sign in sign up
<<
Home , Corbicula, Corbicula fluminalis, Corbicula fluminea, Corbiculidae

Reproduction and Population Structure of fluminea in an Oligotrophic Subalpine Lake Author(s) :Marianne E. Denton, Sudeep Chandra, Marion E. Wittmann, John Reuter and Jeffrey G. Baguley Source: Journal of Shellfish Research, 31(1):145-152. 2012. Published By: National Shellfisheries Association DOI: http://dx.doi.org/10.2983/035.031.0118 URL: http://www.bioone.org/doi/full/10.2983/035.031.0118

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Journal of Shellfish Research, Vol. 31, No. 1, 145–152, 2012.

REPRODUCTION AND POPULATION STRUCTURE OF IN AN OLIGOTROPHIC SUBALPINE LAKE

MARIANNE E. DENTON,1* SUDEEP CHANDRA,1 MARION E. WITTMANN,3† JOHN REUTER3 AND JEFFREY G. BAGULEY2 1Aquatic Ecosystems Analysis Laboratory, Department of Natural Resources and Environmental Science, University of Nevada, 1664 N. Virginia Street, MS 186, Reno, NV, 89512; 2Department of Biology, University of Nevada, 1664 N. Virginia Street, MS 314, Reno, NV 89557; 3Tahoe Environmental Research Center, University of California, One Shields Avenue, Davis, CA, 95616

ABSTRACT Reproductive effort and population structure of the nonnative clam Corbicula fluminea were studied in an oligotrophic subalpine lake. Three shallow sites (5 m) and one deeper site (20 m) were studied between May 11, 2010, and November 5, 2010, to determine spatial variation and the influence of environmental conditions (e.g., temperature and food availability as determined by total organic carbon (TOC) and sediment particulate organic matter (SPOM) on reproductive effort. The clam C. fluminea exhibited a univoltine spawn cued by increases in temperature. Reproductive effort calculated for adult clams (13.67 ± 0.03 mm (SE), n ¼ 1,875) across sites was not influenced by TOC and SPOM concentrations, and overall reproductive effort was less than more productive ecosystems, which may be a result of ’s ultraoligotrophy. All 3 shallow sites had similar levels of reproductive effort. Once were observed, of the 603 clams then dissected, there were 10 ± 2 veligers per clam (±SE), 25 clams had $100 veligers per clam (286 ± 28 veligers per clam), 78 clams contained less than 100 veligers (20 ± 2 veligers per clam), and 498 clams had no veligers present, indicating the population exhibits a highly variable reproductive effort. There was, at a minimum, a 4-wk delay from the point that temperatures reached a threshold for fertilization and release until they were observed in dissected clams. At 20 m, C. fluminea were high in abundance compared with shallow sites, but contained few fully developed juveniles, indicating a potential population sink. Overall population structure was dominated by adult clams ($13 mm), with a minimal presence of juveniles (#4mm).

KEY WORDS: clam, Corbicula fluminea, reproduction, fecundity, population structure

