First record of quagga mussel Dreissena rostriformis bugensis ( Andrusov , 1897 ) ( Bivalvia , Dreissenidae ) from Mexico

The freshwater mussel Dreissena rostriformis bugensis (Andrusov, 1897) has been identified as an invader on different continents. Here, we report the first record of quagga mussel species in México. We detected quagga mussels in El Carrizo reservoir in the Mexican state of Baja California on July 12, 2014. Additional studies in both regions indicated that this species is spreading in the Colorado River basin. However, no specimens were detected in the sites examined in the Mexican portion of the Colorado River Basin. Further sampling is required to assess the invasion area.


Introduction
The quagga mussel Dreissena rostriformis bugensis (Pallas, 1771) is indigenous to the whole Dnieper-Bug estuary, Dnieper River delta, and lower Ingulets River, a zone located in Ukraine (Mills et al. 1996;Zhulidov et al. 2010).By 2004, the quagga has expanded its range to the Romanian section of the Danube River (Micu and Telembici 2004).The first observation in Western Europe was in a freshwater section of the Rhine and Meuse estuary in The Netherlands (Molloy et al. 2007).Bij de Vaate (2010) suggested that ballast water or transport by inland shipping could be potential dispersal mechanisms of quagga mussel in Western Europe.The quagga mussel was first discovered in North America in the Great Lakes in 1989 (Mills et al. 1993).A possible mechanism of introduction is that the mussel was carried in the ballast tanks of ships from Ukranian ports.To date, there are reports of the presence of quagga mussel in 13 states in the United States (Benson 2013).
An unknown mollusk was first noticed about three years ago in the facilities of a drinking water plant in Tijuana (Mercado-Juárez 2014).The water supply of this plant comes from El Carrizo reservoir, which is the end point of the Colorado River-Tijuana aqueduct.The negative impacts of the presence of this mollusk in the Tijuana area include those caused by fouling of drinking water intake pipes and structures.In the last year, The State Commission of Public Services of Tijuana (CESPT for its Spanish acronyms), the government organization that operates drinking water and wastewater plants in Tijuana, stated an increment of the density of this mollusk in pipes and structures of drinking water plants.This situation has increased the cost of cleaning these structures.The volume of the shells removed every three months from the El Florido drinking water plant was 163 cubic meters and CESPT has calculated a cost of 38 million pesos (around 3 million US dollars) to change pipes, filters and tanks to get rid of the fouling organism (Mercado-Juárez 2014).We identified this mollusk as quagga mussel Dreissena rostriformis bugensis from collected specimens in El Carrizo reservoir.This paper describes the first record of quagga mussel in México.

Materials and methods
Two campaigns to detect quagga mussels were conducted on July 12, 2014 in El Carrizo reservoir, Abelardo Rodriguez reservoir, Alamar Creek in the Tijuana area and on August 2, 2014 on eight sites in the valley of Mexicali.All the sites are located in the state of Baja California in the northwestern part of Mexico.Sampling sites are shown in Figure 1.Detection of mussels was conducted by looking for signs of mussel clusters in the hard substrate in each site.
The criteria used to identify the specimens were those described by Mackie and Schlosser (1996) and Benson et al. (2014).Specimens were housed in the mollusk collection of the Yucatán Peninsula at the Agricultural and Biological Sciences Department of the Autonomous University of Yucatán.The area of Tijuana has a dry mediterranean climate with distinct summer and winter seasons.The average annual temperature is 21°C and an average annual precipitation of 220mm, with over 90% occurring during the period from November to April (Implan 2002).However, the climate in the area of Mexicali is hot and dry.The average temperature between October and May is 23°C and the average maximum temperature between June and September is 42°C.The daytime temperature in surface water in this region exceeds 30°C (Minckley 1979).The average annual rainfall is 132 mm (XXI Mexicali City Council, 2014).

Results
Characteristics of the examined sites and records of quagga mussel are shown in Table 1.
We detected freshwater mussels only in El Carrizo reservoir on July 12, 2014 (Figure 2).It is known that the dreissenid species can have different phenotypes; even if they have the same genotype due to different environmental conditions (Claxton et al. 1998).We identified them as Dreissena rostriformis bugensis.
They were found mainly in clusters containing numerous individuals and were firmly attached to solid objects, mainly on submerged rocks at shallow depth (0.5 -1m).
The specimens of quagga mussel collected in El Carrizo reservoir have a total length ranging from 11.43 to 28.6 mm and a weight ranging from 0.231 to 3.6g (Figure 2).The substrate consisted of rocks and mud.Surface water temperature was 25°C; with an electrical conductivity of 1222 µS/cm.Shoreline vegetation is scarce with Chamise Adenostoma fasciculatum, narrowleaf yerba santa Eriodictyon angustifolium and other small plants such as brittlebrush Encelia farinosa.The aquatic vegetation detected was Enteromorpha sp.

