Invasive Mollusks Tarebia Granifera Lamarck, 1822 and Corbicula Fluminea Müller, 1774 in the Tuxpam and Tecolutla Rivers, Mexic

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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 Other human activities including aquaculture, recreation, transport, and trade globalization The Mexican rivers Tecolutla and Tuxpam drain intentionally or accidentally also contribute to into the Gulf of Mexico within the Meso- the spread of invasive aquatic species (Cohen american biodiversity hotspot (Myers et al. and Carlton 1998; Carlton and Geller 1993) that 2000). Throughout much of the Mexican Gulf can use such available spaces. Invasive species coast region human activities such as crude oil are considered the second major cause of bio- extraction, intensive agriculture, water extraction diversity loss in the world (Vitousek et al. 1996; and inputs of untreated wastewater have Leung et al. 2002) and their spread is one of the degraded various aquatic ecosystems (Ortíz- major problems in ecosystem conservation (Ruiz Lozano et al. 2005). Lake (2000), states that et al. 2000). Adverse effects of invasive species several environmental disturbances have a may take different forms: once they have negative impact on native species, through achieved a wide distribution, these species eradication or removal of sensitive species, and produce global homogenization of the patterns of can create spaces available for colonization. distribution, altering the once distinctive

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regional biota, and they may affect aquatic the distribution of species catalogued as invasive ecosystems through competitive exclusion of by CONABIO (2008). It is therefore essential for indigenous biota (Rahel 2000; Sousa et al. 2008). studies to focus on the impact of invasive species Some invasive species displace native species on the native biota and invaded habitats. This through direct competition, predation, intro- paper contributes to the understanding of duction of diseases, changes in biological and patterns of distribution of native and introduced geochemical cycles, and alteration of the trophic mollusk species in the Tuxpam and Tecolutla web, thus causing adverse effects in the invaded rivers, in the Mexican subtropics. The different habitats (Davis et al. 2000; Mack and Lonsdale forms taken by the invasion of two alien species 2001; Sax et al. 2002). in each of these rivers are explained and the risks In Mexico, the National System on Invasive these species pose are evaluated. Species established by the National Commission for the Understanding and Use of Biodiversity (CONABIO 2008) has preliminarily identified at Study area least 1000 invasive species of plants, mollusks, crustaceans, insects, fishes, amphibians, reptiles, Tuxpam and Tecolutla rivers cross the Gulf of birds and mammals. These include 13 species of Mexico coastal plain in the northern part of the invading mollusks: 11 bivalves (four freshwater) state of Veracruz (Figure 1). Both are perennial and two gastropods (one freshwater). CONABIO rivers with high discharges arising in the Eastern (2008) states that these species affect the natural Sierra Madre (more specifically the Sierra Norte wealth of Mexico, deteriorate environmental de Puebla) and flowing through a region of hot conditions in ecosystems and may have negative humid and sub-humid climate with abundant consequences on human health, production and rainfall throughout the year, particularly in the economy and recognizes the urgent need for summer. Discharges of both rivers are affected additional knowledge of the distribution of these by the impact of northern winds and hurricanes. species and their impact on native biota, and the The Tecolutla drainage includes the major need to identify high-risk biodiversity areas. tributaries Necaxa, Tenango, Laxaxalpan, Zem- Mexico has been ranked as one of the five poala, Apulco and Chichicatzapa rivers within its megadiversity countries in the world (Bezaury et total drainage area of 7,903 km2 to discharge a al. 2000), however, knowledge of the diversity of mean of 6,885 million m3, into the Gulf of certain groups within its territory is limited Mexico at Barra de Tecolutla (CONAGUA