INTRODUCTION larval incubation periods as short as 6 days, normally upward to 2 wk or as lengthy as 60 days in a wide range of environmental Nonnative aquatic that are predisposed to reach conditions (King et al. 1986, Kraemer & Galloway 1986, nuisance levels are tolerant to a wide range of environmental McMahon 2000, Rajagopal et al. 2000). Eggs from C. fluminea conditions, able to use food and space efficiently, reach early are held in the inner demibranches of the ctenidia (gills) after sexual maturity, and/or exhibit high fecundity (e.g., Kolar & release from the gonads, then fertilized, and embryos are brooded Lodge 2001, Kulhanek et al. 2011, Karatayev et al. 2009). Within in the same structure. This may result in an annual fecundity rate a newly established area, molluscs with the greatest fecundity, of as many as 68,000 juveniles per individual (Aldridge & resulting from life history strategies such as the type of sexual McMahon 1978, McMahon 2002). Temperature initiates mul- expression, duration of brooding, and life span, are the most tiple stages of reproduction, and C. fluminea generally has a likely to become nuisance organisms (Keller et al. 2007). bivoltine reproductive cycle in response to temperature regimes The freshwater clam Corbicula fluminea, native to south- in rivers, lakes, and reservoirs (Aldridge & McMahon 1978, eastern Asia, has been introduced globally and is generally Kennedy & Van Huekelem 1985, Rajagopal et al. 2000, considered to be an aquatic of nuisance status. Mouthon & Parghentanian 2004). An initial spawn commonly After establishing in the Pacific Northwest of the occurs during the spring after threshold temperatures have been during the 1930s, C. fluminea spread throughout reached (at least 16–18°C for at least 10 degree-days); however, (McMahon 1982). Its establishment has resulted in negative once temperatures exceed 27–28°C, reproductive output is ecological and economic impacts, including colonization in restricted (McMahon 2000, Mouthon 2001, Mouthon 2001b). water intake systems of power generating systems (McMahon A subsequent, weaker spawn may occur after a return to lower tem- 2002). It can dominate the benthic biomass of aquatic ecosystems peratures (Aldridge & McMahon 1978, Kennedy & Van Huekelem (Karatayev et al. 2003) and lead to ecological changes, including 1985, Rajagopal et al. 2000, Mouthon & Parghentanian 2004). disruption of food webs because of the size-selective filtration Although temperature is the primary cue for initiation of of seston (Cohen et al. 1984, Phelps 1994, McMahon 2002), reproduction, food availability is also important for embryo suppression of native mollusc populations (Strayer 1999), and development and successful brooding (Doherty et al. 1987, alteration of nutrient cycling dynamics (Hakenkamp & Palmer Mouthon 2001b). Overall food availability has been found to 1999, Vaughn & Hakenkamp 2001). enhance gonad development and fecundity, and increases both Reproduction of C. fluminea can be prolific as a result of the brood size and individual size of developing embryos hermaphroditism, rapid reproductive maturity, and variable (Beekey & Karlson, 2003). To support growth and reproduc- *Corresponding author. E-mail: [email protected] tion, two feeding strategies are used: suspension feeding from †Current address: Department of Biological Sciences, University of the water column and deposit feeding in the substrate. Notre Dame. Galvin Life Sciences Building, Notre Dame, IN 46556 Suspension feeding rates of C. fluminea are variable but can DOI: 10.2983/035.031.0118 be high, between 300–2,500 L/h (McMahon & Bogan 2001). In

