Parasites of the Woundfin Minnow, Plagopterus Argentissimus, and Other Endemic Fishes from the Virgin River, Utah

Great Basin Naturalist

Volume 46 Number 4 Article 10

10-31-1986

Parasites of the woundfin minnow, Plagopterus argentissimus, and other endemic fishes from the Virgin River, Utah

Richard A. Heckmann Brigham Young University

James E. Deacon University of Nevada, Las Vegas

Paul D. Greger University of Nevada, Las Vegas

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Recommended Citation Heckmann, Richard A.; Deacon, James E.; and Greger, Paul D. (1986) "Parasites of the woundfin minnow, Plagopterus argentissimus, and other endemic fishes from the Virgin River, Utah," Great Basin Naturalist: Vol. 46 : No. 4 , Article 10. Available at: https://scholarsarchive.byu.edu/gbn/vol46/iss4/10

This Article is brought to you for free and open access by the Western North American Naturalist Publications at BYU ScholarsArchive. It has been accepted for inclusion in Great Basin Naturalist by an authorized editor of BYU ScholarsArchive. For more information, please contact [email protected], [email protected]. PARASITES OF THE WOUNDFIN MINNOW, PLAGOPTERUS ARGENTISSIMUS, AND OTHER ENDEMIC FISHES FROM THE VIRGIN RIVER, UTAH

Richard A. Heckmann', James E. Deacon", and Paul D. Greger^ — Abstract. ^Two hundred woundfin minnows, Plagopterus argentlssimus . from four sites along the Virgin River, Utah, were examined on two dates during summer 1985. The foreguts of 211 woundfin and variable numbers of other fishes from the Virgin River near Beaver Dam Wash, Arizona, and Mesquite, Nevada, were examined for cestodes on four dates throughout 1979. Seven parasites were found in P. argentissimus: Posthodiplostomtim minimum (metacercariae), Diplostomum spathaceum (metacercariae), Bothriocephalus acheilognathi. Gijrodactijlus sp., Lernaea cypri- nacea, Trichodina sp., and Ichthyophythirius multifiliis. Fungal infections were noted on two fish during the study. Seventeen Virgin River roundtail chub, Gila robusta seminuda, were examined from two of the four sites in 1985 and 64 specimens from Beaver Dam Wash were examined in 1979. Gila robusta seminuda was infected with Posthodiplosto- mum minimum (metacercariae) and Bothriocephalus acheilognathi, the Asian fish tapeworm. This cestode probably gained entrance into the ichthyofauna of the Virgin River from red shiners, Notropis lutrensis, and has the potential of being very detrimental to the endemic and endangered fishes of the Virgin River. Parasite loads were correlated with water quality and habitat disturbance, with highest number and frequency occurring in "disturbed" sites. Low river flows and increased total dissolved solids appear to be associated with a higher parasite frequency and mean number in fishes of the Virgin River. These data represent the first known published records for parasites of the woundfin minnow and Virgin River roundtail chub.

There is a paucity of information on the etc. (David 1947, Dogiel 1958, Hoffman parasitofauna of the woundfin minnow, 1967).

Plagopterus argentissimus , and other species The primary objectives of this study were as of fish from the Virgin River, Utah-Arizona- follows: Nevada. Many of the fishes in the Virgin River 1. Identify the species of parasites inhabiting the are endemic and have been hsted as endan- woundfin minnow at selected sites in the Virgin River gered species, the woundfin included. Hoff- in Utah. 2. Determine the frequency of occurrence, abundance, man (1967) lists no parasites for the woundfin. and temporal variation of parasites for P. argentissimus Other common fishes in the Virgin River in the summer during the normal period of low flow. drainage include the Virgin roundtail chub, 3. Determine the relationship bet^^'een parasitism and Gila robusta seminuda; speckled dace, the immediate habitat of the host. Rhinichthys osculus; Virgin spinedace, Lepi- 4. Determine the pathogenicity of the parasite to the host. domeda mollispinis; desert sucker, Cato- stomus clarki; flannelmouth sucker, Cato- In a previous study conducted during 1979 stomus latipinnis; and the introduced red (Greger 1983), woundfin minnows examined shiner, Notropis lutrensis. Parasites of these during February and June near Beaver Dam later species are also poorly known (Hoffman Wash, Arizona, were not parasitized by ces- 1967). Parasites can have adverse effects on todes. Cestodes were present, however, in fish populations. Changes in incidence, inten- the foreguts of P. argentissimus and increased sity, or parasite species infecting or infesting a in both number and frequency from Septem- host can provide important clues to the health ber to December. Frequency of infection of and status offish host populations. To under- woundfin with cestodes was much less near stand management options, it is essential to Beaver Dam Wash, Arizona, than was true also know the life cycle of the parasite and its further downstream in Nevada. This sug- effiects at various levels of infection. For exam- gested that woundfin may be more vulnerable ple, parasitism can be responsible for reduced to parasitism in an agriculturalK' disturbed growth rates, reduced egg production, poor habitat than in a more natural environment. swimming performance, aberrant behavior. Because the Virgin River near St. George,

