Syst Parasitol (2015) 91:147–155 DOI 10.1007/s11230-015-9567-y
Sharpilosentis peruviensis n. g., n. sp. (Acanthocephala: Diplosentidae) from freshwater catfishes (Siluriformes) in the Amazonia Olga Lisitsyna • Toma´sˇ Scholz • Roman Kuchta
Received: 20 February 2015 / Accepted: 23 March 2015 Ó Springer Science+Business Media Dordrecht 2015
Abstract Sharpilosentis peruviensis n. g., n. sp. is described from the catfishes Duopalatinus cf. peruanus Eigenmann & Allen (type-host) and Oxydoras niger (Valenciennes) in the River Amazon basin, Peru. The new species belongs to the subfamily Diplosentinae Tubangui & Masilungan, 1937 of the family Diplosentidae Tubangui & Masilungan, 1937 because of its possession of an unarmed trunk, a cylindrical proboscis, proboscis hooks arranged in longitudinal rows and two tubular cement glands of the same length in males. Sharpilosentis n. g. differs from the other genera of the Diplosentidae in the morphology of the reproductive system: males have a large muscular penis covered with small tubercles and the vulva of females is devoid of muscular sphincters and the cephalic ganglion is located between the second and third part of the proboscis receptacle. In addition, proboscis hooks are of three types: large hooks with simple roots in the anterior part of the proboscis, transitional 6th hook in one from two adjacent rows with bifurcated root in the distal part and small hooks
O. Lisitsyna Department of Parasitology, Schmalhausen Institute of Zoology, Ukrainian National Academy of Sciences, 15 Bohdan Khmelnitsky Street, Kiev 01601, Ukraine T. Scholz R. Kuchta (&) Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branisˇovska´ 31, 370 05 Cˇeske´ Budeˇjovice, Czech Republic e-mail: [email protected]
without roots in the posterior part of the proboscis. A partial sequence for the mitochondrial cox1 gene is provided for this new taxon. The taxonomic composition of the family Diplosentidae is discussed.
Introduction Acanthocephalans parasitising freshwater fishes in Amazonia are not well known and only 33 species of 15 genera have been reported (Thatcher, 2006). Characiform fishes are most common fish hosts for acanthocephalans in the Neotropical Region, with 18 species reported, whereas only seven species have been found in catfish (Siluriformes) (Santos et al., 2008). In a survey of the helminth parasites of 897 freshwater fish in the Peruvian Amazonia at Iquitos, during six field trips (2004–2011) several acanthocephalans were collected (de Chambrier et al., 2015). The acanthocephalans found in the intestine of catfishes Duopalatinus cf. peruanus Eigenmann & Allen (Pimelodidae) and Oxydoras niger (Valenciennes) (Doradidae) were assigned to the subfamily Diplosentinae Tubangui & Masilungan, 1937 of the family Diplosentidae Tubangui & Masilungan, 1937, but differed significantly from the species of the other genera of the subfamily, i.e. Diplosentis Tubangui & Masilungan, 1937 and Pararhadinorhynchus Johnston & Edmonds, 1947. In this paper we describe
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Sharpilosentis peruviensis n. g., n. sp. and provide morphological evidence for its generic distinction.
Materials and methods Acanthocephalans studied were found during a survey of the helminth parasites carried out by two of the present authors (R. K. and T. S.) in the upper Amazon River basin around Iquitos, Peru, during six field trips between 2004 and 2011 (see, e.g. de Chambrier et al., 2015). Five acanthocephalans were found in Duopalatinus cf. peruanus, which belongs to the so called ‘long-finned clade’ of pimelodid catfishes (personal communication of John G. Lundberg, Curator Emeritus of Ichthyology, Academy of Natural Sciences of Drexel University, Philadelphia, USA on 15 July 2014) from the Rio Nanay in Santa Clara near Iquitos (10.x.2011; host field No. PI 855; 3 specimens) and in Oxydoras niger from the fish market Bele´n in Iquitos, Peru (4.x.2011; PI 774; 2 specimens). The worms were relaxed in water in refrigerator and then fixed in 4% formalin solution under slight pressure; one specimen was fixed in 96% ethanol. Morphology of the acanthocephalans was studied on temporary total mounts cleared in Berlese’s medium using a compound Zeiss Axio Imager M1 microscope equipped with DIC optics. Drawings were made with the aid of a drawing tube. All measurements are in micrometres unless indicated otherwise. The anterior and posterior part of one female specimen fixed in ethanol was prepared for SEM following the procedure outlined by Kuchta & Caira (2010); the middle part was used for isolation of DNA following the protocol of Georgieva et al. (2013) and sequencing of the partial cytochrome c oxidase subunit 1 (cox1) mitochondrial gene. Partial fragments of the cox1 gene were amplified using the primers of Folmer et al. (1994) (forward: 50 -AGT TCT AAT CAT AA(R) GAT AT(Y) GG-30 ; reverse: 50 -TAA ACT TCA GGG TGA CCA AAA AAT CA-30 ). Polymerase chain reaction (PCR) amplifications were performed with illustra puReTaq Ready-To-Go PCR beads (GE Healthcare, UK) in a total volume of 25 ll (10 pmol of each primer). Cycling conditions were as follows: denaturation at 94°C for 5 min followed by 35 cycles (denaturation at 94°C for 1 min, annealing at 40°C for 1 min, and extension at 72°C for 1 min) and a final extension step at 72°C for 5 min. PCR amplicons were
