(Monogenea: Dactylogyridae) from Hybopsis and Notropis

Proc. Helminthol. Soc. Wash. 54(1), 1987, pp. 78-83

Dactylogyrus (Monogenea: Dactylogyridae) from Hybopsis and Notropis (Cyprinelld) (Pisces: Cyprinidae) from the Tennessee River Drainage, with Descriptions of Three New Species and Remarks on Host Relationships

DONALD G. CLOUTMAN Duke Power Company, Production Environmental Services, Rt. 4, Box 531, Huntersville, North Carolina 28078

ABSTRACT: Three previously described and three new species of Dactylogyrus are reported from Hybopsis and Notropis (Cyprinelld) from the Tennessee River drainage: D. amblops Mueller, 1938, and D. plegadus Rogers, 1967, were found on H. amblops; D. moorei Monaco and Mizelle, 1955, occurred on H. monacha, N. galacturus, and N. spilopterus; D. beckeri sp. n. and D. dissimili sp. n. are described from N. galacturus and H. dissimilis, respectively; D. nuntius sp. n. is described from H. monacha and N. galacturus. No Dactylogyrus species were found on H. cahni and H. insignis. The presence of D. moorei and D. nuntius on H. monacha and members of Notropis (Cyprinelld) corroborates recent ichthyological evidence that H. monacha is more closely related to certain species of Notropis (Cyprinelld) than to Hybopsis. KEY WORDS: Dactylogyrus beckeri sp. n., D. dissimili sp. n., D. nuntius sp. n., fish, taxonomy, morphology, new localities.

From host-parasite lists provided by Mizelle added to make a 10% solution (Putz and Hoffman, and McDougal (1970) and Kritsky et al. (1977), 1963). Museum specimens of some hosts loaned by R. E. Jenkins, Roanoke College, were also examined. it is evident that most species of North American All parasites, collected from the gills of their hosts, Dactylogyrus Diesing, 1850, parasitize either one were mounted in glycerin jelly, and observations were species or groups of closely related hosts. Those made with a phase contrast microscope. Drawings were species of Dactylogyrus that parasitize more than made with the aid of an ocular grid and graph paper one host species should offer supporting evidence (Mayr, 1969). Measurements, in micrometers, were made as presented by Mizelle and Klucka (1953); means for species relationships determined from tra- are followed by ranges in parentheses. All type speci- ditional ichthyological studies. Burkhead and mens of new species and representative specimens of Bauer (1983) and Jenkins and Burkhead (1984) previously described species were deposited in the hel- provided evidence based on morphology and re- minthological collection of the National Museum of Natural History, Smithsonian Institution (USNM). productive behavior that Hybopsis monacha Other nontype material was retained in the author's (Cope) is allied closely with Notropis (Cyprinel- collection. For comparative purposes, all original de- ld), rather than with Hybopsis (Erimystax} where scriptions and redescriptions of North American Dac- it is currently placed. I examined one species of tylogyrus species and type specimens of the following Hybopsis (Hybopsis), four species of Hybopsis species were examined: D. amblops Mueller, 1938, sev- en syntypes (USNM 71453); D. confusus Mueller, 1938, (Erimystax) (including H. monacha), and two five syntypes (USNM 71447); D. plegadus Rogers, 1967, species of Notropis (Cyprinelld) from the Ten- holotype (USNM 61604) and one paratype (USNM nessee River drainage to determine if the Dac- 61605). tylogyrus infesting these hosts indicate the same host relationships suggested by the ichthyological Dactylogyrus amblops Mueller, 1938 studies mentioned above. Three previously de- HOST: Hybopsis amblops (Rafinesque), big- scribed and three new species of Dactylogyrus eye chub. are reported herein, and evolutionary relation- LOCALITIES: Tennessee: Blount Co., Little ships of hosts based on infesting Dactylogyrus River near Waland (USNM 79300, 1 specimen); species are discussed. Lewis Co., Buffalo River at the mouth of Grind- ers Creek (USNM 79299, 3 specimens). Virginia: Materials and Methods Washington Co., North Fork Holston River at "Peatail Island." The species and numbers of hosts examined are list- ed in Table 1. Immediately after capture, some hosts REMARKS: This is the first report of Dacty- were placed in jars containing a 1:4,000 formalin so- logyrus amblops since its original description from lution; after approximately 1 hr, enough formalin was Hybopsis amblops in New York (Mueller, 1938). 78 Copyright © 2011, The Helminthological Society of Washington 79

