article - Aquatic Invasions

Aquatic Invasions (2009) Volume 4, Issue 3: 435-450
DOI 10.3391/ai.2009.4.3.2
© 2009 The Author(s)
Journal compilation © 2009 REABIC (http://www.reabic.net)
This is an Open Access article
Research article
Invasive mollusks Tarebia granifera Lamarck, 1822 and Corbicula fluminea
Müller, 1774 in the Tuxpam and Tecolutla rivers, Mexico: spatial and seasonal
distribution patterns
Eugenia López-López 1* , J. Elías Sedeño-Díaz 2 , Perla Tapia Vega 1 and Eloiza Oliveros 1
1
Laboratorio de Ictiología y Limnología, Escuela Nacional de Ciencias Biológicas. IPN. Prol. de Carpio y Plan de Ayala, Col. Sto.
Tomás, 11340, México D.F.
2
Coordinación del Programa Ambiental.IPN Edificio CFIE, Planta Baja, Av. Wilfrido Massieu esq. Av. Luis Enrique Erro, Unidad
Profesional Adolfo López Mateos, Col. Zacatenco, 07738, México D.F.
E-mail: [email protected] (ELL), [email protected] (JESD)
*
Corresponding author
Received 16 April 2009; accepted in revised form 24 July 2009; published online 13 August 2009
Abstract
The Tuxpam and Tecolutla rivers in the Gulf of Mexico, are located in the Mesoamerican biodiversity hotspot and support
different human activities: crude oil extraction, agriculture and livestock, that provoke environmental disturbances. Aquatic
mollusks, physicochemical water characteristics and substrate type were examined along the main watercourse of these rivers
during three periods of one year: the wet season, dry season, and during the northern winds season, when hurricanes are more
frequent. In both rivers, physicochemical water characteristics, types of substratum and mollusk fauna demonstrated
environmental gradients and differentiate two river zones: freshwater and estuarine. Differences were also found between the dry
season, with higher inorganic salts content, and the wet and northern winds and hurricane seasons, when inorganic and organic
nutrient inputs occurred. The mollusk fauna is composed of nine and eleven taxa in the Tecolutla and Tuxpam rivers,
respectively. In both rivers, the introduced gastropod Tarebia granifera is the dominant species in the freshwater zone with
regard to population density and the area it covers within the ecosystem, followed by the introduced bivalve Corbicula fluminea.
Native mollusk species were confined to point-locations and attained very low densities. The gastropod Neritina virginea and the
bivalve Brachidontes exustus were dominant in the estuarine zone of both rivers. Mollusk population densities declined during
the wet, northern winds and hurricane seasons, while in the dry season both alien species reached higher densities, which could
indicate that alien mollusks are removed by effect of climatic events. T. granifera and C. fluminea exhibit traits characteristic of
invasive species and pose a risk to native mollusk biodiversity in these rivers.
Key words: invasive aquatic mollusks, tropical Mexican rivers, environmental degradation, biodiversity loss
Introduction
The Mexican rivers Tecolutla and Tuxpam drain
into the Gulf of Mexico within the Mesoamerican biodiversity hotspot (Myers et al.
2000). Throughout much of the Mexican Gulf
coast region human activities such as crude oil
extraction, intensive agriculture, water extraction
and inputs of untreated wastewater have
degraded various aquatic ecosystems (OrtízLozano et al. 2005). Lake (2000), states that
several environmental disturbances have a
negative impact on native species, through
eradication or removal of sensitive species, and
can create spaces available for colonization.
Other human activities including aquaculture,
recreation, transport, and trade globalization
intentionally or accidentally also contribute to
the spread of invasive aquatic species (Cohen
and Carlton 1998; Carlton and Geller 1993) that
can use such available spaces. Invasive species
are considered the second major cause of biodiversity loss in the world (Vitousek et al. 1996;
Leung et al. 2002) and their spread is one of the
major problems in ecosystem conservation (Ruiz
et al. 2000). Adverse effects of invasive species
may take different forms: once they have
achieved a wide distribution, these species
produce global homogenization of the patterns of
distribution, altering the once distinctive
435
E. López-López et al.
regional biota, and they may affect aquatic
ecosystems through competitive exclusion of
indigenous biota (Rahel 2000; Sousa et al. 2008).
Some invasive species displace native species
through direct competition, predation, introduction of diseases, changes in biological and
geochemical cycles, and alteration of the trophic
web, thus causing adverse effects in the invaded
habitats (Davis et al. 2000; Mack and Lonsdale
2001; Sax et al. 2002).
In Mexico, the National System on Invasive
Species established by the National Commission
for the Understanding and Use of Biodiversity
(CONABIO 2008) has preliminarily identified at
least 1000 invasive species of plants, mollusks,
crustaceans, insects, fishes, amphibians, reptiles,
birds and mammals. These include 13 species of
invading mollusks: 11 bivalves (four freshwater)
and two gastropods (one freshwater). CONABIO
(2008) states that these species affect the natural
wealth of Mexico, deteriorate environmental
conditions in ecosystems and may have negative
consequences on human health, production and
the economy and recognizes the urgent need for
additional knowledge of the distribution of these
species and their impact on native biota, and the
need to identify high-risk biodiversity areas.
