Distribution of Corbicula Fluminea

Biol Invasions (2015) 17:2087–2101 DOI 10.1007/s10530-015-0862-y

ORIGINAL PAPER

Distribution of Corbicula ﬂuminea (Mu¨ller, 1774) in the invaded range: a geographic approach with notes on species traits variability

Daniel Crespo • Marina Dolbeth • Sara Leston • Ronaldo Sousa • Miguel Aˆ ngelo Pardal

Received: 19 September 2014 / Accepted: 24 February 2015 / Published online: 1 March 2015 Ó Springer International Publishing Switzerland 2015

Abstract Corbicula fluminea is considered one of the globe. Latitude and summer temperature show a most important non-native invasive species (NIS) in relationship with growth and life span. Overall, the aquatic systems mainly due to its widespread distribu- information gathered in this review may be relevant to tion and ecological and economic impacts. This species forecast future distribution patterns of this NIS, and to is known to negatively affect native bivalves, also with anticipate the possible implementation of effective severe effects on biodiversity and ecosystem function- management measures. Moreover, it may constitute a ing. Throughout an exhaustive bibliographic survey and valuable tool in the prediction of population responses to with the aid of Geographic Information Systems tools, an increasingly changing environment. this study tracks the species dispersion from its native range, including the description of important physical Keywords Corbicula fluminea Á Invasive species Á and environmental barriers. Additional analyses were Vectors of dispersion Á Geographic gradients Á conducted to examine possible influences of latitudinal/ Invasion history Á Species traits temperature gradients on important traits (e.g. life span, maximum and mean body length, growth at the end of first year). Altitude and winter minimum temperature Introduction appear to be delaying the invasion worldwide, but it seems inevitable that the species will spread across the In the last decades, globalization has been dissolving natural biogeographic barriers and allowing the

D. Crespo (&) Á M. Dolbeth Á S. Leston Á M. Aˆ . Pardal R. Sousa CFE – Centre for Functional Ecology, Department of Life Interdisciplinary Centre of Marine and Environmental Sciences, University of Coimbra, Calc¸ada Martim de Research (CIIMAR/CIMAR), University of Porto, Rua Freitas, 3000-456 Coimbra, Portugal dos Bragas 289, 4050-123 Porto, Portugal e-mail: [email protected] R. Sousa M. Dolbeth CBMA – Centre of Molecular and Environmental Biology Department & Centre for Environmental and Biology, Department of Biology, University of Minho, Marine Studies (CESAM), University of Aveiro, Campus Campos de Gualtar, 4710-057 Braga, Portugal Universita´rio de Santiago, 3810-193 Aveiro, Portugal