145 146 DENTON ET AL. the absence of suspended food, such as that seen in oligotro- Marla Bay is approximately 1.5 km wide with a maximum phic ecosystems, C. fluminea can ingest sediment particulate depth of 5 m before a steep drop toward profundal depths at organic matter (SPOM) through deposit feeding (Reid et al. the edge of the bay, approximately 0.50 km from the shoreline. 1992), consuming upward of 50 mg/day and doubling growth At Nevada Beach the bottom extends approximately 110 m rates (McMahon & Bogan 2001). from the shoreline to a depth of 5 m, followed by a slope to The objective of this study was to investigate the factors that greater depths. The substrate is dominated by medium sand influence the reproductive efforts (timing and overall fecundity) (0.50–0.30 mm) at both Marla Bay (>50%) and Nevada Beach of a recently established population of C. fluminea in oligotro- (>75%), with the remaining particle sizes ranging from very phic Lake Tahoe (California to Nevada). To our knowledge, fine gravel (4.00 mm) to very fine sand. Lake Tahoe is the highest elevation and deepest lake where this species has established. First observed in 2002, C. fluminea was Field Collection found to be widely established in the southeastern littoral zone of Lake Tahoe by 2008 (Hackley et al. 2008). A recent survey We collected C. fluminea using a Petite Ponar grab (area, found C. fluminea distributed in deeper waters (20–80 m). We 225 cm2) biweekly from May through August (late spring to believe clams living in deeper waters may contribute to the summer) and monthly from September through November recruitment of nearshore populations. Utilizing a combination (fall) 2010. Lake water was collected near the water–substrate of field experiments, dissections of clams, and information interface using a Van Dorn sampler and measured for in situ gathered from a literature review, we tested the following temperature using a hobbyist digital thermometer (Coralife hypotheses: (1) temperature would have the greatest influence ESU Digital Thermometer). In situ point measurements for on the timing of reproductive initiation; (2) food availability, temperature were validated against a continuous temperature represented by a coarse proxy of total organic carbon (TOC) data logger that indicated a clear relationship among the mea- and SPOM, would influence overall reproductive effort; and surements to describe seasonal patterns in temperature (Denton, (3) reproductive efforts would be similar in both shallow and unpubl. data). TOC in the overlying lake water was analyzed with deeper populations, resulting in a source of veligers for populat- an elemental analyzer (Shimadzu TNPC-4110C). SPOM was ing the nearshore environment. gathered from a thin scraping of the surface sediment (#1cmin depth) obtained from the Petite Ponar sample, and measured as METHODS loss on ignition (Froelich 1980). Environmental conditions were analyzed by a 1-way ANOVA for temperature and TOC for site Study Site and date independently, and 2-way ANOVA analyzed SPOM by site by date, and a pairwise difference was determined with Lake Tahoe (39.13° N, 120.05° W) is a large, subalpine Tukey’s HSD post hoc analysis. oligotrophic lake located in the Sierra Nevada mountain range All C. fluminea samples were held in 18-L field buckets with on the California–Nevada border. The 11th deepest lake in sediment and lake water, stored at ;10.0°C, and processed in the world, it has a surface area of 496 km2, maximum depth of the laboratory within 24 h of collection. Samples were elutriated 501 m, and surface elevation of 1,897 m a.s.l. at capacity. The in the laboratory and sieved through 90-mm mesh to retain the surrounding basin has a watershed of 800 km2. Tahoe is a cold smallest individual clams and to calculate abundance (measured monomictic lake, ice-free year-around, with stratification be- as clams per square meter) for each sampling period and location. ginning in early spring, and maximum surface temperatures in All grabs were combined into 1 sample per site per date; therefore, midsummer (Jassby et al. 2003). Although well known for its variations in dates by individual sites were not determined. clear waters, clarity has been decreasing since the late 1960s, with a current annual mean Secchi depth of approximately 20 m Reproductive Effort (Winder et al., 2009). Lake Tahoe’s annual pelagic primary pro- duction has shown a more than 4.5-fold increase in 40 y (Chandra To quantify eggs and developed fertilized larval forms et al. 2005), and it remains a low-nutrient lake (Winder & Hunter (hereafter referred to as veligers), we dissected the gills of 2008) with a change from N limitation to N/P colimitation during approximately 40 clams (shell length, 13 ± 1 mm) per site the early 1980s (Goldman et al. 1993). Littoral zone temperatures across sampling dates. Clams between 11 mm and 19 mm were range from ;6.0°C in winter months and to 21.0°Cinmidsummer. dissected occasionally when the target size class was not met Four sites with established C. fluminea populations were completely. Clams were measured for shell length with digital sampled: Lakeside, Marla Bay, and Nevada Beach each at calipers to the nearest 0.01 mm prior to dissection. Ctenidia a depth of 5 m, and Nevada Beach at a depth of 20 m (hereafter were squash mounted and examined under 1003magnification referred to as LS5, MB5, NV5, and NV20). A benthic sampling light microscopy (Morton 1977, Britton & Morton 1982). and visual evaluation of Lake Tahoe shows that C. fluminea are Developmental stages were determined based on the descrip- largely restricted to the southeastern and southern littoral zones tions from Kraemer & Galloway (1986). Because these data (Wittmann & Chandra, unpubl.). At Lakeside, there is a wide, were determined to be distributed nonnormally (Anderson- shallow shelf with approximately 1.3 km from shoreline to the Darling normality test), they were log10 transformed and ana- greatest depth of 5 m before dropping off to deeper depths. lyzed by a 2-way ANOVA of site by date. Pairwise differences The bottom substrate here is nearly equal amounts of medium were determined with a Tukey HSD post hoc analysis. Mean sand (0.50–0.30 mm) and very fine sand (0.062 mm), with the values and standard error with sample size are reported. All small remainder in the range of fine cobble (64 mm) to clay statistical analyses were performed using SAS 9.2 (SAS In- (<0.003 mm), as determined by the Wentworth particle size stitute, Inc., Cary, NC) and Minitab 15.1 (Minitab, Inc., State distribution (Brakensiek et al. 1979, Gordon et al. 2004). College, PA). REPRODUCTION AND POPULATION STRUCTURE OF C. FLUMINEA 147