'Department of Zoology, Brigham Young University, Provo, Utah 84602. ^Department of Biology, University of Nevada, Las Vegas, Nevada 89154.

662 October 1986 Heckmann ftal.:Woundfin Minnow Parasites 663

Utah, exhibits similar agricultural distur- salmon and trout infected with helminths bances, our hypothesis was that the parasite (Smith and Margolis 1970, Heckman 1983). load in the fish population near St. George These data also demonstrate some nutritional would be higher than in the less disturbed or growth impairments for infected fish. sections of Virgin River in Utah. Other researchers (Wardle 1933, Dogiel The life cycles of cestodes and other para- 1958, Dombroski 1955) have reported that sites of fishes from the Virgin River have not adult pseudophyllidean cestodes can affect been determined in detail. In general, fishes host nutrition and survival. Severe occlusion can be both definitive and intermediate hosts (impaction) of the gut has been reported for for cestodes. Reproductively mature adult infected salmon (Dogiel 1964) and appeared cestodes present in fish will release eggs from to affect the nutritional status in severe cases. gravid proglottids while in the intestine of the Impaction by parasites would also affect re- host. The eggs passs through the host's anus productive potential. Williams and Halvorsen and may settle in the stream sediments. For (1971) negated the belief that contents of the many cestodes, increasing temperature fish host intestine represent an unlimited causes the operculate eggs to hatch, releasing source of food for cestodes. Impaction and a ciliated coracidium (motile oncosphere). Cy- reduced growth and vigor would also reduce clopoid copepods (first intermediate host) in- reproductive potential. gest these larvae and become infected. The Other indirect effects of cestode adults on oncosphere sheds its ciliated coat in the gut of their hosts have been demonstrated in the the copepod and burrows through the intesti- laboratory. Boyce and Clarke (1983) deter- nal wall to the hemocoel, where it develops mined that Sockeye salmon yearlings infected into a procercoid larvae (Cheng 1973). This with tapeworms had a reduced ability to adapt mesacestode-type larva cannot become infec- to seawater as evidenced by increased mortal- tive to a definitive host for about two to three ity and elevated plasma sodium levels. Boyce weeks, until cercomer formation (Cheng and Behrens-Yamada (1977) also reported 1973). If a fish ingests an infected copepod, Sockeye salmon juveniles infected with the the adult cestode may commence develop- same cestode, Eiibothrium salvelini, to be ment in the intestine of the host. Although more sensitive to zinc toxicity. These effects larval (pleroceroid) development in a second could make the infected fish less vigorous and intermediate host (such as a smaller fish) is more susceptible to predation during its sea- possible, it is unlikely to occur in the Virgin ward migration. River ichthyofauna, since no primarily pisciv- The Asian fish tapeworm, Bothriocephalus orous fishes are present. It seems more proba- acheilognathi, introduced into this country by ble that development of the adult cestode in imports of grass carp, has been described as a

Virgin River fishes occurs following ingestion dangerous parasite in Europe (Bauer et al. of an infected copepod. Direct development 1981). This cestode has apparently become of the adult pseudophyllidean cestode Eu- established in the ichthyofauna of southern bothrium salvelini following ingestion of in- Utah. fected Cyclops sp. by Sockeye salmon, The most common fish parasite found in Oncorhynchus nerka, has been reported by this survey was the metacercarial state of the Smith (1973) from a lake in British Columbia. digenetic trematode, Posthodiplostomum min-