Mexico has been ranked as one of the five
megadiversity countries in the world (Bezaury et
al. 2000), however, knowledge of the diversity of
certain groups within its territory is limited
because large areas remain unstudied, especially
in the case of freshwater mollusks (Naranjo
2003). Based on worldwide diversity estimates,
Strong et al. (2008) recognize Mollusca with as
many as 80,000-100,000 described species, as an
extraordinarily diverse phylum, second in
diversity only to arthropods. In Mexico, 16
families of freshwater mollusks have been
recorded, representing five orders, four
subclasses (Naranjo 2003) and 211 species
(Contreras-Arquieta 2000). Furthermore, in a
study of the continental gastropods of Mexico
and Central America, Thompson (2008) found
168 aquatic operculate and 84 aquatic pulmonate
species and emphasized that the mollusk fauna of
Mexico is poorly studied. Thus, the number of
continental mollusk species may exceed current
records, particularly since two zoogeographic
regions, Nearctic and Neotropical, each with its
own characteristic fauna, converge in Mexican
territory sharing a broad transition zone
(Morrone and Márquez 2001). To the paucity of
knowledge on the native freshwater mollusks of
Mexico must be added the lack of information on
436
the distribution of species catalogued as invasive
by CONABIO (2008). It is therefore essential for
studies to focus on the impact of invasive species
on the native biota and invaded habitats. This
paper contributes to the understanding of
patterns of distribution of native and introduced
mollusk species in the Tuxpam and Tecolutla
rivers, in the Mexican subtropics. The different
forms taken by the invasion of two alien species
in each of these rivers are explained and the risks
these species pose are evaluated.
Study area
Tuxpam and Tecolutla rivers cross the Gulf of
Mexico coastal plain in the northern part of the
state of Veracruz (Figure 1). Both are perennial
rivers with high discharges arising in the Eastern
Sierra Madre (more specifically the Sierra Norte
de Puebla) and flowing through a region of hot
humid and sub-humid climate with abundant
rainfall throughout the year, particularly in
summer. Discharges of both rivers are affected
by the impact of northern winds and hurricanes.
The Tecolutla drainage includes the major
tributaries Necaxa, Tenango, Laxaxalpan, Zempoala, Apulco and Chichicatzapa rivers within its
total drainage area of 7,903 km 2 to discharge a
mean of 6,885 million m3 , into the Gulf of
Mexico at Barra de Tecolutla (CONAGUA
2007). The mean air annual temperature is 2126°C, total annual rainfall ranges from 1,200 to
over 4,000 mm, and the rate of evaporation is
1,064-1,420 mm (Sanchez and De la Lanza
1996). The vegetation cover is semi-deciduous
tropical forest, mangrove, halophytic vegetation
and palm grove (Arriaga et al. 2002). Tecolutla
River is listed by CONABIO (Arriaga et al.
2002) as a priority hydrologic region since it
flows through an area of high biodiversity, and is
catalogued as threatened because it supports
diverse land uses (agriculture, livestock, fishing
and tourism).
Tuxpam River watershed covers a surface area
of 5,899 km2 and has a mean annual flow of
2,580 million m3 (CONAGUA 2007). Its principal headwater known as Río Pantepec is joined
by several tributaries before reaching the coastal
plain named Tuxpam to discharge into the Gulf
of Mexico at Barra de Tuxpam. Human activities
in this basin include livestock, agriculture,
fishing and industry. There is a power plant in
Barra de Tuxpan, and a shipyard and the seaport
of Tuxpam are located near the river’s mouth.
Invasive mollusks in rivers of the Gulf of Mexico
Figure 1. Location of study sites in the Tecolutla and Tuxpam rivers. Tx followed by a number indicates the number of the study
site in the Tuxpam river. Tc followed by a number indicates the number of the study site in the Tecolutla river. Geographic
coordinates are in Annex 1
Material and Methods
A total of 11 sites in the Tuxpam River (Tx) and
nine in the Tecolutla River (Tc) were surveyed
(Figure 1, Annex 1). Collection of aquatic
mollusks was made during three different periods
of the year: the wet season (August 2007 in Tc,
September 2007 in Tx), the northern winds and
hurricane season (December 2007 in Tc, January
2008 in Tx) and the dry season (March 2008 in
Tc, April 2008 in Tx). Surveys covered the main
water-courses of the basins including their upper,
middle and lower reaches. Different collection
methods were used depending on stream bed
characteristics and presence/absence of aquatic
vegetation (Wetzel and Likens 2000): collection
within 1-m2 quadrats, sieving of sediments, 1 m2base Surber net, and collection among roots,
stems and foliage in areas of the banks with
aquatic vegetation. Specimens were fixed in 70%
ethanol.
Environmental parameters were measured in
situ at all study sites using a Quanta multiparametric sonde: water temperature (°C),
turbidity (NTU), salinity (PSU) dissolved
oxygen (mg/L) and pH. A General Oceanic flow
meter was used to record current velocity
(m/sec) in transects across the sampled area,
while altitude (masl) and geographic coordinates
were determined with a Sport Trak Magellan
GPS.
Two 500-mL samples of water from each site
were transported in acid washed glass containers
437
E. López-López et al.
at 4°C to the laboratory in order to evaluate
water quality parameters. Two sediment samples
from each site were collected in 1000-mL flasks
for subsequent sediment and organic matter
analyses and for specimen collection.
