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Spread of an Exotic Fish-Gill Trematode: A Far-Reaching and Complex Problem

Andrew J. Mitchell United States Department of Agricultural, [email protected]

Robin M. Overstreet Gulf Coast Research Laboratory, [email protected]

Andrew E. Goodwin University of Arkansas at Pine Bluff

Thomas M. Brandt United States Fish and Wildlife Service

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Mitchell, Andrew J.; Overstreet, Robin M.; Goodwin, Andrew E.; and Brandt, Thomas M., "Spread of an Exotic Fish-Gill Trematode: A Far-Reaching and Complex Problem" (2005). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 441. https://digitalcommons.unl.edu/parasitologyfacpubs/441

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. fish health 11 feature ofessor at the ABSTRACT Andrew J. Mitchell Robin M. Overstreet Andrew E. Goodwin Thomas M. Brandt Mitchell is a fisheries biologist and at the Harry K. Dupree researcher Stuttgart National Aquaculture U. S. Department Center, Research Agricultural of Agriculture, Service, Stuttgart, Research Arkansas. He can be contacted at [email protected]. at The is a professor Overstreet University of Southern Mississippi, Laboratory, Gulf Coast Research Ocean Springs, Mississippi. pr a Goodwin is Center, Aquaculture/Fisheries University of Arkansas at Pine Bluff. of the U. S. Fish Brandt is director and Wildlife Service, National Fish Center, Hatchery and Technology Texas. San Marcos, ) serve as M. Ardea alba Melanoides tubercu- found on ornamental from wild populations from a lake in Pasco County, Heavy losses among cichlids, tetras, M. tuberculatus M. tuberculatus), and tropical cyprinids were first reported by Florida tropical fish producers in the early 1980s (Blazer and Gratzek 1985; and Overstreet 1988). These Vogelbein losses were attributed to an unidentified trematode infecting the gills of the fish. Richard Heard, Vogelbein, Wolfgang and one of the authors (RMO) com- pleted initial life cycle studies on the trematode in 1985 at the Gulf Coast Research Laboratory (GCRL) using the cercaria (the larval stage of a trematode that invades intermediate hosts) from an aquatic snail, the red-rim melania ( fish farms in Central Florida (Vogelbein and Overstreet 1988). These studies were replicated in 1992 (and at later dates) using similar or identical cercaria in in Texas. Independently, James Sullivan Independently, in Texas. (Centers for Disease Control, Atlanta, Georgia) found identically infected In Florida, in December 1985 and later. 1990, K. E. Knott found an unidentified cercaria from the red-rim melania in the San Antonio River near and at Texas, the San Antonio Zoo, Bexar County, Texas Landa Park, New Braunfels, Comal County, Trinity (Alberto Santos and Harold D. Murray, unpublished studies). Knot and Murray University, (1991) reported the responsible agent as the “mystery fluke.” This trematode,one of the authors sent to (RMO) in January 1992, was determined to be the same trematode and observed. The previously studied metacercaria, a juvenile form of the trematode, was tuberculatus ) and the great egret ( ) and the great egret ) C. Nycticorax and for more Xiphophorus hel- the gill trematode, has caused serious losses among fish has caused serious losses among the gill trematode, Carassius auratus Butorides virescens Melanoides tuberculatus , were experimentally ), in the Comal River near San Marcos, Texas. The parasite appears The near San Marcos, Texas. ), in the Comal River that was collected from REVIEWS IN FISH HEALTH FISH IN REVIEWS A SERIES SPONSORED BY THE AFS FISH HEALTH SECTION HEALTH AFS FISH BY THE SPONSORED A SERIES ), green swordtail ( Centrocestus formosanus emerging from the aquatic snail Felix domesticus) ), and an unidentified rat as natural hosts

black-crowned night-heron ( ), an exotic snail, has been found in 15 southern and western states. This snail ), an exotic snail, has been found