S. Leston CEF – Center for Pharmaceutical Studies, Health Sciences Campus, Pharmacy Faculty, University of Coimbra, Azinhaga de Santa Comba, 3000-548 Coimbra, Portugal 123 2088 D. Crespo et al. transport (either inadvertently or not) of many species (USA) during the first half of the twentieth century, (Simberloff et al. 2013;Gutie´rrez et al. 2014). These entered the South American systems in the late 1960s/ transported species, usually defined as non-indigenous, beginning of the 1970s and reached Europe probably non-native or alien, could become invasive. By defini- during the 1980s (Araujo et al. 1993; Mouthon 2001; tion, a non-native invasive species (NIS) needs to Darrigran 2002;Moraisetal.2009). Human activities expand its geographical range into an area not previ- (e.g. ballast water transport, use as bait or as food ously occupied, marked by successive stages of arrival, resource, aquarium hobbyists releases, tourist curiosity) establishment and integration (Vermeij 1996). In intro- are considered the primary introducing vectors for this duced areas some of these NIS find niches with similar species (McMahon 1983;Vermeij1996;Ruizetal.1997; conditions to those available in the native range, but Rigby et al. 1999;Lavoieetal.1999; McMahon 2000; without their natural predators, parasites or competitors Bo´dis 2007;Sousaetal.2008a). Also, pediveligers or (Sakai et al. 2001; Torchin et al. 2003). Not surprisingly, juveniles can be dispersed by natural means, that include NIS have been causing disruptions in native communi- fluvial or tidal currents (Den Hartog et al. 1992;Rosa ties, and ultimately, a global biodiversity reduction due et al. 2012), or adhered with a byssal attachment to to, for example, predation, introduction of diseases and mobile animals such as birds and mammals (Prezant and parasites, competition and altered abiotic conditions Chalermwat 1984; McMahon 2000; Sousa et al. 2008a). (Ruiz et al. 1997; Dukes and Mooney 1999;Revenga As an opportunistic species, it is well adapted to colonize and Kura 2003; Sousa et al. 2008b; Butchart et al. 2010). lotic and lentic ecosystems, with a very plastic feeding The traits that define the invading potential of a behaviour that includes both filter- and deposit–feeding species have not yet been consistently tested, especially (McMahon 1983; Sousa et al. 2008a;Diasetal.2014). in animals. Anyway, high reproductive rate, single parent Populations of C. fluminea seem to be negatively or vegetative reproduction, eurytopy, polyphagy, early affected by the combination of hypoxia and high maturation and small body size have been considered temperatures. The species show a clear preference for important (Kolar and Lodge 2001). Usually, these species well oxygenated sandy substrates (Belanger et al. show r-strategies (opportunist behaviour), with several 1985). Mattice and Dye (1976) determined the lower generations per year, short periods between spawning and upper lethal temperatures as 2 and 34.8 °C, activity and spend a great effort in reproduction and respectively. In the USA, the populations further north recruitment (Den Hartog et al. 1992;Lavoieetal.1999). have been associated with the water outlets of steam However, the characteristics of NIS per se may be a electric power plants, which increase the temperature highly reductionist view to define the invading potential in adjacent areas and allow the survival during colder because the characteristics of the invaded habitat (Byers winters (McMahon 1983; Den Hartog et al. 1992). In 2002) and propagule pressure (Simberloff 2009), at least, addition, despite being usually described as a fresh- mayalsoplayafundamentalrole. water bivalve, it can tolerate salinities of 10-14 NIS are amongst the most serious threats that aquatic (McMahon 1983, 2000), allowing the species to systems are currently facing, and their impacts are not colonize the upstream areas of estuaries (Sousa et al. always easy to follow (Strayer 2010). One faunal group 2006; Franco et al. 2012; Modesto et al. 2013). responsible for high ecological and economic impacts in As for reproduction, it usually presents two major aquatic ecosystems comprises bivalves (Sousa et al. spawning periods per year (McMahon 1983; Ra- 2014). Within this group, Corbicula has become a threat jagopal et al. 2000; Sousa et al. 2008a). Corbicula during the last century due to its invasive potential fluminea is usually described as a simultaneous (Nguyen and De Pauw 2002; Elliott 2008;Sousaetal. hermaphrodite, which incubates fertilised eggs within 2008a, b; Pigneur et al. 2011). With its origins in Asia, its inner demibranchs and releases pediveligers with Australia and Africa, species belonging to this genus reduced mobility to the water column that rapidly have spread worldwide during the twentieth century settle into the sediments (McMahon 1983; Rajagopal (Araujo et al. 1993; Sousa et al. 2007, 2008a)with et al. 2000; Sousa et al. 2008a). This species is capable Corbicula fluminea (Mu¨ller 1774) being considered one of androgenetic self-fertilization, which may increase of the most important NIS in aquatic systems (Sousa et al. its invasive potential: a single individual in the proper 2008a;Moraisetal.2009; Ilarri and Sousa 2012). This environmental conditions has enough potential to start species first established in the United States of America a new population (Pigneur et al. 2011). 123 Distribution of Corbicula fluminea (Mu¨ller, 1774) in the invaded range 2089