because large areas remain unstudied, especially 2007). The mean air annual temperature is 21- in the case of freshwater mollusks (Naranjo 26°C, total annual rainfall ranges from 1,200 to 2003). Based on worldwide diversity estimates, over 4,000 mm, and the rate of evaporation is Strong et al. (2008) recognize Mollusca with as 1,064-1,420 mm (Sanchez and De la Lanza many as 80,000-100,000 described species, as an 1996). The vegetation cover is semi-deciduous extraordinarily diverse phylum, second in tropical forest, mangrove, halophytic vegetation diversity only to arthropods. In Mexico, 16 and palm grove (Arriaga et al. 2002). Tecolutla families of freshwater mollusks have been River is listed by CONABIO (Arriaga et al. recorded, representing five orders, four 2002) as a priority hydrologic region since it subclasses (Naranjo 2003) and 211 species flows through an area of high biodiversity, and is (Contreras-Arquieta 2000). Furthermore, in a catalogued as threatened because it supports study of the continental gastropods of Mexico diverse land uses (agriculture, livestock, fishing and Central America, Thompson (2008) found and tourism). 168 aquatic operculate and 84 aquatic pulmonate Tuxpam River watershed covers a surface area species and emphasized that the mollusk fauna of of 5,899 km2 and has a mean annual flow of Mexico is poorly studied. Thus, the number of 2,580 million m3 (CONAGUA 2007). Its princi- continental mollusk species may exceed current pal headwater known as Río Pantepec is joined records, particularly since two zoogeographic by several tributaries before reaching the coastal regions, Nearctic and Neotropical, each with its plain named Tuxpam to discharge into the Gulf own characteristic fauna, converge in Mexican of Mexico at Barra de Tuxpam. Human activities territory sharing a broad transition zone in this basin include livestock, agriculture, (Morrone and Márquez 2001). To the paucity of fishing and industry. There is a power plant in knowledge on the native freshwater mollusks of Barra de Tuxpan, and a shipyard and the seaport Mexico must be added the lack of information on 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

within 1-m2 quadrats, sieving of sediments, 1 m2- Material and Methods base Surber net, and collection among roots, stems and foliage in areas of the banks with A total of 11 sites in the Tuxpam River (Tx) and aquatic vegetation. Specimens were fixed in 70% nine in the Tecolutla River (Tc) were surveyed ethanol. (Figure 1, Annex 1). Collection of aquatic Environmental parameters were measured in mollusks was made during three different periods situ at all study sites using a Quanta multi- of the year: the wet season (August 2007 in Tc, parametric sonde: water temperature (°C), September 2007 in Tx), the northern winds and turbidity (NTU), salinity (PSU) dissolved hurricane season (December 2007 in Tc, January oxygen (mg/L) and pH. A General Oceanic flow 2008 in Tx) and the dry season (March 2008 in meter was used to record current velocity Tc, April 2008 in Tx). Surveys covered the main (m/sec) in transects across the sampled area, water-courses of the basins including their upper, while altitude (masl) and geographic coordinates middle and lower reaches. Different collection were determined with a Sport Trak Magellan methods were used depending on stream bed GPS. characteristics and presence/absence of aquatic Two 500-mL samples of water from each site vegetation (Wetzel and Likens 2000): collection were transported in acid washed glass containers

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at 4°C to the laboratory in order to evaluate conditions in each river, using a correlation water quality parameters. Two sediment samples matrix of the log (x+1) transformed values of in from each site were collected in 1000-mL flasks situ recorded factors, water quality, sediment for subsequent sediment and organic matter analysis and organic matter, and a second matrix analyses and for specimen collection. with the relative abundance of each mollusk Water samples were processed with a HACH species, transforming values to square roots. DRL2500 spectrophotometer to determine total Statistical analyses were performed with XL- nitrogen (NT mg/L), nitrite (NO2 mg/L), nitrate