Dactylogyrus amblops was found only on H. am- Dactylogyrus beckeri sp. n. blops, where it occurred in mixed infestations (Figs. 1-8) with D. plegadus. TYPE HOST: Notropis galacturus (Cope), Dactylogyrus moorei whitetail shiner. Monaco and Mizelle, 1955 TYPE LOCALITY: Tennessee: Monroe Co., Ci- tico Creek. HOSTS AND LOCALITIES: Hybopsis monacha TYPE SPECIMENS: Holotype, USNM 79289; 7 (Cope)—Virginia: Washington Co., North Fork paratypes, USNM 79290 (6 specimens) and Holston River off Co. Rt. 615 at island, 0.7 air USNM 79291 (1 specimen). km S of jet. of Co. Rts. 614 and 615 (USNM OTHER LOCALITY: Tennessee: Blount Co., 79303, 1 specimen); North Fork Holston River, Little River near Waland. Rt. 614 bridge at Mendota. Notropis galacturus DESCRIPTION: With characters of the genus as (Cope)—Tennessee: Blount Co., Little River near emended by Mizelle and McDougal (1970). Body Waland; Monroe Co., Citico Creek (USNM with thin tegument; length 446 (338-518), great- 79301, 2 specimens). Notropis spilopterus est width 147 (122-187). Two pairs of eyes ap- (Cope)—Tennessee: Blount Co., Little River near proximately equal in size, anterior pair farther Waland; Hancock Co., Clinch River at Frost Ford apart than posterior pair. Peduncle lacking. Hap- (USNM 79302, 1 specimen). tor 54 (43-65) long, 65 (58-72) wide. Single pair REMARKS: Dactylogyrus moorei was de- of dorsal anchors; each composed of solid base scribed from Notropis deliciosus missuriensis (=N. with short deep root and elongate superficial root, stramineus (Cope)) and N. (Cyprinelld) lutrensis solid shaft, and recurved point. Anchor length (Baird and Girard) from Oklahoma (Monaco and 25 (23-26), greatest width of base 16 (14-19). Mizelle, 1955), and has been reported subse- Dorsal bar length 22 (20-24). Vestigial ventral quently from five other species of Notropis (Cy- bar length 15 (14-17). Sixteen hooks (8 pairs), prinelld) from the central and eastern United similar in shape (except 4A), normal in arrange- States (Rogers, 1967; Cloutman, 1974; Kritsky ment (Mizelle and Crane, 1964). Each hook com- et al., 1977). I suspect that the single report of posed of solid base, solid slender shaft, and sick- D. moorei on N. stramineus was the result of le-shaped termination provided with opposable either transposed data or an "accidental" infes- piece (opposable piece lacking in 4A). Hook tation due to close association with N. lutrensis, lengths: No. 1, 15 (13-15); 2, 15 (14-16); 3, 16 and that D. moorei normally infests only mem- (15-17); 4, 16 (14-17); 4A, 6 (5-6); 5, 15 (15- bers of Notropis (Cyprinelld). I have found D. 16); 6, 15 (14-15); 7, 15 (14-17). Copulatory moorei on N. lutrensis from the Smoky Hill Riv- complex composed of cirrus and articulated ac- er, Ellis Co., Kansas (Cloutman, 1974), and Rat- cessory piece. Cirrus with enlarged robust base tlesnake Creek, Stafford Co., Kansas (unpubl. bearing straight process and curved tubular shaft data), but lacking on syntopic N. stramineus. that is attenuated to a point. Cirrus length 58 (46-65). Process length (measured from base of Dactylogyrus plegadus Rogers, 1967 cirrus shaft to distal tip of process) 13 (11-15). HOST: Hybopsis amblops (Rafinesque), big- Shaft length 37 (34-41). Accessory piece bifur- eye chub. cate, distal ramus curved and attenuated to a LOCALITIES: Tennessee: Blount Co., Little point; medial ramus recurved, attenuated to a River near Waland (USNM 79305, 2 speci- point. Accessory piece length 27 (26-28). Vagina mens); Lewis Co., Buffalo River at the mouth of sclerotized, irregular in shape, opening dextro- Grinders Creek (USNM 79304, 3 specimens). ventrally posterior to cirrus. Vitellaria moderate Virginia: Washington Co., North Fork Holston to heavy, usually distributed from pharynx to River at "Peatail Island." haptor. Egg elliptical, 61 (60-61) long and 43 REMARKS: This is the first report of Dacty- (42-44) wide. logyrus plegadus since its original description REMARKS: Dactylogyrus beckeri most closely from Hybopsis amblops and H. winchelli (Girard) resembles D. confusus by possessing similar- (reported as H. amblops by Rogers [1967] before shaped anchors and cirrus, but comparison of Clemmer [1980] resurrected PI. winchelli to the syntypes taken from Clinostomus elongatus species status). Dactylogyrus plegadus appears to (Kirtland) and original description of D. confusus parasitize only species of Hybopsis (Hybopsis}. (Mueller, 1938) reveals some trenchant differ-

