Invasive mollusks Tarebia granifera Lamarck, 1822 and Corbicula
fluminea Müller, 1774 in the Tuxpam and Tecolutla rivers, Mexico:
spatial and seasonal distribution patternsAquatic 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
435
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-López1*, J. Elías Sedeño-Díaz2, Perla Tapia Vega1 and
Eloiza Oliveros1 1Laboratorio de Ictiología y Limnología, Escuela
Nacional de Ciencias Biológicas. IPN. Prol. de Carpio y Plan de
Ayala, Col. Sto. Tomás, 11340, México D.F. 2Coordinación 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 Meso- american 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 (Ortíz- Lozano 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 bio- diversity 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
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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, intro- duction 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
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, Zem- poala, Apulco and Chichicatzapa rivers
within its total drainage area of 7,903 km2 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 21- 26°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 princi-
pal 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.
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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 m2- base 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 multi- parametric 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
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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 (PT 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 (BOD5) 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 (-Ln2 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
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
XL- STAT v. 2008 software (XL-STAT 2008).
Results
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,
NT, 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.
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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)
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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 characte- rized 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 through- out 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
Table 1. List of aquatic mollusk species in Tecolutla (Tc) and
Tuxpam (Tx) rivers (n-native, a-alien)
Aquatic mollusk species Status Tc Tx
Class Gastropoda Family Neritidae Neritina virginea Linnaeus, 1758
n x x Family Ellobiidae Melampus coffeus Linnaeus, 1758 n x Family
Ampullaridae Pomacea flagellata (Say, 1827) n x x Family Thiaridae
Melanoides tuberculatas (O.F.Müller, 1774) a x x
Tarebia granifera Lamarck, 1822 a x x Family Physidae Haitia
mexicana (Philippi, 1841) n x x Family Ancylidae Hebetancylus
excentricus (Morelet, 1851) n x
Family Planorbidae Biomphalaria sp. n x Micromenetus dilatatus
Gould, 1841 n x
Family Succineidae Succinea sp. Drapanaurd, 1801 n x Class Bivalvia
Family Ostreidae Ostrea palmula Carpenter, 1857 n x Family
Mytilidae Brachidontes exustus (Linnaeus, 1758) n x x
Family Corbiculidae Corbicula fluminea (O.F. Müller, 1774) a x
x
Total 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).
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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)
Study sites
Ta re
bi a
gr an
ife ra
C or
bi cu
O st
re a
pa lm
ul a
Tc1 X X X X Tc2 X X X X X Tc3 X X X Tc4 X X X Tc5 X X X Tc6 X X Tc7
X X Tc8 X X Tc9 X X Tx1 X X X Tx2 X X X Tx3 X X X X Tx4 X X Tx5 X X
X X Tx6 X X X X X Tx7 X X X Tx8 X Tx9 X X X Tx10 Tx11 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. virgi-
nea, Haitia mexicana and Melanoides tubercu- lata had mean
densities ranging from 1 to 100 individuals/m2. Brachidontes
exustus, P. flage- llata, Succinea sp. and Biomphalaria sp. all had
mean densities ≤1 individual/m2 (Figure 4). In the Tuxpam River, T.
granifera and Brachi- dontes 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/m2 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
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
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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
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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
excentri- cus, 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 tempera- ture,
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,
Hebetancy- lus excentricus, Haitia mexicana, P. flagellata
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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
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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.
E . López -López e t a l .
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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
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),
I nvas ive mo l lu sks i n r i ve r s o f t he Gu l f o f Mex
ico
447
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; Paunovi 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 (Paunovi 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
E . López -López e t a l .
448
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 re- colonization
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 (IPN- Mexico). Authors thank the reviewers for their
valuable comments to the manuscript and consequent suggestions that
improve this paper.
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450
Annex 1 Geographic coordinates of study sites in Tuxpan and
Tecolutla rivers
Geographic coordinates Study Site Location name
Latitude, N Longitude, W
Altitude, masl.
