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Distribution and occurrence of the exotic digenetic trematode (Centrocestus formosanus), its exotic snail intermediate host (Melanoides tuberculatus), and rates of infection of fish in springs systems in Western Texas.

Centrocestus formosanus, an Asian gill trematode dependent on an operculate snail, red-rim melania snail (Melanoides tuberculatus), as an intermediate host, is thought to have been introduced into North America at least as early as the 1970s (Roessler et al., 1977; Blazer and Gratzek, 1985). Since that time, the red-rim melania snail and trematode have established populations throughout warm-water systems in 15 states (Roessler et al., 1977; Rader et al., 2003; Mitchell et al., 2005, 2007; Tolley-Jordan and Owen, 2008). In North America, the spread of the parasite has been limited because red-rim melania snails are thermally restricted to waters that range between 18 and 32[degrees]C (Mitchell and Brandt, 2005). In Texas, they have established populations in the San Antonio, Guadalupe, and Rio Grande river basins (McDermott, 2000). While the trematode is dependent upon red-rim melania snails in North America, the second intermediate host, fish, is more generalized (Vazquez-Colet and Africa, 1939; Nishigori, 1924; Scholz and Salgado-Maldonado, 2000) and includes many species native to Texas, some federally listed or statelisted as threatened or endangered species (Schenck and Whiteside, 1976; Rader et al., 2003; Fleming et al., 2011).

The trematode encysts in the lamellae of gills of the intermediate fish-host and may result in significant damage of gills and depressed respiratory function at high rates of metacercarial infection (Blazer and Gratzek, 1985; McDonald et al., 2006). More specifically, the metacercariae may cause edema, hemorrhage, loss of respiratory epithelium, fusion of lamellae, proliferation and hyperplastic distortion of cartilage of gills, and destruction of the secondary lamellae of gills thereby reducing respiratory function (Alcaraz et al., 1999; McDonald et al., 2006). Poor respiratory performance resulting from damage of gills in heavily infected fishes has been shown to cause mass mortality of cultured fishes and pathogenic effects (Mohan et al., 1999; Ortega et al., 2009).

Because mortalities of fish are ascribed to high rates of metacercarial infection when fishes are restricted to ponds for production of fish (Paperna, 1996; Mohan et al., 1999; Ortega et al., 2009), it follows that similar rates of mortality might be expected with fish that populate thermally stable spring-fed systems such as those located within Edwards Plateau and Trans Pecos regions of Texas, particularly during periods of reduced discharge. Thermally stable springs within these regions have water temperatures within the range of tolerance for C. formosanus and maintain them year-round (Hubbs, 2001). As a result, they are considered hotspots for infection by C. formosanus (Murray, 1971). Unfortunately, many of the native and endemic fish that populate these spring-fed systems in Texas are federally listed and statelisted as threatened or endangered (Schenck and Whiteside, 1976; Brune, 1981; Hubbs, 2001) and may be at risk for infection of gills by pathogenic parasites (McDonald et al., 2006). Therefore, we examined the geographic distribution and co-occurrence of red-rim melania snails and C. formosanus in native fishes (including federally protected Comanche Springs pupfish Cyprinodon elegans, Leon Springs pupfish C. bovinus, Pecos gambusia Gambusia nobilis, Big Bend gambusia G. gaigei, Clear Creek gambusia G. heterochir, and Devils River minnow Dionda diaboli and Texas-protected, proserpine shiner Cyprinella proserpina, Rio Grande darter Etheostoma grahami, and Conchos pupfish Cyprinodon eximius) collected at 10 spring systems in western Texas during 1999 and 2011, to determine expansion of range after a decade. More specifically, we assessed species-specific percentages of trematode-infection in fish that reside in these spring systems, the number of cysts per fish, and development of parasites (ability of metacercariae to mature in infected gills). We also collected red-rim melania snails at sites within nine of the spring systems and determined rates of infection by Centrocestus formosanus. Finally, we conducted an experiment in the laboratory to determine the differential susceptibility to infection and development of cysts of C. formosanus in Pecos and Big Bend gambusia and western mosquitofish (G. affinis). Given the evidence of the pathogenic effects on fish of the parasitic trematode, it follows that monitoring the spread and rates of infection, particularly for threatened and endangered species, is of critical importance because it can potentially alter the demographics of populations.

Materials and Methods--We sampled 10 spring systems located within Edwards Plateau and Trans Pecos regions of western Texas during 1999 and 2011 (Fig. 1). Sampled sites (n = 16) within the spring systems contained species of fish of concern, and shared common environmental settings included consistent water temperatures that are within the range of the thermal tolerance of the red-rim melania snail, excluding the Big Bend National Park Refugium Pond that exceeds tolerance limits (Mitchell and Brandt, 2005; Fig. 1; Table 1). Dissolved oxygen and temperature (YSI[C], Model 58 and Professional Plus, YSI Incorporated, Yellow Springs, Ohio; salinity (YSI[C], Model 33 and Professional Plus); and pH (Hanna[R] instruments, Model Piccolo, Hanna Instruments US Inc., Woonsocket, Rhode Island, and YSI[C] Professional Plus) were measured during collection of specimens.