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purified directly using Qiagen QIAquickTM PCR purification Kit (Qiagen Ltd, UK) and sequenced from both strands using the same primers. Sequencing was conducted on an ABI Prism 3130xl automated sequencer using ABI Big Dye chemistry (ABI PerkinElmer) according to the manufacturer’s protocol. Contiguous sequence was assembled with Mega v.6 (Tamura et al., 2013) and submitted to GenBank. Family Diplosentidae Tubangui & Masilungan, 1937 Subfamily Diplosentinae Tubangui & Masilungan, 1937 Sharpilosentis n. g. Diagnosis Diplosentidae, Diplosentinae with characters described by Tubangui & Masilungan (1937) and Golvan (1969). Trunk smooth, unarmed, cylindrical. Proboscis cylindrical. Neck short. Proboscis hooks in longitudinal rows. Hooks of three types: (i) large hooks with simple roots in anterior part of proboscis; (ii) transitional 6th hook (only in one of two adjacent rows) with bifurcated root in the distal part; and (iii) small hooks without roots in posterior part of proboscis. Proboscis receptacle double-walled. Cephalic ganglion located between second and third part of proboscis receptacle. Lemnisci tubular, shorter than proboscis receptacle. Lacunar system comprises two large longitudinal lateral canals, connected by transverse anastomoses parallel to each other. Ligament sac single. Reproductive organs in posterior half of trunk. Testes in tandem. Cement glands two, tubular, of same length, parallel, just posterior to posterior testis. Penis large, muscular, surface with small tubercles. Vulva without muscular sphincters. Eggs unknown. Genital pore subterminal in males, terminal in females. Typespecies: Sharpilosentis peruviensis n. sp. Etymology: The genus is named in honour of the late Viktor Sharpilo (Schmalhausen Institute of Zoology, Kyiv, Ukraine) in recognition of his fundamental contribution to helminthology, especially to helminth parasites of reptiles and their life-cycles. Sharpilosentis peruviensis n. sp. Type-host: Duopalatinus cf. peruanus (Eigenmann & Allen) (Siluriformes: Pimelodidae) (see Remarks).
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Other host: Oxydoras niger (Valenciennes) (Siluriformes: Doradidae), ripsaw catfish. Prevalence: Ex D. cf. peruanus: single infected host examined; ex O. niger: 6% (1 out of 16 fish). Intensity of infection: 2–3 worms. Type-locality: Rio Nanay at Santa Clara near Iquitos, Amazon River basin, Loreto, Peru (3°470 400 S; 73°200 2500 W). Other localities: Fish market in Bele´n, Loreto, Iquitos, Peru (fish probably collected around Iquitos, River Amazon basin). Type-material: Holotype and one paratype are deposited in the Helminthological Collection of the Institute of Parasitology, Biology Centre of the Czech ˇ eske´ Budeˇjovice, Czech Academy of Sciences, C Republic (Coll. No. IPCAS A-87); one paratype is deposited in the collection of the Schmalhausen Institute of Zoology, Ukrainian National Academy of Sciences, Kyiv, Ukraine (Coll. No. AP2.1). Etymology: The species is named after the country of its origin. Representative sequence: Sequence of the partial mitochondrial cox1 gene of one specimen from the type-host is available in GenBank (Accession No. KP967562). Description (Figs. 1A–D, 2A–E, 3A–F) General [Based on 4 specimens examined by light microscopy and 1 examined by SEM.] Trunk covered with smooth pores (Fig. 3F), cylindrical. Males and females similar in length. Proboscis cylindrical, with short neck and 21–24 longitudinal rows of hooks, 11–12 hooks in each row. Hook rows begin at different levels in alternating manner. First 5–6 (regularly alternating) hooks with long blades and roots directed backward. Roots of first 5 hooks simple, root of 6th hook (only in 1 from 2 adjacent rows) bifurcated in distal part (Figs. 1C, 2A); the following 6 hooks in each row narrow, rootless. Angle of blades of these hooks gradually increasing from hook 7 to hooks 11–12, making blades of basal hooks almost perpendicular to vertical axis of proboscis (Figs. 1C, 2A). Surface of hooks with pores (Fig. 3C). Proboscis receptacle cylindrical, double-walled, much longer than proboscis. Cephalic ganglion fusiform, situated between second and third part of proboscis receptacle. Lemnisci shorter
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than proboscis receptacle. Gonopore slightly subterminal in males, terminal in females. Male [Based on 3 mature males: 2 specimens ex Duopalatinus cf. peruanus and 1 specimen ex Oxydoras niger, see Figs. 1A–C, 2A–E. Measurements of the holotype are followed by ranges for the whole series.] Trunk 5.35 (4.67–6.15) mm long, 660 (580–750) wide at mid-length. Proboscis 500 (450–520) long, 340 (270–390) wide at mid-length, armed with 21 (21–24) longitudinal rows of 12 (11–12) hooks each. Hook blade length (hooks on anterior part of proboscis): 1, 46 (45–50); 2, 58 (50–60); 3, 60 (60–63); 4, 60 (63); 5, 68 (68–75); 6, 55–65. Hook root length (hooks on anterior part of proboscis): 1, 38–43 (30–43); 2, 58–63 (58–65); 3, 55–58 (58–60); 4, 58 (58–63); 5, 63 (63–68); 6, 45– 63 (50–63). Hook blade length (hooks on posterior part of proboscis): 7, 50; 8, 38 (40–50); 9, 38 (38–40); 10, 40 (40–43); 11, 40 (40–43); 12, 38. Proboscis receptacle 1.27 (1.08–1.29) mm long, 290 (210–290) wide. Neck 110 (90–120) long. Lemnisci almost equal in length, 650–720 9 120 (460–780 9 100–120). Testes in tandem, almost contiguous, or at distance of 100– 110. Anterior testis 340 9 210 (280–320 9 150–300); posterior testis 310 9 200 (300–340 9 150–260). Cement glands 2, cylindrical, parallel, 470 (400–480) long. Saefftigen’s pouch 780 (560–780) long. Penis large, muscular, 280 (260–280) long in invaginated state; its surface covered with small tubercles (Fig. 2D). Invaginated copulatory bursa 1.43 mm long. Inner surface of bursa with small reticular sculpting (Fig. 2E). Gonopore slightly subterminal. Female [Based on 1 immature (without eggs) female ex O. niger and 1 female ex Duopalatinus cf. peruanus observed by SEM; Figs. 1D, 3A–E.] Trunk 5.6 mm long, 550 wide at mid-length. Proboscis 450 9 300, armed with 24 longitudinal rows of 11–12 hooks in row (every other row). Hook blade length (hooks on anterior part of proboscis): 1, 45–50; 2, 55–68; 3, 63– 68; 4, 63–68; 5, 63–73; 6, 63. Hook root length (hooks on anterior part of proboscis): 1, 25–30; 2, 53; 3, 58; 4, 60; 5, 65; 6, 65. Hook blade length (hooks on posterior part of proboscis): 7, 50; 8, 45; 9, 43; 10, 40; 11, 40; 12, 38. Proboscis receptacle 1,005 9 220. Neck 50 long. Lemnisci 530–550 long. Reproductive tract, uterine bell to genital pore, 710 long. Vagina with vaginal funnel and vaginal bulb, without muscular sphincters (Fig. 1D). Eggs not observed. Gonopore terminal.