Water samples were processed with a HACH
DRL2500 spectrophotometer to determine total
nitrogen (NT mg/L), nitrite (NO2 mg/L), nitrate
(NO3 mg/L), ammonia (NH3 mg/L), sulfate (SO4
mg/L), orthophosphate (PO4 mg/L), total
phosphorus (P T mg/L), color (Pt-Co units),
hardness (CaCO3 mg/L), total suspended solids
(TSS mg/L) and total dissolved solids (TDS
g/L). APHA (1985) procedures were used to
measure alkalinity (CaCO3 mg/L), chloride (Cl
mg/L), biochemical oxygen demand (BOD 5 ) and
total and fecal coliforms (MPN/100 mL).
Sediment samples were dried at 60°C for 24 h
and processed for analysis according to EPA
(1986) procedures. The mesh size (mm) of sieves
was: 4.76, 3.36, 2.38, 2, 1.68, 1.41, 0.841, 0.5,
0.42, 0.297, 0.25, 0.21, 0.177, 0.149 and 0.106.
The variable φ (-Ln 2 of the diameter of particle)
was plotted against the cumulative weight of
materials retained in each sieve in order to obtain
the mean particle size and percentages of each
soil texture according to the Wentworth scale.
Organic matter was quantified using the Walkey
and Black method (NOM-021-RECNAT 2000).
Separate sediment samples for specimen
collection were sieved and examined with a
Zeiss stereoscopic microscope. The specimens
obtained were separated and fixed in 70%
ethanol.
Importance value index (IVI) was determined
according to Krebs (1989) for the whole river,
taking into account the frequency of occurrence
(proportion of times that a species occurs in all
the samples taken) and relative abundances
(proportion of specimens for each species in the
total specimens collected) of all mollusk species
for each river: IVI= %FO + relative Ab, where:
%FO = Percent frequency of occurrence and
relative Ab = Relative abundance.
Zones and environmental gradients along each
river were visualized and characterized
by
principal component analysis (PCA) using a
correlation matrix of the log transformed (x+1)
values of physicochemical factors, water quality
parameters, organic matter and mean sediment
particle size at each of the sites during the three
study seasons. Canonical correspondence
analysis (CCA) was used to examine the
correlation of mollusk species with habitat
438
conditions in each river, using a correlation
matrix of the log (x+1) transformed values of in
situ recorded factors, water quality, sediment
analysis and organic matter, and a second matrix
with the relative abundance of each mollusk
species, transforming values to square roots.
Statistical analyses were performed with XLSTAT v. 2008 software (XL-STAT 2008).
Results
Environmental characterization of rivers
Tecolutla River
PCA revealed an environmental gradient with
spatial and seasonal variations. The ordination
biplot (Figure 2) shows the first two axes which
together accounted for 51.43% of the total
variance (PC1: 34.21% and PC2: 17.22%). Three
clusters of sites corresponding to each of the
study seasons are apparent. In August (wet
season) there are high levels of total coliforms,
nutrients (nitrate, nitrite, orthophosphate, PT ),
suspended solids and turbidity. No marked
spatial variations occurred in this month, but at
sites Tc9 and Tc8 the highest content of
coliforms and nutrients was recorded, while sites
Tc1 to Tc6, located at higher altitudes above sea
level, showed higher levels of orthophosphate,
PT and turbidity. In December (the cold, northern
winds season), there was a wider scatter of sites
expressed as spatial variation in the biplot
(Figure 2), as a result of the higher variation of
measured parameters. Tc8 and Tc9, influenced
by sea water, were highest in salinity, total
dissolved solids, chloride and sulfate. Tc1 to
Tc7, on the other hand, were characterized by
higher flow velocity, pH, N T , color, and organic
matter content as well as larger particle size. In
March (dry season), the highest levels of
hardness, alkalinity, BOD5 , ammonia and
dissolved oxygen were recorded. Spatial
variations occurred in this season. Tc9 was found
to be the most different site due to high salinity,
total dissolved solids, sulfate and chloride, while
at site Tc8, the highest content of ammonia was
recorded. PCA differentiated the marine
influence (estuarine zone Tc8 and Tc9 in
December and March, Tc9 in August) from the
freshwater zone (Tc1 to Tc7), and revealed the
seasonal effect of torrential rains when the
salinity was lower and almost all the river
showed environmental homogeneity.
Invasive mollusks in rivers of the Gulf of Mexico
Figure 2. PCA biplot of Tecolutla River. Vectors represent environmental factors. Codes as in Annex 2. Numbers after Tc= indicate
the number of study site and letters after number indicate month of study (Mar= March, Dec= December, Au= August)
Figure 3. PCA biplot of Tuxpam River. Vectors represent environmental factors. Codes as in Annex 2. Numbers after Tx= indicate
the number of study site and letters after number indicate month of study (Apr= April, Jan= January, Sep= September)
439
E. López-López et al.
Tuxpam River
The first two PCA components accounted for
44.27% of the total variance (PC1: 27.43% and
PC2: 16.84%). The biplot of these components
(Figure 3) show the position of sites arrayed as
environmental gradients. Tx8 to Tx11 in January
and April and Tx11 in September were characterized by the highest levels of salinity, chloride,
sulfate and total dissolved solids, making evident
the reach with marine influence. In January (the
cold, northern winds season), the upper reaches
(Tx1 to Tx7) showed the highest flow velocity,
alkalinity, dissolved oxygen and total coliforms
values. In April (dry season), Tx1 to Tx6 were
high in total coliforms and organic matter
content, and Tx7 in BOD5 , hardness, color,
turbidity, NT and PT. In September (wet season),
environmental conditions were uniform throughout the river. This season was characterized by
peak of water temperatures and high nutrient
(nitrite, nitrate, orthophosphate) and organic
matter content. Only one site (Tx11) differed
from the rest of the studied localities due to its
marine influence (chloride, salinity, total
dissolved solids), as well as the high levels of
ammonia and NT. According to the results of
PCA (Figure 3), the estuarine (Tx8 to Tx11) and
freshwater (Tx1 to Tx7) zones were
differentiated, as well as the seasonal dynamic of
the system.
