Great Basin Naturalist
Volume 57 Number 1 Article 8
3-7-1997
Asian tapeworm (Bothriocephalus acheilognathi) in native fishes from the Little Colorado River, Grand Canyon, Arizona
Robert W. Clarkson Research Branch, Arizona Game and Fish Department, Phoenix, Arizona
Anthony T. Robinson Research Branch, Arizona Game and Fish Department, Phoenix, Arizona
Timothy L. Hoffnagle Research Branch, Arizona Game and Fish Department, Phoenix, Arizona
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Recommended Citation Clarkson, Robert W.; Robinson, Anthony T.; and Hoffnagle, Timothy L. (1997) "Asian tapeworm (Bothriocephalus acheilognathi) in native fishes from the Little Colorado River, Grand Canyon, Arizona," Great Basin Naturalist: Vol. 57 : No. 1 , Article 8. Available at: https://scholarsarchive.byu.edu/gbn/vol57/iss1/8
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]. Creat Basin Naturalist 57(]), © 1997, pp. 66--69
ASIAN TAPEWORM (BOTHRIOCEPHALUS ACHEIWGNATHI) IN NATIVE FISHES FROM THE LITTLE COLORADO RIVER, GRAND CANYON, ARIZONA
Robert W. Clarkson 1,2, Anthony T Robinsonl , and limothy L. HolTnagiel
AUSTRACT.-Examination ofgastrointestinal tracts ofnative cyprinids from the Little Colorado River (LCR) in Gr-.md Canyon, Arizona, 1990-1994, revealed varying rates ofprevalence and ioftapopulation levels ofAsian tapeworm (Bothria cepludw adwilob'ntJ1hi). Mean p
Key worcl.s: Bothriocephalus acheilognathi, parasitism, Gila cypha, Rhinichthys osclllus, Little Colorado River, conservation.
During this century, extinctions, extirpations, We report Asian tapeworm temporal and and declines of native fishes in the American numeric infection patterns in 2 native cyprinids Southwest have been attributed to introduc· from the Little Colorado River (LCR) in Grand tious of nonindigenous fishes and physical Canyon, Arizona. The LCR is the major spawn· habitat alterations (Miller 1961, Minckley and ing and early life rearing habitat of the largest Deacon 1968, Minckley and Douglas 1991). remaining population of the federally endan· Fish translocations also may introduce patho· gered humpback chub (Gila cypha) in the Col· gens and parasites (Hoffman and Shubert 1984). orado River Basin (Kaeding and Zimmennan Introduction and spread of Asian tapeworm 1983). Speckled dace (Rhinichthys osculus) is a (Bothriocephalus adIeilognathi) to the Colorado geographically widespread native species that River Basin provides an example of the poten· codominates the LCR fish assemblage with tial effects of such parasite translocations on humpback chub. We also present tapeworm native fishes. This cestode was first detected prevalence data for the nonnative cyprinids fat from the basin in minnows from the Virgin head minnow (Pim.eplwIes prom.elas) and com· Rivel; Arizona, Nevada, and Utah, in 1979 mon carp (Cyprinus carpio), and the cyprin (Heckmann et al. 1986). Heckmann et al. (1987, odontid plains killifish (Fundulus zebrinus). We 1993) later reported it from 2 Virgin River examine implications of Asian tapeworm trans tributaries, Beaver Dam Wash, Arizona, and location on conservation and recovery ofnative Muddy River and other Nevada localities. fishes in the Colorado River Basin. Recently, Asian tapeworm has been reported from the Colorado River (CR) and tributaries METHODS in Grand Canyon, Arizona (Brouder and Hoff· nagle in press), in the San Juan River in Utah The LCR was sampled in 1991-1994 from and New Mexico U. J. Landye, U.S. Fish and the confluence wilh CR upstream approxi Wildlife Service. personal communication). mately 15 km, where we collected primarily and in the Green River in Utah (T E. Chart, early life stage fishes for stomach content anal· Utah Division of Wildlife Resources, personal yses. We also accessed unpublished 1989-1990 communication). LCR data from the Arizona Game and Fish
IIWliearch Bl1Inch, Arlmn3 Game and Fi~h Depw.rtl'OoOlil. 2""1 West GfWPWlly Road, Phoenix. AZ8502.1. !!Pr=cnl addrcu: U.S. UllrlSu ofUeclanlllllon, r.O. Box 9980, Phoenix. AZ 8S068.