STAT v. 2008 software (XL-STAT 2008). (NO3 mg/L), ammonia (NH3 mg/L), sulfate (SO4 mg/L), orthophosphate (PO4 mg/L), total phosphorus (PT mg/L), color (Pt-Co units), Results hardness (CaCO3 mg/L), total suspended solids (TSS mg/L) and total dissolved solids (TDS Environmental characterization of rivers g/L). APHA (1985) procedures were used to Tecolutla River measure alkalinity (CaCO3 mg/L), chloride (Cl mg/L), biochemical oxygen demand (BOD5) and PCA revealed an environmental gradient with total and fecal coliforms (MPN/100 mL). spatial and seasonal variations. The ordination Sediment samples were dried at 60°C for 24 h biplot (Figure 2) shows the first two axes which and processed for analysis according to EPA together accounted for 51.43% of the total (1986) procedures. The mesh size (mm) of sieves variance (PC1: 34.21% and PC2: 17.22%). Three was: 4.76, 3.36, 2.38, 2, 1.68, 1.41, 0.841, 0.5, clusters of sites corresponding to each of the 0.42, 0.297, 0.25, 0.21, 0.177, 0.149 and 0.106. study seasons are apparent. In August (wet The variable φ (-Ln2 of the diameter of particle) season) there are high levels of total coliforms, was plotted against the cumulative weight of nutrients (nitrate, nitrite, orthophosphate, PT), materials retained in each sieve in order to obtain suspended solids and turbidity. No marked the mean particle size and percentages of each spatial variations occurred in this month, but at soil texture according to the Wentworth scale. sites Tc9 and Tc8 the highest content of Organic matter was quantified using the Walkey coliforms and nutrients was recorded, while sites and Black method (NOM-021-RECNAT 2000). Tc1 to Tc6, located at higher altitudes above sea Separate sediment samples for specimen level, showed higher levels of orthophosphate, collection were sieved and examined with a PT and turbidity. In December (the cold, northern Zeiss stereoscopic microscope. The specimens winds season), there was a wider scatter of sites obtained were separated and fixed in 70% expressed as spatial variation in the biplot ethanol. (Figure 2), as a result of the higher variation of Importance value index (IVI) was determined measured parameters. Tc8 and Tc9, influenced according to Krebs (1989) for the whole river, by sea water, were highest in salinity, total taking into account the frequency of occurrence dissolved solids, chloride and sulfate. Tc1 to (proportion of times that a species occurs in all Tc7, on the other hand, were characterized by the samples taken) and relative abundances higher flow velocity, pH, NT, color, and organic (proportion of specimens for each species in the matter content as well as larger particle size. In total specimens collected) of all mollusk species March (dry season), the highest levels of for each river: IVI= %FO + relative Ab, where: hardness, alkalinity, BOD5, ammonia and %FO = Percent frequency of occurrence and dissolved oxygen were recorded. Spatial relative Ab = Relative abundance. variations occurred in this season. Tc9 was found Zones and environmental gradients along each to be the most different site due to high salinity, river were visualized and characterized by total dissolved solids, sulfate and chloride, while principal component analysis (PCA) using a at site Tc8, the highest content of ammonia was correlation matrix of the log transformed (x+1) recorded. PCA differentiated the marine values of physicochemical factors, water quality influence (estuarine zone Tc8 and Tc9 in parameters, organic matter and mean sediment December and March, Tc9 in August) from the particle size at each of the sites during the three freshwater zone (Tc1 to Tc7), and revealed the study seasons. Canonical correspondence seasonal effect of torrential rains when the analysis (CCA) was used to examine the salinity was lower and almost all the river correlation of mollusk species with habitat 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 Table 1. List of aquatic mollusk species in Tecolutla (Tc) The first two PCA components accounted for and Tuxpam (Tx) rivers (n-native, a-alien) 44.27% of the total variance (PC1: 27.43% and PC2: 16.84%). The biplot of these components Aquatic mollusk species Status Tc Tx (Figure 3) show the position of sites arrayed as Class Gastropoda