In 1956, Walter Martin and some colleagues In 1956, Walter An exotic trematode, often referred to as the Etheostoma fonticola Gambusia affinis raised by tropical fish producers since the early 1980s and is believed to be harmful to and is believed to be harmful fish producers since the early 1980s raised by tropical listed endangered fountain darter including the federally wild fish populations, ( has a and Utah. The gill trematode fishes from Hawaii, Florida, Texas, to infect in many birds and occasionally some mam- involving definitive hosts (aquatic complex life cycle several fish species). In the United hosts (aquatic snails and mals) and intermediate heron ( States, the green Centrocestus formosanus, A far-reaching and complex problem complex and A far-reaching Spread of an exotic fish-gill trematode: trematode: fish-gill an exotic of Spread definitive hosts. The first intermediate host, the red-rim melania ( The first intermediate host, the red-rim definitive hosts. latus exhibits resistance to desiccation, molluscicides, and disinfectants and has been docu- exhibits resistance to desiccation, mollusks. Both the gill trematode and its exotic mented to out-compete established United States. snail host continue to spread in the August 2005 | www.fisheries.org | Fisheries August 2005 | www.fisheries.org History of the gill trematode in the United States Introduction found larval stages of a trematode identified as formosanus Stenomelania newcombi ditches in Kaneohe, Oahu, Hawaii (Martin 1958). After finding the trematode the snail, Martin in (1958) reported the western mosquitofish ( lerii), nycticorax for other stages of the same parasite. Several other species, including the goldfish ( and cat ( infected. For the next 27 years, there was no addi- tional report of this or a similar parasite from any region of the presently recognized United States. “gill trematode,” affects the health of both wild and cultured fish species. The trematode is identified tentatively as than 20 years has been a subject of interest and than 20 years has been a subject of interest produc-concern among fisheries scientists and fish ers. This trematode evokes broad interest because it birds and is carried by federally-protected aquatic the invasive exotic snail several and infects many fish hosts, including informa- endangered species. This article contains identification, biology, tion on the history, and unusual aspects of an exotic spread, pathology, trematode now infecting fish in the United States. biolog- The information recorded here comes from ical observations and research efforts. also found in five fish species (Mexican Figure 1. The fountain darter (Etheostoma fonticola), blind/cave tetra Astyanax fasciatus, a federally-listed endangered species. common carp Cyprinus carpio, blue tilapia Oreochromis aureus , redbelly Figure 2. Fountain darters infected (top) and not infected with Centrocestus formosanus. Proliferation tilapia Tilapia zillii, and green swordtail)

of branchial tissue in infected fish may cause the TEXAS STATE UNIVERSITY, from the San Antonio River. opercular flaps to remain flared. Although the destructive gill trema- tode was not identified, it was noted Figure 3. Complex life-cycle of the gill trematode GLENN LONGLEY, that the parasites found in Florida and Centrocestus formosanus involving a definitive bird SAN MARCOS (or mammal) host (A), the first intermediate snail host Texas represented an introduction of a (B), and an intermediate fish host (C). (a) single species that was similar to C. for- Metacercaria from fish eaten by bird, (b) metacercaria mosanus found in other parts of the released from cyst in intestinal tract of definitive host, world. where it attaches to gut epithelium and matures into The destructive nature of the an adult worm within in a few days producing eggs that are shed into the host’s lumen and then defecated into the trematode was recognized by Blazer water; (c) released trematode egg is eaten by snail and then and Gratzek (1985) and Vogelbein hatches, releasing the miracidium; (d) germinal cells from and Overstreet (1988) who described miracidium develop, ultimately producing a redia; (e) redia the damage to the gills that resulted asexually produces large numbers of the cercaria that are from the trematode infection. shed into water; (f) cercaria passively engulfed by fish or actively penetrate it; the tailless cercaria locates near a Juvenile tropical fish losses associated cartilage support in the gill filament; (g) cercaria develops with this trematode were estimated at into an encysted metacercaria and becomes encapsulated $3.5 million (USD) annually by a moderate to extensive cartilaginous response; large (Francis-Floyd et al. 1997). The prob- numbers can harm gills and fish host; (h) metacercaria lem was serious enough that in the exhibiting cartilaginous encapsulation. mid-1990s research efforts were directed to find means to control the snails that serve as vectors for the trematode. In 1997, a study was pub- lished to support an application by the Florida’s Department of