RESULTS a Tukey post hoc analysis showed that August 30, September 13, and October 8 had the greatest abundance of veligers Environmental Conditions present, and the veliger abundance at shallow locations was significantly greater than NV20 (P < 0.0001). Across all 3 At all sites, temperatures were less than 8.0°C on May 11, shallow sites, there were similar levels of reproductive effort, with the greatest increase in temperature from June 16–28 (Fig. with a mean veliger abundance per clam (±SE) of 10 ± 2(n ¼ 1). Seasonal high temperatures were recorded at each site on 603), with ranges of 286 ± 28 (n ¼ 25 for clams with $100 July 20. A temporary decrease in temperatures on August 30 veligers) and 20± 2(n ¼ 78 for clams with <100 veligers), and was associated with a cold front that passed through the Tahoe 498 clams had no veligers present in samples from mid August basin at that time. Temperatures were significantly different over through early November. NV20 had a mean abundance of 3 ± dates (P < 0.0001) but not sites (P ¼ 0.659). TOC concentrations 1 veligers across 4 clams, with 196 clams having no veligers were not significantly different among sites (P ¼ 0.549). Mean present in samples during the same period concentrations (±SE) across all dates (n ¼ 10)ateachsitewere 10.7 ± 0.5 mg/L (LS5), 10.7 ± 0.4 mg/L (MB5), 10.9 ± 0.5 mg/L (NV5), and 10.7 ± 0.5 mg/L (NV20). There was a significant site- Population Structure by-date interaction in SPOM (P < 0.0001). A Tukey post hoc Overall population abundance was significantly different by analysis determined that LS5 (6.8 ± 3.3mg/mg) and NV20 (6.1 ± site over all sampling dates (P ¼ 0.0013), with abundance at 4.4 mg/mg) had greater concentrations of SPOM than MB5 (4.6 ± NV20 (2,541 ± 291 clams/m2) significantly greater than the 2.9 mg/mg) and NV5 (3.6 ± 1.1 mg/mg) during the season (Fig. 2). shallow sites (Fig. 4). The distribution of C. fluminea was Reproductive Activity heterogeneous along the bottom at each site. Across sites for all sampling dates, there was a significant difference in the A total of 1,875 clams were dissected to determine their number of grabs obtained to meet the needs of dissection (P ¼ reproductive status and activity throughout the course of the 0.0014), with LS5 requiring the greatest number of samples over sampling period. The mean shell length at each site during the the dates (9 ± 3 grabs per date), MB5 and NV5 requiring fewer entire sampling period was 13.68 ± 1.3 mm (LS5, n ¼ 461), 13.33 ± but nearly equal numbers of grabs (7 ± 2 and 7 ± 1 grabs per date, 0.7 mm (MB5, n ¼ 479), 13.91 ± 1.0 mm (NV5, n ¼ 478), and respectively), and NV20 requiring the fewest (5 ± 2 grabs per 13.74 ± 1.2 mm (NV20, n ¼ 457). Eggs were present in the date, n ¼ 12; SD is noted because SE values were less than 1). demibranches on all sampling dates from May 11 to November Size class distribution of C. fluminea by site suggests differences 5 (Fig. 3). Egg abundances observed had a significant site-by- in population structure (Fig. 4). Size class distributions in LS5 date interaction (P < 0.0001), and a Tukey post hoc analysis were variable, but no one size class (or group of size classes) determined that the greatest abundance occurred on August 30. dominated the population structure throughout the sampling Veligers were detected in the middle to end of summer and season. Size classes between 13 mm and 17 mm represented occurred in low abundance on August 16, and were in high a majority of the populations in MB5, with clams occasionally abundance on August 30 and September 13. These sampling dates reaching a shell length of 22 mm. Shell lengths of #4 mm were were +27, +41, and +55 days after the critical temperature absent from these samplings. At NV5, the #4-mm size class was threshold needed to initiate a spawning of brooding veligers (King present in all samplings with very low presence during June 16 et al. 1986, Kraemer & Galloway 1986). There was a significant and November 5. The 13–17 mm-size class was large through- site-by-date interaction of brooding veliger abundance, and out the sampling dates, and clams disappeared from the

Figure 1. Temperatures at the water–substrate interface by sampling date and site. Documented threshold temperatures required for reproduction are noted, with the vertical bars indicating when temperatures were recorded at 5 m. A, the onset of spermatogenesis; B, fertilization occurs; C, initial release of veligers. 148 DENTON ET AL.

Figure 2. Values of sediment particulate organic matter (SPOM) within #2 cm of the substrate surface.

population after 22 mm. The #4-mm size class at NV20 was DISCUSSION present on June 16 and September 13. For a majority of the In Lake Tahoe, C. fluminea in Lake Tahoe is univoltine, with other samplings, this size class was completely absent, with reproduction in the late summer and low abundance of brood- a minimal presence on August 2, October 8, and November 5. ing veligers. There was a longer than expected delay between As in the other locations, the largest size class was the 13–17-mm threshold temperatures for required reproduction based on group.