Discussion
The spread of freshwater dreissenids could have potentially undesirable effects in river and lagoon ecosystems.Documented ecological effects of these species include: ecosystem change by reduction of phytoplankton numbers or biomass (Birnbaum 2006); modification of natural benthic communities associated with an increased number of benthic invertebrates (Ward and Ricciardi 2007); habitat alteration by high density colonization in soft substrates can impede fish foraging (Beekey et al. 2004); colonization of hard substrates affects spawning fishes (Marsden and Chotkowski 2001); competition for space with native species (Strayer et al. 1998); and modification of nutrient regime (Bruesewitz et al. 2006).Another ecological impact is the bioaccumulation of pollutants which may harm animals further up the food chain (DAISIE 2006).Negative economic impacts include those caused by the fouling of intake pipes, ship hulls, navigational constructions and aquaculture cages (Idaho Invasive Species Council 2009).
The occurrence of this freshwater mussel in El Carrizo reservoir is most likely to be the result of transporting water from the Colorado River or the introduction of sports fishing boats from a zone where this mussel species is present.The infestation of quagga mussels has been detected in lakes and reservoirs in the U.S., including the state of California since 2007, where 25 reservoirs are infested by quagga mussels.Almost all of them are located in Southern California and receive water from the Colorado River (California Department of Fish and Wildlife 2011).The infested U.S. reservoirs closest to El Carrizo reservoir are Lower Otay and Sweetwater reservoirs, located approximately 25 and 35 kilometers northwest, respectively.El Carrizo reservoir is located eight kilometers east of the urban zone of Tijuana.The reservoir was built in 1977 to store water from the Colorado River-Tijuana aqueduct, with a maximum capacity of 30 million cubic meters and a maximum depth of 286.22m (CESPT 2013).
We visited eight points in the Mexicali and San Luis Río Colorado Valley and no freshwater mussel cluster or individual was detected in the inspected channels and reservoirs.The absence of quagga mussel may be as a result of the environmental conditions in the water bodies (ponds and canals).In this zone there is a high fluctuation of water level due to the heavy demand of water for agriculture and domestic use.Daytime water temperatures in the summer were estimated by Minckley (1979) to exceed 30°C (86°F), but approaching 40°C (104°F) only when insolation was accompanied by high relative humidity (Deacon and Minckley 1974).Antonov and Shkorbatov (1990) determined the effect of temperatures on Ukraine populations of D. rostriformis bugensis.The onset of mortality was at 28.1°C.Fifty percent mortality was recorded at 29.1°C.They also recorded the first D. bugensis with fully opened shell at a temperature of 29.7°C.Another study had shown a rapid mortality of D. bugensis at 30°C (Spidle 1994).
It is possible that some areas in the Mexican portion of the Colorado River basin suffered seasonal mussel colonization during certain times of the year.But some parameters such as low dissolved oxygen and high temperatures can effectively eliminate the settled mussel populations on a regular basis (Mackie and Claudi 2009).Mihuc et al. (1999) reported a seasonal colonization by zebra mussel in a subtropical river: the veligers coming in from upstream locations settle during autumn and winter and are eliminated the following summer by a combination of high ambient temperature and low dissolved oxygen.The colonization of quagga mussel in the Mexican portion of the Colorado River may be possible where temperature and dissolved oxygen conditions are not limiting.
A high number of the exotic crayfish (Procambarus clarki) and an exotic clam (Corbicula fluminea) were observed in El Carrizo reservoir during the sampling period.The   introduction of both Dreissena species is generally associated with an increased benthic macroinvertebrate density and taxonomic richness (Ward and Ricciardi 2007).Biodeposition of organic waste and dense colonization of the benthos by zebra mussels has also substantially altered benthic communities; many invertebrates benefit from the increased food resources and complex habitat (Ward and Ricciardi 2007).
Additional sampling and monitoring is necessary to evaluate the mussel distribution and impacts of this new exotic species in Baja California and establish measures for its control and eradication.

Figure 1 .
Figure 1.Sampling locations in the state of Baja California, México showing A) zone of Tijuana, Baja California.B) Area of the Mexicali Valley, Baja California, México.

Table 1 .
Characteristics of examined sites and records of quagga mussels.