Agriculture and Consumer Services, CERCARIAE WITH HEART-SHAPED BODY BY CHRIS WILSON, UTAH DIVISION OF WILDLIFE RESOURCES, LOGAN Division of Pesticides for an EPA Special Local Needs (SLN) registra- tion for the chemical Bayluscide® to control snails (Francis-Floyd et al. 1997). The trematode is still a serious problem within the tropical fish FOUNTAIN DARTERS BY GLENN LONGLEY, TEXAS STATE UNIVERSITY, SAN MARCOS industry, but snail control efforts have made the problem manageable. GREEN HERON BY TOM VEZO WILDLIFE PHOTOGRAPHY, WWW.TOMVEZO.COM On 19 July 1996, 11 specimens of fountain darter (Etheostoma fonticola), federally listed as an endangered species, were collected from the Comal River, Comal County, Texas, inspected, and then released (Figure 1). One of the specimens had inflamed gills, but it was not exam- ined microscopically. On 2 October 1996, 85% of 70 specimens of the darter collected from the Comal River were observed with inflamed and protruding gills (Figure 2). The next day, three of these fish were examined by David Huffman of Texas State University at San Marcos, and the abnormal gills were found to be associated with encysted metacer- cariae. Most encysted individuals had

12 Fisheries | www.fisheries.org | vol 30 no 8 fish health 13 feature . C. Pimephales Centrocestus and their speci- , golden shiner Morone chrysops proserpine shiner Rhinichthys osculus) Rio Grande darter has a complex life cycle , fathead minnow , and Pecos gambusia ) could be experimentally , Comanche Springs pupfish , Comanche Springs C. formosanus Ictalurus punctatus ; McDermott 2000). Mitchell et al. ; McDermott 2000). Dionda diaboli), sp. at Gandy Warm Springs, Millard sp. at Gandy Warm sp. from Israel and the United States, and the United sp. from Israel ) from red-rim melania taken from the M. saxatilis , and sunshine bass female Gambusia Centrocestus formosanus There are a few reports and observations of fish There are a few reports and observations After metacercariae of the gill trematode of the gill After metacercariae were Cyprinella proserpina), Cyprinodon elegans) Etheostoma grahami) Gambusia nobilis that involves three life stages (Figure 3). The metac- Hosts of the gill trematode × male formosanus infected with this or a similar trematode that are not or Hawaii. Olsen and Pierce from Florida, Texas, (1997) reported a similar trematode steel- infecting Oregon, River, head trout in cages in the Willamette between but there is at least one meristic difference described material of Springs, Utah County, and Goshen Warm County, Utah Division of Wildlife respectively (Chris Wilson, Resources, personal communication). Both springs contain red-rim melania populations. This observa- tion is sufficient to add Utah to the list of states with the gill trematode. infected with cercariae (similar to cercariae of In 2004, 50.0% (5 of 10) of the foun- Comal River. River tain darters examined from the San Marcos trematodewere positive (1 to 3 cysts per fish) for (4 of 145) cysts; this value compared with a 2.8% from prevalence for infection in darters collected the San Marcos River in 1997 and 1998. found in mens. The red-rim melania has been in the geothermal waters in Oregon but not Anderson, River or its tributaries (T. Willamette University of Colorado, unpublished data). During 2002, tropical fish from Georgia exhibiting the gill trematode but, were submitted to HKD-SNARC; considering that the red-rim melania has not been reported from Georgia, we think the parasite might have been imported within the fish from another state. In the spring of 2003, the parasite was observed in western Utah in speckled dace ( and (2004) using species-specific polymerase chain reac- chain polymerase using species-specific (2004) as identifiable material assays against tion Centrocestus of two distinct species indicated Additional DNA sequences are needed to better DNA sequences are Additional genus. the taxonomy of this understand and San Marcos rivers, evaluated from the Comal springs at three west Texas they were documented County; San Solomon Verde (San Felipe Creek, Val and Phantom Lake Springs, Reeves County; where