Egg predation and parasite prevalence in the invasive ...

Aquatic Invasions (2012) Volume 7, Issue 2: 287–290 Open Access

doi: http://dx.doi.org/10.3391/ai.2012.7.2.016
© 2012 The Author(s). Journal compilation © 2012 REABIC

Short Communication

Egg predation and parasite prevalence in the invasive freshwater snail,
Melanoides 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 biodiversity 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
tuberculata prey upon the eggs of endangered
Melanoides tuberculata Müller, 1774 fishes (Phillips et al. 2010) so it is conceivable
(Prosobranchia: Thiaridae), a snail native to that they may also prey on the eggs or juveniles
regions of Asia and Africa (Brown 1980), has of other snails. However, M. tuberculata are
been confirmed in at least 15 states throughout generalist grazers and the ingestion of eggs may
the U.S., including California, Texas, Arizona, not be intentional, but an indirect effect of
Louisiana, and Oregon (Karatayev et al. 2009). grazing.
Thiarid snails, such as M. tuberculata, can
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

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

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

289

Acknowledgements H.L.A. Ladd and D.L. Rogowski

This research was supported by the Nature Conservancy and Lo CT, Lee KM (1996) Pattern of emergence and the effects of
Texas Tech University (Lubbock, Texas). Brian Lang of New temperature and light on the emergence and survival of
Mexico Game and Fish and John Karges of the Nature heterophyid cercariae (Centrocestus formosanus and
Conservancy graciously provided literature, information, and field Haplorchis pumilio). The Journal of Parasitology 82: 347–
guidance throughout the course of this study. We thank Jeff 350, http://dx.doi.org/10.2307/3284178
Bradstreet, Cameron Gallegos, Jimmy Huddleston, Lucas
Schilder, and Jamie Suski for their field and laboratory assistance. Madsen H, Frandsen F (1989) The spread of freshwater snails
We also thank Dr. Christopher J. Salice and Dr. Christopher M. including those of medical and veterinary importance. Acta
Taylor for manuscript proofreading and Dr. Lori Tolley-Jordan Tropica 46: 139–146, http://dx.doi.org/10.1016/0001-
for providing advice and guidance on this research project and for 706X(89)90030-2
reviewing an earlier draft of this manuscript.
McDermott KS (2000) Distribution and infection relationships of
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