J. Helminthol. Soc. Wash. 59(2), 1992, 195-200

Schilbetrematoides pseudodactylogyrus gen. et sp. n. (Monogenoidea, Dactylogyridae, Ancyrocephalinae) from the Gills of (Siluriformes, ) in Togo, Africa

D. C. KRITSKY1 AND S.-D. KULO2 1 College of Health-Related Professions, Idaho State University, Pocatello, Idaho 83209 and 2 Laboratoire de Parasitologie, Ecole des Sciences, Universite du Benin, B.P. 1515, Lome, Togo

ABSTRACT: Schilbetrematoides pseudodactylogyrus sp. n. (Dactylogyridae, Ancyrocephalinae) is described from the gills of Schilbe intermedius Riippell, 1832, Siluriformes, Schilbeidae, in Togo. Schilbetrematoides gen. n. is proposed for this and is characterized, in part, by large, subspherical eye granules; intercecal, overlapping gonads (testis dorsal); a constriction of the vas deferens at its union with the seminal vesicle; dorsal anchors; a ventral pair of 4A's lying near the ends of a simple (vestigial?) ventral bar; a highly modified dorsal bar; 14 hooks in 7 pairs with slender shanks and protruding thumbs. KEY WORDS: Togo, Africa, Monogenoidea, Dactylogyridae, Ancyrocephalinae, Schilbetrematoides gen. n., Schilbetrematoides pseudodactylogyrus sp. n., Schilbe mystus, Schilbe intermedius.

During the relatively short period when Dr. I. es and the number (N) of specimens measured in pa- Paperna worked on the freshwater Dactylogyri- rentheses. Type specimens were deposited in the hel- dae from Africa, he proposed 13 of the 23 genera minthological collections of the U.S. National Museum (USNM), USDA, ARS, Agricultural Research Center- currently accommodating Ethiopian species (see East, Beltsville, Maryland; the University of Nebraska Euzet and Dossou, 1976, and Paperna, 1979). State Museum (HWML), University of Nebraska, Lin- Together, these genera appear to represent a well- coln, Nebraska; the Musee Royal de 1'Afrique Centrale defined picture of the freshwater dactylogyrid (MRAC), B-1980 Tervuren, Belgium; and the British Museum (Natural History) (BM[NH]), London, U.K., fauna of Africa's freshwater fishes. Indeed, since as indicated in the description. A specimen of the host, 1979, only Paraquadriacanthus Ergens, 1988 Schilbe intermedius Ruppel, was deposited in the (=Quadriacanthoides Kritsky and Kulo, 1988; American Museum of Natural History, New York, as see Kritsky, 1990), and Insulacleidus Rakotofi- AMNH 57312. ringa and Euzet, 1983, have been proposed to Schilbetrematoides gen. n. accommodate African species. Similarly, our collections from Togo have not resulted in the DIAGNOSIS: Dactylogyridae, Ancyrocephali- identification of many new generic taxa. In the nae. Body divisible into cephalic region, trunk, present paper, however, a new is erected peduncle, haptor. Tegument thin, smooth. Two for an unusual worm from the gills of a siluri- bilateral, 2 terminal cephalic lobes; head organs form, Schilbe intermedius Ruppel, 1832 (Schil- present; cephalic glands unicellular, comprising beidae), from Togo. Although apparently sister 2 bilateral groups posterolateral to pharynx. Eyes taxon to Schilbetrema Paperna and Thurston, present, generally compact; granules large, sub- 1968 (Ancyrocephalinae), the new genus is char- spherical. Mouth subterminal, midventral; phar- acterized by many features of the Dactylogyri- ynx, esophagus present; intestinal ceca 2, conflu- ent posterior to gonads. Gonads intercecal, overlapping; testis dorsal to ovary. Vas deferens Materials and Methods looping left intestinal cecum, constricting at union with seminal vesicle; seminal vesicle fusiform, Fish hosts, Schilbe intermedius, were collected from lying parallel to left intestinal cecum; distal vas the Mono River near Kolokope, Togo, during 1985- 1989. Methods for collection, preservation, mounting, deferens slightly dilated (secondary seminal ves- and illustration of helminths were as described by Krit- icle?), delicate; single prostatic reservoir closely sky et al. (1987). Measurements, all in micrometers, associated with cirral base. Copulatory complex were made with a filar micrometer according to the comprising proximally articulated cirrus, acces- procedures of Mizelle and Klucka (1953), except that cirral length was an approximation obtained by using sory piece; cirrus a loose clockwise coil (see Krit- a calibrated Minerva curvimeter on camera lucida sky et al., 1985); accessory piece comprising drawings; average measurements are followed by rang- proximal articulating rod, distal complex with 195

