Aquatic Invasions (2012) Volume 7, Issue 2: 287–290 doi: http://dx.doi.org/10.3391/ai.2012.7.2.016 Open Access

© 2012 The Author(s). Journal compilation © 2012 REABIC

Short Communication

Egg predation and parasite prevalence in the invasive , tuberculata (Müller, 1774) in a west Texas spring system

Hallie L.A. Ladd* and David L. Rogowski Department of Natural Resources Management, Texas Tech University, Box 42125, Lubbock, TX 79409, USA E-mail: [email protected] (HLAL), [email protected] (DLR) *Corresponding author

Received: 27 June 2011 / Accepted: 8 October 2011 / Published online: 10 November 2011

Handling editor: Sergey Mastitsky, German Cancer Research Center in Heidelberg, Germany

Abstract

Melanoides tuberculata Müller, 1774 (Thiaridae), a freshwater prosobranch snail native to regions of Asia and Africa, was introduced into the U.S. in the 1960s and is now found in fifteen states. Melanoides tuberculata can affect native communities directly by displacing native snail species and indirectly by introducing foreign trematodes into novel environments. As the exact mechanisms of displacement of native snails by M. tuberculata are unknown, egg predation rates on native snails (Physella spp.) by two different size classes (>30 mm and <30 mm, total length) of M. tuberculata were determined in laboratory experiments. Additionally, M. tuberculata were sampled from Diamond Y Spring (Pecos County, TX) to determine if the exotic trematode Centrocestus formosanus (Nishigori, 1924) has been introduced into the system. No M. tuberculata > 30 mm were found to consume Physella spp. and only 2.8% of M. tuberculata snails consumed egg masses. None of the M. tuberculata collected from Diamond Y Spring were found to be infected with C. formosanus.

Key words: Centrocestus formosanus, Diamond Y Spring, Melanoides tuberculata, predation, Texas

Introduction prevalent in the hopes of reducing populations of vector snails such as Biomphalaria glabrata Invasions of ecosystems by non-native species (Say, 1818) and B. straminea (Dunker, 1848), are increasing, especially in aquatic and thereby reducing the incidence of the disease environments (Byers 2000). The consequences of (Pointer et al. 1984; Pointer and Guyard 1992). these invasions include loss and Yet, quantitative analyses describing the inter- changes in ecosystem structure (Pimentel 2002). actions of M. tuberculata with native snails are Specifically, the establishment of non-native lacking (Tolley-Jordan and Owen 2008) and it is freshwater snails has been associated with not known whether native snails are displaced as changes in ecosystem function (Arango et al. a result of competition, displacement, or perhaps 2009), community structure (Kerans et al. 2005), even predation. Competition and intraguild and the introduction of non-native parasites predation has been shown in some freshwater (Madsen and Frandsen 1989). snail species (Turner et al. 2007). Melanoides Melanoides tuberculata Müller, 1774 tuberculata prey upon the eggs of endangered (Prosobranchia: Thiaridae), a snail native to fishes (Phillips et al. 2010) so it is conceivable regions of Asia and Africa (Brown 1980), has that they may also prey on the eggs or juveniles been confirmed in at least 15 states throughout of other snails. However, M. tuberculata are the U.S., including California, Texas, Arizona, generalist grazers and the ingestion of eggs may Louisiana, and Oregon (Karatayev et al. 2009). not be intentional, but an indirect effect of Thiarid snails, such as M. tuberculata, can grazing. directly alter community structure through Another major concern with the introduction competition with native snails (Pointer et al. of exotic snails is the potential parasites that they 1993). In fact, M. tuberculata has been may carry and their effects on native fauna. Non- introduced in areas where schistosomiasis was native trematodes have been documented to