environmental gradients. Tx8 to Tx11 in January Family Neritidae and April and Tx11 in September were characte- Neritina virginea Linnaeus, 1758 n x x rized by the highest levels of salinity, chloride, Family Ellobiidae sulfate and total dissolved solids, making evident Melampus coffeus Linnaeus, 1758 n x the reach with marine influence. In January (the cold, northern winds season), the upper reaches Family Ampullaridae (Tx1 to Tx7) showed the highest flow velocity, Pomacea flagellata (Say, 1827) n x x alkalinity, dissolved oxygen and total coliforms Family Thiaridae Melanoides tuberculatas values. In April (dry season), Tx1 to Tx6 were a x x high in total coliforms and organic matter (O.F.Müller, 1774) Tarebia granifera Lamarck, 1822 a x x content, and Tx7 in BOD5, hardness, color, Family Physidae turbidity, NT and PT. In September (wet season), environmental conditions were uniform through- Haitia mexicana (Philippi, 1841) n x x out the river. This season was characterized by Family Ancylidae Hebetancylus excentricus (Morelet, peak of water temperatures and high nutrient n x (nitrite, nitrate, orthophosphate) and organic 1851) matter content. Only one site (Tx11) differed Family Planorbidae from the rest of the studied localities due to its Biomphalaria sp. n x Micromenetus dilatatus Gould, marine influence (chloride, salinity, total n x dissolved solids), as well as the high levels of 1841 ammonia and NT. According to the results of Family Succineidae PCA (Figure 3), the estuarine (Tx8 to Tx11) and Succinea sp. Drapanaurd, 1801 n x freshwater (Tx1 to Tx7) zones were Class Bivalvia differentiated, as well as the seasonal dynamic of Family Ostreidae the system. Ostrea palmula Carpenter, 1857 n x Family Mytilidae Mollusk species and patterns of distribution Brachidontes exustus (Linnaeus, n x x 1758) Nine mollusk species were collected in the Family Corbiculidae Tecolutla and 11 in the Tuxpam basins (Table 1). Corbicula fluminea (O.F. Müller, a x x Three alien species occurred in both rivers: two 1774) gastropods (Tarebia granifera and Melanoides Total 9 11 tuberculata) and one bivalve (Corbicula fluminea). The species collected showed marked differences in their pattern of distribution along reaches at Tc2. In the Tuxpam River T. granifera the rivers. was the most widely distributed species in the Distribution of species in Tecolutla and freshwater zone, Tx1-6. C. fluminea was found Tuxpam rivers are shown in Table 2. In at Tx2, Tx6 and Tx7. M. tuberculata occurred at Tecolutla River, T. granifera and C. fluminea Tx1-4 and Tx6. H. mexicana was present in the were widely distributed in the freshwater zone, upper and middle reaches, Tx1-3, Tx5 and Tx6. from Tc1-8. M. tuberculata was found only in N. virginea was found in the lower reaches only the upper reaches from Tc1-3. Haitia mexicana (Tx7-9). B. exustus occurred only at Tx9. is present at Tc4 and Tc5. Brachidontes exustus Species with very limited distribution included and Neritina virginea are restricted to the lower P. flagellata (Tx3 only), Hebetancylus reaches near the river mouth (Tc8). Species with excentricus (Tx5 and Tx6), and Micromenetus a more limited distribution were Pomacea dilatatus (Tx5 and Tx7). Melampus coffeus is flagellata, in the upper reaches at Tc1, and known only from Tx9 and Ostrea palmula only Succinea sp. and Biomphalaria sp. in the upper 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 Tarebia granifera Corbicula fluminea Melanoides tuberculata Haitia mexicana Pomacea flagellata sp. Biomphalaria Succinea sp. Neritina virginea Brachidontes exustus Melampus coffeus Hebetancylus excentricus Micromenetus dilatatus Ostrea palmula