Mollusk species and patterns of distribution
Nine mollusk species were collected in the
Tecolutla and 11 in the Tuxpam basins (Table 1).
Three alien species occurred in both rivers: two
gastropods (Tarebia granifera and Melanoides
tuberculata) and one bivalve (Corbicula
fluminea). The species collected showed marked
differences in their pattern of distribution along
the rivers.
Distribution of species in Tecolutla and
Tuxpam rivers are shown in Table 2. In
Tecolutla River, T. granifera and C. fluminea
were widely distributed in the freshwater zone,
from Tc1-8. M. tuberculata was found only in
the upper reaches from Tc1-3. Haitia mexicana
is present at Tc4 and Tc5. Brachidontes exustus
and Neritina virginea are restricted to the lower
reaches near the river mouth (Tc8). Species with
a more limited distribution were Pomacea
flagellata, in the upper reaches at Tc1, and
Succinea sp. and Biomphalaria sp. in the upper
440
Table 1. List of aquatic mollusk species in Tecolutla (Tc)
and Tuxpam (Tx) rivers (n-native, a-alien)
Aquatic mollusk species
Class Gastropoda
Family Neritidae
Neritina virginea Linnaeus, 1758
Family Ellobiidae
Melampus coffeus Linnaeus, 1758
Family Ampullaridae
Pomacea flagellata (Say, 1827)
Family Thiaridae
Melanoides tuberculatas
(O.F.Müller, 1774)
Tarebia granifera Lamarck, 1822
Family Physidae
Haitia mexicana (Philippi, 1841)
Family Ancylidae
Hebetancylus excentricus (Morelet,
1851)
Family Planorbidae
Biomphalaria sp.
Micromenetus dilatatus Gould,
1841
Family Succineidae
Succinea sp. Drapanaurd, 1801
Class Bivalvia
Family Ostreidae
Ostrea palmula Carpenter, 1857
Family Mytilidae
Brachidontes exustus (Linnaeus,
1758)
Family Corbiculidae
Corbicula fluminea (O.F. Müller,
1774)
Total
Status
Tc
Tx
n
x
x
x
n
n
x
x
a
x
x
a
x
x
n
x
x
n
n
x
x
n
n
x
x
n
x
n
x
x
a
x
x
9
11
reaches at Tc2. In the Tuxpam River T. granifera
was the most widely distributed species in the
freshwater zone, Tx1-6. C. fluminea was found
at Tx2, Tx6 and Tx7. M. tuberculata occurred at
Tx1-4 and Tx6. H. mexicana was present in the
upper and middle reaches, Tx1-3, Tx5 and Tx6.
N. virginea was found in the lower reaches only
(Tx7-9). B. exustus occurred only at Tx9.
Species with very limited distribution included
P. flagellata
(Tx3
only),
Hebetancylus
excentricus (Tx5 and Tx6), and Micromenetus
dilatatus (Tx5 and Tx7). Melampus coffeus is
known only from Tx9 and Ostrea palmula only
Tx11 (Table 2).
Invasive mollusks in rivers of the Gulf of Mexico
X
X
X
Ostrea palmula
X
Micromenetus
dilatatus
Brachidontes
exustus
X
Melampus
coffeus
Neritina
virginea
Succinea sp.
X
X
X
X
X
X
X
X
X
X
X
Hebetancylus
excentricus
X
X
X
X
X
X
X
X
X
Biomphalaria sp.
X
X
X
X
X
X
X
X
Pomacea
flagellata
X
X
X
X
X
X
X
X
Haitia
mexicana
Corbicula
fluminea
Tc1
Tc2
Tc3
Tc4
Tc5
Tc6
Tc7
Tc8
Tc9
Tx1
Tx2
Tx3
Tx4
Tx5
Tx6
Tx7
Tx8
Tx9
Tx10
Tx11
Melanoides
tuberculata
Study
sites
Tarebia
granifera
Table 2. Records of mollusks species at study sites of Tecolutla (Tc) and Tuxpam (Tx) rivers during study period (for locations
of study sites see Figure 1 and Annex 1)
X
X
X
X
X
X
X
Mollusk species showed marked variations in
densities and dominance. In the Tecolutla River,
T. granifera attained mean densities > 100
indivuals/m2 . The species C. fluminea, N. virginea, Haitia mexicana and Melanoides tuberculata had mean densities ranging from 1 to 100
individuals/m2 . Brachidontes exustus, P. flagellata, Succinea sp. and Biomphalaria sp. all had
mean densities ≤1 individual/m2 (Figure 4). In
the Tuxpam River, T. granifera and Brachidontes exustus reached mean densities of 100 to
1,000 individuals/m2 . N. virginea, H. mexicana,
C. fluminea,
Micromenetus
dilatatus
and
Melanoides tuberculata had mean densities of
10-100 individuals/m 2 while mean values for
Hebetancylus excentricus and P. flagellata
ranged from 1 to 10 individuals/m2 . Melampus
coffeus and O. palmula had the lowest mean
densities, with ≤ 1 individual/m2 (Figure 4).
