antero-ventral to spiracle; a slightly 1 2 3 anterior to a and a; a between VL and V; a slightly medial to V. Posterior row: 2 4 5 6

d very long, slender; d, dl and vl slightly shorter; v at least as long as vl; v less 1 2 1 2 than half the length of v. Micro-setae: an irregular row of five towards anterior 1

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, and reaching to or beyond tips of anal struts; vl long, reaching anterior row setae on Ab. 9; v shorter, nearly reaching alveoli of anterior row setae on Ab. 9. Micro-setae and sensilla as on Ab. 1–7.

Ab. 9. D as on Ab. 1–8. No spiracle.

Setation and sensillation: anterior row of five slender setae, a –a; positions of 1 5

a, a as on Ab. 1–7, a between DL and VL, a between VL and V, a directly 1 2 3 4 5 anterior to, or slightly medial of V. Posterior row: d, d, d and dl thickened and 1 2 3

extremely long, extending well beyond tips of anal struts; vl shorter, extending approximately to mid-length of Ab. 10; v shortest, not reaching mid-length of Ab. 10. Three micro-setae towards anterior margin of segment: one dorsal, about in line with a, two ventral, about in line with a, a. Sensilla as in Ab. 1–8.

1 4 5

Ab. 10 (figure 18). 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 nearly reaching tip of anal strut, lower reaching about mid-length; 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 but usually not reaching v-l setae; post-ctenidial seta (p-ct) very short, slender, just behind lateral portion of anal comb. Anal comb usually distinguishable as two discrete rows: anterior row of four to eight short setae each side; posterior row of 8–13 short setae each side. One sensillum antero-lateral to a-v seta.

Anal strut and anal mound: strut finger-like, tip bluntly rounded, slightly curved ventrally, a lightly sclerotized, spined strip on dorsal surface extending forward on to mound; one sensillum on ventral surface of each strut; each mound with 17–21 long and short setae in an irregular band two to three setae across.

First instar larva

Egg burster (figures 25, 26): approximately one-third the length of head capsule, rear end at posterior margin of head capsule; sole-shaped with a bluntly rounded egg tooth, sometimes slightly projecting, at about anterior fourth. Outermost and innermost parietal setae about midway along length of egg burster plate at its margin; the minute, anteriormost parietal alongside frontal suture, near front end of the egg burster plate.

Antenna: shaft slightly constricted distally, shorter than in later instars, but axial seta about half the length of shaft.

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, 2 L, 1 pharate L

I II-III III (+10 WW, 14 XX; also adult and larva Ce. hirundinis , adults and larvae Ce. rusticus , adults Ce. f. farreni , adult and larvae Ca. waterstoni ); Sands of Forvie Nature Reserve, ca NK0227, 16 October 1991, ex D. urbica nests on sea cliff, G. M. Dunnet, 1 L, 8 L, 3 L exuviae ex cocoons containing 3 WW F. laeta (+72 WW, 182 XX; also I II-III III

adults and larvae Ce. rusticus , adults and larvae Ca. waterstoni ); North Broadhaven Bay, NK0328, 3 October 1994, ex D. urbica nests on sea cliff, R. M. Laing, 1 L, 1

I

L, 1 L exuviae, 7 L exuviae ex cocoons containing 1 W, 6 XX F. laeta (+many II-III III III

adults; also adults and larvae Ce. rusticus , adults and larvae Ca. waterstoni ).

Remarks

Frontopsylla laeta has a very localized, disjunct, distribution occurring in D. urbica nests in Scotland, Eire, Switzerland and nearby localities in France and Italy, also in the Caucasus, at elevations from 10 to 2500 m, mainly in nests on natural rock faces (Smit, 1957; Claassens and O’Rourke, 1966; Beaucournu and Launay, 1990). The unusual disposition of the parietal setae and the relatively long coronal suture (figures 25, 26, 31, 32), together with the few, coarse mandibular teeth, clearly differentiate this larva from all others in D. urbica nests in the region under discussion.

