Two new species of Echinostoma (Digenea: Echinostomatidae) from Argentinean bird

Dos nuevas especies de Echinostoma (Digenea: Echinostomatidae) en aves argentinas

Head collar reniform, well developed, muscular, 251-387 long by 386-531 wide (316 × 441). Collar spines large, 35 in number; with following arrangement: 4 angle spines on each lappet (2 ventral and 2 dorsal), 59-90 × 17-21; 8 lateral spines in single row on each side, 71-83 × 17-19, and 11 dorsal spines in double row, 60-79 × 17-19. This collar spines can be included in the third model proposed by Kanev et al. (2009), i.e., 4 angle spines on each side, 10 lateral spines on each side, 2 additional spines on each side and 3 mid-dorsal spines (1 oral-sinistra, 1 aboral-central, 1 oral-dextra), i.e. [4+10+2+3+2+10+4] (Fig. 2).

Oral sucker ventro-subterminal, spherical, muscular, 106-140 × 121-155 (127 × 140). Ventral sucker well developed, muscular, cup-shaped, with deep cavity, located in the first quarter of body, 561-793 × 445-561 (708 × 513). Sucker width ratio 1: 3.6-3.7 (3.6). Prepharynx short, 0-53 (26); pharynx muscular, elongate, longer than oral sucker, 130-164 × 72-126 (153 × 104). Ratio of oral sucker width to pharynx width 1: 1.2-1.4 (1.3). Oesophagus 314-396 (349) long. Intestinal bifurcation closer to ventral sucker; caeca blind, overlapped by vitelline follicles, reaching fairly close to posterior extremity of body.

Testes 2, tandem, elongate-oval, irregular in outline, contiguous or slightly separated, located in the third quarter of body; anterior testis, 483-609 × 338-387 (544 × 354); posterior testis, 609-677 × 319-362 (638 × 340). Post-testicular field long, 1.6-1.7 mm. (T% = 29-31). Cirrus-sac elongate-oval, located dorsally, between anterior margin and mid-level of ventral sucker, 416-483 × 290-314 (445 × 298), contains internal seminal vesicle with saccular posterior portion and elongate anterior portion, strongly developed pars prostatica; pars prostatica well developed; cirrus tubular and unspined (Fig. 3). Genital pore median, anterior to ventral sucker.

Ovary small, entire, slightly transversely oval, located second quarter of body, 203-217 × 242-271 (211 × 256). Mehlis’gland median, contiguous with ovary, 193-285 × 285-290 (238 × 288). Laurer’s canal short. Uterus short, intercaecal, 0.706-1.04 mm (U% = 15-19). Metraterm long, muscular. Eggs numerous, 82-97 × 48-53 (90 × 49). Ratio of egg length to body length 1: 57-68. Vitellarium follicular, forming 2 lateral non-confluent fields, located between posterior margin of ventral sucker to near posterior extremity of body. Excretory vesicle Y-shaped; pore terminal.

Taxonomic summary

Type–host: Guira guira (Gmelin) (Cuculiformes, Cuculidae).

Site of infection: intestine.

Type–locality: La Marcela farm (26°17’35” S, 59°08’38” W), Pirané, Formosa Province, Argentina.

Date of collection: May 2005, September 2009, April 2015.

Specimens studied: holotype MLP-He 7206; paratypes MLP-He 7207 (6 specimens).

Prevalence: 50%.

Mean intensity: 3.

Etymology: the specific name, “guirae” refers to the specific name of the host.

Remarks

In the Neotropical Region, 4 species possessing 35 collar spines as the new species described herein have been recorded: Echinostoma discinctum Dietz, 1909, Echinostoma uncatum Dietz, 1909, Echinostoma crotophagae Gomes de Faria, 1909 and Echinostoma parvum Lutz, 1925.

Echinostoma discinctum, parasite of Cacicus solitarius Vieillot (Passeriformes, Icteridae) from Brazil (Dietz, 1910), was considered as member of Echinoparyphium Dietz 1909 by Yamaguti (1971); we agree with the last author because the collar of this species has 35 spines arranged in a double row. Based on this trait we separate it of E. guirae n. sp.

Echinostoma uncatum has been reported in cuculid birds: Crotophaga major Gmelin and Crotophaga ani L. from Brazil and Piaya cayana (L.) and C. ani from Venezuela (Dietz, 1910; Lutz, 1925; Travassos, 1922). This species has been described and illustrated by Dietz (1910) with 35 spines, 27 arranged all in double row and 4 angle spines on each side. This species differs of E. guirae n. sp. by the arrangement of collar spines and in most metrical characters and relative proportions showed in Table 1.