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. 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 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 Figure 4. Mean density of mollusk species in Tecolutla and densities, with ≤ 1 individual/m2 (Figure 4). Tuxpam rivers. The bar represents SD Very marked spatial and seasonal variations occurred in mean densities of mollusk species. In shift in the species with the highest population the Tecolutla River, the lowest densities densities in the upper reaches (Tc1 to Tc3): occurred in December and the highest in March C. fluminea had the maximum values in August (Figure 5a). In the freshwater zone, Tc5 and Tc7 and March and Melanoides tuberculata in had the highest densities in all three study December (Figure 5b). In the middle reaches, in seasons. Seasonal density changes produced a 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 Relation of environmental parameters, densities in all three seasons (Figure 5b). substratum characteristics and mollusk species In the Tuxpam River, the lowest densities occurred in January (Figure 6a) while peak The first two components in the CCA of the values were attained in April. In the freshwater Tecolutla River account for 81.30% of the zone, Tx3 to Tx6 showed the highest densities. explained variance (Axis 1: 64.93% and Axis 2: In spite of seasonal variations in population 16.37%). The biplots show the relations of densities, there was no change in the higher mollusk species and sites, as well as water ratios at which T. granifera was present in the quality conditions and type of substratum. Three freshwater zone and the species N. virginea and groups of species can be seen in the biplot in B. exustus in the estuarine zone (Figure 6b). Figure 8a. The smallest one is formed by Importance value indicates that T. granifera is N. virginea and B. exustus, which reached their the dominant species in both rivers, with index highest densities at Tc9 in December and March. values of 128 and 96 in the Tecolutla and Similarly, Figure 8b shows these species are Tuxpam rivers, respectively (Figures 7a and 7b). closely correlated with high salinity, total In the Tecolutla River, T. granifera, C. fluminea dissolved solids, chloride, sulfate and hardness. and M. tuberculata (all three non-native species), In the upper left quadrant are T. granifera, account for a cumulative index value of 179 out Haitia mexicana and C. fluminea, which attained of a possible 200. Importance values below 7 maximum densities in Tc4, Tc5, Tc6 to Tc7 in were obtained for all other mollusk in this river March and in Tc3 and Tc7 in August. In both (Figure 7a). In the Tuxpam River, T. granifera, seasons, these sites had the highest levels of two brackish species (N. virginea, B. exustus) coliforms, nitrite, nitrate, ammonia, BOD5, color, and two freshwater species (C. fluminea, Haitia alkalinity, current velocity and water tempera- mexicana) have index values ranging from 10 to ture, with fine and very fine sandy substrata. On 26. Species with IVI< 10 include Micromenetus the right side of the biplot are P. flagellata, dilatatus, P. flagellata, Hebetancylus excentri- which is closely correlated with Tc1 in March, a cus, Melanoides tuberculata and Melampus site in the upper reaches with a substratum of coffeus (Figure 7b). 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- Figure 7. Importance value index of mollusks a) Tecolutla lus excentricus, Haitia mexicana, P. flagellata River and b) Tuxpam River

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and Melanoides tuberculata. These species are such as pebbles, gravel and coarse to fine sand distributed in the freshwater zone (Tx1-6) with (Figures 9a and 9b). CCA identified two groups high levels of nitrite, nitrate, orthophosphate, of mollusks with entirely different distributions alkalinity, pH, turbidity, water temperature and as well as the relation of each group with coliforms, and also at higher altitudes where the contrasting environmental conditions and substratum is predominantly coarser materials 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

(Ortíz-Lozano et al. 2005), which contribute to the inputs of diverse compounds originating in Discussion wastewater discharges, leaching materials and basin runoff. Despite the nutrient and organic Water quality characteristics indicate that the matter enrichment found by this study, the water Tuxpam and Tecolutla rivers receive inputs of of these rivers has been rated good and excellent organic matter, nutrients (orthophosphate, by the CONAGUA (2007) monitoring network. nitrogenous compounds) and coliform bacteria. This agency, however, uses only three Both rivers are located in a region with several parameters (BOD5, Chemical oxygen demand environmental disturbances by human activities and total suspended solids) to rate water quality.

