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And a Myxozoan (Myxobolus Sp.) Associated with Vertebral Deformities in Cyprinid Fishes from the Willamette River, Oregon

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And a Myxozoan (Myxobolus Sp.) Associated with Vertebral Deformities in Cyprinid Fishes from the Willamette River, Oregon Journal of Aquatic Animal Health 16:116±129, 2004 q Copyright by the American Fisheries Society 2004 A Digenean Metacercaria (Apophallus sp.) and a Myxozoan (Myxobolus sp.) Associated with Vertebral Deformities in Cyprinid Fishes from the Willamette River, Oregon M. L. KENT,* V. G. WATRAL, AND C. M. WHIPPS Center for Fish Disease Research, Department of Microbiology, 220 Nash Hall, Oregon State University, Corvallis, Oregon 97331-3404, USA M. E. CUNNINGHAM Department of Fisheries and Wildlife, 104 Nash Hall, Oregon State University, Corvallis, Oregon 97331-3803, USA C. D. CRISCIONE Department of Zoology, Cordley Hall 3029, Oregon State University, Corvallis, Oregon 97331-2914, USA J. R. HEIDEL Veterinary Diagnostic Laboratory, College of Veterinary Medicine, Magruder Hall, Oregon State University, Corvallis, Oregon 97331-0381, USA L. R. CURTIS AND J. SPITSBERGEN Department of Environmental and Molecular Toxicology, 1007 Agricultural and Life Sciences, Oregon State University, Corvallis, Oregon 97331-7301, USA D. F. MARKLE Department of Fisheries and Wildlife, 104 Nash Hall, Oregon State University, Corvallis, Oregon 97331-3803, USA Abstract.ÐA high prevalence of vertebral deformities has been observed in various ®shes, es- pecially cyprinids, from certain regions of the Willamette River for many years. One proposed source of these deformities is exposure to toxicants. Histological evaluation of affected chiselmouth Acrocheilus alutaceus revealed that all lesions associated with vertebrae were associated with metacercariae of digenean trematodes. Approximately half of the northern pikeminnow Ptycho- cheilus oregonensis had infections in which metacercariae were associated with these lesions. Metacercariae were also associated with vertebral lesions in three of four affected peamouth Mylocheilus caurinus. Many metacercariae that were present within the vertebral bodies were associated with bony dysplasia and bony proliferation in all three species. We also evaluated the association of the metacercariae with the vertebral deformities, using intact ®sh that had been cleared with trypsin. Fish from the affected regions had a much higher prevalence of metacercariae and deformities and a greater abundance of metacercariae than those in the reference site. Chi- selmouths had more deformities and metacercariae than northern pikeminnow. In all ®sh species, 77% of deformities were directly associated with metacercariae; in chiselmouths, about 95% of the deformities exhibited this relationship. Two types of metacercariae were identi®ed in affected ®sh: Apophallus sp. (Heterophyidae) and a neascus type (Strigeidida). The Apophallus sp. appeared to be more closely associated with the skeleton deformities. A Myxobolus sp. morphologically similar to M. cyprini was also associated with the vertebral lesions in about 50% of the northern pikeminnow and 5% of the chiselmouths. Intact plasmodia were found in somatic muscle, and lesions containing free spores were often located at bone surfaces. This survey demonstrates that metacercariae (probably Apophallus sp.) and a Myxobolus sp. are major causes of the vertebral deformities seen in cyprinid ®shes from certain regions of the Willamette River. Certain regions of the Willamette River in anthropogenic contamination, and the U.S. Envi- Oregon are considered to have been impacted by ronmental Protection Agency has declared Port- land Harbor a Superfund site (Waite and Carpenter 2000). The Oregon Department of Environmental * Corresponding author: [email protected] Quality (ODEQ) has reported a high prevalence of Received January 6, 2004; accepted June 1, 2004 vertebral anomalies in various ®sh species from 116 PARASITES AND SKELETAL LESIONS 117 this river. The ODEQ studies found that 1±74% of Ferry (RM 72). The reference site was Kiger Is- northern pikeminnow Ptychocheilus oregonensis in land, which is near Corvallis (RM 135) on the the Willamette River had vertebral anomalies, the Willamette River. All ®sh were collected from 20 greatest prevalence being found at river mile (RM) to 29 July 2002. Fish were collected by beach 27±55, an area known as Newberg Pool (Ellis et seine, killed with an overdose of Finquel (tricaine al. 1997). The prevalence of deformities generally methanesulfonate; Argent Chemical Laboratories, decreased with distance upstream and downstream Redmond, Washington) and preserved in 10% of Newberg Pool. In a subsequent survey by Mar- buffered formalin. Preserved whole ®sh in for- kle et al. (2002) no differences in the patterns of malin were radiographed with a Faxitron MX-20 caudal deformities in Willamette River ®shes were radiography unit, and the images were evaluated observed between RM 29 and 71, whereas pre- for the presence of vertebral deformities as de- caudal deformities were substantially more nu- scribed by Markle et al. (2002). merous around the Newberg Pool area (RM 45± Preserved ®sh were decalci®ed before