they infected five Springs, Jeff Davis County) fishes (endangered): Devils state or federally listed River minnow ( ( ( ( ( species (2002) reported that four major aquaculture (channel catfish promelas Notemigonus crysoleucas , , and yellow , a trematode Notropis amabilis) also exhibited heavy C. formosanus contained the most severe contained the most Astyanax mexicanus) Ameiurus natalis) Over the next 2 months, fishes of 10 different next 2 months, fishes Over the From April 1997 until May 1998, more than 350 From April 1997 until May 1998, more than Information on the trematode found in the foun- Etheostoma lepidum) Etheostoma lepidum) August 2005 | www.fisheries.org | Fisheries August 2005 | www.fisheries.org species, including the fountain darter, were col- darter, the fountain species, including San Marcos (Hays the Comal and lected from sent to three fish disease rivers and Texas) County, Health Center, laboratories (Fish diagnostic Center, Fish Technology Pinetop, Arizona; and Harry K. Bozeman, Montana; Aquaculture Research Dupree—Stuttgart National Stuttgart, AR). The Center [HKD-SNARC], from the Comal River were majority of the fish with cysts of the same trema- found to be infected tode. darter and greenthroat darter The fountain ( undergone necrosis, but still exhibited recognizable exhibited but still necrosis, undergone eye-spots. infections. The Texas shiner ( shiner infections. The Texas Mexican tetra ( bullhead ( infections. In the two darters, most of the encysted infections. In the two darters, most of the trematodes appeared necrotic. The host reaction of the darters apparently affected the trematode but response also detrimentally affected the gills (host was found will be discussed later). In 1996, no cyst in the gills of fish from the San Marcos River. Comal specimens of the fountain darter from the and San Marcos rivers were sent to HKD-SNARC trematodeto determine the significance of the Only infection on health and survival of this darter. Marcos 4 of 145 of these fish collected from the San the mean River had the cysts in their gills, and gill arch. intensity for the 4 fish was 0.25 cysts per River All 209 fish examined from the Comal more exhibited infections, with 48 fish averaging more than than 50 cysts per gill arch and 17 having In light of 100 per arch (one with 191 per arch). surprising the evident gill damage, we consider it with that any of these 21 to 35 mm TL individuals noticed more than 100 per arch could survive. We infec- flared opercular flaps associated with heavy tions (average of 50 or more per arch) on the Comal River fountain darters (Figure 2). Both river systems harbored large populations of the exotic red-rim melania. tain darters was presented by one of the authors (AJM) at the Third International Symposium on Aquatic Animal Health in 1998 in Baltimore, Maryland. A parasitologist (Rokkam Madhavi) from India attending the symposium observed the presen- tation on the Comal River trematode and suggested that the parasite was native to Asia but now found in a number of coun- tries. After further consultation with one of the authors (RMO), it was clear that this appeared to be an appropriate tentative identification for the trema- the tode However, (Mitchell et al. 2000). identification of U.S. material still remains question- able because of slight morphological differences and recent molecular data. The study by Dzikowski et al. 14 Centrocestus formosanus only knownfirstintermediatehostof 40 mm.Thissnail,thered-rim melania,isthe spire-shaped shellswithshellheightsof5to Figure 4. fish health Melanoides tuberculatus, feature in theAmericas. ones withgeothermal waters,hadornowhave con- including themost southernstatesandseveralwestern Texas in1964(Murray1964).Atleast15 states, first documentedinthecontinental UnitedStatesin to year-round warmwaters. unpublished data),itappearsthat thesnailisrestricted United States(T. Anderson, UniversityofColorado where thered-rimmelaniahasbeenfoundin and Almeyda-Artigas1994).Basedoninformation world (Abbott1973;Dudgeon1986;Amaya-Huerta its tropicalandsubtropicallocationsthroughoutthe 1989). EventhoughnativetoAsia,itpresentlyinhab- salinities upto30ppt(Roessleretal.1977;Smith 2005). Itoccursprimarilyinfreshwaterbutcansurvive above 17.0°Candbelow32.5°C(MitchellBrandt Experimentally, thesnailcansurvivetemperatures than 70mm(Figure4;Murray1975;Burch1982). mantle’s