Echinostoma crotophagae has been described by Gomes de Faria (1909) parasitizing C. major from Brazil. Viana (1924) listed this species as synonym of E. uncatum, without any discussion, probably because it was described parasitizing C. major from the same country. Travassos et al. (1969) and Fernandes et al. (2015) considered both species as synonyms. Yamaguti (1971) maintained as a valid species to E. crotophagae. We agree with the last author because the collar was described with 32-36 collar spines all in single row, while E. uncatum was described with collar spines arranged all in double row. Furthermore, Rodrigues and Rodrigues (1981) studied specimens of E. uncatum from G. guira deposited of the Helminthological Collection of the Oswaldo Cruz Institute (CHIOC) and described 32-34 collar spines in a single row. We regarded these specimens belonging to E. crotophagae because both species have a similar arrangement of collar spines. This species mainly differs from E. guirae n. sp. by the arrangement of collar spines. Also differs in most metrical characters and relative proportions (Table 1).

Lutz (1925) briefly described Echinostoma parvum based on young worms experimentally obtained in Columba livia Gmelin (Columbidae) from Venezuela. The description of this species is incomplete, because only mentioned the presence of 35 collar spines but their arrangement is not described or illustrated. Therefore, the comparison between E. parvum and E. guirae n. sp. was not possible.

The species of Echinostoma reported previously in Argentina can be easily distinguished from E. guirae n. sp. based on the different number of collar spines: E. platensis

(39-42), E. mendax (37), E. revolutum (37), E. rodriguesi (37), E. chloephagae (36-37), and E. parcespinosum (31-33).

Considering the differences in the distribution and number of collar spines, a new species, Echinostoma guirae n. sp. is proposed.

Echinostoma jacanae n. sp. (Figs. 4-6; Table 2)

Description based on 7 specimens: Body small, elongate, (BW% = 9-11), with maximum width at level of ventral sucker, 3.8-5.2 (4.5) mm long by 355-486 (432) wide. Forebody long, 909-1286 (1057) (FO% = 22-25). Tegument armed with spines.

Head collar reniform, well developed, 179-198 long by 238-271 wide (187 × 258), bearing 45 spines of similar size, with following arrangement: 4 angle spines on each lappet (2 ventral and 2 dorsal), 33-38 × 10; 3 lateral spines in single row on each side, 45 × 10-12, and 31 dorsal spines in double row, 38-41 × 11-12. This collar spines can be included in the eighth model proposed by Kanev et al. (2009), i.e. 4 angle spines on each side, 10 lateral spines on each side, 7 additional spines on each side, 3 mid-dorsal spines (1 oral-sinistra, 1 aboral-central, 1 oral-dextra), i.e. [4+10+7+3+7+10+4] (Fig. 5)

Oral sucker ventro-subterminal, 55-71 × 88-112 (65 × 96). Ventral sucker well developed, muscular, spherical, with shallow cavity, located between first and second quarter of body, 242-329 × 242-333 (291 × 286). Sucker width ratio 1: 2.8-3.8 (1: 3.3). Prepharynx short 45-60 (55); pharynx, muscular elongate-oval, 69-93 × 69-90 (79 × 75); oesophagus long, 604-807 (691); intestinal bifurcation anterior to ventral sucker; caeca blind, overlapped by vitelline follicles, reach fairly close to posterior extremity of body. Ratio of oral sucker width to pharynx width 1: 1.2-1.3.

Testes 2, tandem, smooth, elongate-oval, slightly separated; anterior testis, 290-413 × 174-244 (341 × 216); posterior testis, 309-483 × 174-290 (382 × 222). Post-testicular field long, 754-1160 (944) (T% = 19-24). Genital pore median, post-bifurcal. Cirrus-sac elongate-oval, located dorsally between level of intestinal bifurcation and anterior margin of ventral sucker, 193-386 × 101-169 (265-138), contains simple elongate seminal vesicle, pars prostatica, and cirrus with smooth surface (Fig. 6).

Ovary small, entire, oval, just pre-equatorial 152-246 × 121-217 (205 × 176). Mehlis’ gland median, contiguous with ovary. Laurer’s canal short, opening on dorsal surface immediately posterior to ovary. Uterus intercaecal, long, 0.754-1.13 (0.969) mm (U% = 20-25). Metraterm weakly-muscular. Eggs numerous, 82-97 × 48-59 (88 × 51). Ratio of egg length to body length 1: 44-97 (66). Vitellarium follicular, forming 2 lateral non-confluent fields of large and small follicles overlapping caeca; fields extend from to about half distance between ventral sucker and ovary to near posterior extremity of body.

Excretory vesicle not seen; excretory pore terminal.

Taxonomic summary

Type-host: Jacana jacana (L.) (Charadriiformes, Jacanidae)

Site of infection: intestine

Type-locality: Punta Blanca (34°57’0” S; 57°40’0” W), Buenos Aires Province, Argentina.