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Fig. 1 Sharpilosentis peruviensis n. sp. ex Duopalatinus cf. peruanus. A, Proboscis of holotype male; B, Total view of holotype male; C, Hooks of a longitudinal row of holotype male; D, Terminal part of female reproductive system. Abbreviations: 1B: CG, cephalic ganglion; T, testis; VE, vas efferens; CGL, cement glands; CD, cement duct; SP, Saefftigen’s pouch; VD, vas deferens; P, penis; BW, bursal wall; GG, genital ganglion; G, gonopore; 1D: UB, uterine bell; U, uterus; VF, vaginal funnel; V, vagina; VB, vaginal bulb; G, gonopore. Scale-bars: A, 500 lm; B, 1 mm; C, 100 lm; D, 500 lm
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Fig. 2 Photomicrographs of Sharpilosentis peruviensis n. sp. ex Duopalatinus cf. peruanus. A, Proboscis of holotype male (arrow indicates bifurcated root of hook 6); B, Detail of male reproductive system with penis; C, Detail of penis with invaginated anterior part; D, Detail of penis surface with small tubercles; E, Detail of inner surface of bursa with small reticular sculpting. Scale-bars: A, B, 200 lm; C, 50 lm; D, E, 20 lm
Remarks The new species can be distinguished from species of other diplosentid genera by the characteristics of the new genus listed above. The type-host is provisionally designated as Duopalatinus cf. peruanus but its precise identification is not possible because of taxonomic problems of species of the so called ‘long-finned clade’ of pimelodid catfishes (John G. Lundberg, personal communication). Host tissue fixed with 99% ethanol has been deposited in the collection of Institute of Parasitology, AS CR for future genotyping; a picture of the fish host of field number PI 855 is available at http://tapewormdb.uconn. edu/index.php/hosts/specimen_search/teleost.
The partial sequence of the cox1 mitochondrial gene (602 bp long) for the new species is provided for future comparisons. At present, no further conclusions could be made on the species relationships due to the lack of sequence data on the diplosentid acanthocephalans.
Discussion Both fish hosts of Sharpilosentis peruviensis n. sp., Duopalatinus cf. peruanus and Oxydoras niger, are widely distributed in South America (Reis et al., 2003). These catfishes belong to different families but occur together in white waters, mostly in large rivers. The only acanthocephalan known from doradid catfish
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Fig. 3 Scanning electron micrographs of Sharpilosentis peruviensis n. sp. ex Duopalatinus cf. peruanus, female. A, Proboscis; B, Detail of hooks on the central part of the proboscis; C, Detail of hook surface (arrow indicates pores on the surface of the hook proboscis); D, Detail of hooks on posterior part of proboscis; E, Posterior part of the body; F, Detail of the posterior body surface. Small letters in Fig. 3B, E correspond to the figures showing higher magnification images of these surfaces. Scale-bars: A, 100 lm; B, D, E, 10 lm; C, F, 1 lm
is Paracavisoma impudica (Diesing, 1851) of the family Cavisomidae Meyer, 1932, reported from O. niger and O. kneri Bleeker (see Eiras et al., 1995; Tantalea´n et al., 2005; Kohn et al., 2011). The family Diplosentidae was erected by Tubangui & Masilungan (1937) to accommodate Diplosentis
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amphacanthi Tubangui & Masilungan, 1937 from the white spotted rabbitfish Siganus canaliculatus (Park). Golvan (1969) divided the family into two subfamilies, the monotypic Allorhadinorhynchinae Golvan, 1969 with species of Allorhadinorhynchus Yamaguti, 1959 possessing spines on the trunk, and
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Diplosentinae for species of the genera Diplosentis and Pararhadinorhynchus with unarmed trunk (Golvan, 1969). Pichelin & Cribb (2001) considered some of the main diagnostic characteristics of the Diplosentidae to be controversial, including the number of cement glands in D. amphacanthi, the type-species of Diplosentis. They transferred Diplosentis to the family Cavisomidae, the members of which possess four cement glands, and erected a new family Transvenidae Pichelin & Cribb, 2001 and included the genera Pararhadinorhynchus Johnston & Edmonds, 1947, Transvena Pichelin & Cribb, 2001 and Trajectura Pichelin & Cribb, 2001 with two cement glands into this family. Amin (2013) did not support the taxonomic rearrangement of Pichelin & Cribb (2001) and recognised the validity of the family Diplosentidae, but left two genera, Transvena and Trajectura, in the family Transvenidae. We accept the taxonomic structure of the family Diplosentidae according to the latest classification of acanthocephalans (Amin, 2013) with some modifications: the subfamily Allorhadinorhynchinae is considered to include the genera Allorhadinorhynchus and Amapacanthus Salgado-Maldonado & Santos, 2000 [Amin (2013) placed the latter genus to the Diplosentinae] and the subfamily Diplosentinae including the genera Diplosentis and Pararhadinorhynchus. Inclusion of the genus Golvanorhynchus Noronha, Fabio & Pinto, 1978 with six cement glands into this family is unconvincing. Smales (2012) placed the genus Golvanorhynchus in the family Isthmosacanthidae Smales, 2012 and this proposal is followed here. Sharpilosentis n. g. is placed in the subfamily Diplosentinae of the family Diplosentidae because it possesses two cement glands, its proboscis hooks are arranged in longitudinal rows and the body is smooth, unarmed. Sharpilosetntis n. g. can by distinguished by the morphology of the hooks from the two other genera of the subfamily Diplosentinae. Species of the genera Pararhadinorhynchus and Diplosentis have similar hooks, with hook sizes decreasing from the first to the last and most of the hooks in each row possess roots (only 2–4 basal hooks are without roots), whereas proboscis hooks of S. peruviensis n. sp. are of three types: 5–6 large hooks with simple roots, transitional 6th hook in one from two adjacent rows with bifurcated root distally in the anterior part of the proboscis and 6 small hooks without roots in the posterior part of the proboscis (Figs. 1C, 2A). Also,
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the cephalic ganglion of S. peruviensis n. sp. is located between the second and third part of the proboscis receptacle (Fig. 1B), whereas that of the species of Diplosentis is located in the middle of the proboscis receptacle and the cerebral ganglion of the species of the genus Pararhadinorhynchus is situated at the base of the proboscis receptacle. The females of S. peruviensis n. sp. have a vulva lacking muscular sphincters (Fig. 1D), whereas the females of species of the other genera of the subfamily have the vulva with one muscular sphincter (see figure 20 in Johnston & Edmonds, 1947; figure 4 in Edmonds, 1973). The vaginal funnel is not located in the uterus (Fig. 1D), but posterior to the uterus as is/ are sphincter(s) in other species of acanthocephalans (see, e.g. Petrochenko, 1956; Golvan, 1969). In fact, vaginal sphincters seem to be absent in S. peruviensis, even though only an immature female was available and sphincters may be poorly developed in immature worms. However, sphincters are formed already in female cystacanths in intermediate hosts as found in all known cases (see, e.g. figures 1a, 2b and 3a in Lisitsyna & Tkach, 1994 and figure 1a in Lisitsyna, 2011). In addition, the males of S. peruviensis n. sp. have a large muscular penis covered with small tubercles. Morphological features of the penis of species of Diplosentis and Pararhadinorhynchus have not been described, but judging from the figures (figures 1 and 2 in Tubangui & Masilungan, 1937; figures 12 and 18 in Johnston & Edmonds, 1947; figure 3 in Edmonds, 1973; figure 1 in Gupta & Fatma, 1979), they may not be comparable in magnitude with those on the penis of the species of S. peruviensis n. sp. Pores on the surface of hook blades of S. peruviensis (Fig. 3C) are not unique characteristics of the species. Numerous pores on the outer surface of the hook have been observed also in Acanthocephalus lucii (Mu¨ller, 1776) (see Bra´zova´ et al., 2014). Previously, Miller & Dunagan (1985) described small grooves on the greater curvature on the surface of hook blades of Macracanthorhynchus hirudinaceus (Pallas, 1781) that extended for approximately half of the exposed position of the blade. These authors speculated that these structures are involved in secretory activities. Surface striations of hook blade were also observed in Dentitruncus truttae Sinzar, 1955 by Dezfuli et al. (2008) who assumed that such striations may help in a more effective attachment to the host’s intestine. It is possible that pores on the surface of
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hook blades of S. peruviensis have some secretory function. Pores on the tegumental surface similar to those observed in the present material have also been described in Acanthocephalus ranae (Schrank, 1788), A. lucii (Mu¨ller, 1776), Pomphorhynchus spindetrancatus Amin, Abdullaphah & Mhaisan, 2003 and Acanthogyrus (Acanthosentis) tilapiae (Baylis, 1948) (see Heckmann et al., 2010, 2011; Amin et al., 2011). Acknowledgements Thanks are due to Martin Mortenthaler and his family, Acuario Rı´o Momon, Iquitos, Peru, for providing facilities for fish examination and supplying fish from Santa Clara, Rı´o Nanay, Carlos A. Mendoza-Palmero and Alain de Chambrier for help with fish examination at Iquitos. The authors are much obliged to Simona Georgieva from the Institute of Parasitology who obtained the cox1 sequence for the new species. Support by authorities of the Czech Embassy in Lima, Peru and Peruvian Embassy in Prague, Czech Republic, in particular by Marina Landaveri, Ambassador of Peru in the Czech Republic, is also greatly appreciated. This study was partly supported by the Czech Science Foundation (Project No. P505/12/G112), the Institute of Parasitology, AS CR, Cˇeske´ Budeˇjovice (RVO: 60077344) and the Ukrainian-Czech joint project ‘‘Helminth parasites in aquatic ecosystems: their diversity and life-cycles in the changing world’’.