edge,anditsshellcanreachaheightofmore with roundedwhorlsandfleshyprotuberancesonthe depth discussionofthishostiswarranted. infections;therefore,amorein- controlling trematode wide. Thesnailhostusuallyservesasthetargetfor world- continental UnitedStates,hostthetrematode other membersofthesamefamilynotfoundin family Thiaridae(Dudgeon1989).It,alongwithtwo trumpet snail,andcornucopiabelongsinthe also calledtheMalaysianburrowingsnail, rim melania,thefirstintermediatehost.Thatsnail, The earlylarvalstagesasexuallydevelopinthered- Heard andOverstreet,USM,unpublishedstudies). (Martin 1958;PremvatiandPande1974;Vogelbein, orders,mightalsoserveasfinalhosts and Rodentia eating mammals,includingmembersoftheCarnivora alba) heron ( site, buttodate,wehaveconfirmedonlythegreen mammals. Manypiscivorousbirdsmayhostthepara- occurs intheGItractofspecificpiscivorousbirdsand percichthyid, andpoecilidfamilies.Theadultstage gobid,ictalurid,kuhliida,mugilids,percid, odontid, the centrarchid,characid,cichlid,cyprinid,cyprin- United States,knownfishhostsincludemembersof Rana occasionally theintestinalwallandmusclesoffrogs ercarial stageinfectsthegillsofmanyfishspeciesand The red-rimmelaniahasanelongateconicalshell showing as hostsinthecontinentalUnitedStates.Fish- spp. (Salgado-Maldonadoetal.1995).Inthe Butorides virescens) and thegreategret( Melanoides tuberculatus Ardea was (Mitchell etal.1982;OverstreetandCurran2004). placement, secondarybacterialinfection,anddeath infectionsinfishresultserioustissuedis- trematode Overstreet andCurran2004).Occasionally, heavy fish beingeatenbyadefinitivevertebratehost(e.g., behavior inamannerthatimprovesthechancefor host ing (Hoffman1999)andmayalsomodify minimalmechanicaldamageandhemorrhag- produce Migrationofcercariaethroughhosttissuesmay todes. few fishmounthostresponsesthataffectthetrema- site relationships, wheredamagetothehostisnot life this parasiteisin contrasttowell-adaptedhost-para- death ofheavily-infectedindividuals. Responseto much functionalgilltissue,probably resultinginthe within thecyst,buthostresponse stilldestroys of rate morethanonecyst(Figure 6). Inthetwospecies and Gratzek1985).Theencapsulationmayincorpo- eosinophils, heterophils,andlymphocytes(Blazer other inflammatorycells,includingmacrophages, tion maybefurthercompromisedbyaninfluxof surface areaoftherespiratoryepithelium.Gillfunc- destroying thenormalgillarchitecture,reducing encapsulations maycontinuetothicken,ultimately Vogelbein andOverstreet1988)(Figure5).The lation aroundtheparasite(BlazerandGratzek1985; then chondrocytesthatformacartilaginousencapsu- that apparentlydifferentiateintochondroblastsand characterized byaproliferationofhostfibroblasts parasite inducesanunusualinflammatoryresponse ament cartilage(BlazerandGratzek1985).The nexttothegillfil- after infection,thecercarialodges water fishes(Mitchelletal.2000,2002).Within 1h seriousalterationsinthegillsofmanyfresh- produces Pathology ofthegilltrematode human liverfluke includingtwohumanpathogens,the trematodes al. 1990).Lastly, thered-rimmelania harborsother younginternally(Jacobson1975;Pereraet brood parthenogenicallyandto its abilitytoreproduce petes someestablishedmollusks,partlybecauseof and Brandtunpublisheddata).Thesnailout-com- hold bleachfor60min(Dudgeon1982;Mitchell and 3of10individualssurvivedfullstrengthhouse- 1991). Thesnailcanliveupto8daysinadrypan and disinfectants(Dudgeon1982;Francis-Floyd it exhibitsresistancetodesiccation,molluscicides, Anderson, UniversityofColoradounpublisheddata). firmed wildstocksofthered-rimmelania(T. United States. not yetbeenfoundinred-rimmelaniathe have Murray 1978).Thetwohumantrematodes (Abbott 1952;DundeeandPaine1977;Nollen oriental lungfluke well asaneyefluke( Etheostoma Centrocestus formosanus causeharmtotheirfishhosts,and Few trematodes Because thered-rimmelaniahasanoperculum, Fisheries |www.fisheries.org | vol30no8 in theComalRiver, dies thetrematode (Opisthorchis sinensis) (Paragonimus westermani) Philopthalmus gralli) , unlikemosttrematodes, and the of birds , as 15 fish health R. and (Gastropoda: feature 1991. Mystery Aquaculture Report in 1999. Parasites of North 1991. Use of Bayer 73 to H. D. Murray. encapsulated by proliferated and 1997. Use of Bayuluscide (Bayer Melanoides tuberculata (Francis- fluke in Thiaridae) in the San Antonio Zoo, San Combined Annual Antonio, Texas. Society of Malacologists Meetings, Western and American Malacological Union, American freshwater fishes, 2nd ed., Comstock Publishing Associates, Cornell University Press, Ithaca, New York. Klinger. Klinger. 