This combination of features is found in other species of Frontopsylla . Karandina (1964: 489, for F. (O.) frontalis (Rothschild, 1909) from near Negram, Nakhichevanskaya ASSR, Azerbaidzhanskaya SSR) in her key, couplet 6(5), referred to ‘1 short [seta] between the dorsal setae of the anterior and posterior rows (fig. 10)’ [our translation]. We have examined 14 larvae of this species obtained from the Anti-plague Institute of the Caucasus and Transcaucasus, Stavropol’, Russia: all labelled ‘Coll: N. F. Darskaya [no locality or date], nest #2, [host=(Chekanplyasun’ya)= Oenanthe isabellina (Isabelline Wheatear) ], Fr. frontalis ’. We confirm the seta as our anteriormost, minute, parietal seta. Karandina (her figure 4g) illustrated the mandible in F. (O.) frontalis , in which the teeth are very similar to those in F. (O.) laeta . It is likely that Karandina’s material included specimens from the same series as those we examined, as she acknowledged N. F. Darskaya among the contributors of her study material. Qi and He (1997) illustrated the similar arrangement of the parietal setae and the mandible (their figures 1 and 5, respectively) for Frontopsylla (Frontopsylla) spadix spadix (Jordan and Rothschild, 1927) . We have also examined larvae of the following, typically mammal fleas, in the subgenus Frontopsylla and find the same two features: F. (Frontopsylla) luculenta Jordan and Rothschild, 1923 (ssp.?) [ Russia, Irkutsk, 10 April 1963, insectary; China, Hohhot, reared, 1991, Liu Jun]; F. (F.) semura Wagner and Ioff, 1926 [ Russia, Stavropol’, reared]; F. (F.) elata caucasica Ioff and Argyropulo, 1934 [Stavropol’, insectary, 11 June 1963; Azerbaidzhan, reared at Stavropol’, 2 November 1966]; Frontopsylla sp. indet., from Microtus carruthersi Thomas nest [ Tadjikistan, Gissar Mts, 10 August 1982, M. A. Kiefer].

The arrangement of the parietal setae and the mandible appear to characterize the genus Frontopsylla , though no larvae have been seen of species in the other two subgenera (also from mammal hosts), namely Profrontia Ioff, 1946 and Mafrontia Ioff, 1949.

Key to known flea larvae found in nests of Delichon urbica in Great Britain Characters in the key apply to all instars unless otherwise specified. Ceratophyllus gallinae (Schrank, 1803) is a common, widely distributed species which has a broad range of bird hosts. It is possible that larvae may be encountered in the nests of D. urbica , and for that reason, it has been included in the key. The most recent description of the larva of Ce. gallinae is by Pilgrim and Galloway (2000).

1 Mandible with three to six coarse teeth; apical and second prominent and larger than

remainder (figure 35). Coronal suture in L long, ca one-third length of head behind

II–III

antennal mounds; the long (outermost) and the short (innermost) parietal setae close together at front end of coronal suture; the minute parietal seta alongside posterior fourth of frontal suture (figures 31, 32). The long and the short parietal setae in L at

I

ca mid-length of egg burster plate; the minute parietal seta near front end of the plate (figures 25, 26).............. Frontopsylla laeta *

– Mandible with 6–13 fine teeth, apical larger than remainder (figures 6, 28). Coronal suture in L short <one-quarter length of head behind antennal mounds; all three

II–III

parietal setae aligned near front end of coronal suture (figures 2, 3, 27). All parietal setae in L aligned approximately with mid-length of egg-burster plate (figure 21).. 2

I

2 Mandible with 10–13 teeth (figure 28). V plates on Ab. 9 each with 2 v setae, v and

1

v (v rarely absent, unilaterally) (figure 29)...... Callopsylla waterstoni * 2 2

– Mandible with 6–11 teeth (figure 6). V plates on Ab. 9 each with a single v seta ( Ceratophyllus spp. ).................. 3

3 Anal comb of two discrete rows, anterior row one to six setae each side; anal mound

setae in a single row (figures 15, 16).............. 4

– Anal comb of two to three irregular rows, more densely arranged in a brush flanking the mid-line; anal mound setae in two to three irregular rows (figure 17).... 5

4 Anterior row of anal comb with two (one to three) setae on each side, posterior row

with total of 10–12 setae; each anal mound with five (three to six) setae (figures 15, 16)..................... C. hirundinis *

– Anterior row of anal comb with four or five (two to six) setae on each side, posterior row with total of 12–20 setae; each anal mound with seven or eight (5–10) setae........................ C. gallinae

5 v setae on Th. II–III of L slender, reaching well beyond posterior margin of their

II-III

segments (figure 19). Thoracic v setae in L do not reach posterior margin of their

I

segment.................. C. rusticus * – v setae on Th. II–III of L stout, not, or barely, reaching beyond posterior margin

II-III

of their segments (figure 20). L not seen†......... C. f. farreni *

I

*True parasites of D. urbica .

†In Ce. f. chaoi, the thoracic v setae do not reach the posterior margin of their segments.