Copyright © 2011, The Helminthological Society of Washington 80 PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY ences: D. beckeri possesses smaller hooks, a larg- laria moderate, distributed from pharynx to hap- er cirrus, and longer cirrus process. The cirrus tor. process of D. beckeri is tapered distally, whereas REMARKS: The closest apparent relative of that of D. confusus is enlarged distally. Dactylogyrus dissimili is D. nuntius sp. n., but ETYMOLOGY: Dactylogyrus beckeri is named D. dissimili is easily distinguished by the pres- in honor of the late Dr. David A. Becker, my ence of a process on the cirrus base and a club- mentor at the University of Arkansas. shaped terminus on the distal ramus of the accessory piece. Dactylogyrus dissimili sp. n. ETYMOLOGY: Dactylogyrus dissimili is named (Figs. 9-16) after its host. TYPE HOST: Hybopsis dissimilis (Kirtland), streamline chub. Dactylogyrus nuntius sp. n. TYPE LOCALITY: Tennessee: Hancock Co., (Figs. 17-24) Clinch River at Frost Ford. TYPE HOST: Notropis galacturus (Cope), TYPE SPECIMENS: Holotype, USNM 79292; whitetail shiner. 10 paratypes, USNM 79293 (9 specimens) and TYPE LOCALITY: Tennessee: Hancock Co., USNM 79294 (1 specimen). Clinch River at Frost Ford. OTHER LOCALITY: Virginia: Washington Co., TYPE SPECIMENS: Holotype, USNM 79295; North Fork Holston River at "Peatail Island." 13 paratypes, USNM 79296 (7 specimens) and DESCRIPTION: With characters of the genus as USNM 79297 (6 specimens). emended by Mizelle and McDougal (1970). Body OTHER HOSTS AND LOCALITIES: Notropis ga- with thin tegument; length 210 (187-252), great- lacturus (Cope)—Tennessee: Blount Co., Little est width 75 (58-86). Two pairs of anterior ce- River near Waland; Monroe Co., Citico Creek. phalic lobes, lateral pair smaller than medial pair. Hybopsis monacha (Cope)—Virginia: Washing- Head organs not observed. Two pairs of eyes ton Co., Middle Fork Holston River below ford approximately equal in size, anterior pair farther on Co. Rt. 707, 9.3 air km ESE of Abingdon; apart than posterior pair. Pharynx circular to North Fork Holston River, Fleenor Mill Road; ovate (dorsal view), transverse diameter 20 (16- North Fork Holston River off Co. Rt. 615 at 23), gut not observed. Peduncle lacking. Haptor island, 0.7 air km S of jet. of Co. Rts. 614 and 47 (43-50) long, 54 (43-72) wide. Single pair of 615; North Fork Holston River at Hobbs Ford dorsal anchors; each composed of solid base with off Co. Rt. 614, 1.6 air km E of Mendota; North short deep root and elongate superficial root, and Fork Holston River, Rt. 614 bridge at Mendota solid shaft that curves to a sharp point. Anchor (USNM 79298, 2 specimens). length 43 (42-45), greatest width of base 20 (19- DESCRIPTION: With characters of the genus as 21). Dorsal bar length 26 (23-31). Vestigial ven- emended by Mizelle and McDougal (1970). Body tral bar length 23 (21-26). Sixteen hooks (8 pairs), with thin tegument; length 409 (288-504), great- similar in shape (except 4A), normal in arrange- est width 118 (72-137). Two pairs of anterior ment (Mizelle and Crane, 1964). Each hook com- cephalic lobes, lateral pair smaller than medial posed of solid base, solid slender shaft, and sick- pair. Head organs not observed. Two pairs of le-shaped termination provided with opposable eyes approximately equal in size, anterior pair piece (opposable piece lacking in 4A). Hook ranges from closer to farther apart than posterior lengths: No. 1, 20 (18-22); 2, 21 (20-22); 3, 28 pair. Pharynx circular to ovate (dorsal view), (22-33); 4, 24 (22-26); 4A, 7; 5, 23 (19-27); 6, transverse diameter 28 (25-29); gut not ob- 21 (18-22); 7, 19 (18-20). Copulatory complex served. Peduncle lacking. Haptor 48 (43-72) long, composed of cirrus and articulated accessory 73 (58-86) wide. Single pair of dorsal anchors; piece. Cirrus with small base bearing straight each having solid base with short deep root and process and curving tubular shaft that is bent elongate superficial root, solid, slightly inflated near distal end and attenuated to a point, length shaft, and sharp point. Anchor length 33 (30- 23 (18-30). Accessory piece Y-shaped, distal 35), greatest width of base 14 (11-16). Dorsal ramus with club-shaped terminus and medial bar length 20 (15-23). Vestigial ventral bar length ramus with rounded terminus. Accessory piece 19 (17-22). Sixteen hooks (8 pairs), similar in length 20 (14-25). Vagina not observed. Vitel- shape (except 4A), normal in arrangement (Miz-