Tuxpam River Tx1 La Reforma 20°51.172' 97°53.029' 101 Tx 2 Úrsulo
Galván 20°53.718' 97°47.268' 93 Tx 3 Rancho el Cieruelo 20°57.349'
97°46.472' 44 Tx 4 San Antonio 20°55.447' 97°42.795' 38 Tx 5
Chapopote Nuñez 20°55.601' 97°36.469' 23 Tx 6 Buena Vista
20°55.727' 97°40.797' 20 Tx 7 Tampiquillo 20°57.228' 97°31.699' 19
Tx 8 El Higueral 20°55.556' 97°29.629' 9 Tx 9 Quinta Las Puertas
20°54.963' 97°25.748' 5 Tx 10 Puente Tuxpan 20°56.842' 97°24.054' 3
Tx 11 Boca de la Laguna de Tampamachoco 20°58.007' 97°19.572'
0
Tecolutla River
Tc1 Entabladero 20°16.065' 97°33.475' 87 Tc 2 Arenal 20°15.907'
97°30.647' 70 Tc 3 El Chacal 20°13.223' 97°27.828' 71 Tc 4 Espinal
20°14.503' 97°23.893' 43 Tc 5 Paso de Valencia 20°16.170'
97°19.676' 11 Tc 6 Puente Remolino 20°23.817'' 97°14.169' 8 Tc 7
Ignacio Muñoz Zapotal 20°27.347' 97°11.791' 6 Tc 8 Puente Chalana
20°26.583' 97°07.479' 3 Tc 9 Tecolutla 20°28.492' 96°00.256'
0
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 ag=coarse sand Be= Brachidontes
exustus Alt= altitude am= medium sand Bsp= Biomphalaria sp. BOD=
Biochemical oxygen demand gu= pebbles Cf= Corbicula fluminea Cl=
chloride gr=gravel He= Hebetancylus excentricus Color= color ag=
very coarse sand Hm= Haitia mexicana Ctot= total coliforms amf=
very fine sand Mc= Melampus coffeus DO= dissolved oxygen lg= gross
silt Md= Micromenetus dilatatus Dur= hardness lmf= very fine silt
Mt= Melanoides tuberculatas NH3= ammonia lm= medium silt NV =
Neritina virginia NO2= nitrites lf= fine silt Pc= Pomacea
flagellata NO3= nitrates Ssp= Succinea sp. Ntot= total nitrogen Tg=
Tarebia granifera 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
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/GrayImageDict << /QFactor 0.15 /HSamples [1 1 1 1] /VSamples
[1 1 1 1] >> /JPEG2000GrayACSImageDict << /TileWidth
256 /TileHeight 256 /Quality 30 >> /JPEG2000GrayImageDict
<< /TileWidth 256 /TileHeight 256 /Quality 30 >>
/AntiAliasMonoImages false /CropMonoImages true
/MonoImageMinResolution 1200 /MonoImageMinResolutionPolicy /OK
/DownsampleMonoImages true /MonoImageDownsampleType /Bicubic
/MonoImageResolution 1200 /MonoImageDepth -1
/MonoImageDownsampleThreshold 1.50000 /EncodeMonoImages true
/MonoImageFilter /CCITTFaxEncode /MonoImageDict << /K -1
>> /AllowPSXObjects false /CheckCompliance [ /None ]
/PDFX1aCheck false /PDFX3Check false /PDFXCompliantPDFOnly false
/PDFXNoTrimBoxError true /PDFXTrimBoxToMediaBoxOffset [ 0.00000
0.00000 0.00000 0.00000 ] /PDFXSetBleedBoxToMediaBox true
/PDFXBleedBoxToTrimBoxOffset [ 0.00000 0.00000 0.00000 0.00000 ]
/PDFXOutputIntentProfile () /PDFXOutputConditionIdentifier ()
/PDFXOutputCondition () /PDFXRegistryName () /PDFXTrapped /False
/Description << /CHS
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/CHT
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/DAN
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/DEU
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/ESP
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/FRA
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/ITA
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/JPN
<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>
/KOR
<FEFFc7740020c124c815c7440020c0acc6a9d558c5ec0020b370c2a4d06cd0d10020d504b9b0d1300020bc0f0020ad50c815ae30c5d0c11c0020ace0d488c9c8b85c0020c778c1c4d560002000410064006f0062006500200050004400460020bb38c11cb97c0020c791c131d569b2c8b2e4002e0020c774b807ac8c0020c791c131b41c00200050004400460020bb38c11cb2940020004100630072006f0062006100740020bc0f002000410064006f00620065002000520065006100640065007200200035002e00300020c774c0c1c5d0c11c0020c5f40020c2180020c788c2b5b2c8b2e4002e>
/NLD (Gebruik deze instellingen om Adobe PDF-documenten te maken
voor kwaliteitsafdrukken op desktopprinters en proofers. De
gemaakte PDF-documenten kunnen worden geopend met Acrobat en Adobe
Reader 5.0 en hoger.) /NOR
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/PTB
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/SUO
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/SVE
<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>
/ENU (Use these settings to create Adobe PDF documents for quality
printing on desktop printers and proofers. Created PDF documents
can be opened with Acrobat and Adobe Reader 5.0 and later.)
>> /Namespace [ (Adobe) (Common) (1.0) ] /OtherNamespaces [
<< /AsReaderSpreads false /CropImagesToFrames true
/ErrorControl /WarnAndContinue /FlattenerIgnoreSpreadOverrides
false /IncludeGuidesGrids false /IncludeNonPrinting false
/IncludeSlug false /Namespace [ (Adobe) (InDesign) (4.0) ]
/OmitPlacedBitmaps false /OmitPlacedEPS false /OmitPlacedPDF false
/SimulateOverprint /Legacy >> << /AddBleedMarks false
/AddColorBars false /AddCropMarks false /AddPageInfo false
/AddRegMarks false /ConvertColors /NoConversion
/DestinationProfileName () /DestinationProfileSelector /NA
/Downsample16BitImages true /FlattenerPreset <<
/PresetSelector /MediumResolution >> /FormElements false
/GenerateStructure true /IncludeBookmarks false /IncludeHyperlinks
false /IncludeInteractive false /IncludeLayers false
/IncludeProfiles true /MultimediaHandling /UseObjectSettings
/Namespace [ (Adobe) (CreativeSuite) (2.0) ]
/PDFXOutputIntentProfileSelector /NA /PreserveEditing true
/UntaggedCMYKHandling /LeaveUntagged /UntaggedRGBHandling
/LeaveUntagged /UseDocumentBleed false >> ] >>
setdistillerparams << /HWResolution [2400 2400] /PageSize
[612.000 792.000] >> setpagedevice