Aquatic Invasions (2012) Volume 7, Issue 2: 287290

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

Open Access

Short Communication

Egg predation and parasite prevalence in the invasive freshwater snail,

Melanoides tuberculata (Mller, 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: hallieladd@gmail.com (HLAL), david.rogowski@ttu.edu (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 Mller, 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
Invasions of ecosystems by non-native species
are
increasing,
especially
in
aquatic
environments (Byers 2000). The consequences of
these invasions include biodiversity loss and
changes in ecosystem structure (Pimentel 2002).
Specifically, the establishment of non-native
freshwater snails has been associated with
changes in ecosystem function (Arango et al.
2009), community structure (Kerans et al. 2005),
and the introduction of non-native parasites
(Madsen and Frandsen 1989).
Melanoides
tuberculata
Mller,
1774
(Prosobranchia: Thiaridae), a snail native to
regions of Asia and Africa (Brown 1980), has
been confirmed in at least 15 states throughout
the U.S., including California, Texas, Arizona,
Louisiana, and Oregon (Karatayev et al. 2009).
Thiarid snails, such as M. tuberculata, can
directly alter community structure through
competition with native snails (Pointer et al.
1993). In fact, M. tuberculata has been
introduced in areas where schistosomiasis was

prevalent in the hopes of reducing populations of

vector snails such as Biomphalaria glabrata
(Say, 1818) and B. straminea (Dunker, 1848),
and thereby reducing the incidence of the disease
(Pointer et al. 1984; Pointer and Guyard 1992).
Yet, quantitative analyses describing the interactions of M. tuberculata with native snails are
lacking (Tolley-Jordan and Owen 2008) and it is
not known whether native snails are displaced as
a result of competition, displacement, or perhaps
even predation. Competition and intraguild
predation has been shown in some freshwater
snail species (Turner et al. 2007). Melanoides
tuberculata prey upon the eggs of endangered
fishes (Phillips et al. 2010) so it is conceivable
that they may also prey on the eggs or juveniles
of other snails. However, M. tuberculata are
generalist grazers and the ingestion of eggs may
not be intentional, but an indirect effect of
grazing.
Another major concern with the introduction
of exotic snails is the potential parasites that they
may carry and their effects on native fauna. Nonnative trematodes have been documented to
287

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

negatively affect native communities by

infecting vertebrate hosts lacking the co-evolved
defense mechanisms to keep densities of
parasites at a low level (Taraschewski 2006).
Melanoides tuberculata serves as the first
intermediate host to several species of digenetic
trematodes, including the gill trematode
Centrocestus formosanus (Nishigori, 1924)
(Ben-Ami and Heller 2005; Tolley-Jordan and
Owen 2008). Centrocestus formosanus infects
some vertebrate hosts, such as aquatic migratory
birds (e.g. the green heron Butorides virescens
(Linnaeus, 1758) and great egret Ardea alba
Linnaeus, 1758) (Mitchell et al. 2005) as well as
a wide variety of fish hosts, including several
endangered spring species [e.g. the fountain
darter, Etheostoma fonticola (Jordan and Gilbert,
1886)] (Mitchell et al. 2000). The presence of
C. formosanus produces inflammatory responses
in the gills of many freshwater fishes that can
lead to respiratory stress and eventual mortality
(Mitchell et al. 2000; 2005).
One of the largest and last remaining cienega
systems in west Texas is the Diamond Y Spring
preserve located in Pecos County, Texas. It is a
1502-acre tract of land owned and operated by
the Nature Conservancy (Karges 2003). The
Diamond Y Spring preserve is composed of a
number of springs, seeps, and wetlands. The
saline waters within the preserve provide
critically important habitat for two federally
endangered species of desert fishes (Cyprinodon
bovinus Baird and Girard, 1853 and Gambusia
nobilis (Baird and Girard, 1853)) and a suite of
rare aquatic invertebrates. The non-native
M. tuberculata is well established within the
Diamond Y Spring preserve, albeit no snails
have previously been documented to harbor any
exotic trematodes (McDermott 2000). However,
the spread of C. formosanus into the preserve is
of major concern due to its ability to compromise
the health of the preserves federally endangered
fish species. Additionally, it is not known how
M. tuberculata affects Diamond Ys invertebrate
fauna. Investigating the effects of M. tuberculata
on the preserves species of high conservation
concern is necessary to effectively manage these
rare native populations. Thus, the aims of this
study were to determine whether M. tuberculata
prey upon the eggs of a native snail (Physella
spp.) and if the exotic trematode, C. formosanus,
is present in the M. tuberculata population within
the Diamond Y Spring preserve.
288

Materials and methods

Egg predation
The Diamond Y Spring preserve contains two
endemic springsnails [Tryonia circumstriata
(Leonard and Ho, 1960) and Pseudotryonia
adamantia Taylor, 1987], two native snails
(Physella spp. and Assiminea pecos Taylor,
1987), and the invasive M. tuberculata (Ladd
2010). The Physella spp. was used for our egg
predation trials as they are common and readily
produce egg masses year round in a laboratory
setting (personal observation). Also, the endemic
springsnails are state threatened, while A. pecos
is federally listed as endangered and little is
known about their reproduction or maintaining
them in captivity. Melanoides tuberculata
appeared to considerably vary by size within
Diamond Y, the only spring where this species is
found. No snails 30 mm were found beyond
300 m downstream of the immediate outflow of
the spring head (Ladd 2010). Therefore, we
chose to use two size classes in this experiment
(>30 mm or <30 mm). The experiment was conducted from June-September of 2010 at Texas
Tech University (Lubbock, TX). Adult Physella
spp. were stocked into three polypropylene
shoebox containers (281411 cm deep) filled
with de-chlorinated tap water. Snail egg masses
were then transferred to individual 50 ml vials (1
egg mass per vial) filled with 35 ml of dechlorinated tap water. One M. tuberculata snail
was then placed within each vial and predation
was monitored for five days. We considered an
egg mass to be consumed if the entire egg mass
was gone at the end of the trial. A total of 51
M. tuberculata >30 mm and 56 M. tuberculata
<30 mm were used over the duration of the
experiment. Snails were not reused or fed during
the experiment, nor was the water changed.
Snail infection status
Of the six snail species found within Diamond Y
Spring preserve, only M. tuberculata is known to
serve as an intermediate host for C. formosanus
(Scholz and Salgado-Maldonado 2001; Mitchell
et al. 2005). Therefore, only M. tuberculata were
surveyed for the presence of C. formosanus. Live
M. tuberculata were collected during October
and November of 2009 and March, April, and
May of 2010 from Diamond Y spring. Only
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