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Our results, on the other hand, indicate both Tx11) were both absent. The only areas not rivers sustain nutrient enrichment, although they colonized by these alien species were the are less degraded than the Coatzacoalcos and estuarine zones of the rivers, where N. virginea Pánuco rivers which are also located in the Gulf and B. exustus were dominant. In both freshwater of Mexico coast area (CONAGUA 2007). courses these alien species reached higher The Tuxpam and Tecolutla rivers show densities than others. Melanoides tuberculata, important differences in the estuarine zone due another non-native species, had a limited to their morphology, freshwater discharges and distribution in both rivers as well as lower seasonal variations. Mean annual flow is 2,580 densities than others. million m3 in the former and 6,885 million m3 in Contreras-Arquieta (2000), Naranjo (2003) the latter (CONAGUA 2007). As a result of and Thompson (2008) state that knowledge of these differences in stream flow, the estuarine aquatic mollusks is in an initial stage in Mexico. zone is larger in the Tuxpam River than in the In the Tuxpam and Tecolutla rivers there are no Tecolutla River. In our study PCA allowed historical records of the native aquatic mollusks. identification of environmental gradients along The number of mollusk species found in our each river that are associated with changes in study in both rivers is low, compared to numbers altitude, flow velocity, dissolved solids, organic in more extensively studied areas of Mexico, matter, nutrients and salinity, that differentiate such as Cuatro Ciénegas, Coahuila with 13 two zones: freshwater and estuarine. The rivers species; (Contreras-Arquieta 1998) and El Edén, undergo seasonal variations: during the dry Quintana Roo with 11 species (Cózatl-Manzano season, peak levels of alkalinity and BOD5 and Naranjo-García 2007). Several authors occurred and sea front influence produced a (Davis et al. 2000; Mack and Lonsdale 2001; Sax marked increase in salinity in the estuarine zone. et al. 2002; Sousa et al. 2008), mention that During the wet and the northerly wind seasons, introduced species are able to displace native and favored by the effect of hurricanes, both species through different mechanisms, including rivers showed a tendency to environmental competitive exclusion, introduction of disease homogeneity. Higher levels of nutrients (nitrate, and even habitat change. In the case of the nitrite, orthophosphate, PT) were present and the Tuxpam and Tecolutla rivers the absence of estuarine zone decreased in extent. Turbidity historical malacological fauna records prevents rose while salinity fell markedly. Studies comparison of the native mollusk assemblages showing the effect of seasonal rainfall and before and after the introduction of alien species. drought in watercourses in intertropical areas are The gastropod T. granifera is native to India, scarce. Brodie and Mitchell (2005) found higher Southeast Asia, the Philippines, Japan and nutrient loads during rain episodes and in Hawaii (Abbot 1952). Its introduction to the correlation with land use for agriculture in United States has been documented by Karatayev tropical river basins in Australia. Agriculture is a et al. (2007), who point out that the aquarium major land use in the Tuxpam and Tecolutla trade recognizes its presence in Texas since basins and, along with discharges from small 1935. In our study, the wide distribution of this human settlements near the river, may explain species in the Tuxpam and Tecolutla rivers nutrient inputs, particularly during the wet shows it has been able to establish and is very season. successful in freshwater zones of both rivers, Mathooko and Mavuti (1992) state that although the date of its introduction remains hurricanes and rainy seasons not only alter the unknown. In this respect, only Naranjo and volume of stream flow, they also bring sediment Olivera-Carrasco (2007) record its occurrence in loads and increase benthic organisms drift, Lake Catemaco, Veracruz, in the south of the which affect their population densities. In our Gulf of Mexico. Karatayev et al. (2007) report study in both rivers density values were depleted that this species tolerates a wide range of during the months of rainy, northern winds and temperatures (10 to 38°C). Water temperatures in hurricanes seasons as opposed to the dry season the Tuxpam and Tecolutla rivers (18°C min to when densities rose. 30°C max) are well within this range. Aquatic mollusks of the Tuxpam and Pointier and Jourdane (2000) stress the Tecolutla rivers showed strong dominance of two damage T. granifera has caused, including exotic species: T. granifera and C. fluminea. probable irreversible eradication of several Only at one of nine Tecolutla study sites (Tc9) native mollusks in Cuba (Pachychilus violaceus and in four of 11 Tuxpam study sites (Tx8 to and various species of the genus Biomphalaria),