process- 50). Most of the 14 ®sh species in which they ing for histology. Tissues were placed in Cal-Ex reported vertebral deformities were cyprinids, II solution (Fisher Scienti®c, Pittsburgh, Pennsyl- these deformities being most prevalent in chisel- vania) for 24±48 h. Samples were then rinsed in mouth Arcocheilus alutaceus. running tap water for 2 h, after which they were Skeletal deformities in ®shes can be caused by returned to 10% buffered formalin for 24 h. Tis- various contaminants, including cadmium, lead, sues were embedded, and sagittal sections pre- zinc, and organophosphate pesticides (Bengtsson pared by standard histological techniques were 1974; Bengtsson et al. 1975, 1985; Hiraoka and stained with hematoxylin and eosin. Larger ®sh Okuda 1983). Therefore, vertebral deformities in were divided into thirds in cross sections before ®sh have been suggested to serve as bioindicators processing. Three 6-mm-thick sections were pre- of pollution (Bengtsson 1979; Lemly 1997). How- pared from each block at approximately 50-mm ever, other causes of vertebral deformities are not intervals. directly related to chemicals, such as low pH (Fro- To allow for better correlation with the presence jnar 1977), warmer temperature (Kwain 1975), and of metacercariae associated with vertebral chang- nutritional de®ciencies (Mehrle and Meyer 1975, es, we also examined ®sh in whole mounts in 1982; Mauck et al. 1978; Bengtsson 1979; Walton which ®sh were ®rst cleared with trypsin and et al. 1984; Akiyama et al. 1986). Moreover, sev- stained with alcian blue and alizarin red S (Din- eral infectious agents can cause vertebral defor- gerkus and Uhler 1977; Potthoff 1984). Cleared mities in ®sh, including viruses (LaPatra et al. ®sh were placed in a Petri dish and covered with 2001), bacteria (Conrad and DeCrew 1967; Kent glycerin; the entire ®sh was then examined at 253 et al. 1989), and a wide variety of parasitesÐpar- or 503 magni®cation. Total numbers of metacer- ticularly myxozoans and metacercariae of dige- cariae and the presence and absence of the para- nean trematodes (e.g., Baturo 1980; Bucke and sites directly associated with vertebral deformities Andrews 1985; Hedrick et al. 1998; Matthews et were recorded. Morphological information from al. 2001). the parasites was obtained by using wet mount A multidisciplinary effort was undertaken by preparations, and all measurements of metacer- toxicologists, ®sheries biologists, and pathologists cariae and myxozoan spores were made with a to elucidate the cause of these deformities in ®shes SPOT camera and computer program (SPOT ver- from the Willamette River, including investiga- sions 3.5.5. for Windows; SPOT Diagnostic In- tions into potential chemical or infectious causes. struments, Sterling Heights, Michigan). Here we report the prevalence, associated patho- For molecular analysis of the myxozoan, muscle logical changes, and description of parasites from tissue determined by microscopy to contain My- northern pikeminnow, chiselmouths, and pea- xobolus sp. spores was frozen or placed in 95% mouths from the Willamette River, Oregon. ethanol. To extract DNA, we used the DNeasy Kit (QIAGEN Inc., Valencia, California). A region of Methods the small subunit (SSU) ribosomal DNA (rDNA) Samples and specimen processing.ÐUnderyear- was ampli®ed by means of the polymerase chain ling and yearling northern pikeminnow, chisel- reaction (PCR) with primers (18E and Myxgen2r) mouths, and peamouths were collected from the and conditions as described by Kent et al. (2000). Willamette River near the affected zones: Ash Is- Using the above PCR primers and the methods of land, Newberg Pool (RM 51.5), and Wheatland Whipps et al. (2003), we obtained a sequence ap- 118 KENT ET AL. TABLE 1.ÐHistological evaluation of the prevalence and association of parasites with lesions compared with vertebral deformities identi®ed by radiograph (X-ray) analysis in chiselmouths (CHM), northern pikeminnow (NPM), and pea- mouths (PEAM) from the Willamette River. Chiselmouths were identi®ed as underyearlings, peamouths as yearlings, and northern pikeminnow as either underyearlings (21) or ®sh more than 1 year old (11). The term ``lesions'' indicates parasites associated with vertebral lesions. Note that fewer lesions were detected by histology in ®sh that were positive for deformities by radiography because vertebral deformities were not always located by the former method. Metacercariae Myxobolus Fish X-ray No. Prevalence (%) Lesions (%) Prevalence (%) Lesions (%) NPM (21) Positive 28 12/28 (43) 12/24 (50) 9/28 (32) 8/24 (33) NPM (21) Negative 18 4/18 (22) 2/3 (0) 5/18 (25) 0/3 (0) NPM (21) Combined 46 16/46 (35) 14/27 (37) 14/46 (30) 8/27 (30) NPM (11) Positive 21 16/21 (76) 3/17 (18) 18/21 (86) 13/17 (76) NPM (11) Negative 6 1/6 (16) 0/0 (0) 2/6 (33) 0/0 (0) NPM (11) Combined 27 17/27 (63) 0/0 (0) 20/27 (74) 0/0 (0) CHM Positive 21 21/21 (100) 21/21 (100) 2/21 (9) 0/12 (0) CHM Negative 5 4/5 (80) 0/0 (0) 1/5 (20) 0/0 (0) CHM Combined 26 25/26 (96) 0/0 (0) 2/26 (8) 0/0 (0) PEAM Positive 4 3/4 (75) 3/4 (75) 0/4 (0) 0/4 (0) PEAM Negative 4 1/4 (25) 0/0 (0) 0/4 (0) 0/0 (0) PEAM Combined 8 4/8 (50) 0/0 (0) 0/8 (0) 0/0 (0) proximately 850 base pairs (bp) long.
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