We attempted to collect 20 specimens of protected fish from each spring system using dip-nets and seines. We also collected individuals of other species of fish that comprised the assemblage. All specimens of fish were overdosed with MS-222 (tricaine methanesulfonate, Finquel[R] Argent Chemical Laboratories, Inc., Redmond, Washington), preserved in 10% formalin, and transported to the San Marcos National Fish Hatchery and Technology Center in San Marcos, Texas. Total length of fish was measured to the nearest millimeter. We determined rates of metacercarial infection for each fish by removing the four left gill arches. Gill arches were examined with a dissecting microscope to enumerate and identify the developmental stage of all enclosed metacercariae. Developmental stages were determined as either immature (having visible eyespots within the cyst) or developing (having faded eyespots or an X-shaped excretory vesicle within the cyst; Chen, 1948; Fleming et al., 2011). We determined the total number of metacercarial cysts in a single host by multiplying the count determined from the left gill arches by two because infections are more or less evenly distributed between left and right gills (Madhavi, 1986; Lo and Lee, 1996a). We determined the percentage of a specified host-group (by site, year, spring system, and parasite-developmental stage) infected with one or more parasites. We calculated prevalence as the mean number of infected individuals for each species divided by the total number of fish examined. Intensity was calculated as the mean number of cysts found in individuals for each species. Other parasites found in the gills were noted.

We also collected about 100 live red-rim melania snails (>20 mm in length) from sites at nine of the spring systems after collecting fish. Snails were transported to the National Fish Hatchery and Technology Center in aerated river water. Snails from each site were maintained in separate aquaria filled with aerated well-water at 22-25[degrees]C. Snails were measured to the nearest millimeter. We cracked the shells of each live red-rim melania snail between the first and second body whorl, removed the digestive tract, and examined each for rediae and cercaria of trematodes with a dissecting microscope at 100x total magnification. Snails were recorded as infected (with species of trematode noted) or uninfected.

In 1999, we obtained live Big Bend gambusia (n = 20) from Dexter National Fish Hatchery and Technology Center, western mosquitofish (n = 20) from Uvalde National Fish Hatchery, and Pecos gambusia (n = 20) from Diamond Y Springs to determine species-specific susceptibility to metacercarial infection and to document parasitic development after 7, 14, 21, and 28 days. All fishes were maintained at the National Fish Hatchery and Technology Center in separate aquaria filled with aerated well-water at 22-25[degrees]C. We also collected 50 live red-rim melania snails (>20 mm in length) from the Comal River, Comal County, Texas, and maintained them in aquaria with aerated well-water (22-25[degrees]C) at the hatchery. We obtained cercariae from red-rim melania snail using the positive-phototaxis methods described by Lo and Lee (1996b) and Umadevi and Madhavi (1997). For each trial, we placed five individuals of each species of fish into a subdivided aquarium and stocked the tank with about 5,000 cercariae/fish. After 1 h, the fish were removed and rinsed briefly in well-water (to ensure that additional infection would not take place); then each species of fish was placed into a separate aquarium. Each trial was replicated four times. At the end of 7, 14, 21, and 28 days, we euthanized the fish from a replication using MS-222, measured total length, and removed the left gill arches. We examined the gill arches for metacercariae and determined the number of infections per host-fish and developmental stage of parasites as previously described. Interspecific comparisons of the number of infections per host-fish were made using analysis of variance (ANOVA). Significant ANOVAs (P < 0.05) were followed by pairwise tests using Tukey's mean-comparison test. Differences in development of cysts over time among the three species were visually assessed and noted.

RESULTS--Red-rim melania snails were present at four (San Felipe Creek, San Solomon Springs, Phantom Lake, and Diamond Y Springs) of the nine spring systems in 1999 (Table 2). Unfortunately, snails had populated spring-areas associated with two additional streams since 1999, the Devils River and Pinto Creek. Four of the systems (East Sandia Springs, Independence Creek, Big Bend National Park Refugium Pond, and Clear Creek) did not contain red-rim melania snails in 1999 and still remain negative for this species. Of the spring systems that were populated with snails, all contained the trematode and were positive for branchial infection in fish, except Diamond Y Springs that contained uninfected snails and fish during both years.

We collected 1,418 fish comprised of 21 species from the 10 spring systems (Table 3). We found a high prevalence of branchial infection for fish collected regardless of species. Seventeen of the 21 species were positive for infection by trematodes. Two of the species, Big Bend and Clear Creek gambusia, that were not infected had been collected from sites that did not have any red-rim melania snails or the trematode. Conversely, the other two species that did not exhibit infection were the headwater catfish Ictalurus lupus and sucker mouth catfish Hypostomus plecostomus, even though infected redrim melania snails and other species of fish collected at the same sites were, at times, heavily infected. On average, the most infected genera were Micropterus (100%), and Lepomis (100%), followed in decreasing order by Etheostoma (90%), Dionda (89%), Astyanax (81%), Cichlasoma (69%), Notropis (68%), Cyprinella (55%), Gambusia (52%), Ictalurus (50%), and Hypostomus (0%; Table 3).

We collected seven of the nine state-listed or federally listed species that we hoped to collect (Table 4). Leon Springs pupfish were not collected because of the very low numbers that exist in the wild. Conchos pupfish was not collected because of its low numbers, cryptic and elusive behavior, and difficulties of collecting in the habitats the fish use. All of the listed species, excluding the Rio Grande darter, that were collected had a relatively high percentage (mean = 52%) of developing metacercarial cysts. These six species had an average number of cysts in gills ranging from <1-299 (Table 4). Conversely, the Rio Grande darter had relatively few developing metacercarial cysts (mean = 14%) despite 90% of the fish collected from invaded sites having an average of 92 immature metacercarial cysts (Table 4).