73) for snail control in fish ponds. Journal of Aquatic Animal Health 9:41-48. Series. Florida Department of Agriculture and Consumer Services, Tallahassee. rDNA polymorphism for identification of heterophyidae infecting freshwater fishes. Diseases of Aquatic Organisms 59:35-41. control snails in ornamental fish ponds. Pages 467-490 Knot, K. E., Hoffman, G. L. Francis-Floyd, R., J. Gildea, P. Reed, Francis-Floyd, R., J. Gildea, P. Francis-Floyd, R. Gill filaments of an experimentally infected Figure 6. Figure of hybrid striped bass containing multiple metacercariae Centrocestus formosanus cartilage tissue. (Muller) ornamental fish ponds, a ponds, fish ornamental M. tuberculatus Melanoides 2004. Use of 1977. Ecology of ) in New Orleans, A. Paine. I. Paperna. and (Muller, 1774) (Gastropoda: (Muller, Melanoides tuberculata 1982. Aspects of the desiccation and The red-rim melania can be purchased in many The red-rim melania pet shops throughout the country and over the pet shops throughout be taken not to allow it to Internet. Care must in melania-free warm waters. become established transferred on vegetation from The snail can also be hatchlings, 2 to 3 mm shell one site to another (snail to aquatic vegetation); there- height, readily attach advise anyone to transport fore, we do not melania vegetation from water inhabited by red-rim the to those not inhabited by the snail. Limiting of the spread of the carrier snail will limit the spread gill trematode. Floyd et al. 1997). Fish should not be stocked for at 1997). Fish should Floyd et al. Bayluscide has U.S. after application. least 10 days Special Local Protection Agency Environmental in Florida and Arkansas only, Needs labels for use single season Section 18 and has been legal under in other southeastern states. Emergency Exemptions unpublished studies). In studies). unpublished treatment of Bayluscide at 1.1 kg/ha of pond bot- of pond 1.1 kg/ha at of Bayluscide treatment nuisance snail for controlling tom is effective including populations Opisthorchis sinensis intermediate host of the human liver fluke ( Louisiana. The Nautilus 91:17-20. Flowers, dynamics and productivity of tuberculata Prosobranchia: Thiaridae) in Hong Kong. Journal of Zoology 208:37-53. Kong Thiaridae (Gastropoda: Prosobranchia). Malacological Review 22:39-53. tolerance of four species of benthic mollusca Hong Kong. from Plover Cove Reservoir, 24:267-271. The Veliger Experimental and Descriptive Malacology, Niwot, Colorado. the snail, Centrocestus formosanus. Dzikowski, R., M. G. Levy, M. F. Poore, J. R. M. F. Dzikowski, R., M. G. Levy, _____. 1989. Ecological strategies of Hong Dundee, D. S., _____. 1986. The life cycle, population Dudgeon, D. . 1985. in the United Proliferated cartilage surrounding Proliferated Centrocestus ) of the oriental Figure 5. Figure cyst of metacercarial R. J. Almeyda- ). Proceedings of Melanoides tuberculata and J. B. Gratzek. C. formosanus and Paragonimus (Nishigori, 1924) Price, 1932 Thiara granifera 1952. A study of an intermediate 1982. North American freshwater 1994. Confirmation of (10 ppm), a ® snail host ( Artigas. Cartilage proliferation in response to metacercarial infections of fish gills. Journal of Comparative Pathology 95:273-280. formosanus Keys to the freshwater gastropods snails. V. of North America. Society for (Trematoda: Heterophyidae) in Mexico. (Trematoda: Research and Reviews in Parasitology 54:99-103. lung fluke ( the United States National Museum 102:71-116. The Nautilus 87:29. The control of The control Burch, J. B. Blazer, V. S., V. Blazer, Abbott, R. T. References _____ . 1973. Spread of Amaya-Huerta, D., States is complex because of the involvement of States is complex because of which include exotic and three life stages, some Managing the parasite will be endangered species. avian hosts are highly mobile, difficult because the has and is spreading infected human intervention many different fish species are fish and snails, and practical approach will be to susceptible. The most develop methods to treat and prevent the further and hardy exotic snail. spread of this very prolific that red-rim melania with Research has shown mm can be killed by a 3 min shell heights of 2 to 40 residential exposure to 50°C (temperature of most and