Figure 3. Mean values (%SE) for eggs (no shading) and veligers (shading), and percentage of populations with eggs (solid line) and veligers (dotted line). REPRODUCTION AND POPULATION STRUCTURE OF C. FLUMINEA 149

Figure 4. Population structure of sampling sites across dates expressed as a percentage on the primary vertical axis. Abundance (number of clams per square meter) is represented by a line on the secondary vertical axis. 150 DENTON ET AL. previously published literature and empirical observations of In determining the similarities, if any, of reproductive effort brooding veligers made during dissections. Given that oogen- between the shallow- and deep-water populations, an interest- esis occurs independent of temperature (Kraemer & Galloway ing observation is the low count of veligers seen in dissections 1986), we expected eggs to be present during all dissections. from NV20, the deeper water site. Veligers were found on only 1 Because spermatogenesis and fertilization require minimum sampling date (August 30), with just 13 veligers seen in 4 clams. temperature thresholds to be met (10.0°C and 14.0°C, respec- However, this site has the highest overall abundance among tively), brooding veligers should not have been present until sites, with significant increases in observed abundance in the temperatures were at least 14°C for 10 consecutive degree-days late summer. Population size structure at this site indicated an (Kraemer & Galloway 1986). Temperatures across all shallow increase in abundance is toward the larger size classes (>13 mm) sampling sites reached this threshold by July 20, with a mean of rather than recruitment of juveniles (<4 mm; Fig. 4). This 19.7 ± 0.4°C. A typical cycle of initial fertilization, larval suggests that deep-water populations are not reproductively maturity, to release of veligers is 6–14 days (Kraemer & Galloway active, and therefore are potentially a sink of clams rather than 1986), with release occurring at least 16.0°C. In other systems, a source. If this is the case, clams would have had to be C. fluminea are observed to be bivoltine, with the first spawn transported from the shallow depths to these deeper popula- occurring in late spring to early summer, and resuming in late tions. Movement of clams to this deeper region may occur in 2 summer.Thispatternhasbeenattributedtometabolicdeclines ways. One documented means of dispersal for C. fluminea is via resulting from temperature increases greater than 27.5°C floatation. Prezant and Chalermwat (1984) found that clams up (Aldridge & McMahon 1978, Mouthon 2001a). When spawning to 14 mm, when exposed to a current of 10–20 cm/sec, would did occur in Lake Tahoe after a 4-wk delay, the overall push off the substrate with their foot while extending both abundance of veligers observed in the shallow sites (10 ± 2 siphons. They excrete a long mucus thread that allows them to veligers per clam) was much lower than the veliger abundance be lifted and carried in the water column until the current observed in more productive reservoir or riverine ecosystems. subsides. This current is typically not found in the nearshore of In these ecosystems, veliger reproductive efforts range from 588 lakes. Another possibility is that wind-driven waves creating to 735/clam per day in spring and fall (Aldridge & McMahon high-energy turbulence may transport clams from shallow 1978) and 1,800 to 1,200/clam per day from late June and early depths to deeper locations. Redjah et al. (2010) found that the October, respectively (Doherty et al. 1987). Recent studies have clam Mya arenaria, up to 20 mm, was displaced when subjected shown that Lake Tahoe’s surface waters are warming at a faster to turbulence in a level experimental flume with a high wave- rate than ambient air temperatures (Schneider et al. 2009, Coats current flow. In addition, in a sandy substrate similar to the 2010). In the future, this increase in water temperatures may NV5 and NV20 sampling sites, St-Onge and Miron (2007) expand the spawning potential of C. fluminea to an earlier found that between 40–90% of M. arenaria were eroded initiation of reproductive development, and a longer fertiliza- (transported) at stream velocities of 29–35 cm/s. With an tion and release period. It is unlikely, however, that a bivol- approximate horizontal distance of 60 m between the 5-m and tine spawning event will occur in Lake Tahoe because current 20-m depth at Nevada Beach, an estimated slope of 18 deg, and temperature warming forecasts for the nearshore do not suggest documented populations of clams at 10 m and 15 m (unpublished an increase in temperature that would stop and reinitiate samplings for 2008 and 2009), it is conceivable that high-energy spawning, as found in warmer ecosystems. Alternatively, turbulence resulting from internal lake currents and other warming of the lake in the winter prior to the spawning cycle physical waves could transport both juvenile dispersers and adult could enhance the reproductive success of C. fluminea (Weitere clams along the slope to deeper depths. et al. 2009). Throughout the 2010 sampling period, the juvenile size class In other systems, food availability has been observed to (<4 mm) appeared sporadically across all sites and was probably be a significant contributor to spawning events of C. fluminea a result of carryover from reproduction in 2009. Unlike other to meet the energetic demand of brooding (Mouthon 2001b). systems that show a pyramid-shape size class population Corbicula fluminea brood veligers within the inner demibranches structure, with less than 4 mm as the dominating the population of the gills, which have secretory cells believed to provide (Hall 1984, Mouthon & Parghentanian 2004), the Lake Tahoe nutrients to developing embryos (Britton & Morton 1982, population contained more individuals in the 10–17 mm size Doherty et al. 1987). Although other studies reported chloro- classes, with a sharp decline in abundance of larger individuals phyll a concentrations in systems with successful C. fluminea in the range of 19–23 mm. Joy (1985) reported no shell growth populations ranging from 3 to 100 mg/L (Cohen et al. 1984, for C. fluminea for water temperatures between 0°C and 13.0°C. Mouthon 2001b, Mouthon & Parghentanian 2004), chlorophyll Given that newly released veligers are 0.2 mm, and depending a concentrations in Lake Tahoe range from 0.5–1.5 mg/L on the previous season’s release period, it is conceivable that the (TERC 2010). These low concentrations could limit C. fluminea 2009 spawn would appear as a new size class the following growth and could reduce nourishment for brooding embryos. midsummer 2010. Temperatures in this study were less than TOC at the water–substrate interface suggests similarly low 13.0°C by November; therefore, juveniles spawned in the 2010 food concentrations from this source. Although there were season would likely not experience shell growth until May 2011 significant site-by-date differences for SPOM, overall reproduc- or June 2011. tive effort was not significantly different among the sites, suggesting that variable concentrations of SPOM and TOC ACKNOWLEDGMENTS are not predictors of the fecundity of C. fluminea in Lake Tahoe. Further investigation of food availability—in particular, food Gratitude is acknowledged to the anonymous reviewers quality—is needed to understand its role in Lake Tahoe clam whose comments enhanced this paper. In addition, we grate- reproductive effort with respect to water temperature. fully acknowledge funding provided by the Nevada Division of REPRODUCTION AND POPULATION STRUCTURE OF C. FLUMINEA 151