Red-rim melania snails (n = 1,490; range of 11-48 mm in total length) were collected at four and five of the nine spring systems in western Texas, respectively, during 1999 and 2011 (Table 5). Although Pinto Creek was not sampled for snails, infected fish collected from the site in 2009 and 2010 for another study (McMillan, 2011) indicate the presence of the snail. Rates of infection in snails were variable between years and sites. In 1999, San Solomon Springs had the greatest percentage of snails containing rediae and cercariae (26.8%) followed in decreasing percentages by San Felipe Creek (13.8%) and Phantom Lake Springs (9.6%). Rates of infection in snails were greater in 1999 than in 2011. Snails collected from three of the spring systems were infected with species of rediae and cercariae other than C. formosanus (Table 5). Other trematodes collected were Philophthalmus gralli, an eye fluke found in waterfowl, and Haplorchis, a trematode that encysts in muscle of fish at the maxillary, operculum, and insertions of fins. Philopthalmus gralli was found in San Felipe Creek and San Solomon Springs in 1999 and 2011. Haplorchis pumilio was found in Phantom Lake Springs only in 1999 and in San Felipe Creek in 1999 and 2011.

Our laboratory study suggests that the three species of fish we tested had different susceptibility to infection by trematodes after they were exposed to 5,000 C. formosanus cercariae/fish for 1 h. Western mosquitofish had significantly (P < 0.01) more cysts when compared to Pecos and Big Bend gambusia, which were not significantly different in rates of infection (Fig. 2). Developmental rates of C. formosanus were similar among species of Gambusia. Most parasites (98%) were mature at 21 days.

DISCUSSION--The geographic range of red-rim melania snails and the parasitic trematode has expanded since 1999. Their range expansion is in part due to the relatively constant water-conditions within many springfed systems in Texas (Brune, 1981; Hubbs, 2001) and because they are relatively long-lived, iteroparous, and parthenogenetic, allowing them to rapidly populate an area (Rader et al., 2003). Although our laboratory study demonstrates that Big Bend gambusia can become infected by the trematode, the wild population remains uninfected presumably because the spring-fed system exceeds the thermal range of tolerance for the intermediate host, red-rim melania snail (Mitchell and Brandt, 2005). We hypothesize that, if abiotic conditions of the system are altered, red-rim melania snails and the trematode could successfully colonize this spring-fed system. It also is likely that, if red-rim melania snails are introduced within spring-fed systems similar to those in our study, colonization would be successful and expansion of its geographic range will continue, thereby, providing a transmission vector for expansion of the range of the trematode. While our results show that some of the spring systems have not been colonized by the redrim melania snail or trematode, the lack of success in these systems does not imply that they or similar systems will not be colonized in the future. Although natural expansion of their ranges is possible, given the definitive avian host for the parasite in central Texas is the green heron (Butorides virescens; Kuhlman, 2007), it is more likely that human-mediated expansions of range will occur for these species. This is concerning given the low species-specificity for the fish-host of the trematode (Salgado-Maldonado et al., 1995; Scholz and Salgado-Maldonado, 2000; Ortega et al., 2009; Fleming et al., 2011) and the imperiled status of many of the endemic species of fish that populate these spring-fed systems (Brune, 1981).

Our results indicate that all of the state-listed and federally listed species collected were suitable hosts for the parasite, with the exception of the Clear Creek gambusia (which was not found at an infected location or tested in the laboratory). Rates of metacercarial infection (ranging from the 10s-100s) observed from fish collected from these spring systems were similar to those observed in river systems in Mexico (Scholz and Salgado-Maldanado, 2000) but not as great as those reported for the Comal River in Texas (Cantu, 2003; as high as 1,600 cysts in an individual fish). Our study also indicates that, while rates of infection may be low for some of the endemic species we examined, the parasitic trematode appears to be able to complete its development, regardless of the hostspecies excluding the Rio Grande darter. Our study suggests that the Rio Grande darter possesses a mechanism that enables the species to curtail development of trematodes. In our study, two species (headwater catfish, Ictalurus lupus; sucker-mouth catfish Hypostomus plecostomus, an exotic species from Central and South America) were not infected even though red-rim melania snails and the trematode had infected other fish at the same sites. Given that previous studies have shown that suckermouth catfish and congeneric species of headwater catfish, such as the channel catfish (Ictalurus punctatus) can become infected with the trematode (Ortega et al., 2009; Scholz and Salgado-Maldonado, 2000), we presume the lack of infection is an artifact of small sample sizes as opposed to differential susceptibility of species. Although our laboratory results demonstrate that Pecos gambusia are susceptible to the trematode and the green heron has been observed at Diamond Y Springs (J. Kargas, pers. comm.), none of the red-rim melania snails or fish collected from Diamond Y Springs was infected. The absence of the trematode at this site may be because it never was introduced at the site. It also may be indicative of subtleties in abiotic conditions that negatively influence growth or reproduction of trematodes. Further research is needed to examine these hypotheses. Regardless of the lack of infection observed for headwater and suckermouth catfish, the vast majority of the assemblages of fish we sampled were infected. Consequently, adverse effects appear likely for other populations residing within spring-fed systems colonized by the trematode.

Although our results show that the average numbers of metacercarial infections per fish in situ and in our laboratory experiments were lower than those reported to cause mortality (McDonald et al., 2006), demographic change within these populations in spring systems will likely result due to a linear additive sequence of acute stressors coupled with increasingly higher rates of metacercarial infection during periods of reduced or altered spring-discharge (Mitchell et al., 2000). Discharge of water at Phantom Lake Springs has been reduced over the last 50 years (J. G. Ashworth et al., in litt.); nevertheless, species residing within this system have not been extirpated presumably because all other critical factors (e.g., abiotic conditions, habitat, forage, etc.) have been adequate for survival and reproductive success. However, if multiple factors negatively change simultaneously or in sequence, populations could become altered and depressed. For example, warmer waters and low levels of dissolved oxygen increase respiration (Cech et al., 1985) thereby increasing the potential for infection because cercarial shedding increases as water temperatures rise (Lo and Lee, 1996b). While in isolation, these abiotic changes may not be sufficient enough to cause fatal hypoxia. The combination of these changes coupled with either high rates of metacercarial infection or the resulting damage or deformities of gills (i.e., Blazer and Gratzek, 1985; Mitchell et al., 2000), however, could ultimately result in fatal hypoxia. Additionally, larval and juvenile fish have less tolerance for cercarial infections than adults (McDonald et al., 2006). As a result, strength of year-class could be negatively affected, ultimately reducing reproductive success of infected species by limiting the number of fish that mature sexually (McDonald et al., 2006). Thus, the longevity of these populations of endemic fish may be at risk. As a result, we suggest that future efforts not only include monitoring these populations but also their rates of infection, particularly during periods of altered spring-discharge as well as other variables critical to their survival and reproductive success.