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and endangerment of others (Hemisinus brevis association with diverse human activities. and H. cubanianus). The extremely low densities However, Souza et al. (2008), also mention this of other mollusks in the Tuxpam and Tecolutla species was adversely affected in sites with rivers are in agreement with statements by inputs of organic contaminants, while De la Hoz Karatayev et al. (2008) who suggested this is one (2008) found it was adversely affected by drops of the major impacts of T. granifera on the in the water level. Likewise, Sousa et al. (2008) indigenous mollusk fauna and is a preliminary report C. fluminea is successful in environments stage in the eradication of native species. without considerable water level fluctuations. In Pointier et al. (1998) found that the introduction our study, the Tuxpam and Tecolutla rivers were of thiarids to eradicate schistosomiasis in found to receive nutrient and organic matter Martinique island affected two species of inputs and to fluctuate in water level as a result Biomphalaria, but impacts were negligible on of floods and torrential flows due to rainfall of neritids. This is also in agreement with our northern winds and hurricane seasons, as findings in the Tuxpam and Tecolutla rivers opposed to the dry season when flow decreases. since N. virginea is the dominant species in the These factors are perhaps responsible for the low estuarine zone where T. granifera has not densities and limited distribution of C. fluminea become established. Pointier et al. (1998) state in these rivers, despite reports by other authors that the attributes of T. granifera favoring its of its invasive capability (Mouthon 2001; rapid spread include parthenogenesis, extremely Mouhton and Parghentanian 2004). Phelps high densities, ability to support faster currents (1994) states that C. fluminea may experience and dislodgement, and use of the entire stream population declines after reaching the lag period bed. In our study the CCA indicates that of invasion. This species may therefore be T. granifera in the Tuxpam and Tecolutla rivers undergoing a population decline since records of is able to establish in a wide variety of fine to its presence in the state of Veracruz date back to coarse substrata under nutrient-rich conditions 1992 (Naranjo and Olivera-Carrasco 2007). This, (particularly nitrogen) and with high BOD5. along with unfavorable abiotic factors, may These capabilities make T. granifera a successful explain the low densities and the relative limited invasive species and provide an explanation for distribution of this species in the Tuxpam and its pattern of distribution and extremely high Tecolutla rivers. Type of substratum is another densities in both rivers. factor that has been examined in regard to the The bivalve C. fluminea is native to Asia establishment of C. fluminea. It has been found (China, Korea and southeastern Russia) primarily in fine to coarse sandy substrata (McMahon 1999; Mouthon 2001) and colonizes (Cordeiro and MacWilliams 1999; Paunović et both fresh and brackish waters (salinity <10 al. 2007; Sousa et al. 2008), although De la Hoz PSU) (Sousa et al. 2009). It was possibly (2008) reports its occurrence in a muddy introduced for the first time in North America substratum. In the Tuxpam and Tecolutla rivers before 1924 in British Columbia, Canada it was present in substrata ranging from coarse (Naranjo and Olivera-Carrasco 2007) and in sand to fine-grained sediment. 1938 to the US, most probably by Chinese Negative impacts due to high densities of immigrants who use this species as food C. fluminea include biofouling (especially in (McMahon 1999). In Mexico it is known from power facilities), occlusion of small diameter the northern part of the country on both the Gulf pipelines, irrigation canals and domestic water and Pacific slopes. In the south its first record supply systems. It is also able to alter the dates back to 1992 in Catemaco, Veracruz substratum and affect native species (Paunović et (Naranjo and Olivera-Carrasco 2007). In the al. 2007). There are no records of biofouling by Tecolutla and Tuxpam rivers, C. fluminea this species in our study area, but a potential risk showed different patterns of distribution and exists, particularly in the Tuxpam River in which abundance, ranking second and fourth in IVI, C. fluminea has colonized the estuarine zone respectively. It had a more limited distribution in where a seaport and a power plant are located. Tuxpam River than in Tecolutla River, and was It has been reported that when T. granifera is found in the estuarine zone in the Tecolutla (at introduced in places previously occupied by Tx7). Sousa et al. (2008) say the attributes of M. tuberculata, the former rapidly outnumbers C. fluminea favoring its role as an invasive the latter in terms of density (Pointier et al. species include rapid growth, early sexual 1998). Contreras-Arquieta et al. (1995) record maturity, short lifespan, high fecundity and its presence of M. tuberculata in both the Tuxpam