State Lands and the Southern Nevada Public Lands Manage- Moore of California Fish and Game in assisting our un- ment Act to S. C., M. W., G. S., and J. E. R. Invaluable field and derstanding of the gonadal structures of bivalves is greatly laboratory support was provided by members of the University appreciated. The review of dissection photographs by Marvin of Nevada, Reno, Aquatic Ecosystems Laboratory (Joseph Galloway, Francis Parchas, and David Aldridge were an Sullivan, Rob Bolduc, Christine Ngai, John Umek, Jessica essential component of this study. Participants of the 2009 Rasmussen, Robert Barnes, and Alex Denton) and the Uni- Tahoe Baikal Institute’s Summer Environmental Exchange versity of California, Davis, Tahoe Environmental Research were instrumental in refining the preliminary methodology for Center (Raph Townsend, Katie Webb). The support of Jim this study.

LITERATURE CITED Aldridge, D. W. & R. F. McMahon. 1978. Growth, fecundity and Karatayev, A. Y., L. E. Burlakova, T. Kesterson & D. K. Padilla. 2003. bioenergetics in natural populations of the freshwater clam, Cor- Dominance of the Asiatic clam, Corbicula fluminea (Mu¨ller), in the bicula manilensis Phillippi, from north central Texas. J. Molluscan benthic community of a reservoir. J. Shellfish Res. 22:487–493. Stud. 44:49–70. Karatayev, A. Y., L. E. Burlakova, D. K. Padilla, S. E. Mastisky & Beekey, M. A. & R. H. Karlson. 2003. Effect of food availability on S. Olenin. 2009. Invaders are not a random selection of species. Biol. reproduction and brood size in a freshwater brooding bivalve. Can. Invasions 11:2009–2019. J. Zool. 81:1168–1173. Keller, R. P., J. M. Drake & D. M. Lodge. 2007. Fecundity as a basis for Brakensiek, D. L., H. B. Osborn & W. J. Rawls, coordinators. 1979. risk assessment of nonindigenous freshwater molluscs. Conserv. Field manual for research in agricultural hydrology. Agriculture Biol. 21:191–200. handbook no. 224. Washington, DC: US Government Printing Kennedy, V. S. & L. Van Huekelem. 1985. Gametogenesis and larval Office. 550 pp. production in a population of the introduced Asiatic clam, Britton, J. C. and B. Morton, 1982. Dissection guide, field and Corbicula sp. (: ), in Maryland. Biol. Bull. laboratory manual for the introduced bivalve: Corbicula fluminea. 168:50–60. Malacol. Rev. Suppl. 3. Pp. 56–57. King, C. A., C. J. Langdon & C. L. Counts, III. 1986. Spawning and Chandra, S., M. J. Vander Zanden, A. C. Heyvaert, B. C. Richards, early development of Corbicula fluminea (Bivalvia: Corbiculidae) in B. C. Allen & C. R. Goldman. 2005. The effects of cultural eutrophi- laboratory culture. Am. Malacol. Bull. 4:81–88. cation on the coupling between pelagic primary producers and benthic Kolar, C. S. & D. M. Lodge. 2001. Progress in invasion biology: consumers. Limnol. Oceanogr. 50:1368–1376. predicting invaders. Trends Ecol. Evol. 16:199–204. Coats, R. 2010. Climate change in the Tahoe basin: regional trends, Kraemer, L. R. & M. L. Galloway. 1986. Larval development of impacts and drivers. Clim. Change 102:435–466. Corbicula fluminea (Muller) (Bivalvia: Corbiculidae): an appraisal Cohen, R. R. H., P. V. Dresler, E. J. P. Phillips & R. L. Cory. 1984. The of its heterochrony. Am. Malacol. Bull. 4:61–79. effect of the Asiatic clam, Corbicula fluminea, on of Kulhanek, S. A., A. Ricciardi & B. Leung. 2011. Is invasion history the Potomac River, Maryland. Limnol. Oceanogr. 