Date of collection: September 1994.

Specimens studied: holotype MLP-He, 3729/1; paratypes MLP-He 3728/1 (1 specimen), 3729/2 (3 specimens); voucher specimens MLP-He 3729/3 (2 specimens).

Table 2

Comparative measurements of Echinostoma jacanae n. sp. with related species.

Species	Echinostoma jacanae n. sp.	Echinostoma siticulosum	Echinostoma exile	Echinostoma attenuatum
Source	Present study	Dietz (1910)	Kohn and Fernandes (1975)	Alves-Pinto and Melo (2012)	Lumsden and Zischke (1963)
Hosts	Natural Jacana jacana	Natural Crypturellus undulatus Crypturellus variegatus Crypturellus noctivagus	E×perimental Columba livia Porphyrio martinicus	E×perimental Columba livia	Natural Rallus elegans Rallus longirostris
Country	Argentina	Brazil	Brazil	Brazil	USA
Bl (mm)	3.83-5.20	5.5-7.5	2.89-5.91	4.56-6.93	7.22-11.2
Bw	355-486	700-940	630-900	702-1,390	885-1,590
Hcl	179-198	—	—	—	—
Hcw	238-271	430-480	—	—	425-743
Cs	45	41, 43, 45	43-45	45	45
As	33-38 × 10	60-115 × 19-26	21-54 × 9-14	40-50 × —	53-106 × 14-28
Ls	45 × 10-12	74-95 × 14-20	56-95 × 14-22	—	—
Ds	38-41 × 11-12	53-87 × 14-20	—	—	—
OS	55-71 × 88-112	170-200 × 140-150	90-120 × 90-140	116-150 × 123-171	166-256 × 140-256
VS	242-329 × 242-333	560-590 × 470-500	460-620 × 400-760	409-717 × 430-717	0.673-1.333 mm
VS/OS	1: 2.8-3.8	1: 3.3-3.4*	1: 3.2-5.1	1: 3.5-4.2*	1: 3.6
PL	45-60	60-170	—	—	short
Ph	69-93 × 69-90	116-130 × 88-102	90-130 × 90-110	89-184 × 61-137	128-217 × 102-153
OeL	604-807	530-570	130-230	205-239	243-448
CS	193-386 × 101-169	308-492 × 215-292	190-500 × 110-200	102-211 × 177-375	371-896 × 153-425
AT	290-413 × 174-244	830-1350 × 215-385	210-700 × 150-350	389-819 × 212-375	814-1345 × 212-566
PT	309-483 × 174-290	190-730 × 130-320	382-887 × 191-321	956-1,593 × 177-531
Ov	152-246 × 121-217	260-380 × 200-370	60 -310 × 160-220	116-320 × 116-375	204-422 × 179-435
E	82-97 × 48-59	94-103 × 50-55	93-121 × 56-65	101-111 × 63-75	90-115 × 50-67
Fb (mm)	0.91-1.29	—	0.525-0.659*	—	0.512-1.097
DVS-O (mm)	0.754-1.13	—	1.08-1.25*	—	1.1-1.95
PTF (mm)	0.75-1.16	—	1.40-1.43*	—	2.52*
BW%	9-11	13*	14-16*	—	11.9*
FO%	22-25	17*	10-12*	—	9.4*
U%	20-25	22*	20-23*	—	15*
T%	19-24	12*	25-26*	—	36*

* Calculated from original descriptions or estimated from the published drawing.

 

Etymology: the specific name, “jacanae” refers to the specific name of the host.

Remarks

So far, 3 species belonging to Echinostoma with 45 collar spines have been described in American birds: Echinostoma siticulosum Dietz, 1909 found parasitizing tinamiform birds from Brazil, Crypturellus undulatus (Temminck) (as Tinamus u.), Crypturellus variegatus (Gmelin) (as Tinamus v.) and Crypturellus noctivagus (Wied-Neuwied) [as Tinamus ? n. (Max.)] (Dietz, 1910); Echinostoma exile Lutz, 1924 described in Brazil based on experimental hosts, Columba livia and Porphyrio martinicus (L.) (Rallidae) (Alves-Pinto & Melo, 2012; Kohn & Fernandes, 1975; Lutz, 1924); and Echinostoma attenuatum Lumsden and Zischke, 1963 found parasitizing Rallus elegans Audubon, and Rallus longirostris Boddaert (Rallidae) from USA (Bates & Meade, 1972; Heard, 1970;
Lumsden & Zischke, 1963; Underwood & Dronen, 1986).