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Figures 1-24. 1-8. Dactylogyrus beckeri. 1, 3. Cirrus. 2, 4. Accessory piece. 5. Anchor. 6. Dorsal bar. 7. Ventral bar. 8. Hook. 9-16. Dactylogyrus dissimili. 9, 11. Cirrus. 10,12. Accessory piece. 13. Anchor. 14. Dorsal bar. 15. Ventral bar. 16. Hook. 17-24. Dactylogyrus nuntius. 17, 19. Cirrus. 18, 20. Accessory piece. 21. Anchor. 22. Dorsal bar. 23. Ventral bar. 24. Hook. elle and Crane, 1964). Each hook composed of rounded base, bearing a curving tubular shaft solid base, solid slender shaft, and sickle-shaped bent near distal end and attenuated to a point, termination provided with opposable piece (op- length 31 (28-35). Accessory piece Y-shaped, posable piece lacking in 4A). Hook lengths: No. distal ramus recurved and pointed, medial ramus 1, 17 (15-18); 2, 18 (15-20); 3, 20 (17-22); 4, 19 with knoblike terminus. Accessory piece length (17-22); 4A, 4; 5, 19 (18-21); 6, 17 (14-19); 7, 20 (18-22). Vagina not observed. Vitellaria mod- 18 (15-20). Copulatory complex composed of erate to heavy, usually distributed from pharynx cirrus and articulated accessory piece. Cirrus with to haptor.

Table 1. Prevalence (% infestation), range, and relative density (total number of parasites/total number of hosts) of Dactylogyrus infesting species of Hybopsis and Notropis (Cyprinella) from the Tennessee River drainage. Numbers in parentheses represent the number of hosts.

Relative Prevalence Range density

Hybopsis (Hybopsis) amblops (Rafinesque), bigeye chub (10) Dactylogyrus amblops Mueller, 1938 100.0 1-6 3.7 Dactylogyrus plegadus Rogers, 1967 90.0 0-16 5.9 Hybopsis (Erimystax) cahni Hubbs and Crowe, slender chub (10) Hybopsis (Erimystax) dissimilis (Kirtland), streamline chub (7) Dactylogyrus dissimili sp. n. 100.0 7-21 15.7 Hybopsis (Erimystax) insignis Hubbs and Crowe, blotched chub (11) Hybopsis (Erimystax) monacha (Cope), spotfin chub (14) Dactylogyrus moorei Monaco and Mizelle, 1955 14.3 0-1 0.1 Dactylogyrus nuntius sp. n. 92.9 0-5 2.4 Notropis (Cyprinella) galacturus (Cope), whitetail shiner (10) Dactylogyrus beckeri sp. n. 80.0 13-15 3.9 Dactylogyrus moorei Monaco and Mizelle, 1955 30.0 0-13 2.1 Dactylogyrus nuntius sp. n. 40.0 0-15 3.1 Notropis (Cyprinella) spilopterus (Cope), spotfin shiner (3) Dactylogyrus moorei Monaco and Mizelle, 1955 66.7 0-1 0.7