Corbicula fluminea can affect hydrology, biogeo- theses and web sites devoted to the NIS C. fluminea. chemical cycling and biotic interactions via two general The present work focused on population traits such mechanisms: assimilatory-dissimilatory (uptake and as the number of reproductive periods, life cycle release of energy and materials) and physical ecosystem duration, first year growth, number of simultaneous engineering (physical environmental modification by cohorts, density, biomass, mean and maximum body organisms), with impacts ranging from individuals to length. Nevertheless, literature was very sparse with ecosystems (Sousa et al. 2008a, 2009). This species respect to some of those data and therefore it was not alters community features, especially evenness, as it possible to use all of those population traits. The creates large monoculture patches on the invaded traits with more extensive and useful data were life systems. Those changes often affect other natural span, maximum body length, mean body length and processes such as productivity, nutrient cycles and length at the end of the first year. Another metric that community stability, by using resources in a different was looked at was the year of invasion. For each way (Ilarri and Sousa 2012). Several impacts of the population, the geographic position was identified, species are reported in the literature: —C. fluminea is either using the precise coordinates, whenever they responsible for the creation of a different habitat matrix were reported, or searching by their toponym with for benthic fauna via bioturbation and shell production the Google EarthÒ search engine. In the case of wide (Ilarri et al. 2012); —it has high filtration rates (Sousa areas and/or unspecified geographic coordinates, the et al. 2008a); —it is a highly productive species, which central point of the system was chosen. The may cause disruption on food chains, either as food geographic data were loaded in the open-source source for higher trophic levels mainly when massive software Quantum GIS (QGIS) Desktop 2.2.0- die-offs occur (Sousa et al. 2008b, 2012) and as a con- Valmiera together with all population traits associ- sumer, by reducing phytoplankton availability for other ated with their respective coordinates. Data were species and; —it may be responsible for alterations in transformed to raster layer using the Data Interpo- biogeochemical cycles due to their pedal feeding, with lation tool. The method used was the Inverse consequential alterations in the abiotic characteristics of Distance Weight (IDW). The river basin shape files the top layer of the sediments and high rates of nitrogen were obtained in the Water Base project site (http:// excretion (Sousa et al. 2008a, and references therein). www.waterbase.org/home.html) (George and Leon Taking into account the ecological importance of 2007). The invaded basins were selected and for this species and its high invasive potential, the better visualization, a fixed distance (1 map units) objective of this work is to evaluate, through an buffer was created. These shapes were used to cut the exhaustive bibliographic survey, the effect of geo- interpolation surfaces. The grids for temperature and graphic gradients relating to environmental variables altitude were obtained in the WorldClim site (http:// on the most descriptive population traits, such as the www.worldclim.org/) (Hijmans et al. 2005), with a life span, maximum and mean body length and growth 2.5 arc-minutes resolution. at first year. Simultaneously, we look upon those Information on the population traits was plotted gradients in order to detect possible pathways of against temperature and latitude classes (boxplots). dispersion and areas of potential future introduction These data were tested with an ANOVA being each and establishment of the species. This information population trait the dependent variable and tem- may help us anticipate future distribution patterns of perature and latitude the explanatory variables. Prior this NIS and also to aid in the implementation of to the analyses, we checked for collinearity among management measures. Moreover, this information explanatory variables with variation inflations factors may be used in the prediction of population responses (VIF, Zuur et al. 2009). The assumptions of the linear to an increasingly changing environment. regression were verified with graphical validation tools (Zuur et al. 2009). For the non-parametric data, Kruskal–Wallis tests were used. Also, the sighting Materials and methods sites were grouped and characterized according to geographic and temperature classes and their relation For this review, a wide bibliographic survey was assessed. All analyses were performed with R soft- conducted on scientific publications, technical reports, ware (R Development Core team 2012). 123 2090 D. Crespo et al.

