Strigea proteolytica, Drago, Fabiana B., Lunaschi, Lía I. & Draghi, Regina, 2014

Drago, Fabiana B., Lunaschi, Lía I. & Draghi, Regina, 2014, Digenean fauna in raptors from northeastern Argentina, with the description of a new species of Strigea (Digenea: Strigeidae), Zootaxa 3785 (2), pp. 258-270 : 259-263

Strigea proteolytica n. sp.

( Figs. 1–4 ; Tables 2 , 3 )

Type host: Buteogallus urubitinga (Gmelin) , great black-hawk ( Accipitridae )

Site of infection: small intestine.

Type locality: La Marcela farm (26°17’35”S; 59°06’38”W), Pirané, Formosa Province, Argentina.

Type material: Holotype MLP 6709; paratypes, MLP 6710 (6 specimens).

Voucher specimens: MLP 6711 (4 specimens).

Prevalence: 3 of 4 (75 %).

Mean intensity: 8.3 (1–13).

Etymology: The specific name refers to its large and conspicuous proteolytic gland.

Description: Based on 12 specimens. Body plump, distinctly bipartite, 1.789–2.305 (1.992) mm long. Forebody cup-shaped, with a large opening, 580–1000 (756) long by 725–861 (803) wide; dorsal wall armed with minute, densely arranged tegumental spines. Hindbody subcylindrical, strongly curved dorsally, without true neck region, 1.064–1.518 (1.237) mm long by 561–667 (598) wide. Ratio of forebody length to hindbody length 1:1.2– 2.6 (1.7). Oral sucker elliptical, well developed, terminal, usually projecting from opening, 83–143 (124) long by 106–145 (131) wide. Ventral sucker round to elliptical, well developed, always larger than oral sucker, located in second half of forebody, 207–266 (225) long by 190–275 (235) wide. Suckers width ratio 1:1.5–2.1 (1.8). Prepharynx short; pharynx elliptical, immediately posterior to oral sucker, 129–167 (143) long by 105–136 (122) wide; esophagus present; ceca not discernible. Ratio of oral sucker width to pharynx width 1:0.8–1.1 (1). Pseudosuckers absent. Holdfast organ lobes usually projected from opening. Proteolytic gland multilobed, large, conspicuous, situated at base of forebody, usually displaced toward the dorsal wall, with some lobes overlapping ventral sucker, 112–290 (228) long by 248–410 (320) wide. Testes tandem, entire, occupying middle third of hindbody; anterior testis 193–338 (267) long by 294–386 (341) wide; posterior testis 159–386 (281) long by 217– 425 (340) wide. Seminal vesicle long, folded on itself, posterior to posterior testis. Copulatory bursa poorly delimited, 217–425 (303) long by 241–430 (309) wide; genital atrium, 143–242 (192) in depth; genital cone well delimited from body parenchyma, strongly muscular, obliquely oriented, 202–275 (244) long by 143–290 (224) wide; ejaculatory duct and uterus join at base of genital cone forming a broad hermaphroditic duct. Muscular ring (Ringnapf) well developed and conspicuous. Ratio of genital cone length to hindbody length 1:4–6 (5). Preovarian region occupying 12%–24% of hindbody. Ovary bilobed, 97–150 (124) long by 179–251 (215) wide, located at 130–314 (233) from junction of fore– and hindbody. Laurer’s canal short, opening dorsally between ovary and anterior testis. Vitelline follicles similar in size in both parts of body; in forebody invading principally the ventral lobe of holdfast organ, while in body wall dispersed, with few follicles in area of intersegmental constriction and in equatorial region; in hindbody occupying almost entire width in pre–ovarian region, extending ventrally to testes, up to the genital cone region. Mehlis’ gland and vitelline reservoir in intertesticular region. Uterus ventral, containing 1–40 large eggs, 81–112 (100) long by 45–62 (54) wide, some with eye–spotted miracidia. Ratio of egg length to body length 1:17–26 (20). Ratio of egg length to genital cone length 1: 1.9–5.7 (3.6). Excretory vesicle and pore, not observed.