The effects of adult cestodes upon fish hosts imum. "Black spot, " for example, is caused by have not been studied in detail. Rees (1967), metacercarie found in melanin-pigmented after an extensive review of the literature, cysts in the skin. This larval stage of flukes reached no definitie conclusions regarding may be found in all tissues of fish (Spall and the lethal effects of adult cestodes. Other in- Summerfelt 1969b). vestigators have suggested that adverse effects are considerable. Smith (1973) reported Materials and Methods that noninfected salmon smolts grew 5%-7% longer and 17%-24% heavier than infected The 1979 collections were made in Febru- smolts. Field observations and swimming ary, June, September, and December near performance tests suggested cases of reduced Beaver Dan Wash, Arizona, and Mesquite, swimming abilities and earlier fatigue in Nevada (Fig. 1). At each location, the foregut 664 Great Basin Naturalist Vol. 46, No. 4

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SCALE October 1986 HECKMANNETAL: WOUNDFIN MiNNOW PARASITES 665

Table 2. Summary of parasite data from woundfin captured at each of four locatious 27-28 July (N = 25) and 23-25 August (N = 23). August data are in parentheses. 666 Great Basin Naturalist Vol. 46, No. 4

Table 3. Results of parasite inventory for other fish species examined from Twin Bridges, 27-28 July (1-12) and 23 August (13-15) 1985. October 1986 Heckmann etal: Woundfin Minnow Parasites 667

Table 5. Frequency of occurrence (%) and mean number of the cestode, Bothrioceplialus acheilognatlii, (Order: Pseudophyllidea) from the foreguts of fishes collected from the Virgin River near Beaver Dam Wash, Arizona, 1979. Abbreviations are as follows: R = Rhinichtnys osculus; G = Gila robusta; L = Lepidoineda; P = Plagopterus; N = Notropis lutrensis.

F. Month Ratio N February

June

September

Decembt No. 4 Great Basin Naturalist Vol. 46, 668

ol Fo>,ho.U,.b„o,„, .,i.» n (PI fron, Fig^ 2a. b. The ,ne,acercarial stage '''VlTJrlLrHemofrS'grR) .rB.'Hs„,„.,s.N„.ee„eapsula.io„(E)ofd,ela,vaU,ema,.,dea.do,ga,.e,,mpre.^,..o^^^^^^ 21^-UUA. encapsulation. Magnilkatlon. 2a-100X, has occurred near the site of metacercarial October 1986 670 Great Basin Naturalist Vol. 46, No. 4 infection of P. niinimum metacercariae, in Fife Lake, Michigan, dying in large numbers. This represents an example of a questionable cause-and-eflFect relationship because the parasite is ubiquitous and usually numerically abundant. More than circumstantial evidence is required to substantiate an allegation of P. minijnum being a cause for fish mortality. Wild fish, with several hundreds of encysted metacercariae in the liver, sinus venosus, heart, and kidneys, are often observed to suf- fer no obvious debilitating effects. Colley and Olsen (1963) found as many as 991 metacercariae per bluegil, with metacercariae so dense as to be clumped en masse. Spall and Summerfelt (1969a) have observed 2,041 metacercariae in a bluegill from an Oklahoma reservoir. Mortality due to stress and trauma from penetration of the cercariae has been observed in the laboratory following exposure of suitable host fish to high numbers of cercariae (Hunter 1937, Bedinger and Meade 1967). Host reactions following cercarial penetration include petechial hemorrhage at the site of Fig. 4. A scanning electron micrograph of the Asian fish invasion followed by congestion of surround- tapeworm, Bothriocephalus acheilognathi, from the in- ing venules and local edema, and an aggrega- testine of the Virgin River roundtail chub, Gila rohusta seminuda. Note the pit-viper shaped scolex (SC) and tion of leucocytes at the point of entry, partic- numerous proglottids (P). Photographed at lOOX magnifi- ularly the phagocytic elements. Pathological cation. effects include increased rate of excretion, increased plasma globulin and albumin, increased liver respiration, and decreased he- adult worm, this parasite has become of major matocrits (Smitherman 1964). Hemorrhage or concern to fish and game officials throughout a decrease in erythropoiesis would reduce he- the country. E.xcellent reviews of the histo- matocrits. The increase in the plasma proteins pathology, biology, life history, control, and may represent a homeostatic response to the management oi Bothriocephahis are found in nutritional demands of the parasite, altered a series of papers bv Nakajima and Egusa liver function, or effects on capillary perme- (1947a, b, c, 1976a, b). ability. The Asian fish tapeworm, characterized by