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155 Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725–2729. Tantalea´n, M., Sa´nchez, L., Go´mez, L., & Huiza, A. (2005). Acanthocephalan from Peru. Revista Peruana de Biologı´a, 12, 83–92. Thatcher, V. E. (2006). Amazon fish parasites (2nd ed.). Sofia Moscow: Pensoft Publishers, 508 pp. Tubangui, M. A., & Masilungan, V. A. (1937). Diplosentis amphacanthi gen. et sp. nov., an Acanthocephala parasitic in a marine fish. Philippine Journal of Science, 62, 183– 189.
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Sharpilosentis peruviensis n. g., n. sp. (Acanthocephala: Diplosentidae) from freshwater catfishes (Siluriformes) in the Amazonia Olga Lisitsyna • Toma´sˇ Scholz • Roman Kuchta
Received: 20 February 2015 / Accepted: 23 March 2015 Ó Springer Science+Business Media Dordrecht 2015
Abstract Sharpilosentis peruviensis n. g., n. sp. is described from the catfishes Duopalatinus cf. peruanus Eigenmann & Allen (type-host) and Oxydoras niger (Valenciennes) in the River Amazon basin, Peru. The new species belongs to the subfamily Diplosentinae Tubangui & Masilungan, 1937 of the family Diplosentidae Tubangui & Masilungan, 1937 because of its possession of an unarmed trunk, a cylindrical proboscis, proboscis hooks arranged in longitudinal rows and two tubular cement glands of the same length in males. Sharpilosentis n. g. differs from the other genera of the Diplosentidae in the morphology of the reproductive system: males have a large muscular penis covered with small tubercles and the vulva of females is devoid of muscular sphincters and the cephalic ganglion is located between the second and third part of the proboscis receptacle. In addition, proboscis hooks are of three types: large hooks with simple roots in the anterior part of the proboscis, transitional 6th hook in one from two adjacent rows with bifurcated root in the distal part and small hooks
O. Lisitsyna Department of Parasitology, Schmalhausen Institute of Zoology, Ukrainian National Academy of Sciences, 15 Bohdan Khmelnitsky Street, Kiev 01601, Ukraine T. Scholz R. Kuchta (&) Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branisˇovska´ 31, 370 05 Cˇeske´ Budeˇjovice, Czech Republic e-mail: [email protected]
without roots in the posterior part of the proboscis. A partial sequence for the mitochondrial cox1 gene is provided for this new taxon. The taxonomic composition of the family Diplosentidae is discussed.
Introduction Acanthocephalans parasitising freshwater fishes in Amazonia are not well known and only 33 species of 15 genera have been reported (Thatcher, 2006). Characiform fishes are most common fish hosts for acanthocephalans in the Neotropical Region, with 18 species reported, whereas only seven species have been found in catfish (Siluriformes) (Santos et al., 2008). In a survey of the helminth parasites of 897 freshwater fish in the Peruvian Amazonia at Iquitos, during six field trips (2004–2011) several acanthocephalans were collected (de Chambrier et al., 2015). The acanthocephalans found in the intestine of catfishes Duopalatinus cf. peruanus Eigenmann & Allen (Pimelodidae) and Oxydoras niger (Valenciennes) (Doradidae) were assigned to the subfamily Diplosentinae Tubangui & Masilungan, 1937 of the family Diplosentidae Tubangui & Masilungan, 1937, but differed significantly from the species of the other genera of the subfamily, i.e. Diplosentis Tubangui & Masilungan, 1937 and Pararhadinorhynchus Johnston & Edmonds, 1947. In this paper we describe
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Sharpilosentis peruviensis n. g., n. sp. and provide morphological evidence for its generic distinction.
Materials and methods Acanthocephalans studied were found during a survey of the helminth parasites carried out by two of the present authors (R. K. and T. S.) in the upper Amazon River basin around Iquitos, Peru, during six field trips between 2004 and 2011 (see, e.g. de Chambrier et al., 2015). Five acanthocephalans were found in Duopalatinus cf. peruanus, which belongs to the so called ‘long-finned clade’ of pimelodid catfishes (personal communication of John G. Lundberg, Curator Emeritus of Ichthyology, Academy of Natural Sciences of Drexel University, Philadelphia, USA on 15 July 2014) from the Rio Nanay in Santa Clara near Iquitos (10.x.2011; host field No. PI 855; 3 specimens) and in Oxydoras niger from the fish market Bele´n in Iquitos, Peru (4.x.2011; PI 774; 2 specimens). The worms were relaxed in water in refrigerator and then fixed in 4% formalin solution under slight pressure; one specimen was fixed in 96% ethanol. Morphology of the acanthocephalans was studied on temporary total mounts cleared in Berlese’s medium using a compound Zeiss Axio Imager M1 microscope equipped with DIC optics. Drawings were made with the aid of a drawing tube. All measurements are in micrometres unless indicated otherwise. The anterior and posterior part of one female specimen fixed in ethanol was prepared for SEM following the procedure outlined by Kuchta & Caira (2010); the middle part was used for isolation of DNA following the protocol of Georgieva et al. (2013) and sequencing of the partial cytochrome c oxidase subunit 1 (cox1) mitochondrial gene. Partial fragments of the cox1 gene were amplified using the primers of Folmer et al. (1994) (forward: 50 -AGT TCT AAT CAT AA(R) GAT AT(Y) GG-30 ; reverse: 50 -TAA ACT TCA GGG TGA CCA AAA AAT CA-30 ). Polymerase chain reaction (PCR) amplifications were performed with illustra puReTaq Ready-To-Go PCR beads (GE Healthcare, UK) in a total volume of 25 ll (10 pmol of each primer). Cycling conditions were as follows: denaturation at 94°C for 5 min followed by 35 cycles (denaturation at 94°C for 1 min, annealing at 40°C for 1 min, and extension at 72°C for 1 min) and a final extension step at 72°C for 5 min. PCR amplicons were