Results invaded, especially in low altitude regions (Fig. 2a) and above -10 °C winter air temperature (Fig. 2b). In the bibliographic survey we retrieved 1058 sites Central America shows a more recent invasion that with sightings, based in 96 studies with data about C. started around 1998 (Fig. 1). The number of sites for fluminea: 74 scientific papers, 8 conference proceed- Central America is low (Fig. 2). Nevertheless, is ings, 5 reports, 2 bulletins, 2 books, 2 book chapters possible to track an invasion pathway that crosses and 1 MSc thesis. Mexico and reaches some Caribbean islands, in The first occurrence of C. fluminea outside its particular Puerto Rico (Williams et al. 2001). native range was recorded in North America in 1924 at The first reference in South America is in Rio de la Vancouver Island, British Columbia (Fig. 1). That Plata estuary (Ituarte 1981) by the end of the 1960s occurrence refers to an empty shell found in a natural (Fig. 1). The number of invaded sites was lower than system. From the Vancouver Island, the species spread in North America (Figs. 2, 3). Still, invaded sites are across the USA, apparently from Northwest along the mostly at low altitude, although the species can also be coastal states, then crossing the southern states. The present at high altitude (Fig. 3a), and in considerably south-eastern states were reached during the 1950s. high temperature regions (around 30 °C, Fig. 3b). The The most recent invasions of water basins by C. progression from Argentina towards the Northeast of fluminea occurred in the twenty-first century, on the Brazil took nearly 40 years. North and Northeast USA. Besides the 1924 event in In Europe, the first records were described in the the Vancouver Island, the species only appeared again Tagus Estuary in Portugal and the Garrone Estuary in in Canada in 2006 (Simard et al. 2012). Nowadays a France in 1980 (Mouthon 1981), followed by the River high percentage of North and Northeast USA has been Rhine, near Rotterdam (Holland) in 1985 (Fig. 1). The

Fig. 1 Dates and main paths for Corbicula ﬂuminea in the invaded range 123 Distribution of Corbicula ﬂuminea (Mu¨ller, 1774) in the invaded range 2091

Fig. 2 North and Central America digital elevation model (a), and average air temperature for January (1950–2000) (b). The invaded sites found in the bibliography are represented by dots

most recent invasions in Europe were recorded in Africa recorded its ﬁrst invasion in Morocco in Ireland (Caffrey et al. 2011), in some central European 2008 (Fig. 1) (Clavero et al. 2012). systems (Schmidlin et al. 2012) and in an Italian lake The invaded sites exhibited some similar charac- on the Alps (Kamburska et al. 2013). Almost all rivers teristics in terms of geography and temperature and oligohaline estuarine areas in Portugal have been (Fig. 5). 88 % of invaded sites were below 500 m invaded by the species (Fig. 4). In remaining Euro- altitude (Fig. 5a) and more than 90 % were between pean countries, C. ﬂuminea distribution appears latitudes 30° and 55° (Fig. 5b). In fact, no records or sparser, with exception of France. Again, its distribu- only recent records were reported in high altitudes tion seems preferentially associated to low-altitude such as Rocky Mountains (USA, Fig. 2a), the Andes areas (Fig. 4a) and to regions with winter temperature (South America, Fig. 3a) or Alps and Pyrenees higher than -5 °C (Fig. 4b). (Europe, Fig. 4a), although the species appeared in

123 2092 D. Crespo et al.

record was found below -10 °C, and only occasional occurrences were registered around -5 °C (Figs. 2, 3 and 4a). For summer temperatures, almost 97 % of the sites fall in the 15–30 °C range (Fig. 5d). For annual average temperature, almost 90 % of the invaded sites were within 5–20 °C, and from this range 40 % were located in the 10–15 °C interval (Fig. 5e). Corbicula fluminea population traits were plotted against geographic and environmental gradients to identify trends in those relationships (Figs. 6, 7, 8 and 9). The data used included all available information related to the traits more frequently found in the bibliographic survey. No statistical differences were found between the classes of life span, growth at the 1st year and mean body mass (ANOVA Life span: F-statistic = 1.528, p = 0.2168; 1st year growth: F-statistic = 1.251, p [ 0.05; mean body length F-s- tatistic = 2.487, p value: 0.0793). Yet, some trends could be identified: longer life span and higher mean body mass were found in higher altitude regions (apparent positive relation), while the growth in the first year generally decreased with increasing altitude (Fig. 6). In addition, a negative relationship between latitude and growth at the end of the 1st year and mean body mass seemed to occur. Temperature (summer and winter) showed a positive effect on 1st year growth and mean body length (Figs. 8, 9). With regard to maximum body length alone, higher maximum body mass was associated with higher altitude (Kruskal–Wallis Chi squared— KW = 17.9156, p value \0.001), with higher temperatures (Summer temperature KW = 59.6941, p value \0.001; Winter temperature KW = 66.4444, p value \0.001) and lower latitude (KW = 52.8702, p value\0.001).