After encystment (19 days), mortality infre- its arrow or heart-shaped scolex (Fig. 4), has

quently occurs. There is no experimental evi- been a dangerous parasite for cultured grass dence to indicate mortality or other detrimen- carp and German carp fingerlings in Europe

tal effects from the occurrence of encysted (Bauer et al. 1981). In Europe it has also been metacercariae. found in European catfish, guppies, mosquito fish, and other species (Hoffman 1983, Hoff- and Shubert 1984). In the United States Bothriocephalus acheilognathi = man it has been found in golden shiners and fat- (B. gowkongenesis = head minnows (Hoffinan 1976), as well as in B. opsalichthydes) grass carp, Colorado scjuawfish, and moscjuito The Asian fish tapeworm, Bothriocephalus fish. We add speckled dace, roimdtail chub. acheih)gnathic represents a new introduction Virgin spinedace, woundfin, and red shiner to

in North America, brought in through imports that list. of grass carp to this country from China. Be- The best known carj^ parasite transported cause of the new introduction and size of the to the fish ponds of many countries with the Heckmann ETAL: WouNDFiN Minnow Parasites

Fig. 5a, b. Trichodina (T) infesting the gill lamellae (G) oi Plagopterus argentissmus. Note the macronucleus (M) and

cilia (arrow) characteristic of this ciliate. There is tissue granulation and hypertrophy (gh) of the host gill tissue near one parasite. lOOOX magnification. 672 Great Basin Naturalist Vol. 46, No. 4

Chinese carp is Bothriocephalus acheilo- these were described as new only because gnathi { = B. gowkongensis, = B. op- they were found on a different host or in an- salichthijdis) (Bauer et al. 1981). All Eu- other geographic location. In many cases the ropean countries that culture carp in large descriptions were inadequate since the uni- quantities now have this pathogen. The form body structure of these ciliates yields few spread of this parasite to new localities usually characters for differentiation of the species results in heavy infection of young fishes dur- (Lom 1961, 1970, Mueller 1937). The inexact ing the first years after it appears. Bothrio- and insufficient descriptions of most early au- cephalus acheilognathi , a thermophyllic para- thors make the identification of many species site, can infect many fish species. Presumably doubtful. But the recently employed silver- it traveled to the United States by airplane in impregnation technique of Klein and Chat- grass carp shipped from Asia. ton-Lwoff (Corliss 1953) reveals details of the adhesive disk that are important features of trichodinid taxonomy. Padnos and Nigrelli Trichodina: Trichodinosis (1942) used the silver-impregnation tech-

This is a ciliated protozoan that was com- nique to determine the ciliar patterns of tri- monly observed on the gills of the woundfin chodinids. But, according to Lom (1958), minnow in August (Table 2). Raabe (1950) was the first to employ this tech-