Submitted 10 May 2012. Acceptance recommended by Associate Editor Fredric R. Govedich 6 January 2014.

We thank T. Bonner, S. Curran, J. Fries, C. Hubbs, J. Landye, R. Overstreet, M. Collyer, and D. Propst for critical review and improvements to various drafts of the manuscript. G. Garrett provided guidance and field-assistance, and the Nature Conservancy of Texas and numerous landowners graciously provided access to sites. I. Castro-Arellano graciously provided the Spanish translation. Fish were collected under Texas Parks and Wildlife Scientific Research Permit Number SPR-0390-045 and Department of the Interior, United States Fish and Wildlife Service, Federal Fish and Wildlife Permit Number TEB76611-2. This research was funded through the Quick Response Program of the United States Geological Survey. The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the United States Fish and Wildlife Service.


ALCARAZ, G., G. PEREZ-PONCE DE LEON, P. LUIS GARCIA, V. LEONREGAGNON, AND C. VANEGAS. 1999. Respiratory responses of grass carp Ctenopharyngodon idella (Cyprinidae) to parasitic infection by Centrocestus formosanus (Digenea). Southwestern Naturalist 44:222-226.

BLAZER, V. S., AND J. B. GRATZEK. 1985. Cartilage proliferation in response to metacercarial infections in fish gills. Journal of Comparative Pathology 95:273-280.

BRUNE, G. 1981. Springs of Texas. Volume I. Branch-Smith, Inc., Fort Worth, Texas.

CANTU, V. 2003. Spatial and temporal variation of Centrocestus formosanus in river water and endangered fountain darters (Etheostoma fonticola) in the Comal River, Texas. M.S. thesis, Southwest Texas State university, San Marcos.

CECH, J. J., JR., M. J. MASSINGILL, B. VONDRACEK, AND A. L. LINDEN. 1985. Respiratory metabolism of mosquitofish, Gambusia affinis: effects of temperature, dissolved oxygen, and sex difference. Environmental Biology of Fishes 13:297-307.

CHEN, H. T. 1948. Some early larval stages of Centrocestus formosanus (Nishigori, 1924). Linnean Science Journal 22:93-105.

FLEMING, P. B., D. G. HUFFMAN, T. H. BONNER, AND T. M. BRANDT. 2011. Metacercarial distribution of Centrocestus formosanus among fish hosts in the Guadalupe River Drainage of Texas. Journal of Aquatic Animal Health 23:117-124.

HUBBS, C. 2001. Environmental correlates to the abundance of spring-adapted versus stream-adapted fishes. Texas Journal of Science 53:299-326.

KUHLMAN, T. 2007. The predominant definitive avian hosts of the invasive Asian trematode, Centrocestus formosanus, in the headwaters of the Comal, San Antonio, and San Marcos rivers. M.S. thesis, Texas State University, San Marcos.

LO, C. T., AND K M. LEE. 1996a. Infectivity of the cercariae of Centrocestus formosanus and Haplorchis pumilio (Digenea: Heterophyidae) in Cyprinus carpio. Zoological Studies 35:255-260.

LO, C. T., AND K. M. LEE. 1996b. Pattern of emergence and the effects of temperature and light on the emergence and survival of heterophyid cercaria (Centrocestus formosanus and Haplorchis pumilio). Journal of Parasitology 82:347-350.

MADHAVI, R. 1986. Distribution of metacercariae of Centrocestus formosanus (Trematoda: Heterophyidae) on the gills of Aplocheilus panchax. Journal of Fish Biology 29:685-690.

MCDERMOTT, K. 2000. Distribution and infection relationships of an undescribed digenetic trematode, its exotic intermediate host, and endangered fishes in springs of west Texas. M.S. thesis, Southwest Texas State University, San Marcos.

MCDONALD, D. L., T. H. BONNER, T. M. BRANDT, AND G. H. TREVINO. 2006. Size susceptibility of trematode-induced mortality in the endangered fountain darter (Etheostoma fonticola). Journal of Freshwater Ecology 21:293-299.

MCMILLAN, S. M. 2011. Reproductive and feeding ecology of two sympatric Dionda (cyprinidae) in the Rio Grande Basin, Texas. M.S. thesis, Texas State University, San Marcos.

MITCHELL, A. J., AND T. M. BRANDT. 2005. Temperature tolerance of red-rim melania Melanoides tuberculatus, an exotic aquatic snail established in the United States. Transactions of the American Fisheries Society 134:126-131.

MITCHELL, A. J., M. S. HOBBS, AND T. M. BRANDT. 2007. The effect of chemical treatments on red-rim melania (Melanoides tuberculata), an exotic aquatic snail that serves as a vector of trematodes to fish and other species in the USA. North American Journal of Fisheries Management 27:1287-1293.