29:170–180. a useful tool for predicting the impacts of the world’s worst aquatic Doherty, F. G., D. S. Cherry & J. Cairns, Jr. 1987. Spawning periodicity invasive species? Ecol. Appl. 21:189–202. of the Asiatic clam Corbicula fluminea in the New River, Virginia. McMahon, R. F. 1982. The occurrence and spread of the introduced Amer. Midl. Nat. 117:71–82. Asiatic freshwater clam, Corbicula fluminea (Mu¨ller) in North Froelich, P. N. 1980. Analysis of organic carbon in marine sediments. America 1924–1982. Nautilus 96:134–141. Limnol. Oceanogr. 25:564–572. McMahon, R. F. 2000. Invasive characteristics of the Goldman, C. R., A. D. Jassby & S. H. Hackley. 1993. Decadal, Corbicula fluminea. In: Claudi, R., J. Leach (eds.), Non-indigenous interannual, and seasonal variability in enrichment bioassays at Lake Freshwater Organisms: Vectors, Biology and Impacts. Lewis Pub- Tahoe, California–Nevada, USA. Can. J. Fish. Aquat. Sci. 50:1489– lishers, Boca Raton, pp 315–343. 1496. McMahon, R. F. 2002. Evolutionary and physiological adaptations of Gordon, N. D., T. A. McMahon, B. L. Finlayson, C. J. Gippel & aquatic invasive : R selection versus resistance. Can. J. Fish. R. J. Nathan. 2004. Stream hydrology: an introduction for ecolo- Aquat. Sci. 59:1235–1244. gists, 2nd edition. West Sussex, UK: Wiley. 443 pp. McMahon, R. F. & A. E. Bogan. 2001. : Bivalvia. In Hackley, S., B. Allen, G. Schladow, J. Reuter, S. Chandra & M. Wittmann. J. H. Thorp & A. P. Covich, editors. Ecology and classification of 2008. Lake Tahoe aquatic invasive species incident report: notes on North American freshwater invertebrates, 2nd edition. San Diego, visual observations of clams in Lake Tahoe and on the beaches along CA: Academic Press. pp 331–430. the southeast shore—Zephyr Cove to Timber Cove Marina: April Morton, B. 1977. The population dynamics of Corbicula fluminea 25, 2008. University of California at Davis Tahoe Environmental (Bivalvia: ) in Plover Cove Reservoir, Hong Kong. Research Center. (Not peer reviewed). http://www.terc.ucdavis.edu/ Journal of Zoology, 181: 21–42 research/CorbiculaIncidentReport_05_07_08.pdf. Mouthon, J. 2001a. Life cycle and population dynamics of the Asian Hakenkamp, C. C. & M. A. Palmer. 1999. Introduced bivalves in clam Corbicula fluminea (Bivalvia: Corbiculidae) in the Rhoˆne River freshwater ecosystems: the impact of Corbicula on organic matter at Creys-Malville (France). Arch. Hydrobiol. 151:57–589. dynamics in a sandy stream. Oecologia 119:445–451. Mouthon, J. 2001b. Life cycle and population dynamics of the Asian Hall, J. J. 1984. Production of immature Corbicula fluminea (Bivalvia: clam Corbicula fluminea (Bivalvia: Corbiculidae) in the Saoˆne River Corbiculidae) in Lake Norman, North Carolina. Nautilus 98:153–159. at Lyon (France). Hydrobiologia 452:109–119. Jassby,A.D.,J.E.Reuter&C.R.Goldman.2003.Determining Mouthon, J. & T. Parghentanian. 2004. Comparison of the life cycle and long-term water quality change in the presence of climate vari- population dynamics of two Corbicula species, C. fluminea and C. ability: Lake Tahoe (U.S.A.). Can. J. Fish. Aquat. Sci. 60:1452– fluminalis (Bivalvia: Corbiculidae) in two French canals. Arch. 1461. Hydrobiol. 161:267–287. Joy, J. E. 1985. A 40-week study on the growth of the Asian clam, Phelps, H. L. 1994. The Asiatic clam (Corbicula fluminea) invasion and Corbicula fluminea (Mu¨ller), in the Kanawha River, West Virginia. system-level ecological change in the Potomac River Estuary near Nautilus 99:110–116. Washington, D.C. Estuaries 17:614–621. 152 DENTON ET AL.