Very marked spatial and seasonal variations
occurred in mean densities of mollusk species. In
the Tecolutla River, the lowest densities
occurred in December and the highest in March
(Figure 5a). In the freshwater zone, Tc5 and Tc7
had the highest densities in all three study
seasons. Seasonal density changes produced a
X
X
X
X
X
X
X
Figure 4. Mean density of mollusk species in Tecolutla and
Tuxpam rivers. The bar represents SD
shift in the species with the highest population
densities in the upper reaches (Tc1 to Tc3):
C. fluminea had the maximum values in August
and March and Melanoides tuberculata in
December (Figure 5b). In the middle reaches, in
spite of seasonal variations, the species with the
441
E. López-López et al.
Figure 5. Absolute and relative density of the aquatic mollusk species in Tecolutla River
Figure 6. Absolute and relative density of the aquatic mollusk species in Tuxpam River
442
Invasive mollusks in rivers of the Gulf of Mexico
highest densities was T. granifera, while in the
lower reaches N. virginea had the highest
densities in all three seasons (Figure 5b).
In the Tuxpam River, the lowest densities
occurred in January (Figure 6a) while peak
values were attained in April. In the freshwater
zone, Tx3 to Tx6 showed the highest densities.
In spite of seasonal variations in population
densities, there was no change in the higher
ratios at which T. granifera was present in the
freshwater zone and the species N. virginea and
B. exustus in the estuarine zone (Figure 6b).
Importance value indicates that T. granifera is
the dominant species in both rivers, with index
values of 128 and 96 in the Tecolutla and
Tuxpam rivers, respectively (Figures 7a and 7b).
In the Tecolutla River, T. granifera, C. fluminea
and M. tuberculata (all three non-native species),
account for a cumulative index value of 179 out
of a possible 200. Importance values below 7
were obtained for all other mollusk in this river
(Figure 7a). In the Tuxpam River, T. granifera,
two brackish species (N. virginea, B. exustus)
and two freshwater species (C. fluminea, Haitia
mexicana) have index values ranging from 10 to
26. Species with IVI< 10 include Micromenetus
dilatatus, P. flagellata, Hebetancylus excentricus, Melanoides tuberculata and Melampus
coffeus (Figure 7b).
Figure 7. Importance value index of mollusks a) Tecolutla
River and b) Tuxpam River
Relation of environmental parameters,
substratum characteristics and mollusk species
The first two components in the CCA of the
Tecolutla River account for 81.30% of the
explained variance (Axis 1: 64.93% and Axis 2:
16.37%). The biplots show the relations of
mollusk species and sites, as well as water
quality conditions and type of substratum. Three
groups of species can be seen in the biplot in
Figure 8a. The smallest one is formed by
N. virginea and B. exustus, which reached their
highest densities at Tc9 in December and March.
Similarly, Figure 8b shows these species are
closely correlated with high salinity, total
dissolved solids, chloride, sulfate and hardness.
In the upper left quadrant are T. granifera,
Haitia mexicana and C. fluminea, which attained
maximum densities in Tc4, Tc5, Tc6 to Tc7 in
March and in Tc3 and Tc7 in August. In both
seasons, these sites had the highest levels of
coliforms, nitrite, nitrate, ammonia, BOD5 , color,
alkalinity, current velocity and water temperature, with fine and very fine sandy substrata. On
the right side of the biplot are P. flagellata,
which is closely correlated with Tc1 in March, a
site in the upper reaches with a substratum of
gravel and very coarse sand; Melanoides
tuberculata, related with Tc1 and Tc2 in August
and with fine gravel and very fine sandy
substrata; and Biomphalaria sp. and Succinea
sp., occurring at Tc2 in March and related with
fine gravel and coarse sandy substrata; seasons
and conditions that are exactly opposite those of
the first group of species. CCA showed species
assemblages, their divergent patterns of
distribution and most importantly their relation
with habitat conditions.
In the CCA of Tuxpam River, the first two
components accounted for 75.89% of the
explained variance (Axis 1: 55.37% and Axis 2:
20.53%). Biplots show the species separated into
two groups. The group on the right side includes
B. exustus, Micromenetus dilatatus, Melampus
coffeus and N. virginea. These species were
present at Tc7, Tc8, Tc9, Tc10 and Tc11 in all
study seasons (Figure 9a) and are related with
high levels of total dissolved solids, salinity,
chloride, ammonia, sulfate, NT , PT and BOD5 ,
and very fine sandy and coarse to very fine silty
substrata (Figure 9b). On the left side of the
biplot are T. granifera, C. fluminea, Hebetancylus excentricus, Haitia mexicana, P. flagellata
443
E. López-López et al.
and Melanoides tuberculata. These species are
distributed in the freshwater zone (Tx1-6) with
high levels of nitrite, nitrate, orthophosphate,
alkalinity, pH, turbidity, water temperature and
coliforms, and also at higher altitudes where the
substratum is predominantly coarser materials
such as pebbles, gravel and coarse to fine sand
(Figures 9a and 9b). CCA identified two groups
of mollusks with entirely different distributions
as well as the relation of each group with
contrasting environmental conditions and
substrata.