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purified directly using Qiagen QIAquickTM PCR purification Kit (Qiagen Ltd, UK) and sequenced from both strands using the same primers. Sequencing was conducted on an ABI Prism 3130xl automated sequencer using ABI Big Dye chemistry (ABI PerkinElmer) according to the manufacturer’s protocol. Contiguous sequence was assembled with Mega v.6 (Tamura et al., 2013) and submitted to GenBank. Family Diplosentidae Tubangui & Masilungan, 1937 Subfamily Diplosentinae Tubangui & Masilungan, 1937 Sharpilosentis n. g. Diagnosis Diplosentidae, Diplosentinae with characters described by Tubangui & Masilungan (1937) and Golvan (1969). Trunk smooth, unarmed, cylindrical. Proboscis cylindrical. Neck short. Proboscis hooks in longitudinal rows. Hooks of three types: (i) large hooks with simple roots in anterior part of proboscis; (ii) transitional 6th hook (only in one of two adjacent rows) with bifurcated root in the distal part; and (iii) small hooks without roots in posterior part of proboscis. Proboscis receptacle double-walled. Cephalic ganglion located between second and third part of proboscis receptacle. Lemnisci tubular, shorter than proboscis receptacle. Lacunar system comprises two large longitudinal lateral canals, connected by transverse anastomoses parallel to each other. Ligament sac single. Reproductive organs in posterior half of trunk. Testes in tandem. Cement glands two, tubular, of same length, parallel, just posterior to posterior testis. Penis large, muscular, surface with small tubercles. Vulva without muscular sphincters. Eggs unknown. Genital pore subterminal in males, terminal in females. Typespecies: Sharpilosentis peruviensis n. sp. Etymology: The genus is named in honour of the late Viktor Sharpilo (Schmalhausen Institute of Zoology, Kyiv, Ukraine) in recognition of his fundamental contribution to helminthology, especially to helminth parasites of reptiles and their life-cycles. Sharpilosentis peruviensis n. sp. Type-host: Duopalatinus cf. peruanus (Eigenmann & Allen) (Siluriformes: Pimelodidae) (see Remarks).
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Other host: Oxydoras niger (Valenciennes) (Siluriformes: Doradidae), ripsaw catfish. Prevalence: Ex D. cf. peruanus: single infected host examined; ex O. niger: 6% (1 out of 16 fish). Intensity of infection: 2–3 worms. Type-locality: Rio Nanay at Santa Clara near Iquitos, Amazon River basin, Loreto, Peru (3°470 400 S; 73°200 2500 W). Other localities: Fish market in Bele´n, Loreto, Iquitos, Peru (fish probably collected around Iquitos, River Amazon basin). Type-material: Holotype and one paratype are deposited in the Helminthological Collection of the Institute of Parasitology, Biology Centre of the Czech ˇ eske´ Budeˇjovice, Czech Academy of Sciences, C Republic (Coll. No. IPCAS A-87); one paratype is deposited in the collection of the Schmalhausen Institute of Zoology, Ukrainian National Academy of Sciences, Kyiv, Ukraine (Coll. No. AP2.1). Etymology: The species is named after the country of its origin. Representative sequence: Sequence of the partial mitochondrial cox1 gene of one specimen from the type-host is available in GenBank (Accession No. KP967562). Description (Figs. 1A–D, 2A–E, 3A–F) General [Based on 4 specimens examined by light microscopy and 1 examined by SEM.] Trunk covered with smooth pores (Fig. 3F), cylindrical. Males and females similar in length. Proboscis cylindrical, with short neck and 21–24 longitudinal rows of hooks, 11–12 hooks in each row. Hook rows begin at different levels in alternating manner. First 5–6 (regularly alternating) hooks with long blades and roots directed backward. Roots of first 5 hooks simple, root of 6th hook (only in 1 from 2 adjacent rows) bifurcated in distal part (Figs. 1C, 2A); the following 6 hooks in each row narrow, rootless. Angle of blades of these hooks gradually increasing from hook 7 to hooks 11–12, making blades of basal hooks almost perpendicular to vertical axis of proboscis (Figs. 1C, 2A). Surface of hooks with pores (Fig. 3C). Proboscis receptacle cylindrical, double-walled, much longer than proboscis. Cephalic ganglion fusiform, situated between second and third part of proboscis receptacle. Lemnisci shorter
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than proboscis receptacle. Gonopore slightly subterminal in males, terminal in females. Male [Based on 3 mature males: 2 specimens ex Duopalatinus cf. peruanus and 1 specimen ex Oxydoras niger, see Figs. 1A–C, 2A–E. Measurements of the holotype are followed by ranges for the whole series.] Trunk 5.35 (4.67–6.15) mm long, 660 (580–750) wide at mid-length. Proboscis 500 (450–520) long, 340 (270–390) wide at mid-length, armed with 21 (21–24) longitudinal rows of 12 (11–12) hooks each. Hook blade length (hooks on anterior part of proboscis): 1, 46 (45–50); 2, 58 (50–60); 3, 60 (60–63); 4, 60 (63); 5, 68 (68–75); 6, 55–65. Hook root length (hooks on anterior part of proboscis): 1, 38–43 (30–43); 2, 58–63 (58–65); 3, 55–58 (58–60); 4, 58 (58–63); 5, 63 (63–68); 6, 45– 63 (50–63). Hook blade length (hooks on posterior part of proboscis): 7, 50; 8, 38 (40–50); 9, 38 (38–40); 10, 40 (40–43); 11, 40 (40–43); 12, 38. Proboscis receptacle 1.27 (1.08–1.29) mm long, 290 (210–290) wide. Neck 110 (90–120) long. Lemnisci almost equal in length, 650–720 9 120 (460–780 9 100–120). Testes in tandem, almost contiguous, or at distance of 100– 110. Anterior testis 340 9 210 (280–320 9 150–300); posterior testis 310 9 200 (300–340 9 150–260). Cement glands 2, cylindrical, parallel, 470 (400–480) long. Saefftigen’s pouch 780 (560–780) long. Penis large, muscular, 280 (260–280) long in invaginated state; its surface covered with small tubercles (Fig. 2D). Invaginated copulatory bursa 1.43 mm long. Inner surface of bursa with small reticular sculpting (Fig. 2E). Gonopore slightly subterminal. Female [Based on 1 immature (without eggs) female ex O. niger and 1 female ex Duopalatinus cf. peruanus observed by SEM; Figs. 1D, 3A–E.] Trunk 5.6 mm long, 550 wide at mid-length. Proboscis 450 9 300, armed with 24 longitudinal rows of 11–12 hooks in row (every other row). Hook blade length (hooks on anterior part of proboscis): 1, 45–50; 2, 55–68; 3, 63– 68; 4, 63–68; 5, 63–73; 6, 63. Hook root length (hooks on anterior part of proboscis): 1, 25–30; 2, 53; 3, 58; 4, 60; 5, 65; 6, 65. Hook blade length (hooks on posterior part of proboscis): 7, 50; 8, 45; 9, 43; 10, 40; 11, 40; 12, 38. Proboscis receptacle 1,005 9 220. Neck 50 long. Lemnisci 530–550 long. Reproductive tract, uterine bell to genital pore, 710 long. Vagina with vaginal funnel and vaginal bulb, without muscular sphincters (Fig. 1D). Eggs not observed. Gonopore terminal.