(Tolley-Jordan and Owen 2008). Presence of
trematodes was assessed using two methods. The
first method consisted of cracking the shell of
M. tuberculata between the first and second
body whorl, removing the digestive tract and
gonads, and examining each for rediae and
cercaria of C. formosanus under a binocular
dissecting
microscope
at
100
total
magnification. The second method consisted of
placing individual snails into 50 ml vials filled
with 35 ml of de-chlorinated water and setting
two lamps equipped with 60-watt incandescent
light bulbs over the vials for 24 hours to ensure
that the temperature of the water reached at least
28C (Lo and Lee 1996). We then pipetted two
ml of water from each vial into petri dishes and
looked for swimming cercariae using a
dissecting scope at 3040 total magnification.
A total of 250 snails were examined for parasite
presence. Fifty and 200 snails were examined
using the first and second method, respectively.
The second method was adopted as our preferred
means of assessment as it has been found to be a
quick and effective way of determining snail
infections [C. formosanus cercariae emerge from
infected snails when exposed to light and
temperatures between 1535C (Lo and Lee
1996)].
As parasites in hosts can be in low numbers
and patchily distributed (Anderson and May
1979), we wanted to determine if our sample size
of 250 was adequate for detecting infected
snails. A Monte Carlo simulation was used to
determine the probability of obtaining a sample
of 250 snails from a population with trematode
prevalence levels of 15% and observing no
infected snails within the sample. Using Pop
Tools (Hood 2010), we simulated a population
of 1000 snails with a 5% infection rate. Two
hundred and fifty snails were randomly sampled
from that population 4999 times. Then, we
counted how many times the sample of 4999
equaled zero infected snails. We repeated this
procedure for 4, 3, 2, and 1 percent parasite
prevalence.
Results and discussion
None of the M. tuberculata >30 mm consumed
any egg masses, while only 3/56 (5.4%) egg
masses were consumed in trials using
M. tuberculata <30 mm. Of 250 M. tuberculata
collected from the spring, none were found to be

infected with C. formosanus. Results of the

simulation indicated that the probability of
obtaining zero parasitized snails in a sample of
250 snails at 5, 4, 3, 2, and 1 percent parasite
prevalence was 0.000, 0.000, 0.008, 0.0776, and
0.0826, respectively.
Though the total percentage of egg predation
in our experiment was 2.8% (3/107),
M. tuberculata may be present in large enough
numbers to affect native snail populations
directly through egg predation. For example, the
estimated abundance of M. tuberculata within
Diamond Y Spring is 187,000 individuals (Ladd
2010). If only 2.8% of M. tuberculata consume
egg masses, approximately 5000 snails could
conceivably consume native egg masses, which
may lead to a significant reduction in native snail
populations. Future studies focusing on food
preference, egg consumption, and natural egg
mortality rates in situ are necessary to
understand the significance of egg predation as a
mechanism for displacing native snail species by
M. tuberculata.
Results from our study and a previous study
conducted by McDermott (2000) indicate that the
trematode C. formosanus is not likely present at
the Diamond Y Spring preserve. In M. tuberculata native habitats, trematode prevalence is less
than 5%, and infections tend to be spatially
aggregated (Anderson and May 1979). However,
in areas where the snails have been introduced,
infection rates can be as high as 53% (Boga et
al. 2005). Although we did not detect any
trematodes, this does not mean that they are not
present within the M. tuberculata population of
the Diamond Y Spring preserve. According to
the results of our simulation, parasite prevalence
could be two percent or lower.
A variety of fish hosts and three species that
serve as definitive hosts for C. formosanus have
been documented at the Diamond Y Spring
preserve: the green heron (B. virescens), great
egret (Adrea alba), and black-crowned-night
heron [Nycticorax nycticorax (Linnaeus, 1758)]
(Mitchell et al. 2005; J. Karges, personal
communication). In addition, C. formosanus has
been documented in fishes and M. tuberculata
from other west Texas springs (McDermott
2000), which suggests that fishes and
M. tuberculata from Diamond Y Spring are
likely to become infected, eventually. Therefore,
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

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

Acknowledgements
This research was supported by the Nature Conservancy and
Texas Tech University (Lubbock, Texas). Brian Lang of New
Mexico Game and Fish and John Karges of the Nature
Conservancy graciously provided literature, information, and field
guidance throughout the course of this study. We thank Jeff
Bradstreet, Cameron Gallegos, Jimmy Huddleston, Lucas
Schilder, and Jamie Suski for their field and laboratory assistance.
We also thank Dr. Christopher J. Salice and Dr. Christopher M.
Taylor for manuscript proofreading and Dr. Lori Tolley-Jordan
for providing advice and guidance on this research project and for
reviewing an earlier draft of this manuscript.

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