Prezant, R. W. & K. Chalermwat. 1984. Floatation of the bivalve St-Onge, P. & G. Miron. 2007. Effects of current speed, shell length and Corbicula fluminea as a means of dispersal. Science 225:1491– type of sediment on the erosion and transport of juvenile softshell 1493. clams (Mya arenaria). J. Exp. Mar. Biol. Ecol. 349:12–26. Rajagopal, S., G. van der Velde & A. bij de Vaate. 2000. Reproductive Strayer, D. L. 1999. Effects of alien species on freshwater mollusks in biology of the Asiatic clams Corbicula fluminalis and Corbicula North America. J. North Am. Benthol. Soc. 18:74–98. fluminea in the river . Arch. Hydrobiol. 149:403–420. TERC. 2010. State of the lake report 2010. terc.ucdavis.edu/stateofthelake/ Redjah, I., F. Olivier, R. Tremblay, B. Myrand, F. Pernet, U. Neumeier StateOfTheLake2010.pdf. & L. Chevarie. 2010. The importance of turbulent kinetic energy on Vaughn, C. C. & C. C. Hakenkamp. 2001. The functional role of burrowing transport of juvenile clams (Mya arenaria). Aquaculture 307:20–28. bivalves in freshwater ecosystems. Freshw. Biol. 46:1431–1446. Reid, R. G. B., R. F. McMahon, D. O´. Foighil & R. Finnigan. 1992. Weitere, M., A. Vohmann, N. Schulz, C. Linn, D. Dietrich & H. Arndt. Anterior inhalant currents and pedal feeding in bivalves. Veliger 2009. Linking environmental warming to the fitness of the invasive 35:93–104. clam Corbicula fluminea. Glob. Change Biol. 15:2838–2851. Schneider, P., S. J. Hook, R. G. Radocinski, G. K. Corlett, G. C. Hully, Winder, M. & D. A. Hunter. 2008. Temporal organization of phytoplank- S. G. Schladow & T. E. Steinssberg. 2009. Satellite observations ton communities linked to physical forcing. Oecologia 156:179–192. indicate rapid warming trend for lakes in California and Nevada. Winder, M., J. E. Reuter & S. G. Schladow. 2009. Lake warming favors Geophys. Res. Lett. 36:L22402. small-sized planktonic diatom species. Proc. Biol. Sci. 276:427–435.