287 H.L.A. Ladd and D.L. Rogowski negatively affect native communities by Materials and methods infecting vertebrate hosts lacking the co-evolved defense mechanisms to keep densities of Egg predation parasites at a low level (Taraschewski 2006). The Diamond Y Spring preserve contains two Melanoides tuberculata serves as the first endemic springsnails [Tryonia circumstriata intermediate host to several species of digenetic (Leonard and Ho, 1960) and Pseudotryonia trematodes, including the gill trematode adamantia Taylor, 1987], two native snails Centrocestus formosanus (Nishigori, 1924) (Physella spp. and Assiminea pecos Taylor, (Ben-Ami and Heller 2005; Tolley-Jordan and 1987), and the invasive M. tuberculata (Ladd Owen 2008). Centrocestus formosanus infects 2010). The Physella spp. was used for our egg some vertebrate hosts, such as aquatic migratory predation trials as they are common and readily birds (e.g. the green heron Butorides virescens produce egg masses year round in a laboratory (Linnaeus, 1758) and great egret Ardea alba setting (personal observation). Also, the endemic Linnaeus, 1758) (Mitchell et al. 2005) as well as springsnails are state threatened, while A. pecos a wide variety of fish hosts, including several is federally listed as endangered and little is endangered spring species [e.g. the fountain known about their reproduction or maintaining darter, Etheostoma fonticola (Jordan and Gilbert, them in captivity. Melanoides tuberculata 1886)] (Mitchell et al. 2000). The presence of appeared to considerably vary by size within C. formosanus produces inflammatory responses Diamond Y, the only spring where this species is in the gills of many freshwater fishes that can found. No snails ≥ 30 mm were found beyond lead to respiratory stress and eventual mortality 300 m downstream of the immediate outflow of (Mitchell et al. 2000; 2005). the spring head (Ladd 2010). Therefore, we One of the largest and last remaining cienega chose to use two size classes in this experiment systems in west Texas is the Diamond Y Spring (>30 mm or <30 mm). The experiment was con- preserve located in Pecos County, Texas. It is a ducted from June-September of 2010 at Texas 1502-acre tract of land owned and operated by Tech University (Lubbock, TX). Adult Physella the Nature Conservancy (Karges 2003). The spp. were stocked into three polypropylene Diamond Y Spring preserve is composed of a “shoebox” containers (281411 cm deep) filled number of springs, seeps, and wetlands. The with de-chlorinated tap water. Snail egg masses saline waters within the preserve provide were then transferred to individual 50 ml vials (1 critically important habitat for two federally egg mass per vial) filled with 35 ml of de- endangered species of desert fishes (Cyprinodon chlorinated tap water. One M. tuberculata snail bovinus Baird and Girard, 1853 and Gambusia was then placed within each vial and predation nobilis (Baird and Girard, 1853)) and a suite of was monitored for five days. We considered an rare aquatic invertebrates. The non-native egg mass to be consumed if the entire egg mass M. tuberculata is well established within the was gone at the end of the trial. A total of 51 Diamond Y Spring preserve, albeit no snails M. tuberculata >30 mm and 56 M. tuberculata have previously been documented to harbor any <30 mm were used over the duration of the exotic trematodes (McDermott 2000). However, experiment. Snails were not reused or fed during the spread of C. formosanus into the preserve is the experiment, nor was the water changed. of major concern due to its ability to compromise the health of the preserve’s federally endangered Snail infection status fish species. Additionally, it is not known how Of the six snail species found within Diamond Y M. tuberculata affects Diamond Y’s invertebrate Spring preserve, only M. tuberculata is known to fauna. Investigating the effects of M. tuberculata serve as an intermediate host for C. formosanus on the preserve’s species of high conservation (Scholz and Salgado-Maldonado 2001; Mitchell concern is necessary to effectively manage these et al. 2005). Therefore, only M. tuberculata were rare native populations. Thus, the aims of this surveyed for the presence of C. formosanus. Live study were to determine whether M. tuberculata M. tuberculata were collected during October prey upon the eggs of a native snail (Physella and November of 2009 and March, April, and spp.) and if the exotic trematode, C. formosanus, May of 2010 from Diamond Y spring. Only is present in the M. tuberculata population within snails > 17 mm were used during this study since the Diamond Y Spring preserve. that is the minimum length recorded for infection