Copyright © 2011, The Helminthological Society of Washington 196 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY grooved cirral guide. Oviduct short; uterus del- form connecting rod, distal sheath with several icate; vagina dextral, opening near body mid- variable branches, 1 of which serving as cirral length; seminal receptacle ventral to anterior end guide. Testis elongate ovate, 51 (42-61; N = 3) of ovary. Haptor armed with dorsal pair of an- x 23 (22-24; ./V = 3); constriction of vas deferens chors; ventral pair of 4A's lying near ends of with external spiral filament; seminal vesicle with simple ventral bar; dorsal, ventral bars; 14 (7 distinct wall, fusiform; distal vas deferens pyri- pairs) hooks with ancyrocephaline distribution form; prostatic reservoir saccate. Ovary bacilli- (Mizelle, 1936; see Mizelle and Price, 1963); dor- form, 43 (40-45; N = 4) x 20 (17-23; TV = 3); sal anchor filaments present. Hooks with slender vagina funnel-shaped, with distal loop opening shanks, protruding thumb. into large central seminal receptacle; vitellaria TYPE SPECIES, HOST, AND LOCALITY: Schilbe- dense throughout trunk, except absent in fields trematoides pseudodactylogyrus gen. et sp. n., of reproductive organs. from Schilbe intermedius Riippel, Mono River SPECIMENS STUDIED: Holotype, USNM near Kolokope, Togo. 82093, 13 paratypes, USNM 82094, HWML ETYMOLOGY: The generic name indicates the 34290, MRAC 37.326, BM(NH) 1991.10.9.22. apparent close relationship of this taxon to Schil- ETYMOLOGY: The specific name refers to the betrema Paperna and Thurston, 1968. superficial resemblance of the species to mem- bers of Dactylogyrus (Dactylogyridae, Dactylo- Schilbetrematoides pseudodactylogyrus gyrinae). gen. et sp. n. (Figs. 1-9) Discussion DESCRIPTION: Body 388 (240 [contracted]- Our proposal of sister-group relationship of 548; N = 8) long, fusiform; greatest width 79 Schilbetrematoides and Schilbetrema Paperna (62-109 [contracted]; N = 8] in posterior trunk. and Thurston, 1968, is supported by several Cephalic lobes, cephalic glands poorly differen- shared, apparently synapomorphic features. tiated. Eyes 4; posterior pair slightly larger, mem- Among them, characteristics of the hooks, cop- bers of respective pairs equidistant; accessory ulatory complex, eye granules, vagina, seminal granules uncommon in cephalic, anterior trunk vesicle, and distal vas deferens, and presence of regions. Pharynx spherical, 22 (16-25; N = 8) in a constriction of the vas deferens at its union diameter; esophagus short. Peduncle broad; hap- with the seminal vesicle, appear to be the most tor subhexagonal, 64 (56-78; N = 5) wide, 79 significant (see Kritsky and Kulo, 1992). Basic (57-89; N = 7) long. Dorsal anchor 62 (56-70; features of the reproductive system of members N = 10) long, with elongate superficial root hav- of both genera are identical. However, these gen- ing superficial pustule near midlength, short deep era are presently differentiated primarily on hap- root, curved shaft, point; base width 26 (22-31; toral structure. Although some components are N = 7); anchor filament ancyrocephaline. Ventral highly modified, the distribution of haptoral scle- 4A: 10-11 (N = 3) long, proximally expanded rites in Schilbetrema spp. is typically ancyro- about »/2 total length. Ventral bar 29 (25-34; ./V cephaline, i.e., dorsal and ventral anchor/bar = 8) long, rod-shaped, with irregular anterior complexes present. In Schilbetrematoides, spe- margin. Dorsal bar 17(15-24; N = 5) long, plate- cies possess a haptoral organization approaching like, with enlarged ends, large projection arising that found in the Dactylogyrinae, i.e., dorsal an- from anterior bar margin; projection complex, chor/bar complex present, ventral pair of 4A's with 2 elbowlike bends, the last serving as guide present, ventral bar absent or vestigial. for anchor points; length of most dorsal fold (an- Without totally discounting the possibility of teroposterior measurement) 66 (60-70, N = 7). dispersal of some dactylogyrine ancestor to a si- Hooks similar; each 16 (14-17; N = 22) long, luriform host and subsequent convergence of with slightly depressed thumb, delicate point, many morphologic features, occurrence of Schil- shank; FH loop about 0.75 shank length. Cirrus betrematoides pseudodactylogyrus on a schilbeid a loose coil of less than 1 ring, frequently ap- (Siluriformes) host further supports the sister- pearing J-shaped, cirral base with sclerotized group relationship proposed herein. "Fahren- margin; cirral length 48 (47-55; N = 6), ring holz' Rule" states that the phylogeny of parasite diameter 12 (10-16, TV = 5). Accessory piece 27 groups usually directly corresponds to the natural (24-31; N = 4) long, comprising proximal uni- relationships of their hosts (Eichler, 1948). Al-