Echinostoma exile has morphological characteristics compatible with E. jacanae n. sp.; however, differs in the arrangement of spines collar (5 angle spines on each side + 33 or 35 spines in a double row). Moreover, the specimens of E. exile described by Kohn and Fernandes (1975) and Alves-Pinto and Melo (2012) can be differentiated of the new species by having larger suckers, shorter oesophagus, larger eggs and shorter forebody (notably short vs. long) (Table 2).

Echinostoma attenuatum includes specimens with a collar spines similar to those of the specimens here studied, but differs by having a forebody notably short (FO%: 9.4 vs. 22-25), uterus short (U%: 15 vs. 20-25), post-testicular field very long (T%: 36 vs. 19-24), as well as the dimensions of body size, spines, suckers, oesophagus, cirrus sac, testes, and ovary (Table 2).

Echinostoma siticulosum was described by Dietz (1910) with 41, 43 or 45 spines; 4 angle spines on each side and the remaining (33, 35 or 37) arranged in a double row. Mendheim (1940) re-described these specimens finding 43 spines in most of them, 41 in two specimens, and not mentioned the existence of 45 collar spines; however, this author agrees with the distribution pattern provided by Dietz (1910). Echinostoma siticulosum mainly differs of E. jacanae n. sp. by the disposition of collar spines. Also differs in most metrical characters and relative proportions (Table 2).

Three other species of Echinostoma with 45 spines have been described in the Palaearctic, Oriental and Australasian Regions: Echinostoma australasianum Nicoll, 1914, in Antigone rubicunda (Perry) (as Antigone australasiana) from North Queensland Australia, with collar spines arranged in two uninterrupted rows (see Nicoll, 1914); Echinostoma coromandum Odening, 1962 in Bubulcus ibis coromandus (Boddaert) from Berlin Zoological Garden, originally from India, with collar spines apparently in single row and 4 spines in each ventral lappet (see Odening 1962, Fig. 16b), and Echinostoma gotoi Ando and Ozaki, 1923 in anatid birds and mammals from Asia with collar spines in a double row, not interrupted, with 6 spines in each ventral lappet (see MacDonald, 1981, Fig. 31.24). These species can be easily differentiated from E. jacanae n. sp. by the arrangement of collar spines (a single row in E. coromandum and a double row in E. australasianum and E. gotoi).

Based on all these morphological and morphometric differences, a new species: Echinostoma jacanae n. sp., is proposed.

Discussion

Kostadinova (2005) characterized the genus Echinostoma by possessing a collar composed by 31-55 spines, with lateral spines arranged in single row, dorsal spines in double row and 5 angle spines on each side. Kanev et al. (2009) considered that the number of spines in this genus is uneven, varying among 31-51, with 4 angle spines; these authors consider that even number of spines in this genus reflect specimens with spines lost, retracted, or supernumerary. These last authors provided 11 arrangement models of collar spines, highlighting that these are identical in larval and adult forms.

The arrangement of collar spines in E. uncatum, E. crotophagae, E. exile, E. siticulosum, E. australasianum, E. gotoi and E. coromandum is different to that established by Kostadinova (2005) for Echinostoma. In E. uncatum, E. siticulosum, E. exile, E. gotoi and E. australasianum dorsal and lateral spines are disposed in a double row. This arrangement is similar to that provided by Kostadinova (2005) for Echinoparyphium. However, this genus is also characterized by having a forebody long to extremely long (FO% >20), a post-testicular field short (T% = 15-30), and a uterus short to very short (U% = 3-20), with few eggs. Therefore, further researches are necessary on these 4 species to evaluate its accurate taxonomic position, since some its relative proportions, does not correspond to the diagnosis of genus.

Echinostoma crotophagae and E. coromandum have an uninterrupted collar spines, with dorsal and lateral spines in a single row. Both characters of E. crotophagae are similar to those provided by Kostadinova (2005) for Longicollia Bykhovskaya-Pavlovskaya, 1954, but the remaining diagnostic traits differ considerably. Finally, the number and arrangement of collar spines of E. coromandum is not coincident with any genus of the family. Considering all the differences referred above respecting to the number and pattern of collar spines established for Echinostoma by Kostadinova (2005), we believe necessary further studies on them, in order to clarify their real taxonomic position.

Echinostoma parvum is here regarded as species inquirenda, given that only is mentioned the presence of 35 collar spines and the arrangement of collar spines is not described or illustrated.

Acknowledgments

The authors express their gratitude to Luis Pagano for assistance in collecting the hosts, to Sonia Fontana, Thomas Giesecke and Lyudmila Shumilovskikh for their invaluable help for obtaining and translations of some papers in German and Russian, to Luis García Prieto for his constructive comments on the manuscript. Fabiana B. Drago and Verónica Núñez are members of the “Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CIC). The present study was funded by CIC (Res. Nº 048/16) and UNLP (11/N 751).

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