Figure 8. Biplot of CCA of Tecolutla River. a) study sites and species and b) factors and species. Numbers after Tc indicate the
number of study site, letters after number indicate month of study (Mar= March, Dec= December, Au= August). See Annex 2 for the
code of abbreviations of environmental factors and species
444
Invasive mollusks in rivers of the Gulf of Mexico
Figure 9. Biplot of CCA of Tuxpam River. a) study sites and species and b) factors and species. Numbers after Tx indicate the
number of study site, letters after number indicate month of study (Apr= April, Jan= January, Sep= September). See Annex 2 for the
code of abbreviations of environmental factors and species
Discussion
Water quality characteristics indicate that the
Tuxpam and Tecolutla rivers receive inputs of
organic matter, nutrients (orthophosphate,
nitrogenous compounds) and coliform bacteria.
Both rivers are located in a region with several
environmental disturbances by human activities
(Ortíz-Lozano et al. 2005), which contribute to
the inputs of diverse compounds originating in
wastewater discharges, leaching materials and
basin runoff. Despite the nutrient and organic
matter enrichment found by this study, the water
of these rivers has been rated good and excellent
by the CONAGUA (2007) monitoring network.
This agency, however, uses only three
parameters (BOD5 , Chemical oxygen demand
and total suspended solids) to rate water quality.
445
E. López-López et al.
Our results, on the other hand, indicate both
rivers sustain nutrient enrichment, although they
are less degraded than the Coatzacoalcos and
Pánuco rivers which are also located in the Gulf
of Mexico coast area (CONAGUA 2007).
The Tuxpam and Tecolutla rivers show
important differences in the estuarine zone due
to their morphology, freshwater discharges and
seasonal variations. Mean annual flow is 2,580
million m3 in the former and 6,885 million m3 in
the latter (CONAGUA 2007). As a result of
these differences in stream flow, the estuarine
zone is larger in the Tuxpam River than in the
Tecolutla River. In our study PCA allowed
identification of environmental gradients along
each river that are associated with changes in
altitude, flow velocity, dissolved solids, organic
matter, nutrients and salinity, that differentiate
two zones: freshwater and estuarine. The rivers
undergo seasonal variations: during the dry
season, peak levels of alkalinity and BOD5
occurred and sea front influence produced a
marked increase in salinity in the estuarine zone.
During the wet and the northerly wind seasons,
and favored by the effect of hurricanes, both
rivers showed a tendency to environmental
homogeneity. Higher levels of nutrients (nitrate,
nitrite, orthophosphate, PT ) were present and the
estuarine zone decreased in extent. Turbidity
rose while salinity fell markedly. Studies
showing the effect of seasonal rainfall and
drought in watercourses in intertropical areas are
scarce. Brodie and Mitchell (2005) found higher
nutrient loads during rain episodes and in
correlation with land use for agriculture in
tropical river basins in Australia. Agriculture is a
major land use in the Tuxpam and Tecolutla
basins and, along with discharges from small
human settlements near the river, may explain
nutrient inputs, particularly during the wet
season.
Mathooko and Mavuti (1992) state that
hurricanes and rainy seasons not only alter the
volume of stream flow, they also bring sediment
loads and increase benthic organisms drift,
which affect their population densities. In our
study in both rivers density values were depleted
during the months of rainy, northern winds and
hurricanes seasons as opposed to the dry season
when densities rose.
Aquatic mollusks of the Tuxpam and
Tecolutla rivers showed strong dominance of two
exotic species: T. granifera and C. fluminea.
Only at one of nine Tecolutla study sites (Tc9)
and in four of 11 Tuxpam study sites (Tx8 to
446
Tx11) were both absent. The only areas not
colonized by these alien species were the
estuarine zones of the rivers, where N. virginea
and B. exustus were dominant. In both freshwater
courses these alien species reached higher
densities than others. Melanoides tuberculata,
another non-native species, had a limited
distribution in both rivers as well as lower
densities than others.
Contreras-Arquieta (2000), Naranjo (2003)
and Thompson (2008) state that knowledge of
aquatic mollusks is in an initial stage in Mexico.
In the Tuxpam and Tecolutla rivers there are no
historical records of the native aquatic mollusks.
The number of mollusk species found in our
study in both rivers is low, compared to numbers
in more extensively studied areas of Mexico,
such as Cuatro Ciénegas, Coahuila with 13
species; (Contreras-Arquieta 1998) and El Edén,
Quintana Roo with 11 species (Cózatl-Manzano
and Naranjo-García 2007). Several authors
(Davis et al. 2000; Mack and Lonsdale 2001; Sax
et al. 2002; Sousa et al. 2008), mention that
introduced species are able to displace native
species through different mechanisms, including
competitive exclusion, introduction of disease
and even habitat change. In the case of the
Tuxpam and Tecolutla rivers the absence of
historical malacological fauna records prevents
comparison of the native mollusk assemblages
before and after the introduction of alien species.