Copyright © 2011, The Helminthological Society of Washington OF WASHINGTON, VOLUME 59, NUMBER 2, JULY 1992 197

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0 4

Figures 1-9. Schilbetrematoides pseudodactylogyrus gen. et sp. n. 1. Ventral view of holotype. 2. Hook. 3. 4A. 4. Ventral bar. 5. Copulatory complex. 6. Dorsal bar (dorsal view). 7. Dorsal anchor. 8. Lateral view of haptor (only sinistral members of hook pairs shown). 9. Dorsal anchor/bar complex (lateral view). All drawings are to the 25-jum scale, except Figures 1 and 8 (lOO-ftm and SO-jim scale, respectively).

Copyright © 2011, The Helminthological Society of Washington 198 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY though explanation of monogenoidean species independent loss of the ventral anchor pair hap- on their hosts frequently requires instances of pened in one or more of these genera, the family "host switching" (Boeger and Kritsky, 1989; (s.s.) is likely polyphyletic. Thus, loss of an an- Guegan and Agnese, 1991; Wheeler and Bever- chor pair has a very limited value in defining this ley-Burton, 1989; among others), Fahrenholz' familial taxon. Secondary loss of an anchor pair(s) Rule is likely reflected in relationships of S. pseu- has already been assumed to have occurred in- dodactylogyrus and Schilbetrema spp., all of dependently outside the Dactylogyridae (s.s.) in which are exclusively parasites of African schil- Trinigyrus Hanek, Molnar, and Fernando, 1974 beids. (Ancyrocephalinae); Pseudodactylogyrus Gus- Bychowsky and Nagibina (1978) split the An- sev, 1965 (Pseudodactylogyrinae);Anonchohap- cyrocephalinae from the Dactylogyridae and el- tor Mueller, 1938, and Icelanonchohaptor Leiby, evated it to family status based primarily on hap- Kritsky, and Peterson, 1972 (Pseudomurraytre- toral characteristics. These characters now appear matidae); and Anacanthorus Mizelle and Price, to be insufficient to justify their action. Kritsky 1965, and Anacanthoroides Kritsky and Thatch- and Boeger (1989) provide evidence using cla- er, 1976 (Anacanthorinae). In species of the an- distics that the Ancyrocephalidae (sensu By- cyrocephaline genera, Eutrianchoratus Paperna, chowsky and Nagibina, 1978) is paraphyletic and 1969, Heteronchocleidus Bychowsky, 1957, and recommend that it be considered a junior syn- Trianchoratus Price and Berry, 1966, 1 member onym of the Dactylogyridae (sensu Yamaguti, of the ventral anchor pair has been lost as a rec- 1963). Our finding of Schilbetrematoides and the ognizable anchor but remains as a remnant re- characteristics it displays continue to cloud jus- sembling an early developing anchor. tification for the Ancyrocephalidae and, in ad- Another feature that is used to place dactylo- dition, suggest probable polyphyly of the Dac- gyrid species lacking 1 or both of the anchor pairs tylogyrinae (Dactylogyridae sensu stricto of in the Dactylogyrinae is the presence of 4A's Bychowsky and Nagibina, 1978) as well. (Mizelle and Price, 1963) in the haptor (e.g., Gus- Kritsky and Boeger (1989), among others, con- sev, 1978; Kritsky etal., 1978; Beverley-Burton, sider the presence of a single pair of anchors 1984). Circumstantial evidence, some of which (dorsal) in the Dactylogyrinae to represent a sec- is provided by Schilbetrematoides pseudodacty- ondary loss of the ventral anchor pair. Taxa, based logyrus, continues to mount supporting the ho- primarily on loss of structure(s), have a high risk mology of the 4A with the respective lost anchor. of polyphyly because loss could have occurred This homology, implying each 4A to be an an- many times with recognition of these indepen- chor vestige, was assumed by Kearn (1968) based dent occurrences difficult. In addition, structural on its relative position in the haptor and its tem- loss in an evolutionary sense and particularly in poral development in the larva and by Kritsky parasites is potentially a more common occur- and Boeger (1989) based on parsimony. If S. rence than the development of new structures. pseudodactylogyrus is sister to Schilbetrema as As such, convergence, as shown by the absence proposed herein, the 4A's of the former are not of a structure, should be an expected outcome; homologues of those of the Dactylogyrinae, and proposal of new or the splitting of existing taxa presence or absence of this feature can no longer based primarily on these characters, as engen- be used to separate dactylogyrids (sensu stricto) dered by Bychowsky and Nagibina, 1978, should from so-called "ancyrocephalids." If 4A's are ac- be done conservatively. tually homologues of ventral anchors, they should Schilbetrematoides and perhaps some other be expected in any taxon within or without the genera (Nanotrema Paperna, 1969, Trinidactylus Dactylogyrinae showing incomplete loss of the Hanek, Molnar, and Fernando, 1974, Curvian- haptoral anchors. choratus Hanek, Molnar, and Fernando, 1974, We recognize that our proposal of the mono- and Acolpenteron Fischthal and Allison, 1940) typic Schilbetrematoides gen. n. may result in whose members occur on noncypriniform hosts paraphyly of Schilbetrema, because synapo- and are considered by Gussev (1976, 1978) to morphic characters for the latter are not appar- comprise, in part, the Dactylogyridae sensu stric- ent. If Schilbetrematoides pseudodactylogyrus has to, are potential groups in which loss of the ven- a common ancestor (i.e., is sister species) with tral anchor pair may have occurred more than one or more of the Schilbetrema species infesting once throughout their evolutionary history. If Schilbe intermedius, the new genus should be