Remarks: At present, in the Neotropical region 14 species of Strigea Abildgaard, 1790 have been reported parasitizing strigiform, ciconiiform, falconiform, caprimulgiform, passeriform, gruiform, trogoniform and anseriform birds (see Lunaschi & Drago 2013). Among these species, only 3 of them share with S. proteolytica n. sp. the body shape, the absence of true neck region in hindbody and the distribution of vitelline follicles in forebody, which are scarce and extend into the lobes of the holdfast organ. These species are Strigea vaginata (Brandes) Szidat, 1928 from Cathartidae , Falconidae , Accipitridae , Cariamidae , Threskiornithidae and Anatidae from Argentina, Brazil, Colombia, Cuba and Venezuela ( Dubois 1968, Drago & Lunaschi 2011b), Strigea falconis brasiliana from Accipitridae , Falconidae Cathartidae and Phalacrocoracidae from Cuba, Brazil, Venezuela and Argentina ( Dubois 1968, Lunaschi & Drago 2006, 2009a, Drago et al. 2011) and Strigea inflecta Lunaschi & Drago, 2012 from Cariama cristata (L.) ( Cariamidae ) from Argentina ( Lunaschi & Drago 2012). Strigea vaginata ( Table 2 ) can be easily distinguished from S. proteolytica n. sp. by being larger (up to 7000 vs. 1789–2305), by having a proteolytic gland with two flaps that penetrate in the hindbody, and an enormous genital cone, that can reach up to half the length of the hindbody (480– 2000 x 300–900 vs. 202–275 x 143–290). Strigea falconis brasiliana ( Table 2 ) differs mainly from the specimens here studied by having a slender hindbody, testes lobed, smaller proteolytic gland (105–130 x 120–190 vs. 112–290 x 248–410), forebody (319–590 x 314–700 vs. 580– 1000 x 725–861) and pharynx (73–95 x 48 –95 vs. 129–167 x 105–136). Strigea inflecta ( Table 2 ) can be distinguished from S. proteolytica n. sp. by the absence of muscular ring (Ringnapf), by having a larger genital cone (372–459 x 203–319 vs. 202–275 x 143–290), smaller proteolytic gland (72–121 x 121–174 vs. 112–290 x 248–410) and ratio Hi/Gc (2.4–3.1 vs. 4–6).

Three species of the genus reported parasitizing accipitrid birds from others zoogeographical regions are similar to the new species by having scarce vitelline glands in forebody: Strigea sarcogyponis ( Vidyarthi, 1937) Dubois, 1966 reported in Sarcogyps calvus (Scopoli) by Vidyarthi (1937) and Accipiter badius (Gmelin) by Gupta & Mishra (1976) from India; Strigea macroconophora Dubois & Rausch, 1950 reported in Buteo jamaicensis borealis (Gmelin) and Buteo platypterus (Vieillot) by Dubois & Rausch (1950) from USA and Strigea subglandulosa Dubois & Beverley-Burton, 1971 described parasitizing Circus ranivorus (Daudin) by Dubois & Beverley-Burton (1971) from Zambia. Strigea sarcogyponis ( Table 3 ) differs from the new species mainly by being larger (up to 5000 vs. 1789–2305), by having a medium opening, a true neck region (37%–50% of hindbody), a proteolytic gland situated in intersegmental region and multilobed testes. Strigea macroconophora ( Table 3 ) can be Calculated from original descriptions; ** Buteo albicaudatus Vieillot , Buteo jamaicensis umbrinus Bangs , R. magnirostris , Spizaetus ornatus (Daudin) ; *** Caracara plancus

Miller), Herpetotheres cachinnans (L.). Abbreviations (used also in Table 3 ): At—anterior testis; B—body length; Cb—copulatory bursa; E—eggs; Fo—forebody; Ga—genital

atrium; Gc—genital cone; Hi—hindbody; O—ovary; Os—oral sucker; Pg—proteolytic gland; Ph—pharynx; Pt—posterior testis; Vs—ventral sucker; B/E—body length/egg

length; Gc/E—genital cone length/egg length; Hi/Fo—hindbody length/forebody length; Hi/Gc—hindbody length/genital cone length; Ph /Os—pharynx width /oral sucker width;

/Os—suckers width ratio.