MITCHELL, A. J., R. M. OVERSTREET, A. E. GOODWIN, AND T. M. BRANDT. 2005. Spread of an exotic fish-gill trematode: a far-reaching and complex problem. Fisheries 30:11-16.

MITCHELL, A. J., M. J. SALMON, D. G. HUFFMAN, A. E. GOODWIN, AND T. M. BRANDT. 2000. Prevalence and pathogenicity of a heterophyid trematode infecting the gills of an endangered fish, the fountain darter, in two central Texas spring-fed rivers. Journal of Aquatic Animal Health 12:283-289.

MOHAN, C. V., K. M. SHANKER, AND K. S. RAMESH. 1999. Mortalities of juvenile common carp, Cyprinus carpio associated with larval trematode infection - a case study. Journal of Aquaculture in the Tropics 14:137-142.

MURRAY, H. D. 1971. The introduction and spread of thiarids in the United States. Biologist 53:133-135.

NISHIGORI, M. 1924. On a new species of fluke, Stamnosoma formosanum and its life history. Taiwan Igakkai Zasshi 234:181-238.

ORTEGA, C., R. FAJARDO, AND R. ENRIQUEZ. 2009. Trematode Centrocestus formosanus infection and distribution in ornamental fishes in Mexico. Journal of Aquatic Animal Health 21:18-22.

PAPERNA, I. 1996. Parasites, infections and diseases of fishes in Africa--an update. CIFA Technical Paper 31:1-220.

RADER, R., M. BELK, AND M. KELEHER. 2003. The introduction of an invasive snail (Melanoides tuberculata) to spring ecosystems of the Bonneville Basin, Utah. Journal of Freshwater Ecology 18:647-657.

ROESSLER, M. A., C. L. BEARDSLEY, AND D. C. TABB. 1977. New records of the introduced snail, Melanoides tuberculata (Mollusca: Thiaridae) in South Florida. Florida Scientist 40:87-94.

SALGADO-MALDONADO, G., M. I. RODRIGUEZ-VARGAS, AND J. CAMPOSPEREZ. 1995. Metacercariae of Centrocestus formosanus (Nishigori, 1924) (Trematoda) in freshwater fishes in Mexico and their transmission by the thiarid snail Melanoides tuberculata. Studies on Neotropical Fauna and Environment 30:245-250.

SCHENCK, J. R., AND B. G. WHITESIDE. 1976. Distribution, habitat preference and population size estimate of Etheostoma fonticola. Copeia 4:697-703.

SCHOLZ, T., AND G. SALGADO-MALDONADO. 2000. The introduction and dispersal of Centrocestus formosanus (Nishigori, 1924) (Digenea: Heterophyidae) in Mexico: a review. American Midland Naturalist 143:185-200.

TOLLEY-JORDAN, L. R., AND J. M. OWEN. 2008. Habitat influences snail community structure and trematode infection levels in a spring-fed river, Texas, USA. Hydrobiologia 600:29-40.

UMADEVI, K., AND R. MADHAVI. 1997. Effects of light and temperature on the emergence of Haplorchispumilio cercariae from the snail host, Thiara tuberculata. Acta Parasitologica 42:12-17.

VAZQUEZ-COLET, A., AND C. M. AFRICA. 1939. Determination of the piscine intermediate hosts of Philippine heterophyid trematodes by feeding experiments. Philippine Journal of Science 70:201-215.


Rocky Mountain Field Institute, 3310 W Colorado Avenue, Colorado Springs, CO 80904 (KSM)

Llano River Field Station, Texas Tech University, 254 Red Raider Lane, Junction, TX 76849 (TLA)

United States Fish and Wildlife Service, National Fish Hatchery and Technology Center, 500 East McCarty Lane, San Marcos, TX 78666 (TMB, DCH, KGO)

* Correspondent:

TABLE 1--Abiotic conditions at nine spring systems in western Texas
during collection of Melanoides tuberculatus and fish used to assess
rates of infection by Centrocestus formosanus during 1999 and 2011.

Spring system            Latitude, longitude    Year   Temperature

Big Bend National Park   29[degrees]10'45 "N,   1999       33.5
  Refugium Pond          102[degrees]57'14 "W   2011       33.1
Clear Creek Springs      30[degrees]54'25"N,    1999       22.7
                          99[degrees]57'40"W    2011       22.5
Devils River             29[degrees]54'04 "N,   1999       28.0
                         100[degrees]59'58 "W   2011       27.1
Diamond Y Springs        31[degrees]00'04 "N,   1999       21.3
                         102[degrees]55'27 "W   2011       22.0
East Sandia Springs      30[degrees]59'28 "N,   1999       24.0
                         103[degrees]43'44 "W   2011       21.0
Independence Creek       30[degrees]28'08 "N,   1999       26.0
                         101[degrees]48'12 "W   2011       26.4
Phantom Lake Springs     30[degrees]56'06 "N,   1999       25.2
                         103[degrees]50'59 "W   2011       24.9
Pinto Creek              29[degrees]24'17 "N,   1999        --
                         100[degrees]28'45 "W   2011        --
San Felipe Creek         29[degrees]22'25 "N,   1999       23.6
                         100[degrees]53'06 "W   2011       24.8
San Solomon Springs      30[degrees]56'39 "N,   1999       26.0
                         103[degrees]47'16 "W   2011       26.3

Spring system            pH    Dissolved oxygen   Salinity (ppt)

Big Bend National Park
  Refugium Pond          7.1          4.7              0.0
Clear Creek Springs      7.2          6.9              0.4
                         7.3          6.4              0.3
Devils River             8.1         10.5              0.0
                         7.9          6.2              0.0
Diamond Y Springs        6.8          4.1              4.0
                         7.0          6.3              2.5
East Sandia Springs      7.1          n/a              3.0
                         7.1          6.1              2.4
Independence Creek       8.0          8.0              0.5
                         7.8          7.5              0.0
Phantom Lake Springs     7.1          1.0              2.0
                         6.8          6.3              3.2
Pinto Creek              --           --                --
                         --           --                --
San Felipe Creek         7.6          7.9              0.0
                         7.8          5.9              0.0
San Solomon Springs      6.9          3.7              2.0
                         7.2          5.2              0.0

Table 2--Presence (P) or absence (A) of red-rim melania snails
Melanoides tuberculatus, snails infected with Centocestus formosanus,
and fish infected with C. formosanus collected from nine spring
systems in western Texas in 1999 and 2011.