The gastropod T. granifera is native to India,
Southeast Asia, the Philippines, Japan and
Hawaii (Abbot 1952). Its introduction to the
United States has been documented by Karatayev
et al. (2007), who point out that the aquarium
trade recognizes its presence in Texas since
1935. In our study, the wide distribution of this
species in the Tuxpam and Tecolutla rivers
shows it has been able to establish and is very
successful in freshwater zones of both rivers,
although the date of its introduction remains
unknown. In this respect, only Naranjo and
Olivera-Carrasco (2007) record its occurrence in
Lake Catemaco, Veracruz, in the south of the
Gulf of Mexico. Karatayev et al. (2007) report
that this species tolerates a wide range of
temperatures (10 to 38°C). Water temperatures in
the Tuxpam and Tecolutla rivers (18°C min to
30°C max) are well within this range.
Pointier and Jourdane (2000) stress the
damage T. granifera has caused, including
probable irreversible eradication of several
native mollusks in Cuba (Pachychilus violaceus
and various species of the genus Biomphalaria),
Invasive mollusks in rivers of the Gulf of Mexico
and endangerment of others (Hemisinus brevis
and H. cubanianus). The extremely low densities
of other mollusks in the Tuxpam and Tecolutla
rivers are in agreement with statements by
Karatayev et al. (2008) who suggested this is one
of the major impacts of T. granifera on the
indigenous mollusk fauna and is a preliminary
stage in the eradication of native species.
Pointier et al. (1998) found that the introduction
of thiarids to eradicate schistosomiasis in
Martinique island affected two species of
Biomphalaria, but impacts were negligible on
neritids. This is also in agreement with our
findings in the Tuxpam and Tecolutla rivers
since N. virginea is the dominant species in the
estuarine zone where T. granifera has not
become established. Pointier et al. (1998) state
that the attributes of T. granifera favoring its
rapid spread include parthenogenesis, extremely
high densities, ability to support faster currents
and dislodgement, and use of the entire stream
bed. In our study the CCA indicates that
T. granifera in the Tuxpam and Tecolutla rivers
is able to establish in a wide variety of fine to
coarse substrata under nutrient-rich conditions
(particularly nitrogen) and with high BOD5 .
These capabilities make T. granifera a successful
invasive species and provide an explanation for
its pattern of distribution and extremely high
densities in both rivers.
The bivalve C. fluminea is native to Asia
(China, Korea and southeastern Russia)
(McMahon 1999; Mouthon 2001) and colonizes
both fresh and brackish waters (salinity <10
PSU) (Sousa et al. 2009). It was possibly
introduced for the first time in North America
before 1924 in British Columbia, Canada
(Naranjo and Olivera-Carrasco 2007) and in
1938 to the US, most probably by Chinese
immigrants who use this species as food
(McMahon 1999). In Mexico it is known from
the northern part of the country on both the Gulf
and Pacific slopes. In the south its first record
dates back to 1992 in Catemaco, Veracruz
(Naranjo and Olivera-Carrasco 2007). In the
Tecolutla and Tuxpam rivers, C. fluminea
showed different patterns of distribution and
abundance, ranking second and fourth in IVI,
respectively. It had a more limited distribution in
Tuxpam River than in Tecolutla River, and was
found in the estuarine zone in the Tecolutla (at
Tx7). Sousa et al. (2008) say the attributes of
C. fluminea favoring its role as an invasive
species include rapid growth, early sexual
maturity, short lifespan, high fecundity and its
association with diverse human activities.
However, Souza et al. (2008), also mention this
species was adversely affected in sites with
inputs of organic contaminants, while De la Hoz
(2008) found it was adversely affected by drops
in the water level. Likewise, Sousa et al. (2008)
report C. fluminea is successful in environments
without considerable water level fluctuations. In
our study, the Tuxpam and Tecolutla rivers were
found to receive nutrient and organic matter
inputs and to fluctuate in water level as a result
of floods and torrential flows due to rainfall of
northern winds and hurricane seasons, as
opposed to the dry season when flow decreases.
These factors are perhaps responsible for the low
densities and limited distribution of C. fluminea
in these rivers, despite reports by other authors
of its invasive capability (Mouthon 2001;
Mouhton and Parghentanian 2004). Phelps
(1994) states that C. fluminea may experience
population declines after reaching the lag period
of invasion. This species may therefore be
undergoing a population decline since records of
its presence in the state of Veracruz date back to
1992 (Naranjo and Olivera-Carrasco 2007). This,
along with unfavorable abiotic factors, may
explain the low densities and the relative limited
distribution of this species in the Tuxpam and
Tecolutla rivers. Type of substratum is another
factor that has been examined in regard to the
establishment of C. fluminea. It has been found
primarily in fine to coarse sandy substrata
(Cordeiro and MacWilliams 1999; Paunović et
al. 2007; Sousa et al. 2008), although De la Hoz
(2008) reports its occurrence in a muddy
substratum. In the Tuxpam and Tecolutla rivers
it was present in substrata ranging from coarse
sand to fine-grained sediment.
Negative impacts due to high densities of
C. fluminea include biofouling (especially in
power facilities), occlusion of small diameter
pipelines, irrigation canals and domestic water
supply systems. It is also able to alter the
substratum and affect native species (Paunović et
al. 2007). There are no records of biofouling by
this species in our study area, but a potential risk
exists, particularly in the Tuxpam River in which
C. fluminea has colonized the estuarine zone
where a seaport and a power plant are located.