66 1997] AsIAN TAPEWORM IN NATIVE FISHES 67
Department. Sampling in 1991-1994 was pri Tapewonn infrdpopulations (mean number marily by seine and dip net, while earlier col per infected Rsh) in bumpback chub GI trdCts lections also inclnded trammel, gill, and hoop were 3.7 for larvae (n = 23), 3.5 for postlarvae net caphues of larger fish. Fish were mea (n = 15), 6.9 for age-O juveniles (n = 67), and sured to total length (mm) and preserved in 10.4 for age-l+ specimens (n = 12). Maxi 10% formalin immediately following capture. mum numbers observed in hwnpbaek cbub Larvae and early posllarvae were identified to were 12 in larvae, 9 in postlaIVae. 44 in age-O species using keys of Snyder (1981) and Sny juveniles, and 46 in age-l + specimens. Tape der and Muth (1990). Gastrointestinal (GI) worms accounted for a mean relative volume tracts were excised in the lab, where contents of GI tract contents of 51% (maximum 100%) were identified and enumerated when possi in infected humpback chub. ble. Relative volumes of GI tract content eate Infrapopulations in speckled dace were 0.5 gories were visually estimated. J. J. Landye of (n = 2) in larvae « 19 mm total length), 5.3 (n the U.S. Fish and Wildlife Service (personal = 10) in juveniles (19-50 mm), and 3.5 (n = communication 1991) made the initial identifi 32) in adults (>50 mm), wbile maximum den cation of this distinctive tapeworm, and it was sities were 1, 18, and 28, respectively. Relative later confirmed using Mitchell's (1994) key. volume of tapeworms in infected speckled dace averaged 38%. Tapewonn infrapopula RESULTS hons were 2 (n = 6; 6 maximum) in fathead minnow (17% relative volume), 3 (0 = 1) in The first observation ofAsian tapeworm in conunon carp « 1% relative volume), and 7 (n the LCR was from 2 subadult humpback chub = 1) in plains killifish (100% relative volume). collected in May 1990 (Minckley 1990). None of the 24 age-l+ humpback chub (>100 mm DISCUSSION total length), 3 age-O juveniles (51-100 mm), 12 postlarvae (26-50 mm), and 6 larvae «26 Seasonal (or ontogenetic) and annual differ mm) examined from 1989 were infected. Dur ences in prevalence of Asian tapeworm in ing 1990, 92.5% of age-O (including larvae) humpback chub and speckled dace presumably and 44.4% of age-l+ specimens harbored reflect complex interactions among environ tapeworms (Table 1). We did not detect Asian mental conditions and intermediate (eyclopoid tapeworm in the 1991 humpback cbub cohort copepod) and deRnitive bost populalions until it approached 50 mm in total length (Granath and Eseh 1983a, 1983b, Riggs and beginning in Septcmber. Prevalence in 1992 Esch 1987, Marcogliese and Esch 1989). Infra was 48% overall, but the tapeworm was not populalion dynamics of the parasite may be found in larval humpback chuh. We recorded related to temperature, temperature-depen the parasite in 1 of 62 early life stage bump dent rejection responses, immune responses, hack chub examined in 1993, and the parasite host distributions, density-dependent factors, was absent from 107 larvae examined in 1994 or other poorly studied phenomena (Granath (Table 1). and Escb 1983a). Asian tapeworm occun-ence in speckled dace Pathological effects of Asian tapeworm on also was greatest in 1990 at 46%; prevalence fish hosts may include intestinal abrasion and in 1991-1993 ranged from 5% to 14% (Table disintegration, loss or separation of gut micro 1). The cestode was absent from early life villi and enterocytes (Hoole and Nisao 1994), stages ofspeckled dace examined in 1994. or blockage and perforation of the GI tract Fathead minnow harbored Asian tapeworm (Hollinan 1980, Mitchell1994). Chronic ellects in 6 of 75 specimens (8%) collected between are not well studied but may include the 1991 and 1994 (Table 1). Single specimens of following: emacialion and anemia (Scott and plains hllillsb (n = 21) and common carp (n = Grizzle 1979); decreases in intestinal, liver, 4) were found infected during this period. The and pancrealic enzymes (Hoole 1994); reduced parasite was not found in 480 bluehead sucker growtb and reproductive capacity, depressed (Pantoste1tS discobolus), 7lflannelmoutb sucker swimming ability via elevated muscle fatigue, (Catostornu.> latipinllis), 21 channel catfish (leta and other debilitating influences (Heckmann lurus ,,"nctolttS), or 2 rainbow trout (Oncorhyn et al. 1986, Hoole 1994). Weakened IIsh may chus mykiss) examined from 1990 to 1994. develop secondary bacterial infections (Mitchell 68 GREAT BASIN NATURALIST [Volume 57