This ciliate is ubiquitous among fish para- nique in the study of the structure of the sites throughout the world and usually is of adhesive disk. minor concern for fish health. Members of the Trichodina rarely give rise to pathological genus Trichodina Ehrenbert (Family; Urce- manifestations of disease. It may be sporadi- olariidae Stein) are commonly seen on all cally found in living fish, but it will only multi- kinds of aquatic animals. In fish they may ply in moribund and weakened ones. A settle on the skin in such numbers as to ob- macronucleus, mironucleus, and numerous scure the normal structure (Fig. 5a, 5b), and food vacuoles are to be seen in the cytoplasm. they are easily recognized by their similarity In our study we observed Trichodina on the to a suction disk. Classification methods have gill surface (Fig 5a, 5b) of woundfin minnows been reviewed by Tripathi (1954). Trichodina in August. parasitizes the skin, gills, and urinary bladder of the fish and is found both in freshwater and Discussion the sea. The species of Trichodina that occur on Deacon and Hardy (1984) referred to seg- North American freshwater fishes have not ments of the Virgin River above Washington received the attention that they have in other Diversion and above Mesquite Diversion as areas of the world even though they are one of relatively undisturbed. Segments of the river the most important groups of ectoparasites of below these two diversions were referred to as freshwater fishes. Frequent references to tri- disturbed largely by irrigation withdrawals. chodinids parasitizing fish occur in fish cul- Table 7 demonstrates that mean and mini- ture literature but the species are not named, mum ffows in May-November were substan- as in the case for our study. Only Mueller tially reduced at Bloomington below the (1937, 1938), David (1947), Lom (1963), Lom Washington Diversion in 1985. Table 8 and Hoffman (1964), Hoffman (1967), and demonstrates a similar reduction in flow at Wellborn (1967) have made major contribu- Riverside, below the Mesquite Diversion in tions to the knowledge of the taxonomy and 1979. In addition, water quality in disturbed

distribution of Trichodina of North American segments of Virgin River is also reduced, freshwater fishes. Because of their small size, largely as a conse(iuence of its use for agricul- supposed lack of specific characters, and diffi- tural irrigation (Sandberg and Sultz 1985). In culty of removal from their hosts, they have June 1985 discharge from a salt spring (Pah been largely ignored. Tempe Spring) suddenly increased dramati- More than 90 species of Trichodina have cally, resulting in degradation of water quality been described from the skin and gills of throughout the Utah portion of the Virgin marine and freshwater fishes of the world River (Table 9). Therefore, our 1979 data (Hofi'man 1967, Wellborn 1967). Manv of clearly contrast parasite loads in fishes ex- October 1986 HECKMANNETAL: WOUNDFIN MiNNOW PARASITES 673

Table 7. Provisional mean, maximum, and minimum daily discharge (cfs) of the Virgin River at Hurricane and Bloomington, Utah, in 1985. 674 Great Basin Naturalist Vol. 46, No. 4 tional complication of a sudden reduction in of the Virgin River. water quality throughout the entire Utah seg- The discovery of the Asian fish tapeworm, ment of the river one to two months prior to B. acheilognathi, in the fish population of the the time of our collections. Nevertheless, it is Virgin River is of major concern. The parasite clear that the parasite burden in fishes of Vir- was probably introduced into the U.S. by the gin River living in more disturbed habitats is grass carp. It is considered to be especially much higher than for the same species living dangerous in Europe, where it was also intro- in less disturbed habitats. duced. W. L. Minckley (personal communi- Cestodes (Bothriocephalus acheilognathi) cation) reports that it is especially damaging to occurred in all Cyprinids inhabiting the lower Colorado squawfish at the Dexter National mainstream of the Virgin River in Arizona and Endemic Fish Hatchery in Deming, New Nevada in 1979 (Tables 5, 6). The exotic red Mexico. The high incidence of infection with shiner, Notropis lutrensis, was infected more large numbers of tapeworms in the endan- frequently and with a greater number of ces- gered roundtail chub near Beaver Dam Wash todes per individual than were all native spe- (Table 5) demonstrates the probability that it cies except the Virgin roundtail chub, Gila is similarly damaging to roundtail chubs. rohusta seminuda. Infection frequency and Other native fish species showed lower inci- density were variable seasonally, with heavi- dence of infection, but all cyprinids were in- est parasite loads in general occurring in fall fected at levels that could severely damage and winter and lightest parasite loads in sum- the populations. The exotic red shiner was as mer (Tables 5, 6). The woundfin in the "dis- susceptible to infection at the roundtail chub. turbed" segment of the lower mainstream Of the 17 chubs we examined from the river (Table 6) was more heavily infected than was near St. George in July and August 1985, only the population in the "undisturbed" segment 3 (18%) contained Asian fish tapeworms. We