Copyright © 2011, The Helminthological Society of Washington OF WASHINGTON, VOLUME 59, NUMBER 2, JULY 1992 199 considered a synonym of Schilbetrema with the Price, 1942 (Monogenea). International Journal new species a highly derived member. The spiral for Parasitology 19:425-440. Bychowsky, B. E., and L. F. Nagibina. 1978. Revi- filament of the constriction of the vas deferens sion of Ancyrocephalinae Bychowsky, 1937. Par- may be a character supporting this synonymy if azitologicheskii Sbornik 28:5-15. its presence is the apomorphic state; a filamented De Vos, L., and P. Skelton. 1990. Name changes for constriction in Schilbetrema has only been ob- two common African . Rehabilitation of served in species infesting Schilbe intermedius. Schilbe intermedius Riippel, 1832 (Siluriformes, Schilbeidae). Cybium 14:323-326. However, if the filament is synapomorphic for EichIer,W. 1948. Some rules in ectoparasites. Annals Schilbetrema + Schilbetrematoides, the char- and Magazine of Natural History 1(12):588-598. acter would not affect monophyly of the genera. Euzet, L., and C. Dossou. 1976. Decouverte de Mo- Other characters, particularly associated with the nogenes (Bouixella n. g.) chez les Mormyridae (Te- highly modified haptoral sclerites in Schilbetre- leostei) au Benin. Comptes Rendus Hebdoma- daires des Seances de 1'Academie des Sciences, ma, may provide synapomorphies for this genus. Paris, Serie D, 283:1413-1416. An objective analysis will be required to deter- Guegan, J.-F., and J.-F. Agnese. 1991. Parasite evo- mine phylogenetic support for Schilbetrema- lutionary events inferred from host phytogeny: the toides. case of Labeo species (Teleostei, Cyprinidae) and their dactylogyrid parasites (Monogenea, Dactylo- In order to avoid potential confusion, we add gyridae). Canadian Journal of Zoology 69:595-603. the following concerning recent proposals for Gussev, A. V. 1976. Freshwater Indian Monogenoi- change in the nomenclature of the host. Based dea. Principles of systematics, analysis of world on the International Code of Zoological Nomen- faunas and their evolution. Indian Journal of Hel- clature and on the type specimen ofSilurus mys- minthology 25 & 26:1-241. . 1978. Monogenoidea of freshwater fishes. tus Linnaeus, 1758, De Vos and Skelton (1990) Principles of systematics, analysis of the world fau- indicate that the epithet "Schilbe mystus" must na and its evolution. Parazitologicheskii Sbornik be applied to schilbeids currently assigned to Eu- 28:96-198. tropius niloticus (Riippel, 1829). As a result, these Kearn, G. C. 1968. The development of the adhesive organs of some diplectanid, tetraonchid and dac- authors indicate that Schilbe intermedius Riip- tylogyrid gill parasites (Monogenea). Parasitology pel, 1832, is the oldest available name for fishes 58:149-163. previously included in the taxon S. mystus. In Kritsky, D. C. 1990. Synonymy of Paraquadriacan- the present paper, we accept De Vos and Skel- thus Ergens, 1988 and Quadriacanthoides Kritsky ton's (1990) nomenclatural changes for the host. et Kulo, 1988 (Monogenea Dactylogyridae) and their type species. Folia Parasitologica 37:76. It should be recognized, therefore, that the epi- , and W. A. Boeger. 