Discussion

Invasion history, paths and current record of C. ﬂuminea

The dispersion in North America could be described as Fig. 3 South America digital elevation model (a), and average air temperature for June (1950–2000) (b). The invaded sites an arch, avoiding the central states of the USA until found in the bibliography are represented by dots very recent years (Fig. 1). This may be related with the Rocky Mountains, crossing the continent from north to surrounding areas. More than 75 % of the sites were south, which acts as a barrier to the invasion of eastern characterized by winter air temperatures between -5 areas. Indeed, many examples confirm the Rocky to 10 °C (Fig. 5c). In fact, for all continents only one Mountains as a biogeographic barrier for fishes (e.g. 123 Distribution of Corbicula fluminea (Mu¨ller, 1774) in the invaded range 2093

Fig. 4 Europe and North Africa digital elevation model (a), and average air temperature for January (1950–2000) (b). The invaded sites found in the bibliography are represented by dots

Kruse et al. 1997; Adams et al. 2001; Rahel 2007; the invasion spread into new areas decreased with time Smith et al. 2010) and invertebrates (e.g. Finn et al. for North America, taking about 82 years to spread 2006). The natural dispersion of C. ﬂuminea seems to from the Northwest to the Northeast coast. Still, there be limited by high slopes, characterized by low order were some areas close to the oldest invasion sites with streams. In the north, the limit is also deﬁned by winter very recent introductions, probably related to human temperatures that fall below the lower lethal tem- activities: (a) the building of new channels for water peratures (2 °C, Mattice and Dye 1976). Apparently, diversion, or channel widening can create new

123 2094 D. Crespo et al.

(A) (B) 45 45 40 40 35 35

es 30 30 25 25 20 20

vaded sit 15 15

% invaded sites 10 %in 10 5 5 0 0 [0; 100[ [100; 500[ [500; 1000[ [1000; 2000[ [2000; 2500[ [0; 10[ [10; 20[ [20; 30[ [30; 40[ [40; 50[ [50; 60[ Altitude (m) Latitude (º) (C) (D) 45 45 40 40 35 35 30 30

sites 25 25 20 20 15 15

invaded

% % invaded sites 10 10 5 5 0 0 [-15; -10[ [-10; -5[ [-5; 0[ [0; 5[ [5; 10[ [10; 15[ [15; 20[ [20; 25[ [25; 30[ [0; 5[ [5; 10[ [10; 15[ [15; 20[ [20; 25[ [25; 30[ Winter average temp. (ºC) Annual average temp. (ºC) (E) 45 40 35 30 25 20 15

% invaded sites 10 5 0 [10; 15[ [15; 20[ [20; 25[ [25; 30[ [30; 35[ Summer average temp. (ºC)

Fig. 5 Percentage of invasion sightings for a altitude; b latitude; c winter average temperature; d summer average temperature; e annual average temperature (n = 1058) available niches for the species; (b) new industrial 2011). Similarly to North America, Central America facilities that use water as cooling medium, create mountain ranges seemed untouched by this NIS. preferable conditions for new introductions, and In South America, the origin of the introduction is therefore allowing for the species to appear in systems still uncertain, although genetic studies suggest that that, until that time, were protected against invasion; south American populations shared some genetic (c) the opening of water courses to recreational similarities with North American populations (Lee ﬁsheries or other recreational activities could also be et al. 2005). Therefore, hypotheses of a North responsible for the introduction of the species in American or Asian source are both viable. Apparently, previously uninvaded areas. the species has been kept away from the Amazonian The invasion in Central America probably resulted Basin until recently. The high diversity that charac- from a branch of the North American main invasive terizes tropical habitats may be responsible for higher path. Some Caribbean isles were also invaded, biological resistance (i.e. higher predation pressure, probably following the main land invasion. This more parasites and diseases) and higher competition insular invasion was quite recent (1998) and, like for resources, and therefore less susceptible to NIS similar island introductions, it was due to human establishment (Stachowicz and Byrnes 2006). Simul- activities since, as a freshwater species, C. ﬂuminea is taneously, many of the water bodies in the Amazonian unable to survive an oceanic crossing (Verbrugge et al. Basin are known to have anoxic waters (Scarpelli