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and Tecolutla rivers, but did not report References T. granifera. Thus, it appears that in these rivers T. granifera is an alien species that may have Abbot RT (1952) A study of an intermediate snail host recently established in these rivers that are (Thiara granifera) of the oriental lung fluke (Paragonimus). Proceedings of the United States experiencing changes in species invasion National Museum 102: 71-116 processes that are resulting in T. granifera being APHA (American Public Health Asociation) (1985) Standard favored over the two other non-indigenous methods: for the examination of water and wastewater. species. In agreement with Pointier et al. (1998) APHA, AWWA, WPCF, Washington, DC Arriaga L, Aguilar V, Alcocer D (2002) Aguas continentales y it appears from our study that T. granifera diversidad biológica de México. Comisión Nacional para attains its higher population densities through el Conocimiento y Uso de la Biodiversidad. 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Conocimiento y Uso de la Biodiversidad. http://www.co Tarebia granifera has capabilities for re- nabio.gob.mx/invasoras (Accessed 13 February 2009) CONAGUA (2007) Estadísticas del agua en México. colonization after torrential rains and their Secretaría de Medio Ambiente y Recursos Naturales. populations respond quickly during the dry México DF. México 259 pp http://www.CONAGUA07/ season when nutrients favor the food availability, Noticias/EAM_2007.zip (Accessed 10 January 2009) and in such situations may be more successful Contreras-Arquieta A (1998) News records of the snail Melanoides tuberculata (Müller 1774) (Gastropoda: than C. fluminea and M. tuberculata. All three Thiaridae) in the Cuatro Cienegas Basin, and its alien species, however, constitute a serious threat distribution in the state of Coahuila, México. The to native aquatic mollusks, since they have Southwestern Naturalist 43(2): 243-286 become the dominant components of the Contreras-Arquieta A (2000) Bibliografía y lista taxonómica de las especies de moluscos dulceacuícolas en México. malacological community in both these rivers, Mexicoa 2(1):40-53 where native species have been localized to Contreras-Arquieta A, Guajardo-Martínez G, Contreras- narrow habitats and occur in relatively low Balderas S (1995) Thiara (Melanoides) tuberculata densities. (Müller 1774) (Gastropoda: Thiaridae), su probable impacto ecológico en México. Publicaciones Biológicas. FCB UANL, México 8(1):17-24 Cordeiro JR, MacWilliams S (1999) Ocurrence of the Asian Acknowledgements clam Corbicula fluminea (Müller, 1774) (Bivalvia: Sphaeriacea: Corbiculidae) in Colorado. Veliger 42 (3): 278-280 This research was financed by the Joint Fund of Cózatl-Manzano R, Naranjo-García E (2007) First records of the National Science and Technology Council freshwater molluscs from the ecological reserve El Edén, (CONACyT Mexico) and the Veracruz state Quintana Roo, Mexico. Revista Mexicana de Bio- government (Project 41750) as well as by the diversidad 78:303-310 Davis MA, Grime JP, Thompson K (2000) Fluctuating Research and Postgraduate Studies Secretariat resources in plant communities: a general theory of (SIP) of the National Polytechnic Institute (IPN- invasibility. Journal of Ecology 88: 528-534 Mexico). Authors thank the reviewers for their doi:10.1046/j.1365-2745.2000.00473.x valuable comments to the manuscript and De la Hoz AMV (2008) Primer registro en Colombia de Corbicula fluminea (Mollusca: Bivalvia: Corbiculidae), consequent suggestions that improve this paper. una especie invasora. Boletín de Investigaciones Marinas y Costeras 37(1): 197-202

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Karatayev, AY, Padilla DK, Minchin D, Boltovskoy D, Ortíz-Lozano L, Granados-Barba A, Solís-Weissa V, García- Burlakova LE (2007) Changes in global economies and Salgado MA (2005) Environmental evaluation and trade: the potential spread of exotic freshwater bivalves. development problems of the Mexican Coastal Zone. Biological Invasions 9:161-180 doi:10.1007/s10530- Ocean & Coastal Management 48: 161-176 doi:10.1016/ 006-9013-9 j.ocecoaman.2005.03.001 Karatayev AY, Burlakova LE, Karatayev YV, Padilla DK Paunović M, Csányi B, Knežević S, Simić V, Nenadić D, (2008) Introduction, distribution, spread, and impacts of Jakovčev-Todorović D, Stojanović B, Cakić P (2007) exotic freshwater gastropods in Texas. Hydrobiologia Distribution of Asian clams Corbicula fluminea (Müller, 619: 181-194 doi:10.1007/s10750-008-9639-y 1774) and C. fluminalis (Müller, 1774) in Serbia. Krebs CJ (1989) Ecological methodology. 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Annex 1 Geographic coordinates of study sites in Tuxpan and Tecolutla rivers

Study Geographic coordinates Altitude, Location name Site Latitude, N Longitude, W 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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