Spring System            Year   Snails   Infected   Infected
                                          snails      fish

Big Bend National Park   1999     A         A          A
  Refugium Pond          2011     A         A          A
Clear Creek Springs      1999     A         A          A
                         2011     A         A          A
Devils River             1999     A         A          A
                         2011     P         P          P
Diamond Y Springs        1999     P         A          A
                         2011     P         A          A
East Sandia Springs      1999     A         A          A
                         2011     A         A          A
Independence Creek       1999     A         A          A
                         2011     A         A          A
Pinto Creek (a)          1999     --        --         P
                         2011     --        --         P
Phantom Lake Springs     1999     P         P          P
                         2011     P         A          P
San Felipe Creek         1999     P         P          P
                         2011     P         P          P
San Solomon Springs      1999     P         P          P
                         2011     P         A          P

(a) No snails collected at site but presumed to be present because
infected fish were collected.

TABLE 3--Distribution of the Asian gill trematode Centrocestus
formosanus among species of fish collected nine spring systems in
western Texas.

Species of fish            No. of specimens    No. of sites with
                              collected       the species present

Astyanax mexicanus                97                  10
Cichlasoma cyanoguttatum          45                   7
Cyprinella proserpina             27                   2
Cyprinella venusta                38                   2
Cyprinodon elegans                47                   2
Dionda argentosa                 103                   6
Dionda diaboli                   243                   4
Dionda episcopa                    7                   1
Etheostoma grahami                42                   4
Gambusia affinis                 147                   6
Gambusia gagei                    20                   1
Gambusia geiseri                  68                   2
Gambusia heterochir               12                   1
Gambusia nobilis                 137                   5
Hypostomus plecostomus            21                   1
Ictalurus lupus                    2                   2
Ictalurus punctatus                7                   1
Lepomis cyanelllus                11                   1
Lepomis microlophus                3                   1
Micropterus salmoides             28                   5
Notropis amabilis                 60                   5

Species of fish             No. of sites with      No. of sites with
                           the parasite present   the parasite present
                             and the species        and the species
                                 infected              uninfected

Astyanax mexicanus                  5                      4
Cichlasoma cyanoguttatum            5                      2
Cyprinella proserpina               2                      0
Cyprinella venusta                  2                      0
Cyprinodon elegans                  2                      0
Dionda argentosa                    4                      0
Dionda diaboli                      3                      1
Dionda episcopa                     1                      0
Etheostoma grahami                  4                      0
Gambusia affinis                    4                      0
Gambusia gagei                      0                      0
Gambusia geiseri                    2                      0
Gambusia heterochir                 0                      0
Gambusia nobilis                    3                      0
Hypostomus plecostomus              0                      1
Ictalurus lupus                     0                      2
Ictalurus punctatus                 1                      0
Lepomis cyanelllus                  1                      0
Lepomis microlophus                 1                      0
Micropterus salmoides               3                      2
Notropis amabilis                   5                      0

Species of fish               Proportion of
                            specimens infected
                            at sites with the
                           parasite present (%)

Astyanax mexicanus                 81.2
Cichlasoma cyanoguttatum           68.9
Cyprinella proserpina             100.0
Cyprinella venusta                 41.3
Cyprinodon elegans                 24.3
Dionda argentosa                   85.2
Dionda diaboli                     83.5
Dionda episcopa                   100.0
Etheostoma grahami                 90.2
Gambusia affinis                   51.0
Gambusia gagei                      --
Gambusia geiseri                   47.4
Gambusia heterochir                 --
Gambusia nobilis                   58.9
Hypostomus plecostomus              --
Ictalurus lupus                     0.0
Ictalurus punctatus               100.0
Lepomis cyanelllus                100.0
Lepomis microlophus               100.0
Micropterus salmoides             100.0
Notropis amabilis                  67.8

TABLE 4--The number of state-listed and federally listed species of
fish infected with the Asian gill trematode Centrocestus formosanus in
spring systems in western Texas between 1999 and 2011. Developing
cysts are the average percentage of cysts having visibly faded
eyespots or an X-shaped excretory vesicle in metacercariae.

Spring system            Year (month)       Species

Big Bend National Park   1999 (May)         Gambusia gaigei
Refugium Pond            2011 (October)     G. gaigei
Clear Creek Springs      1999 (May)         Gambusia heterochir
                         2011 (October)     G. heterochir

Devils River             1999 (May)         Etheostoma grahami
                                            Gambusia nobilis
                                            Dionda diaboli
                         2009 (September)   D. diaboli
                         2009 (October)     D. diaboli
                         2009 (November)    D. diaboli
                         2009 (December)    D. diaboli
                         2010 (January)     D. diaboli
                         2010 (February)    D. diaboli
                         2010 (March)       D. diaboli
                         2010 (April)       D. diaboli
                         2010 (May)         D. diaboli
                         2010 (June)        D. diaboli
                         2010 (July)        D. diaboli
                         2010 (August)      D. diaboli
                         2011 (August)      E. grahami
                                            G. nobilis
                                            D. diaboli