REMARKS: The closest apparent relative of (Erimystax) cannot be ruled out because of the Dactylogyrus nuntius is D. dissimili (see remarks apparent close relationship between D. dissimili for D. dissimili). and D. nuntius. ETYMOLOGY: The specific name is Latin (nuntius = a messenger), referring to the parasite Acknowledgments providing evidence that its two hosts are closely I thank Dr. Robert E. Jenkins, Roanoke Col- related (see discussion for details). lege, and Robert Wallus, TVA, for providing some of the host specimens. Dr. J. Ralph Lich- Discussion tenfels loaned type specimens of Dactylogyrus The apparent close relationship of Dactylo- from the USNM. gyrus dissimili and D. nuntius may indicate that their hosts (Table 1) are phyletically linked. This Literature Cited hypothesis supports the traditional placement of Hybopsis monacha with H. dissimilis in Hybopsis Burkhead, N. M., and B. H. Bauer. 1983. An inter- generic cyprinid hybrid, Hybopsis monacha x No- (Erimystax), but fails to explain the presence of tropis galacturus, from the Tennessee River drain- D. nuntius on Notropis galacturus. The presence age. Copeia 1983:1074-1077. of D. nuntius on H. monacha and N. galacturus Clemmer, G. H. 1980. Hybopsis winchelli (Girard), and its absence from other fishes (Table 1) in- clear chub. Page 195 in D. S. Lee et al. Atlas of North American Freshwater Fishes. North Caro- dicate a close relationship between these two lina State Museum of Natural History, Raleigh. hosts. This interpretation is further strengthened 854 pp. by the presence of D. moorei on //. monacha, N. Cloutman, D. G. 1974. Monogenean and copepod galacturus, N. spilopterus (Table 1), and other parasites of fishes from the Smoky Hill River, Ellis species of Notropis (Cyprinella), and its absence County, Kansas. Transactions of the Kansas Academy of Science 77:225-229. from other hosts (see remarks for D. moorei). Jenkins, R. E., and N. M. Burkhead. 1984. Descrip- Dactylogyrus moorei and D. nuntius provide tion, biology and distribution of the spotfin chub, strong evidence corroborating the findings of Hybopsis monacha, a threatened cyprinid fish of Burkhead and Bauer (1983) and Jenkins and the Tennessee River drainage. Bulletin of the Al- abama Museum of Natural History 8:1-30. Burkhead (1984) that H. monacha is most closely Kritsky, D. C., R. J. Kayton, and P. D. Leiby. 1977. allied with Notropis (Cyprinella), although some Dactylogyrus unguiformis sp. n. (Monogenea) from relationship between H. monacha and Hybopsis the mottled sculpin, Coitus bairdi Girard, in Ida-

ho, with some taxonomic considerations in the Monaco, L. H., and J. D. Mizelle. 1955. Studies on genus Dactylogyrus. Proceedings of the Helmin- monogenetic trematodes. XVII. The genus Dac- thological Society of Washington 44:142-147. tylogyrus. American Midland Naturalist 53:455- Mayr, E. 1969. Principles of Systematic Zoology. 477. McGraw-Hill, Inc., New York. 428 pp. Mueller, J. F. 1938. Additional species of North Mizelle, J. D., and J. W. Crane. 1964. Studies on American Gyrodactyloidea (Trematoda). Ameri- monogenetic trematodes, XXIII. Gill parasites of can Midland Naturalist 19:220-235. Micropterus salmoides (Lacepede) from a Califor- Putz, R. E., and G. L. Hoffman. 1963. Two new nia pond. Transactions of the American Micro- Gyrodactylus (Trematoda: Monogenea) from cyp- scopical Society 83:343-348. rinid fishes with synopsis of those found on North , and A. R. Klucka. 1953. Studies on mono- American fishes. Journal of Parasitology 49:559- genetic trematodes. XIV. Dactylogyridae from 566. Wisconsin fishes. American Midland Naturalist Rogers, W. A. 1967. Studies of Dactylogyrinae (Mon- 49:720-737. ogenea) with descriptions of 24 new species of , and H. D. McDougal. 1970. Dactylogyrus in Dactylogyrus,5newspeciesofPellucidhaptor,an