1989. The phylogenetic thet "Schilbe mystus" used in previous parasi- status of the Ancyrocephalidae Bychowsky, 1937 tological literature refers to the species S. inter- (Monogenea: Dactylogyroidea). Journal of Para- medius, and that "Eutropius niloticus" of the sitology 75:207-211. older parasitological literature is now referred to -, and V. E. Thatcher. 1985. Neotrop- ical Monogenea. 7. Parasites of the pirarucu, Ar- S. mystus. apaima gigas (Cuvier), with descriptions of two new species and redescription of Dawestrema cy- Acknowledgments cloancistrium Price and Nowlin, 1967 (Dactylo- gyridae: Ancyrocephalinae). Proceedings of the Bi- The authors thank Dr. Mary Beverley-Burton ological Society of Washington 98:321-331. for a presubmission review of the manuscript. —, and S.-D. Kulo. 1992. Schilbetrema Paperna The study was supported, in part, by a grant (556) and Thurston, 1968 (Monogenoidea, Dactylogyr- idae), with descriptions of four new species from from the Faculty Research Committee, Idaho African Schilbeidae (Siluriformes). Transactions State University. of the American Microscopical Society. (In press.) -, and W. A. Boeger. 1987. Resurrec- tion of Characidotrema Paperna and Thurston, Literature Cited 1968 (Monogenea: Dactylogyridae) with descrip- Beverley-Burton, M. 1984. Monogenea and Turbel- tion of two new species from Togo, Africa. Pro- laria. Pages 5-203 in L. Margolis and Z. Kabata, ceedings of the Helminthological Society of Wash- eds. Guide to the Parasites of Fishes of Canada. ington 54:175-184. Part 1. Canadian Special Publication of Fisheries —, J. D. Mizelle, and F. M. Bilqees. 1978. Stud- and Aquatic Sciences 74. Department of Fisheries ies on Monogenea of Pakistan. III. Status of the and Oceans, Ottawa, Canada. Calceostomatidae (Parona and Perugia, 1890) with Boeger, W. A., and D. C. Kritsky. 1989. Phytogeny, a redescription of Neocalceostoma elongatum Tri- coevolution, and revision of the Hexabothriidae pathi, 1957 and the proposal of Neocalceosto-

Copyright © 2011, The Helminthological Society of Washington 200

moides gen. n. Proceedings of the Helmintholog- Paperna, I. 1979. Monogenea of inland water fish in ical Society of Washington 45:149-154. Africa. Annales-Serie IN-8°-SciencesZoologiques, Mizelle, J. D. 1936. New species of trematodes from Musee Royal de 1'Afrique Centrale 226:1-131, 48 the gills of Illinois fishes. American Midland Nat- plates. uralist 17:785-806. Wheeler, T. A., and M. Beverley-Burton. 1989. Sys- , and A. R. Klucka. 1953. Studies on mono- tematics of Onchodeidus Mueller, 1936 (Mono- genetic trematodes. XIV. Dactylogyridae from genea: Ancyrocephalidae): phylogenetic relation- Wisconsin fishes. American Midland Naturalist ships, evolution, and host associations. Canadian 49:720-733. Journal of Zoology 67:706-713. , and C. E. Price. 1963. Additional haptoral Yamaguti, S. 1963. Systema Helminthum. IV. hooks in the genus Dactylogyrus. Journal of Par- Monogenea and Aspidocotylea. Interscience Pub- asitology 49:1028-1029. lishers, New York. 699 pp.

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