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Fig. 1 Sharpilosentis peruviensis n. sp. ex Duopalatinus cf. peruanus. A, Proboscis of holotype male; B, Total view of holotype male; C, Hooks of a longitudinal row of holotype male; D, Terminal part of female reproductive system. Abbreviations: 1B: CG, cephalic ganglion; T, testis; VE, vas efferens; CGL, cement glands; CD, cement duct; SP, Saefftigen’s pouch; VD, vas deferens; P, penis; BW, bursal wall; GG, genital ganglion; G, gonopore; 1D: UB, uterine bell; U, uterus; VF, vaginal funnel; V, vagina; VB, vaginal bulb; G, gonopore. Scale-bars: A, 500 lm; B, 1 mm; C, 100 lm; D, 500 lm
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Fig. 2 Photomicrographs of Sharpilosentis peruviensis n. sp. ex Duopalatinus cf. peruanus. A, Proboscis of holotype male (arrow indicates bifurcated root of hook 6); B, Detail of male reproductive system with penis; C, Detail of penis with invaginated anterior part; D, Detail of penis surface with small tubercles; E, Detail of inner surface of bursa with small reticular sculpting. Scale-bars: A, B, 200 lm; C, 50 lm; D, E, 20 lm
Remarks The new species can be distinguished from species of other diplosentid genera by the characteristics of the new genus listed above. The type-host is provisionally designated as Duopalatinus cf. peruanus but its precise identification is not possible because of taxonomic problems of species of the so called ‘long-finned clade’ of pimelodid catfishes (John G. Lundberg, personal communication). Host tissue fixed with 99% ethanol has been deposited in the collection of Institute of Parasitology, AS CR for future genotyping; a picture of the fish host of field number PI 855 is available at http://tapewormdb.uconn. edu/index.php/hosts/specimen_search/teleost.
The partial sequence of the cox1 mitochondrial gene (602 bp long) for the new species is provided for future comparisons. At present, no further conclusions could be made on the species relationships due to the lack of sequence data on the diplosentid acanthocephalans.
Discussion Both fish hosts of Sharpilosentis peruviensis n. sp., Duopalatinus cf. peruanus and Oxydoras niger, are widely distributed in South America (Reis et al., 2003). These catfishes belong to different families but occur together in white waters, mostly in large rivers. The only acanthocephalan known from doradid catfish
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Fig. 3 Scanning electron micrographs of Sharpilosentis peruviensis n. sp. ex Duopalatinus cf. peruanus, female. A, Proboscis; B, Detail of hooks on the central part of the proboscis; C, Detail of hook surface (arrow indicates pores on the surface of the hook proboscis); D, Detail of hooks on posterior part of proboscis; E, Posterior part of the body; F, Detail of the posterior body surface. Small letters in Fig. 3B, E correspond to the figures showing higher magnification images of these surfaces. Scale-bars: A, 100 lm; B, D, E, 10 lm; C, F, 1 lm
is Paracavisoma impudica (Diesing, 1851) of the family Cavisomidae Meyer, 1932, reported from O. niger and O. kneri Bleeker (see Eiras et al., 1995; Tantalea´n et al., 2005; Kohn et al., 2011). The family Diplosentidae was erected by Tubangui & Masilungan (1937) to accommodate Diplosentis
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amphacanthi Tubangui & Masilungan, 1937 from the white spotted rabbitfish Siganus canaliculatus (Park). Golvan (1969) divided the family into two subfamilies, the monotypic Allorhadinorhynchinae Golvan, 1969 with species of Allorhadinorhynchus Yamaguti, 1959 possessing spines on the trunk, and
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Diplosentinae for species of the genera Diplosentis and Pararhadinorhynchus with unarmed trunk (Golvan, 1969). Pichelin & Cribb (2001) considered some of the main diagnostic characteristics of the Diplosentidae to be controversial, including the number of cement glands in D. amphacanthi, the type-species of Diplosentis. They transferred Diplosentis to the family Cavisomidae, the members of which possess four cement glands, and erected a new family Transvenidae Pichelin & Cribb, 2001 and included the genera Pararhadinorhynchus Johnston & Edmonds, 1947, Transvena Pichelin & Cribb, 2001 and Trajectura Pichelin & Cribb, 2001 with two cement glands into this family. Amin (2013) did not support the taxonomic rearrangement of Pichelin & Cribb (2001) and recognised the validity of the family Diplosentidae, but left two genera, Transvena and Trajectura, in the family Transvenidae. We accept the taxonomic structure of the family Diplosentidae according to the latest classification of acanthocephalans (Amin, 2013) with some modifications: the subfamily Allorhadinorhynchinae is considered to include the genera Allorhadinorhynchus and Amapacanthus Salgado-Maldonado & Santos, 2000 [Amin (2013) placed the latter genus to the Diplosentinae] and the subfamily Diplosentinae including the genera Diplosentis and Pararhadinorhynchus. Inclusion of the genus Golvanorhynchus Noronha, Fabio & Pinto, 1978 with six cement