Species Strigea proteolytica n. sp. Strigea sarcogyponis Strigea macroconophora S . subglandulosa

Country Argentina India USA Zambia Hosts Buteogallus urubitinga Sarcogyps calvus Accipiter badius Buteo jamaicensis borealis Circus ranivorus Buteo platypterus

Calculated from original descriptions; ** In parentheses measurements of specimens from A. badius originally described as Srigea thapari Gupta & Mishra, 1976, and

synonymized with S. sarcogyponis by Dubois (1982). See Table 2 for abbreviations.

distinguished from S. proteolytica n. sp. by having a forebody with a narrow opening, a proteolytic gland situated in the intersegmental region and deeply lobed testes, smaller ventral sucker (190–200 x 140–160 vs. 207–266 x 190–275) and pharynx (100–119 in diam vs. 129–167 x 105–136), and larger anterior testis (370–600 x 430–600 vs. 193–338 x 294–386), posterior testis (360–510 x 440–595 vs. 159–386 x 217–425) and genital cone (340–660 x 405–510 vs. 202–275 x 143–290). Finally, Strigea subglandulosa differs from the new species in most of the metrical characters ( Table 3 ), and by possessing deeply lobed testes.

Figures

FIGURES 1 – 3. Strigea proteolytica n. sp. from Buteogallus urubitinga. 1. Holotype, entire worm, scale bar = 250 µm. 2. Paratype, entire worm, scale bar = 300 µm. 3. Paratype, enlarged view of terminal genitalia, scale bar = 200 µm. Abbreviations: cb, copulatory bursa; dlHo, dorsal lobe of holdfast organ; gc, genital cone; hd, hermaphroditic duct; mr, muscular ring; s, spermatozoids; sv, seminal vesicle; T, testis; u, uterus; vf, vitelline follicles; vlHo, ventral lobe of holdfast organ.

FIGURES 4 – 11. Digeneans from raptors. 4. Strigea proteolytica n. sp. from Buteogallus urubitinga, scale bar = 250 µm. 5. Strigea falconis brasiliana Szidat, 1929 from Caracara plancus, scale bar = 250 µm. 6. Neodiplostomum travassosi Dubois, 1937 from Buteogallus meridionalis, scale bar = 200 µm. 7. Tylodelphys brevis Drago & Lunaschi, 2008 from Busarellus nigricollis, scale bar = 100 µm. 8. Posthodiplostomum macrocotyle Dubois, 1937 from B. nigricollis, scale bar 200 µm. 9. Enlarged view of copulatory bursa of P. macrocotyle, scale bar 50 µm. 10. Spaniometra variolaris (Fuhrmann, 1904) from R. sociabilis, scale bar 500 µm. 11. Megalophallus deblocki Kostadinova, Vaucher & Gibson, 2006 from R. sociabilis, scale bar 100 µm. Abbreviations: B, body wall; Gc, genital cone; P, prepuce.

Tables

TABLE 2. Comparative data for Strigea proteolytica n. sp. and related species of the Neotropical Region.

Species Strigea proteolytica n. sp. Country Argentina	Strigea vaginata Brazil, Venezuela	Cuba	Strigea falconis brasiliana Brazil, Cuba Argentina	Strigea inflecta Argentina
Source Present study B 1789–2305	Dubois (1968) up to 7000	Dubois & Macko (1972) up to 5600	Dubois (1968) Lunaschi & Drago (2006) up to 2500 1305–1392	Lunaschi & Drago (2012) 1605–1982
Fo 580–1000 x 725–861	680–1280 x 540–1070	740–1360 x 700–1300	380–590 x 420–700 319–415 x 314–367	561–754 x 783–1006
Hi 1064–1518 x 561–667	1160–1940 x 580–1290	1170–4240 x 580–1120	1110–1830 x 340–580 890–1073 x 362–435	967–1257 x 532–841
Os 83–143 x 106–145	115–210 x 100–210	110–170 x 100–150	100–125 x 85–115 76 x 55	183–241 x 126–155
Vs 207–266 x 190–275	165–296 x 133–285	185–280 x 160–240	160–235 x 140–200 152–162 x 71–105	179–290 x 174–256
Ph 129–167 x 105–136	96–165 x 100–165	105–150 x 90–145	73–95 x 70–95 74 x 48	140–169 x 109–126
Pg 112–290 x 248–410	––––	190-270 x 210-370	105–130 x 120–190 ––––	72–121 x 121–174
O 97–150 x 179–251	100–350 x 140–360	100–230 x 200–380	110–200 x 175–300 59–68 x 101–107	111–237 x 155–222
At 193–338 x 294–386	180–620 x 320–630	210–500 x 290–750	235–360 x 235–410 169–227 x 174–190	135–232 x 401–483
Pt 159–386 x 217–425	230–600 x 340–660	220–500 x 350–710	275–370 x 235–420 197–217 x 179–241	150–193 x 338–483
Cb 217–425 x 241–430	––––	––––	–––– 183–241 x 215–226	314–435 x 483–652
Gc 202–275 x 143–290	580–2000 x 300–900	480–1500 x 350–875	240–350 x 220–310 128–167 x 129–143	372–459 x 203–319
Ga 143–242	––––	––––	–––– ––––	232–290
E 81–112 x 45–62	80–106 x 46–65	99–104 x 57–70	67–91 x 42–55 82–88 x 48–52	86–111 x 50–58
Hi/Fo 1.2–2.6	1.5–2.5	1.5–3.1	1.9–3.6 2.1–3.4	1.5–1.7
Vs/Os 1.5–2.1	1.3–1.4*	1.6*	1.6–1.7* 1.9	1.4–2.1
Ph/Os 0.8–1.1	0.8–1*	0.9–1*	0.8* 0.9*	0.8–0.9*
B/E 17–26	66–88*	54–57*	27–37* 15–17*	16–19
Hi/Gc 4–6	––––	2.4–2.8*	4.6–5.2* 6.4–7*	2.4–3.1
Gc/E 1.9–5.7	7-19*	5–15*	3–5* 1.5–2*	3.5–4.8
Hosts Buteogallus urubitinga	Cathartes aura aura (L.)	Cathartes aura aura	Accipitridae ** Rupornis magnirostris Falconidae ***	Cariama cristata