and commercial hot water systems; Mitchell dipnets, Brandt 2005). Therefore, items such as containing boots, and seines that contact waters red-rim melania should be dipped in this hot water bath for at least 5 min before being used in any waters without the snail. No other effective method of dis- infection is presently a low reported; however, concentration of Roccal- D Plus quaternary ammonium product, for 24 h appears promising in killing all red-rim melania tested (Mitchell and Brandt August 2005 | www.fisheries.org | Fisheries August 2005 | www.fisheries.org Control of the gill trematode of the gill Control threatening. Perhaps one reason some groups of groups reason some one Perhaps threatening. and introduced, both native fishes, so susceptible are being naive to the results from their to mortality introduced parasite. Proceedings and Abstracts from the Joint Mitchell, A. J., A. E. Goodwin, M. J. Salmon parasites in Cuba. Malacological Review Annual Meeting. Berkeley, California and T. M. Brandt. 2002. Experimental 23:47-52. Jacobson, M. K. 1975. The freshwater infection of an exotic heterophyid Premvati, G., and V. Pande. 1974. On Tarebia ganifera Centrocestus formosanus, prosobranch, , in Oriente, trematode, in four Centrocestus formosanus (Nishigori, 1924) Cuba. The Nautilus 89:106. aquaculture fishes. North American Journal Martin, W. E. 1958. The life histories of some of Aquaculture 64:55-59. Price, 1932 and its experimental infection Hawaiian heterophyid trematodes. Journal Murray, H. D. 1964. Tarebia granifera and in white leghorn chicks. Japanese Journal of of Parasitology 44:305-323. Melanoides tuberculata in Texas. Abstract. Parasitology 23(3):79-84. McDermott, K. S. 2000. Distribution and Annual Reports American Malacological Roessler, M. A., C. L. Beardsley, and D. C. infection relationships of an undescribed Union 1964:15-16. Tabb. 1977. New records of the introduced digenetic trematode, its exotic intermediate _____. 1975. Melanoides tuberculata (Muller), snail, Melanoides tuberculata (Mollusca: host, and endangered fishes in springs of Las Moras Creek, Bracketville, Texas. Thiaridae) in South Florida. Florida West Texas. Thesis, Southwest Texas State Bulletin of the American Malacological University, San Marcos. Union 1975:43. Scientist 40:87-94. Mitchell, A. J., and T. M. Brandt. 2005. Nollen, P. M., and H. D. Murray. 1978. Salgado-Maldonado, G., M. I. Rodriguez- Temperature tolerance of red-rimmed Philophthalmus gralli: identification, growth Vargas and J. J. Campos-Perez. 1995. melania, an exotic aquatic snail established characteristics, and treatment of an oriental Metacercariae of Centrocestus formosanus in the United States. Transactions of the eyefluke of birds introduced into the (Nishigori, 1924) (Trematoda) in American Fisheries Society 134:126-131. continental United States. Journal of freshwater fishes in Mexico and their Mitchell, A. J., C. E. Smith G. L. and Parasitology 64:178-180. transmission by the thiarid snail Melanoides Hoffman. 1982. Pathogenicity and Olsen, R. E., and J. R. Pierce. 1997. A histopathology of an unusually intense trematode metacercaria causing gill tuberculata. Studies on Neotropical Fauna infection of white grubs (Posthodiplostomum cartilage proliferation in steelhead trout and Environment 30(4):245-250. m. minimum) in the fathead minnow from Oregon. Journal of Wildlife Diseases Smith, B. J. 1989. Traveling snails. Journal of (Pimephales promelas). Journal of Wildlife 33:886-890. Medical and Applied Malacology 1:195- Diseases 18:51-57. Overstreet, R. M., and S. S. Curran. 2004. 204. Mitchell, A. J., M. J. Salmon, D. G. Huffman, Defeating diplostomoid dangers in USA Vogelbein, W. K., and R. M. Overstreet. 1988. A. E. Goodwin, T.M. Brandt. and 2000. catfish aquaculture. Folia Parasitologica Life-history and pathology of a heterophyid Prevalence and pathogenicity of a 51:153-165. heterophyid trematode infecting the gills of Perera, G., M., Yong, J. R. Ferrer, C. Arrinda, trematode infecting Florida-reared an endangered fish, the fountain darter, in and O. Amador. 1990. Effectiveness of ornamental fishes. International two central Texas spring-fed rivers. Journal three biological control agents against Association for Aquatic Animal Medicine of Aquatic Animal Health 12:283-289. intermediate hosts of snail-mediated Proceedings 19:138.

16 Fisheries | www.fisheries.org | vol 30 no 8