123 Distribution of Corbicula ﬂuminea (Mu¨ller, 1774) in the invaded range 2095

7 50 N=27 N=190 6 40 5 4 30 3 20

Life span (years) 2 [0:100[ [100:500[ [0:100[ [100:500[ [500:1000[ Altitute (m) Max body length (mm) Altitute (m)

25 30 N=23 N=28 25 20 20 15 15 10 10

5 1st growth (mm) 5 [0:100[ [100:500[ [500:1000[ [0:100[ [100:500[ [500:1000[ Mean body length (mm) Altitute (m) Altitute (m)

Fig. 6 Boxplots of the variation of life span, maximum and 25th, 50th, and 75th percentiles; the maximum length of each mean body length and length at the 1st year of growth per whisker represents the 5th and 95th percentiles altitude. The middle line and extremities of the box are at the

7 50 N=27 N=190 6 40 5 4 30 3 20

Life span (years) 2 Max body length (mm) [10:20[ [20:30[ [30:40[ [40:50[ [50:60[ [10:20[ [20:30[ [30:40[ [40:50[ [50:60[ Latitude (º) Latitude (º)

25 30 N=23 25 N=28 20 20 15 15 10 10

5 1st growth (mm) 5 Mean body length (mm) [0:10[ [20:30[ [30:40[ [40:50[ [10:20[ [20:30[ [30:40[ [40:50[ [50:60[ Latitude (º) Latitude (º)

Fig. 7 Boxplots of the variation of life span, maximum and 25th, 50th, and 75th percentiles; the maximum length of each mean body length and length at the 1st year of growth per whisker represents the 5th and 95th percentiles latitude. The middle line and extremities of the box are at the

2005; Bracho-Nunez et al. 2012; Junk et al. 2012), also acted as a restrictive factor to the invasion, at least impairing the establishment of this species. in the southernmost areas of the continent, where the The species invasion did not occur in the higher average temperatures for June can be close to or below mountain range of the Andes, where the high altitude 0 °C. In addition, the oligotrophic conditions that probably acted as a barrier for invasion success. The characterize high mountain ranges act as an important winter temperatures, on average higher than those limiting factor for the survival of many freshwater recorded in the North American continent, might have bivalves (Dillon 2004).

123 2096 D. Crespo et al.

7 50 N=27 N=190 6 40 5 4 30 3 20

Life span (years) 2 [15:20[ [20:25[ [25:30[ [10:15[ [15:20[ [20:25[ [25:30[

Summer Temp. (ºC) Max body length (mm) Summer Temp. (ºC)

25 30 N=23 N=28 25 20 20 15 15 10 10 5 5 1st growth (mm) [15:20[ [20:25[ [25:30[ [15:20[ [20:25[ [25:30[ Mean body length (mm) Summer Temp. (ºC) Summer Temp. (ºC)

Fig. 8 Boxplots of the variation of life span, maximum and of the box are at the 25th, 50th, and 75th percentiles; the mean body length and length at the 1st year of growth per classes maximum length of each whisker represents the 5th and 95th of summer average temperature. The middle line and extremities percentiles

7 50 N=27 N=190 6 40 5 4 30 3 20

Life span (years) 2 * * [0:5[ [0:5[ Max body length (mm) [5:10[ [5:10[ [−5:0[ [−5:0[ [15:20[ [10:15[ [20:25[ [10:15[ [15:20[ [20:25[ [25:30[ [−10:−5[ Winter Temp. (ºC) [−15:−10[ Winter Temp. (ºC)

25 30 N=23 N=28 25 20 20 15 15 10 * 10 5 1st growth (mm) 5 Mean body length (mm) [0:5[ [0:5[ [5:10[ [5:10[ [−5:0[ [−5:0[ [10:15[ [20:25[ [25:30[ [10:15[ [15:20[ Winter Temp. (ºC) Winter Temp. (ºC)