288 Egg predation and parasite prevalence in the invasive freshwater snail in M. tuberculata in the Comal River, Texas infected with C. formosanus. Results of the (Tolley-Jordan and Owen 2008). Presence of simulation indicated that the probability of trematodes was assessed using two methods. The obtaining zero parasitized snails in a sample of first method consisted of cracking the shell of 250 snails at 5, 4, 3, 2, and 1 percent parasite M. tuberculata between the first and second prevalence was 0.000, 0.000, 0.008, 0.0776, and body whorl, removing the digestive tract and 0.0826, respectively. gonads, and examining each for rediae and Though the total percentage of egg predation cercaria of C. formosanus under a binocular in our experiment was 2.8% (3/107), dissecting microscope at 100 total M. tuberculata may be present in large enough magnification. The second method consisted of numbers to affect native snail populations placing individual snails into 50 ml vials filled directly through egg predation. For example, the with 35 ml of de-chlorinated water and setting estimated abundance of M. tuberculata within two lamps equipped with 60-watt incandescent Diamond Y Spring is 187,000 individuals (Ladd light bulbs over the vials for 24 hours to ensure 2010). If only 2.8% of M. tuberculata consume that the temperature of the water reached at least egg masses, approximately 5000 snails could 28C (Lo and Lee 1996). We then pipetted two conceivably consume native egg masses, which ml of water from each vial into petri dishes and may lead to a significant reduction in native snail looked for swimming cercariae using a populations. Future studies focusing on food dissecting scope at 30–40 total magnification. preference, egg consumption, and natural egg A total of 250 snails were examined for parasite mortality rates in situ are necessary to presence. Fifty and 200 snails were examined understand the significance of egg predation as a using the first and second method, respectively. mechanism for displacing native snail species by The second method was adopted as our preferred M. tuberculata. means of assessment as it has been found to be a Results from our study and a previous study quick and effective way of determining snail conducted by McDermott (2000) indicate that the infections [C. formosanus cercariae emerge from trematode C. formosanus is not likely present at infected snails when exposed to light and the Diamond Y Spring preserve. In M. tubercu- temperatures between 15–35°C (Lo and Lee lata native habitats, trematode prevalence is less 1996)]. than 5%, and infections tend to be spatially As parasites in hosts can be in low numbers aggregated (Anderson and May 1979). However, and patchily distributed (Anderson and May in areas where the snails have been introduced, 1979), we wanted to determine if our sample size infection rates can be as high as 53% (Bogéa et of 250 was adequate for detecting infected al. 2005). Although we did not detect any snails. A Monte Carlo simulation was used to trematodes, this does not mean that they are not determine the probability of obtaining a sample present within the M. tuberculata population of of 250 snails from a population with trematode the Diamond Y Spring preserve. According to prevalence levels of 1–5% and observing no the results of our simulation, parasite prevalence infected snails within the sample. Using Pop could be two percent or lower. Tools® (Hood 2010), we simulated a population A variety of fish hosts and three species that of 1000 snails with a 5% infection rate. Two serve as definitive hosts for C. formosanus have hundred and fifty snails were randomly sampled been documented at the Diamond Y Spring from that population 4999 times. Then, we preserve: the green heron (B. virescens), great counted how many times the sample of 4999 egret (Adrea alba), and black-crowned-night equaled zero infected snails. We repeated this heron [Nycticorax nycticorax (Linnaeus, 1758)] procedure for 4, 3, 2, and 1 percent parasite (Mitchell et al. 2005; J. Karges, personal prevalence. communication). In addition, C. formosanus has been documented in fishes and M. tuberculata from other west Texas springs (McDermott Results and discussion 2000), which suggests that fishes and M. tuberculata from Diamond Y Spring are None of the M. tuberculata >30 mm consumed likely to become infected, eventually. Therefore, any egg masses, while only 3/56 (5.4%) egg we strongly recommend yearly sampling of M. masses were consumed in trials using tuberculata for C. formosanus within Diamond Y M. tuberculata <30 mm. Of 250 M. tuberculata Spring and other west Texas springs to monitor collected from the spring, none were found to be the spread of this harmful fish pathogen.

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