(Table 5). The red shiner was equally heavily suggest that this is most likely a reflection of infected in both river segments (Tables 5, 6). the fact that the tapeworm is just beginning to In 1985 cestodes were not detected in establish itself in the Utah segment of the woundfin minnows at any of the four locations river. The tapeworm probably arrived in the sampled in Utah. Since we sampled only dur- spring of 1984 along with the red shiner, ing late July and August, it is possible that the Notropis lutrensis, which first appeared in absence ofcestodes reflects only seasonal vari- April collections offish from the Virgin River. ation. Both frequency and density of Red shiners first became common in the St. trematode infection in woundfin, however, George portion of the Virgin River during the are much greater in the lower, more dis- summer of 1985. They were one of the most turbed portion of the river near St. George heavily infected species in the lower river in

(Table 2). 1979 (tables 5, 6). Twenty-four of 88 red shin- The reduced flows near St. George may ers (27%) collected from the lower Virgin force fish into slow-flowing pools or ponded River near Mesquite, Nevada, on 15 August waters. The more ponded conditions proba- 1985 contained 37 adult Asian tapeworms. bly permit the development of dense popula- The red shiner, an excellent host for the Asian tions of cercariae that are released by snails, tapeworm, was recently established in the an intermediate host in the trematode life Utah portion of the Virgin River and probably cycle. These same conditions make the fish brought the cestode into Utah. more vulnerable to piscivorous birds, facilitat- ing completion of the trematode life cycle. Acknowledgments The degraded water quality resulting from agricultural return flows may also increase We thank Drs. Glenn Hoffman and Lauritz stress on the fish population, which may mani- A. Jensen for the identification of the Asian fest itself in an increased parasite load. If this fish tapeworm. This study was funded by the is a significant factor, the increased total dis- Utah Division of Wildlife Resources (Randy solved solids from increased flows of Pah Radant). James Allen and the Electron Optics Tempe Springs beginning in summer 1985 staff' at Brigham Young University provided (Table 9) may result in an increased parasite space and help for the scanning electron mi- burden in fishes throughout the Utah portion croscopy part of this study. October 1986 Heckmann et al. Woundfin Minnow Parasites 675

Literature Cited Hoffman, G. L. 1958, Experimental studies on the cercaria and metacercaria of a strigeid trematode, Postho-

diplostomum minimum. Expt. Parasitol. 7: 23-50. 1965. Experimental AVAULT, W , Jr., and R Allison. J. 1967. Parasites of North American freshwater biological control of a trematode parasite of fishes. University of California Press, Berkeley bluegill. Expt. Parasitol. 17; 296-301. and Los Angeles. 486 pp. Bauer, O N , S Egusa, andG L Hoffman 1981. Para- 1976. The Asian tapeworm, Bothriocephalus gow- sitic infections of economic importance in fishes. kongenesis, in the United States, and research needs Pages 425-443 in W. Slusarski, ed., Review of in fish parasitology. Proceedings Fish Farming Con- advances in parasitology. Polish Academy of Sci- ference and Annual Convention Catfish Farmers of ence. Texas, Texas A & M University 1976; 84-90.

Bedinger, C. a , Jr., and T G Meade 1967. Biology of a 1983. Asian fish tapeworm, Bothriocephalus op- new cercaria for Posthodiplostoimim minimum sarichthydis, prevention and control. Fish Dis- (Trematoda: Diplostomidae). Parasitol. 53: J. ease Leaflet: USFWS: USDA: 1-4. 985-988. Hoffman, G L , and G Schubert 1984. Some parasites

BoYCE, N P , and S Behrens Yamada 1977. Effects of a of exotic fishes. Pages 233-261 in W. R. Courtney parasite Eubothrium salvelini (Cedstoda: Pseudo- and J. R. Staffer, eds.. Distribution, biology, and phyllidea) on the resistance of juvenile sockeye management of exotic fishes. Johns Hopkins Uni-