TABLE L Percent frequency of occurrence (sample size in parentheses) of Asian tapeworm (Bothriocephalus acheilo- gnathi) in gastrointestinal tracts of fishes from the lower Little Colorado River, Arizona, 1990-1994. With the exception oflarvae, age/stage designations are approximate. Dashes indicate no fish specimens were collected. Year Species and length 1990 1991 1992 1993 1994
HuMPBACK CHlJB larvae (~25 mm) 91.7(24) 0(50) 0(28) 1.8 (56) 0(107) postlarvae (26-50 mm) 100 (13) 3.0 (33) 100 (I) 0(6) older age-O (51-100 mm) 66.7 (3) 81.2 (32) 67.2 (58) age-l+ (>100 mm) 44.4 (18) 37.5 (8) 66.7 (12) 100 (1) SPECKLED DACE larvae «18 mm) 0(1) 0(128) 3.0 (33) 2.8 (36) 0(95) juveniles (19-50 mm) 60.0 (10) 4.0 (50) 26.7(30) 0(15) 0(1) adults (>50 mm) 0(2) 17.7(79) 14.4 (III) 50.0 (4) FATHEAD MINNOW larvae (~18 mm) 0(4) juveniles (19-50 mm) 0(3) 6.9 (29) 0(4) 0(3) adults (>50 mm) 0(2) 8.7 (23) 33.3 (6) COMMON CARP juveniles (51-100 mm) 25.0 (4) PLAINS KILLIfISH larvae (";;18 mm) 0(2) juveniles (19-50 mm) 0(5) 50.0 (2) 0(8) adults (>50 mm) 0(1) 0(3)
1994). Granath and Esch (1983c) showed that hosts), with most of those already endangered, Asian tapeworm significantly reduced labora threatened, or of special concern. The endan tory survivorship of mosquitofish (Gambusia gered poeciliid Gila topminnow (Poeciliopsis affinis) compared to controls, but cautioned o. occidentalis) ofthe Gila River subbasin may that these effects would not necessarily be be vulnerable to this parasite. Because biotic exhibited in the wild. changes to the Colorado River Basin resulting More research is needed to determine exact from fish and pathogen translocations are vir effects of this parasite on native fish popula tually ubiquitous and seemingly irreversible, tions in Grand Canyon and elsewhere, but they must be considered among the most seri clearly Asian tapeworm has the potential to ous threats to conservation and recovery of regulate fish populations. The observed patterns native fish populations, of Asian tapeworm prevalence and infrapopu latious in humpback chub and speckled dace ACKNOWLEDGMENTS in the LCR may arise from (1) mortality ofhosts with high infrapopulations, (2) density-depen This work was funded under Cooperative dent mortality of parasites, and (3) acquired Agreement 9-FC-40-07940 with the u.s. Bureau host resistance to reinfection (Anderson 1982). of Reclamation, Glen Canyon Environmental The fact that our study area is the humpback Studies, Flagstaff, Arizona. We thank D. Kubly chub's only major spawning and early life rear and S. Sacco of the Arizona Game and Fish ing site in Grand Canyon adds concern for the Department for 1989-1990 data, and D. Hen status ofthis population. drickson and C. Minckley for information on Since its initial detection in the Virgin River initial observations ofthe tapeworm from 1990. in 1979, the rapidity with which Asian tape C. Minckley, D. Kubly, W. Shoop, T. Dresser, worm has spread to different drainages of the J. Landye, W Persons, and an anonymous Colorado River Basin likely portends an even reviewer improved earlier drafts ofthis article. tual cosmopolitan basin distribution in lower elevations suitable to the parasite's thermophilic LITERATURE CITED life history. Roughly half of the native ichthy ANDERSON, R. M. 1982. Epidemiology. Pages 204-251 in ofauna in this geographic range comprises F. E. G. Cox, editor, Modern parasitology. Blackwell cyprinids (Asian tapeworm's most common Scientific Publications, Oxford, u.K. 1997] ASIAN TAPEWORM IN NATIVE FISHES 69