TABLE 3. Comparative data for Strigea proteolytica n. sp. and related species of the Oriental, Holarctic and Ethiopian Regions.

Source B	Present study 1789–2305	Dubois (1968) up to 5000	Gupta & Mishra (1976)** 3190 (2900–3470)	Dubois (1968) up to 3100	Dubois & Beverley-Burton (1971) 1040–1340
Fo	580–1000 x 725–861	1400–1580 x 1260–1390	1010 x 830 (660–810 x 680–790)	600–810 x 730–1050	400–470 x 450–580
Hi Os	1064–1518 x 561–667 83–143 x 106–145	3420–3640 x 1020–1190 180–190 x 190–205	2180 x 580 (2120–2710 x 510–580) 100 x 140 (75–85 x 100–125)	1410–2340 x 750–900 100–153 x 85–120	640–960 x 360–560 105–130 x 80–105
Vs	207–266 x 190–275	250–285 in diam.	225 x 240 (180–225 x 190–235)	190–200 x 140–160	135–185 x 90–160
Ph	129–167 x 105–136	128–133 x 92–96	105 x 127 (100–125 x 100–130)	100–119 in diam.	60–84 x 68–86
Pg	112–290 x 248–410	320 x 480	325 x 410 (175–185 x 220–300)	––––	100–155 x 180–245
O	97–150 x 179–251	260 x 340	150 x 240 (190–235 x 150–250)	130–190 x 250–270	60–120 x 125–220
At	193–338 x 294–386	460 x 770	290 x 532 (325–425 x 340–425)	370–600 x 430–600	100–200 x 210–330
Pt	159–386 x 217–425	460–595 x 790	390 x 570 (360–490 x 400–490)	360–510 x 440–595	130–270 x 205–330
Cb Gc	217–425 x 241–430 202–275 x 143–290	–––– ––––	–––– ––––	–––– 340–660 x 405–510	–––– 120–160 x 100–120
Ga	143–242	––––	––––	225–405	140–220
E	81–112 x 45–62	115–120 x 68–70	(87–90 x 70–80)	90–99 x 63–70	85–94 x 52–63
Hi/Fo Vs/Os	1.2–2.6 1.5–2.1	2.6–2.7 1.3–1.4*	2.16(2.7–3.9) 1.7(1.9)*	2.9–3.1 (2.3–2.6, in contracted specimens) 1.3–1.6*	1.5–2.3 1.1–1.5*
Ph/Os	0.8–1.1	0.5*	0.9(0.96–1)*	0.99–1.4*	0.8–0.9*
B/E	17–26	42–43*	(32–40)*	31–34*	11–16*
Hi/Gc Gc/E	4–6 1.9–5.7	–––– ––––	–––– ––––	3.5–4.1* 3–7*	5.3–6* 1.3–1.9*