salmon {Oncorhijnchis nerka ) from Banine Lake, versity Press, Baltimore and London. British Columbia. Canadian Fish. Aquat. Sci. J. Hughes, R C 1928. Studies on the trematode family 34: 706-709. Strigeidae (Holostomidae) No. IX. Neascus van P., 1983. Eubothrium BoYCE, N. AND W. C Clarke cleavei (Agersborg). Trans. Amer. Micro. Soc. 47: salvelini (Cestoda: Pseudophyllidea) impairs sea- 320-341. ward adaptation of migrant sockeye salmon year- Hunter, G W , III. 1937. Parasitism of fishes in the lower lings Oncorhynchus nerka from Banine Lake, Hudson area. Pages 264-273 in A biological sur- British Columbia. Canadian Fish. Aquat. Sci. J. vey of the lower Hudson watershed. Biological 40: 821-824. Survey No. XI (1936), Suppl. to the Twenty-sixth Cheng, T C. 1973. General parasitology. Academic Ann. Rept., New York State Conservation Dept. Press. 965 pp. 1940. Studies on the development of the metacer- CoLLEY, F. C, AND A. C Olson 1963. Posthodiplosto- caria and the nature of the cyst of Posthodoplosto- 7nu7n minimum (Trematoda: Diplostomidae) in mum minimum (MacCallum, 1921) (Trematoda; fishes of lower Otay Reservoir, San Diego County, Streigeidae). Trans. Amer. Micro. Soc. 59; 52-63. California. Parasitol. 49: 149. J. Lom, J 1958. A contribution to the systematics and mor- Corliss, J O 1953. The Chatton-Lwoff silver impregna- phology of endoparasitic trichodinids from am- tion technique. Stain Tech. 28: 97-100. phibians, with a proposal of uniform specific char- Davis, H S 1936. Pathological studies on the penetration acteristics. J. Protozool. 5: 251-263. of the cercaria of the strigeid trematode, Diplosto- 1961. Protozoan parasites found in Czechoslo- 329-337. mumflexicaudum. J. Parasitol. 22: vakian fishes. I. Myxosporidia, Suctoria. ool. Listy 1947. Studies of the protozoan parasites of fresh- Fol. Zool. 10(24): 45-58. water fishes. U.S. Dept. Interior Fishery Bull. 1963. The ciliates of the family Urceoloariidae #41: 1-29. inhibiting gills of fishes (the Trichodinella-group).

Deacon, J E , and T B Hardy. 1984. Streamflow re- Acta Soc. Zool. Bohemoslov. 27: 7-19. quirements of woundfin (Plagopterus argentis- 1970. Observations on trichodinid ciliates from

simus): Cyprinidae in the Virgin River, Utah, Ari- freshwater fishes. Archiv f^ Protistenkunde 112: zona, Nevada. Festschrift for Walter W. 153-177. Dalquest. Pages 45-56 in N. V. Horner, ed. Mid- Lom, J AND G L Hoffman 1964. Geographical distribu- western State University Press. tion of some species of Trichodinids (Ciliata: Per- DoGlEL, V A. 1958. Ecology of parasites of freshwater itricha) parasitic on fishes. J. Parasit. 50: 30-35. fishes. In Parasitology of fishes. Oliver and Boyd, Miller, J H 1954. Studies on the life history of Edinburgh. Posthodiplostomum minimum (MacCallum, 1921). 1964. General parasitology. Oliver and Boyd, Ed- J. Parasitol. 40: 255-270.

inburgh and London. Mueller, J F. 1937. Some species of Trichodina (Ciliata) Dombroski, E. 1955. Cestode and nematode infection of from freshwater fishes. Trans. Amer. Micr. Soc. sockeye smolts from Banine Lake, British Colum- 56; 117-184. 93-96. bia. J.' Fish. Res. Bd. Canada 12: 1938. A new species oi Trichodina (Ciliata) from Ferguson, M S 1938, Experimental studies on the urinary tract of the muskalonge, with a reparti-

Posthodiplostomum minimum (MacCallum, 1921), tion of the genus. J. Parasit. 23: 251-258.

a trematode from herons. J. Parasitol. 24 (Suppl.): Nakajima, K , AND S. Egusa. 1974a. Bothriocephalus op- 31. sariichthydis Yamagutii {Cestoda: Pseudophyl- Greger, P. D. 1983. Food partitioning among fishes of the lidea) found in the gut of cultured carp, Cyprinus Virgin River. Unpublished thesis. University of carpio (Linne)—I. Morphology and taxonomy. Nevada, Las Vegas. Fish Pathology 9(1): 31-39. Heckmann, R A 1983. Eye fluke {Diplostomum 1974b. Bothriocephalus opsariichthydis Yamagutii

spathaceum) of fishes from the Upper Salmon {Cestoda: Pseudophyllidea ) found in the gut of cul- River near Obsidian, Idaho. Great Basin Nat. 43: tured carp, Cyprinus carpio (Linne)—II. Incidence 675-683. and histopathology. Fish Pathology 9(1): 40-45. —