It has been reported that when T. granifera is
introduced in places previously occupied by
M. tuberculata, the former rapidly outnumbers
the latter in terms of density (Pointier et al.
1998). Contreras-Arquieta et al. (1995) record
presence of M. tuberculata in both the Tuxpam
447
E. López-López et al.
and Tecolutla rivers, but did not report
T. granifera. Thus, it appears that in these rivers
T. granifera is an alien species that may have
recently established in these rivers that are
experiencing changes in species invasion
processes that are resulting in T. granifera being
favored over the two other non-indigenous
species. In agreement with Pointier et al. (1998)
it appears from our study that T. granifera
attains its higher population densities through
competitive advantage.
In conclusion, this study lends further support
to earlier evidence that T. granifera is a very
successful alien species. It has become the
dominant mollusk in both the Tuxpam and
Tecolutla rivers. C. fluminea, is the other main
component in the benthic freshwater zones of
both rivers. Environmental conditions prevailing
in the Tuxpam and Tecolutla rivers are suitable
for T. granifera and C. fluminea species
invaders, such as water temperature regimes,
substratum availability and high levels of
nutrients which increase food availability.
Pronounced depletions in density during the
rainy and northern winds and hurricanes seasons
could indicate that the mollusks are removed by
the current during stormy torrential floods.
Tarebia granifera has capabilities for recolonization after torrential rains and their
populations respond quickly during the dry
season when nutrients favor the food availability,
and in such situations may be more successful
than C. fluminea and M. tuberculata. All three
alien species, however, constitute a serious threat
to native aquatic mollusks, since they have
become the dominant components of the
malacological community in both these rivers,
where native species have been localized to
narrow habitats and occur in relatively low
densities.
Acknowledgements
This research was financed by the Joint Fund of
the National Science and Technology Council
(CONACyT Mexico) and the Veracruz state
government (Project 41750) as well as by the
Research and Postgraduate Studies Secretariat
(SIP) of the National Polytechnic Institute (IPNMexico). Authors thank the reviewers for their
valuable comments to the manuscript and
consequent suggestions that improve this paper.
448
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Annex 1
Geographic coordinates of study sites in Tuxpan and Tecolutla rivers
Study
Site
Geographic coordinates
Location name
Latitude, N
Longitude, W
Altitude,
masl.
20°51.172'
20°53.718'
20°57.349'
20°55.447'
20°55.601'
20°55.727'
20°57.228'
20°55.556'
20°54.963'
20°56.842'
20°58.007'
97°53.029'
97°47.268'
97°46.472'
97°42.795'
97°36.469'
97°40.797'
97°31.699'
97°29.629'
97°25.748'
97°24.054'
97°19.572'
101
93
44
38
23
20
19
9
5
3
0
20°16.065'
20°15.907'
20°13.223'
20°14.503'
20°16.170'
20°23.817''
20°27.347'
20°26.583'
20°28.492'
97°33.475'
97°30.647'
97°27.828'
97°23.893'
97°19.676'
97°14.169'
97°11.791'
97°07.479'
96°00.256'
87
70
71
43
11
8
6
3
0
Tuxpam River
Tx1
Tx 2
Tx 3
Tx 4
Tx 5
Tx 6
Tx 7
Tx 8
Tx 9
Tx 10
Tx 11
La Reforma
Úrsulo Galván
Rancho el Cieruelo
San Antonio
Chapopote Nuñez
Buena Vista
Tampiquillo
El Higueral
Quinta Las Puertas
Puente Tuxpan
Boca de la Laguna de Tampamachoco
Tecolutla River
Tc1
Tc 2
Tc 3
Tc 4
Tc 5
Tc 6
Tc 7
Tc 8
Tc 9
Entabladero
Arenal
El Chacal
Espinal
Paso de Valencia
Puente Remolino
Ignacio Muñoz Zapotal
Puente Chalana
Tecolutla
Annex 2
Code of abbreviations: species, environmental factors and sediment type in the ACP and CCA biplots
Environmental abbreviations:
Sediment abbreviations:
Species abbreviations:
Alc= alkalinity
Alt= altitude
BOD= Biochemical oxygen demand
Cl= chloride
Color= color
Ctot= total coliforms
DO= dissolved oxygen
Dur= hardness
NH3= ammonia
NO2= nitrites
NO3= nitrates
Ntot= total nitrogen
om= organic matter
OrtPO4= orthophosphate
Pt= total phosphorus
Sal= salinity
SO4= sulfates
TDS= total dissolved solids
Tmp= medium size particle
TSS= total suspended solids
Turb= turbidity
Twat= water temperature
V curr= current velocity
ag=coarse sand
am= medium sand
gu= pebbles
gr=gravel
ag= very coarse sand
amf= very fine sand
lg= gross silt
lmf= very fine silt
lm= medium silt
lf= fine silt
Be= Brachidontes exustus
Bsp= Biomphalaria sp.
Cf= Corbicula fluminea
He= Hebetancylus excentricus
Hm= Haitia mexicana
Mc= Melampus coffeus
Md= Micromenetus dilatatus
Mt= Melanoides tuberculatas
NV = Neritina virginia
Pc= Pomacea flagellata
Ssp= Succinea sp.
Tg= Tarebia granifera
450