glands into this family is unconvincing. Smales (2012) placed the genus Golvanorhynchus in the family Isthmosacanthidae Smales, 2012 and this proposal is followed here. Sharpilosentis n. g. is placed in the subfamily Diplosentinae of the family Diplosentidae because it possesses two cement glands, its proboscis hooks are arranged in longitudinal rows and the body is smooth, unarmed. Sharpilosetntis n. g. can by distinguished by the morphology of the hooks from the two other genera of the subfamily Diplosentinae. Species of the genera Pararhadinorhynchus and Diplosentis have similar hooks, with hook sizes decreasing from the first to the last and most of the hooks in each row possess roots (only 2–4 basal hooks are without roots), whereas proboscis hooks of S. peruviensis n. sp. are of three types: 5–6 large hooks with simple roots, transitional 6th hook in one from two adjacent rows with bifurcated root distally in the anterior part of the proboscis and 6 small hooks without roots in the posterior part of the proboscis (Figs. 1C, 2A). Also,
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the cephalic ganglion of S. peruviensis n. sp. is located between the second and third part of the proboscis receptacle (Fig. 1B), whereas that of the species of Diplosentis is located in the middle of the proboscis receptacle and the cerebral ganglion of the species of the genus Pararhadinorhynchus is situated at the base of the proboscis receptacle. The females of S. peruviensis n. sp. have a vulva lacking muscular sphincters (Fig. 1D), whereas the females of species of the other genera of the subfamily have the vulva with one muscular sphincter (see figure 20 in Johnston & Edmonds, 1947; figure 4 in Edmonds, 1973). The vaginal funnel is not located in the uterus (Fig. 1D), but posterior to the uterus as is/ are sphincter(s) in other species of acanthocephalans (see, e.g. Petrochenko, 1956; Golvan, 1969). In fact, vaginal sphincters seem to be absent in S. peruviensis, even though only an immature female was available and sphincters may be poorly developed in immature worms. However, sphincters are formed already in female cystacanths in intermediate hosts as found in all known cases (see, e.g. figures 1a, 2b and 3a in Lisitsyna & Tkach, 1994 and figure 1a in Lisitsyna, 2011). In addition, the males of S. peruviensis n. sp. have a large muscular penis covered with small tubercles. Morphological features of the penis of species of Diplosentis and Pararhadinorhynchus have not been described, but judging from the figures (figures 1 and 2 in Tubangui & Masilungan, 1937; figures 12 and 18 in Johnston & Edmonds, 1947; figure 3 in Edmonds, 1973; figure 1 in Gupta & Fatma, 1979), they may not be comparable in magnitude with those on the penis of the species of S. peruviensis n. sp. Pores on the surface of hook blades of S. peruviensis (Fig. 3C) are not unique characteristics of the species. Numerous pores on the outer surface of the hook have been observed also in Acanthocephalus lucii (Mu¨ller, 1776) (see Bra´zova´ et al., 2014). Previously, Miller & Dunagan (1985) described small grooves on the greater curvature on the surface of hook blades of Macracanthorhynchus hirudinaceus (Pallas, 1781) that extended for approximately half of the exposed position of the blade. These authors speculated that these structures are involved in secretory activities. Surface striations of hook blade were also observed in Dentitruncus truttae Sinzar, 1955 by Dezfuli et al. (2008) who assumed that such striations may help in a more effective attachment to the host’s intestine. It is possible that pores on the surface of
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hook blades of S. peruviensis have some secretory function. Pores on the tegumental surface similar to those observed in the present material have also been described in Acanthocephalus ranae (Schrank, 1788), A. lucii (Mu¨ller, 1776), Pomphorhynchus spindetrancatus Amin, Abdullaphah & Mhaisan, 2003 and Acanthogyrus (Acanthosentis) tilapiae (Baylis, 1948) (see Heckmann et al., 2010, 2011; Amin et al., 2011). Acknowledgements Thanks are due to Martin Mortenthaler and his family, Acuario Rı´o Momon, Iquitos, Peru, for providing facilities for fish examination and supplying fish from Santa Clara, Rı´o Nanay, Carlos A. Mendoza-Palmero and Alain de Chambrier for help with fish examination at Iquitos. The authors are much obliged to Simona Georgieva from the Institute of Parasitology who obtained the cox1 sequence for the new species. Support by authorities of the Czech Embassy in Lima, Peru and Peruvian Embassy in Prague, Czech Republic, in particular by Marina Landaveri, Ambassador of Peru in the Czech Republic, is also greatly appreciated. This study was partly supported by the Czech Science Foundation (Project No. P505/12/G112), the Institute of Parasitology, AS CR, Cˇeske´ Budeˇjovice (RVO: 60077344) and the Ukrainian-Czech joint project ‘‘Helminth parasites in aquatic ecosystems: their diversity and life-cycles in the changing world’’.
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