Fig. 9 Boxplots of the variation of life span, maximum and of the box are at the 25th, 50th, and 75th percentiles; the mean body length and length at the 1st year of growth per classes maximum length of each whisker represents the 5th and 95th of winter average temperature. The middle line and extremities percentiles. *Classes with no occurrences

For Europe it was very hard to track a deﬁned maritime transportation (ballast water). Those intro- invasion path. The ﬁrst records of the species were ductions were responsible for the dispersal across almost simultaneous and scattered across different Europe towards the Mediterranean and Eastern part of geographic locations. This fact supports the theory that the continent. Britain and Ireland were recently the introduction of the species across large scale invaded, probably, from already established popula- distances is human mediated and connected with tions in central and northern Europe. The Pyrenees

123 Distribution of Corbicula fluminea (Mu¨ller, 1774) in the invaded range 2097 range might have acted as a physical barrier to the survival of the species in those locations was probably progression of C. fluminea, therefore, the central related to site-specificities: e.g. areas near industrial European populations could have origin on invasion and residential water discharges that allow Asian clam episodes different of the Iberian ones (Fig. 1). In populations to receive a constant input of warm water. general, the invasion success was somewhat limited in These artificial conditions, in which the water tem- the higher mountain ranges, low temperature regions perature never goes under the vital limits of the and oligotrophic conditions. species, allow the survival of C. fluminea in those For Africa, there are only recent records of the geographic locations. Interestingly, in the northern species in Morocco (Clavero et al. 2012). However, hemisphere C. fluminea invaded further higher the species invasion in other African areas is possible, latitudes probably due to human activities that in one but going unnoticed due to the lack of environmental hand increased their dispersion rates and on the other management and scientific awareness. hand enhanced the probabilities of establishment due The data records presented in this study reflected to the thermal pollution associated with larger human the first invasive reference found in the literature, and agglomerates. In the southern hemisphere we have a the dates might present a slight delay relative to the less dense human population and thermal pollution is real introduction dates. Nevertheless, Fig. 1 represents probably much less severe. Therefore, the thermal an accurate illustration of the main paths history of C. boundary is more effective in South America, only fluminea invasion. Even so, many uncertainties still allowing the survival of C. fluminea at higher atmo- exist about the global dispersion of this NIS and spheric temperature and lower absolute latitude. further biogeographic studies encompassing genetic According to this study, the preferable habitat for C. data may be highly informative. fluminea seems to be under 500 m of altitude, between The USA showed a large record of invasion when the latitudes of 30–508 and annual mean temperature compared with other countries. As the first country to between 5 and 20 °C, preferably 10–15 °C. Higher be invaded by C. fluminea outside its native range, the altitudes and the oligotrophic conditions associated awareness of the risk associated with the species has with the higher mountain slopes seem to limit the been raised very early on, as reflected, for example, on natural upstream dispersion of C. fluminea. A tem- the US Geological Survey web site (http://nas2.er. perature of 10–15 °C allows all vital biological usgs.gov/viewer/omap.aspx?SpeciesID=92), which activities of the species, including reproduction. In a displays a vast number of records of the species, with scenario of predicted global warming, this may different levels of accuracy. Some regions across the represent an increased challenge for management, globe may be less aware (e.g. South and Central because it widens an already extensive susceptible America, Eastern Europe or Africa), and therefore the range for invasion (McDowell et al. 2014). number of sightings might be underestimated. This In the present study, the distinct distribution could justify the difference on the number of sightings patterns across the invaded areas could be justified when comparing USA and the rest of the world. by three main reasons, gradually more relevant: (1) a In the worldwide invaded range, the southernmost differential biological resistance to invasion; (2) reference is Negro River at Chimpay (Patagonia— distinct amounts of human activities in the studied Argentina) (Cazzaniga and Pe´rez 1999), with the areas and; (3) an uneven research effort on the species. latitude of -39.2034° and longitude -66.159203°.In the North Hemisphere, the most northern reference is Geographic and environmental gradients the Shannon River at Carrick