Diamond Y Springs        1999 (May)         G. nobilis
                         2011 (September)   G. nobilis

East Sandia Springs      1999 (May)         G. nobilis
                         2011 (September)   G. nobilis

Phantom Lake Springs     1999 (May)         G. nobilis
                                            Cyprinodon elegans
                         1999 (October)     C. elegans
                         2011 (September)   G. nobilis
                                            C. elegans

Pinto Creek              2009 (September)   D. diaboli
                         2009 (October)     D. diaboli
                         2009 (November)    D. diaboli
                         2009 (December)    D. diaboli
                         2010 (January)     D. diaboli
                         2010 (February)    D. diaboli
                         2010 (March)       D. diaboli
                         2010 (April)       D. diaboli
                         2010 (May)         D. diaboli
                         2010 (June)        D. diaboli
                         2010 (July)        D. diaboli
                         2010 (August)      D. diaboli

San Felipe Creek         1999 (May)         E. grahami
                                            D. diaboli
                                            Cyprinella proserpina
                         2000 (February)    E. grahami
                                            D. diaboli
                                            C. proserpina
                         2011 (September)   E. grahami
                                            D. diaboli
                                            G. nobilis

San Solomon Springs      1999 (May)         Cyprinodon elegans
                                            G. nobilis
                         1999 (October)     G. nobilis
                         2011 (August)      C. elegans

Spring system            Year (month)       No. of fish

Big Bend National Park   1999 (May)                 20
Refugium Pond            2011 (October)             20
Clear Creek Springs      1999 (May)                 20
                         2011 (October)             12

Devils River             1999 (May)                 20
                         2009 (September)            6
                         2009 (October)             11
                         2009 (November)            10
                         2009 (December)             7
                         2010 (January)             10
                         2010 (February)            10
                         2010 (March)                5
                         2010 (April)               10
                         2010 (May)                 10
                         2010 (June)                 6
                         2010 (July)                 7
                         2010 (August)               7
                         2011 (August)               9

Diamond Y Springs        1999 (May)                 20
                         2011 (September)           17

East Sandia Springs      1999 (May)                 20
                         2011 (September)           19

Phantom Lake Springs     1999 (May)                 23
                         1999 (October)             18
                         2011 (September)           24

Pinto Creek              2009 (September)            7
                         2009 (October)              9
                         2009 (November)             9
                         2009 (December)             7
                         2010 (January)              7
                         2010 (February)             7
                         2010 (March)                6
                         2010 (April)               10
                         2010 (May)                  9
                         2010 (June)                 6
                         2010 (July)                10
                         2010 (August)               9

San Felipe Creek         1999 (May)                 11
                         2000 (February)            10
                         2011 (September)           12

San Solomon Springs      1999 (May)                 22
                         1999 (October)             18
                         2011 (August)              17

Spring system            Year (month)       Prevalence (%)

Big Bend National Park   1999 (May)                   0.0
Refugium Pond            2011 (October)               0.0
Clear Creek Springs      1999 (May)                   0.0
                         2011 (October)               0.0

Devils River             1999 (May)                   0.0
                         2009 (September)             0.0
                         2009 (October)               0.0
                         2009 (November)              0.0
                         2009 (December)              0.0
                         2010 (January)               0.0
                         2010 (February)              0.0
                         2010 (March)                 0.0
                         2010 (April)                 0.0
                         2010 (May)                   0.0
                         2010 (June)                  0.0
                         2010 (July)                 14.3
                         2010 (August)                0.0
                         2011 (August)               66.7

Diamond Y Springs        1999 (May)                   0.0
                         2011 (September)             0.0

East Sandia Springs      1999 (May)                   0.0
                         2011 (September)             0.0

Phantom Lake Springs     1999 (May)                  78.0
                         1999 (October)              28.0
                         2011 (September)            29.2

Pinto Creek              2009 (September)           100.0
                         2009 (October)             100.0
                         2009 (November)            100.0
                         2009 (December)            100.0
                         2010 (January)             100.0
                         2010 (February)            100.0
                         2010 (March)               100.0
                         2010 (April)               100.0
                         2010 (May)                  89.0
                         2010 (June)                 50.0
                         2010 (July)                100.0
                         2010 (August)              100.0

San Felipe Creek         1999 (May)                 100.0
                         2000 (February)            100.0
                         2011 (September)            92.0

San Solomon Springs      1999 (May)                  36.0
                         1999 (October)              78.0
                         2011 (August)               11.8

Spring system            Year (month)       Mean intensity   Developing
                                                             cysts (%)

Big Bend National Park   1999 (May)                  0.00         0.00
Refugium Pond            2011 (October)              0.00         0.00
Clear Creek Springs      1999 (May)                  0.00         0.00
                         2011 (October)              0.00         0.00

Devils River             1999 (May)                  0.00         0.00
                                                     0.00         0.00
                                                     0.00         0.00
                         2009 (September)            0.00         0.00
                         2009 (October)              0.00         0.00
                         2009 (November)             0.00         0.00
                         2009 (December)             0.00         0.00
                         2010 (January)              0.00         0.00
                         2010 (February)             0.00         0.00
                         2010 (March)                0.00         0.00
                         2010 (April)                0.00         0.00
                         2010 (May)                  0.00         0.00
                         2010 (June)                 0.00         0.00
                         2010 (July)                 0.02       100.00
                         2010 (August)               0.00         0.00
                         2011 (August)               4.40         0.00
                                                     8.00        97.00
                                                     0.00         0.00

Diamond Y Springs        1999 (May)                  0.00         0.00
                         2011 (September)            0.00         0.00