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1974c. Bothriocephalus opsariichthydis Ya- Smith, H D , and L Margolis. 1970. Some effects of niagutii {Cestoda: Pseudophyllidea) found in the Euhothrium salvelini Schrank (1970) on sockeye gut of cultured carp, Cyprinus carpio (Linne) salmon (Oncorhynchus nerka Walbaum) in Ba-

III. Anthelmintic effects of some chemicals. Fish nine Lake, British Columbia. J. Parasitol. 56(11):

Pathology 9(1): 46-49. .321-322. 1964. Effects ofinfections with the 1976a. Bothriocephalus opsariichthydis Ya- SmithermanR O ,Jr strigeid trematode, Posthodiplostomum minimum magutii (Cestoda: Pseudophyllidea) found in the (MacCallum), upon the bluegill, Lepomis macro- gut of cultured carp, Cyprinus carpio (Linne) chirus Rafinesque. Unpublished dissertation. IV. Observations on the egg and coracidium. Fish Auburn University, Auburn, Alabama. 55 pp. Pathology 11(1): 17-22.

Spall, R D , and R C Summerfelt 1969a. Host-para- 1976b. Bothriocephalus opsariichthydis Ya- site relations of certain endoparasitic helminths of magutii (Cestoda: Pseudophyllidea) found in the the channel catfish and white crappie in an Okla- gut of cultured carp, Cyprinus carpio (Linne)—V. homa reservoir. Bull. Wild. Dis. Assoc. 5: 48-67. Ovicial effects of drying, freezing, ultraviolet rays, 1969b. Life cycle of the white grub, Postho- and some chemicals. Fish Pathology 11(1): 23-26. diplostomum minimum (MacCallum 1921: Trema-

Padnos, , AND R F NiGRELLi 1942. Trichodina M toda, Diplostomatidae), and observations on host- spheroidesi and Trichodina halli spp. nov. para- parasite relationships of the metacercariae in fish. sitic on the gills and skin of marine fishes, with Pages 218-230 in S. F. Snieszko, ed., A sympo- special reference to the life-history of T. sium of diseases of fishes and shellfishes. Special spheroidesi. Zoologica 27: 65-72. Publ. No. 5AFS. 1950. Uwagi Ureceolariidae (Ciliata-Per- Raabe, Z o Tripathi, Y R 1954. Studies on parasites of Indian fishes. itricha) skrzel ryb. Ann. Univ. M. Curie- III. Protozoa. 2. (Mastigophora and ciliophora). Sklodowska, Lublin 5: 292-310. Rec. Indian Mus. ,52: 221-230. Rees.G 1967. Pathogenesis of adult cestodes. Helminth. Wardle, R a 1933. The parasitic helminths of Canadian Abstracts (36): 1-23. animals: the Cestodaria and Cestoda. Canadian J.

Sandberg, G W , and L G Sultz 1985. Reconnaissance Res. 8: 317-333. of the quality surface water in the Upper Virgin Wellborn, T L , Jr 1967. Tricodina (Ciliata: Urceolari- River Basin, Utah, Arizona, and Nevada. idae) of freshwater fishes of the southeastern 1981-82. Utah Dept. of Natural Resources Tech. United States. Journal of Protozoology 14(3): Bull. 83: 1-69. 399-412.

Smith. H D 1973. Observations of the Cestode Euboth- Williams, H H , and O Halvorsen 1971. The inci- rium salvelini in juvenile sockeye salmon dence and degree of infection ofGadus morhua L. (Oncorhynchus nerka Walbaum) at Banine Lake, 1758 with Ahorthrium gadi Beneden 1871 (Ces- 30: of 19: British Columbia. J. Fish. Res. Bd. Canada toda Pseudophyllidea). Norway J. Zoology 947-964. 193-199.