on Shannon (Ireland), versus population traits responses with the latitude of 53.9422° and longitude of -8.087545542° (Minchin 2014). The average winter Despite the trends of lower 1st year growth and larger air temperature in Chimpay falls to 7.3 °C whereas at maximum and mean body mass with increasing Carrick on Shannon it drops to 4.3 °C. Nevertheless, latitude, winter temperatures do not seem to have there were other latitudes with more extreme negative such a clear influence on the body mass. This situation winter temperatures: the coldest site in our database, might be related to the thermal pollution in some of with a winter average temperature of -13.8 °CisatSt. these low winter temperature areas (e.g. in -1 °C air Louis, USA (N 47.02257876°; W 92.21607517°). The temperature, Gollasch 2006). Summer temperature 123 2098 D. Crespo et al. seems to have a larger influence in the population the most successful invasive species in aquatic traits, namely in the growth at the end of the 1st year ecosystems. This progression is human mediated and in the maximum body length. This could be and, apparently, only delayed by orographic con- related to more efficient metabolism during the straints (e.g. high slope and oligotrophic conditions) growing season (Mattice and Dye 1976; Vidal et al. and low temperature. However, the thermal pollution 2002). may help the species to establish beyond their current Life span showed a positive relationship with the latitudinal and temperature limits. latitudinal gradient. Populations from higher latitudes It was possible to identify trends between latitude have a slower growth, reflecting in general a slower (and summer temperature) and some population traits metabolism and a longer life span. This type of such as growth in the first year and life span. Still, the relationship has been described for other mollusk highly ecophenotypic plasticity of the species makes species, including freshwater bivalves (e.g. Cardoso those relationships less clear than expected. Simulta- et al. 2002; Verdelhos et al. 2011; Varandas et al. 2013). neously, the lack of a standard protocol for the study of On the contrary, populations at lower latitudes, with the species population traits makes it harder to provide higher water temperatures, have higher growth rates worldwide generalizations on the relationships be- and, consequently, shorter life spans. Also, the avail- tween traits and invasion success. ability of food may be impaired at higher latitudes due to Nevertheless, with the predicted climate change, shorter sunlight periods. Colder environments reduce one could expect that the species will go further phytoplankton standing stocks on which C. fluminea beyond its current limits, invading freshwater and mainly rely (although the species can also pedal feed estuarine systems further north and south. Some of the and consume organic matter available in the sediments; high altitude systems have been already invaded. With Hakenkamp and Palmer 1999). Altitude may also play a the data gathered in this work, we hope to contribute to role in this, because at higher altitudes nutrients future models, where the susceptibility of certain availability is usually reduced. geographical areas to invasion by C. fluminea may be We expected to have clearer patterns regarding the predicted more accurately. Those models could be a population traits and environmental gradient. Never- precious help in order to detect the invasion in its theless, the species shows a high ecophenotypic earlier phases, eventually allowing successful eradica- plasticity (McMahon 2000) and local conditions may tion at lower ecologic and economic costs. have a decisive role on the populations traits, which could confound the general latitudinal and geographic Acknowledgments This research was supported by FCT gradients. (Portuguese Foundation for Science and Technology), through a PhD grant attributed to D. Crespo (SFRH/BD/80252/2011), a The availability of calcium is also a fundamental post-doc grant attributed to S. Leston (SFRH/BPD/91828/2012) issue for bivalves, as the shell is built on it. Organic and M Dolbeth (SFRH/BPD/41117/2007) and BIOCHANGED matter is also fundamental for the growth of soft project (PTDC/MAR/111901/2009), subsidized by the tissues as well as for the shell. Despite the lack of data European Social Fund and MCTES (Ministe´rio da Cieˆncia, Tecnologia e Ensino Superior) National Funds, through the on the hardness and nutrients for most of the sites POPH (Human Potential Operational Programme), QREN where C. fluminea is present, it is expected that higher (National Strategic Reference Framework) and COMPETE altitudes present lower calcium concentrations and (Programa Operacional Factores de Competitividade). We also oligotrophic conditions, thus contributing to the acknowledge two anonymous reviewers for their helpful and constructive comments which improved the manuscript. limiting of the species progression and populations growth in a synergistic effect with temperature.

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