East Sandia Springs      1999 (May)                  0.00         0.00
                         2011 (September)            0.00         0.00

Phantom Lake Springs     1999 (May)                  6.00        26.00
                                                     9.60        90.00
                         1999 (October)              1.60        53.00
                         2011 (September)            0.80        80.00
                                                     0.80        33.00

Pinto Creek              2009 (September)          184.80        97.00
                         2009 (October)            224.00        94.00
                         2009 (November)           236.00        97.00
                         2009 (December)           288.50        97.00
                         2010 (January)            299.00        95.00
                         2010 (February)           262.60        99.00
                         2010 (March)              205.30        99.00
                         2010 (April)              299.40        98.00
                         2010 (May)                247.50       100.00
                         2010 (June)                 1.30         0.00
                         2010 (July)                68.60        55.00
                         2010 (August)              77.30        86.00

San Felipe Creek         1999 (May)                130.00        54.00
                                                    16.00        88.00
                                                    81.00        95.00
                         2000 (February)           195.60         0.01
                                                   142.40        97.00
                                                   236.70        97.00
                         2011 (September)          112.60         0.00
                                                    62.60        89.00
                                                    10.00        80.00

San Solomon Springs      1999 (May)                  1.30        14.00
                                                     1.90        23.00
                         1999 (October)             27.20        97.00
                         2011 (August)               0.35        33.00

TABLE 5--The number of red-rim melania snails Melanoides tubculatus
collected in 1999 and 2011 from spring systems in western Texas and
the average percentage of individuals infected with cercaria of
Centrocestus formosanus and other trematodes.

Spring system            Year (month)           Snails    Parasite
                                                present   present

Big Bend National Park   1999 (May)
  Refugium Pond          2011 (May)
Clear Creek Springs      1999 (May)
                         2011 (September)
Devils River             1999 (May)
                         2011 (September)          X         X
Diamond Y Springs        1999 (May)                X         X
                         2011 (September)          X
East Sandia Springs      1999 (May)
                         2011 (September)
Independence Creek       1999 (May)
                         2011 (September)
Phantom Lake Springs     1999 (May)                X         X
                         2011 (September) (a)      X
Pinto Creek              1999 (May)
                         2011 (September) (b)                X
San Felipe Creek         1999 (May)                X         X
                         2011 (September)          X         X
San Solomon Springs      1999 (May)                X         X
                         2011 (September) (a)      X

Spring system            Year (month)           No. of     Range of
                                                snails   shell length

Big Bend National Park   1999 (May)                 0         0
  Refugium Pond          2011 (May)                 0         0
Clear Creek Springs      1999 (May)                 0         0
                         2011 (September)           0         0
Devils River             1999 (May)                 0         0
                         2011 (September)         175       16-43
Diamond Y Springs        1999 (May)               204       20-40
                         2011 (September)         100       17-31
East Sandia Springs      1999 (May)                 0         0
                         2011 (September)           0         0
Independence Creek       1999 (May)                 0         0
                         2011 (September)           0         0
Phantom Lake Springs     1999 (May)               111       15-31
                         2011 (September) (a)      94       15-34
Pinto Creek              1999 (May)                 0         0
                         2011 (September) (b)       0         0
San Felipe Creek         1999 (May)               169       18-36
                         2011 (September)         306       11-48
San Solomon Springs      1999 (May)               131       20-42
                         2011 (September) (a)     200       14-36

Spring system            Year (month)           Infected with
                                                cercaria of C.
                                                formosanus (%)

Big Bend National Park   1999 (May)                       0.0
  Refugium Pond          2011 (May)                       0.0
Clear Creek Springs      1999 (May)                       0.0
                         2011 (September)                 0.0
Devils River             1999 (May)                       0.0
                         2011 (September)                 0.6
Diamond Y Springs        1999 (May)                       0.0
                         2011 (September)                 0.0
East Sandia Springs      1999 (May)                       0.0
                         2011 (September)                 0.0
Independence Creek       1999 (May)                       0.0
                         2011 (September)                 0.0
Phantom Lake Springs     1999 (May)                       9.6
                         2011 (September) (a)             0.0
Pinto Creek              1999 (May)                       0.0
                         2011 (September) (b)             0.0
San Felipe Creek         1999 (May)                      13.8
                         2011 (September)                 7.4
San Solomon Springs      1999 (May)                      26.8
                         2011 (September) (a)             0.0

Spring system            Year (month)           Infected with
                                                other cercaria

Big Bend National Park   1999 (May)                       0.0
  Refugium Pond          2011 (May)                       0.0
Clear Creek Springs      1999 (May)                       0.0
                         2011 (September)                 0.0
Devils River             1999 (May)                       0.0
                         2011 (September)                 0.0
Diamond Y Springs        1999 (May)                       0.0
                         2011 (September)                 0.0
East Sandia Springs      1999 (May)                       0.0
                         2011 (September)                 0.0
Independence Creek       1999 (May)                       0.0
                         2011 (September)                 0.0
Phantom Lake Springs     1999 (May)                      14.1
                         2011 (September) (a)             0.0
Pinto Creek              1999 (May)                       0.0
                         2011 (September) (b)             0.0
San Felipe Creek         1999 (May)                       7.1
                         2011 (September)                15.3
San Solomon Springs      1999 (May)                       8.2
                         2011 (September) (a)             0.5

(a) Parasite not found in snails but fish were infected.

(b) Snails not collected but assumed to be present because of the
presence of the parasite in fish collected.
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Author:McDermott, Kelly S.; Arsuffi, Thomas L.; Brandt, Thomas M.; Huston, Daniel C.; Ostrand, Kenneth G.
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1USA
Date:Jun 1, 2014
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