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.
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.
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KELLY S. MCDERMOTT, THOMAS L. ARSUFFI, THOMAS M. BRANDT, DANIEL C. HUSTON, AND KENNETH G. OSTRAND *
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: Kenneth_Ostrand@fws.gov
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 ([degrees]C) 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) (mg/L) 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 20 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 22 6 Diamond Y Springs 1999 (May) 20 2011 (September) 17 East Sandia Springs 1999 (May) 20 2011 (September) 19 Phantom Lake Springs 1999 (May) 23 28 1999 (October) 18 2011 (September) 24 8 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 1 18 2000 (February) 10 18 9 2011 (September) 12 19 1 San Solomon Springs 1999 (May) 22 14 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 0.0 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 59.1 0.0 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 89.0 1999 (October) 28.0 2011 (September) 29.2 25.0 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) 100.0 100.0 100.0 2000 (February) 100.0 100.0 100.0 2011 (September) 92.0 100.0 100.0 San Solomon Springs 1999 (May) 36.0 50.0 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 (mm) 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.|
|Date:||Jun 1, 2014|
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