BROUDER, M. J., AND '[ L. HOFFNAGLE. In press. Distrib KAEDING, L. R, AND M. A. ZIM\lEHMAN. 1983. Life histOTY ution and prevalence of the Asian fish tapeworm, and ecology ofthe humpback chub in the Little Col Bothrj~)cephalus acheilognathi, in the Colorado River orado and Colorado rivers of the Grand Canyon. and tributaries, Grand Canyon, Arizona, including Transactions of the American Fisheries Society 112: two new host records. Journal ofthe Helminthologi 577-594. cal Society ofWashington. MAHUX;LIESE, D. J., AND G. WESCH. 1989. Alterations in GHANATH, W. 0., AND G. W. ESCH. 1983a. Temperature seasonal dynamics of Bothriocephalus acheilo[!,nathi and other factors that regulate the composition and in a North Carolina cooling reservoir over a scven infrapopulation densities of Bothriocephalus acheil year period. Journal ofParasitology 75: 378-382. ognathi (Cestoda) in Gambusia affinis (Pisces). Jour MILLER, R. R. 1961. Man and the changing fish fauna of nal ofParasitology 69: 1116-1124. the American Southwest. Papers of the Michig,m __,,' 1983b. A comparison of the seasonal dynamics of Academy of Science, Arts, and Letters 46: 365-404. Bothriocephalus acheilognathi in ambient and ther MINCKLEY, C. O. 1990. Final report on research conducted mally altered areas of a North Carolina cooling on the Little Colorado River population of the reservoir. Proceedings of the Helminthological Soci humpback chub, during April-May, 1990. Submitted ety onVashington 50: 205-218. to Arizona Game and Fish Department, Phoenix. ___. 1983c. Survivorship and parasite-induced host MrNCKLEY, W. L., AND J. E. DEACON. 1968. Southwestern mortality among mosquitofish in a predator-free, fishes and the enigma of "cndmlgered species." Sci North Carolina cooling reservoir. American Midland ence 159: 1424-1432. Naturalist 110: 314-323. MINCKLEY, '\Z L., AND M. E. DOUGLAS. 1991. Discovery HECKMANN, R. A., J. E. DEACON, AND P. D. GREGER. 1986. and extinction of western fishes: a blink of an eye in Parasites ofthe woundfin minnow, Plagopterus argen geologic time. Pages 7-17 in W L. MilH:kley and tissimus, and other endemic fishes from the Virgin J. E. Deacon, editors, Battle against extinction: native River, Utah. Great Basin Naturalist 46: 662-676. fish management in the American West. University HECKMANN, R. A., P. 0. GI\EGER, AND J. E. DEACON. 1987. ofArizona Press, Tucson. New host records for the Asian tapeworm, Bothrio MITCHELL, A. 1994. Bothriocephalosis. Chapter XII, pages cephalus acheilognathi, in endangered fish species 1-7 in J. c. Thoesen, editor, Suggested procedures from the Virgin River, Utah, Nevada, and Arizona. for the detection and identification of certain finfish Journal ofParasitology 73: 226-227. and shellfish pathogens. Fish Health Section, Ameri HECKMANN, R. A., P. 0. GREGER, AND R. C. FUHTEK. 1993. can Fisheries Society. The Asian tapeworm, Bothriocephalus acheilognathi, RIGGS, M. R., AND G. \i\Z ESCH. 1987. The suprapopulation in fishes from Nevada. Journal ofthe Helminthologi dynamics ofBothtiocephalus acheilvgnathi in a North cal Society ofWashington 60: 127-128. Carolina reservoir: abundance, dispersion, and pre HOFFMAN, G. L. 1980. Asian tapeworm, Bothriocephalus valence. Journal ofParasitology 73: 877--892. acheilognathi Yamaguti, 1934, in North America. Fisch Scan; A. L., AND J. ~. GRIZZLE. 1979. Pathology ofcyprinid und Umwelt 8: 69-75. fishes caused by Bothriocephalus gowkongenesis Yea, HOFFMAN, G. L., AND G. SCHUBERT. 1984. Some pm'asites 1955 (Cestoda: Pseudophyllidea). Journal of Fish of exotic fishes. Pages 233-261 in W R. Courtenay, Diseases 2: 69-73. Jr., and J. R. Stauffer, Jr., editors, Distribution, biol SNYDER, 0. E. 1981. Contributions to a guide to the cypri ogy, and management of exotic fishes. John Hopkins niform fish larvae of the upper Colorado River sys University Press, Baltimore, MD. tem in Colorado. Bureau of Land Management Bio HOOLE, 0. 1994. Tapeworm infections in fish: past and logical Sciences Series 3: 1--81. future problems. Pages 119-140 in A. W Pike and SNYDER, D. K, AND R. T. MUTH. 1990. Descriptions and J. w: Lewis, editors, Parasitic diseases offish. Samara identification ofrazorback, flannelmouth, white, Utah, Publishing Lirrlited, U.K. bluehead, and mountain sucker larvae and early HOOLE, D., AND H. NISA:'{. 1994. Ultrastructural studies juveniles. Colorado Division of Wildlife Technical on intestinal response ofcarp, Cyprinus carpio L., to Publication 38: 1-1.52. the pseudophyllidean tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934. Journal of Fish Dis Received 23 July 1996 eases 17: 623-629. Accepted 4 Decemher 1996