Reproduction and population structure of Corbicula fluminea in an oligotrophic subalpine lake.
Article Type: Report
Subject: Animal populations (Research)
Population biology (Research)
Clams (Physiological aspects)
Clams (Environmental aspects)
Lakes (Environmental aspects)
Authors: Denton, Marianne E.
Chandra, Sudeep
Wittmann, Marion E.
Reuter, John
Baguley, Jeffrey G.
Pub Date: 04/01/2012
Publication: Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2012 National Shellfisheries Association, Inc. ISSN: 0730-8000
Issue: Date: April, 2012 Source Volume: 31 Source Issue: 1
Topic: Event Code: 310 Science & research
Product: Product Code: 0913030 Clams NAICS Code: 114112 Shellfish Fishing SIC Code: 0913 Shellfish
Geographic: Geographic Scope: United States Geographic Code: 1USA United States
Accession Number: 288172747
Full Text: 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 [+ o r -] 0.03 mm (SE), n = 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 Lake Tahoe's ultraoligotrophy. All 3 shallow sites had similar levels of reproductive effort. Once veligers were observed, of the 603 clams then dissected, there were 10 [+ or -] 2 veligers per clam ([+ or -] SE), 25 clams had [greater than or equal to] 100 veligers per clam (286 [+ or -] 28 veligers per clam), 78 clams contained less than 100 veligers (20 [+ or -] 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 veliger 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 ([greater than or equal to] 13 mm), with a minimal presence of juveniles ([less than or equal to] 4 mm).

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

INTRODUCTION

Nonnative aquatic species that are predisposed to reach nuisance levels are tolerant to a wide range of environmental conditions, able to use food and space efficiently, reach early sexual maturity, and/or exhibit high fecundity (e.g., Kolar & Lodge 2001, Kulhanek et al. 2011, Karatayev et al. 2009). Within a newly established area, molluscs with the greatest fecundity, resulting from life history strategies such as the type of sexual expression, duration of brooding, and life span, are the most likely to become nuisance organisms (Keller et al. 2007).

The freshwater clam Corbicula fluminea, native to southeastern Asia, has been introduced globally and is generally considered to be an aquatic invasive species of nuisance status. After establishing in the Pacific Northwest of the United States during the 1930s, C.fluminea spread throughout North America (McMahon 1982). Its establishment has resulted in negative ecological and economic impacts, including colonization in water intake systems of power generating systems (McMahon 2002). It can dominate the benthic biomass of aquatic ecosystems (Karatayev et al. 2003) and lead to ecological changes, including disruption of food webs because of the size-selective filtration of seston (Cohen et al. 1984, Phelps 1994, McMahon 2002), suppression of native mollusc populations (Strayer 1999), and alteration of nutrient cycling dynamics (Hakenkamp & Palmer 1999, Vaughn & Hakenkamp 2001).

Reproduction of C. fluminea can be prolific as a result of hermaphroditism, rapid reproductive maturity, and variable 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 conditions (King et al. 1986, Kraemer & Galloway 1986, McMahon 2000, Rajagopal et al. 2000). Eggs from C. fluminea are held in the inner demibranches of the ctenidia (gills) after release from the gonads, then fertilized, and embryos are brooded in the same structure. This may result in an annual fecundity rate of as many as 68,000 juveniles per individual (Aldridge & McMahon 1978, McMahon 2002). Temperature initiates multiple stages of reproduction, and C. fluminea generally has a bivoltine reproductive cycle in response to temperature regimes in rivers, lakes, and reservoirs (Aldridge & McMahon 1978, Kennedy & Van Huekelem 1985, Rajagopal et al. 2000, Mouthon & Parghentanian 2004). An initial spawn commonly occurs during the spring after threshold temperatures have been reached (at least 16-18[degrees]C for at least 10 degree-days); however, once temperatures exceed 27-28[degrees]C, reproductive output is restricted (McMahon 2000, Mouthon 2001, Mouthon 2001b). A subsequent, weaker spawn may occur after a return to lower temperatures (Aldridge & McMahon 1978, Kennedy & Van Huekelem 1985, Rajagopal et al. 2000, Mouthon & Parghentanian 2004).

Although temperature is the primary cue for initiation of reproduction, food availability is also important for embryo development and successful brooding (Doherty et al. 1987, Mouthon 2001b). Overall food availability has been found to enhance gonad development and fecundity, and increases both the brood size and individual size of developing embryos (Beekey & Karlson, 2003). To support growth and reproduction, two feeding strategies are used: suspension feeding from the water column and deposit feeding in the substrate. Suspension feeding rates of C. fluminea are variable but can be high, between 300-2,500 L/h (McMahon & Bogan 2001). In the absence of suspended food, such as that seen in oligotrophic ecosystems, C. fluminea can ingest sediment particulate organic matter (SPOM) through deposit feeding (Reid et al. 1992), consuming upward of 50 mg/day and doubling growth rates (McMahon & Bogan 2001).

The objective of this study was to investigate the factors that influence the reproductive efforts (timing and overall fecundity) of a recently established population of C. fluminea in oligotrophic Lake Tahoe (California to Nevada). To our knowledge, Lake Tahoe is the highest elevation and deepest lake where this species has established. First observed in 2002, C. fluminea was found to be widely established in the southeastern littoral zone of Lake Tahoe by 2008 (Hackley et al. 2008). A recent survey found C. fluminea distributed in deeper waters (20-80 m). We believe clams living in deeper waters may contribute to the recruitment of nearshore populations. Utilizing a combination of field experiments, dissections of clams, and information gathered from a literature review, we tested the following hypotheses: (1) temperature would have the greatest influence on the timing of reproductive initiation; (2) food availability, represented by a coarse proxy of total organic carbon (TOC) and SPOM, would influence overall reproductive effort; and (3) reproductive efforts would be similar in both shallow and deeper populations, resulting in a source of veligers for populating the nearshore environment.

METHODS

Study Site

Lake Tahoe (39.13[degrees] N, 120.05[degrees] W) is a large, subalpine oligotrophic lake located in the Sierra Nevada mountain range on the California-Nevada border. The 11th deepest lake in the world, it has a surface area of 496 [k.sup.2], maximum depth of 501 m, and surface elevation of 1,897 m a.s.1, at capacity. The surrounding basin has a watershed of 800 [k.sup.2]. Tahoe is a cold monomictic lake, ice-free year-around, with stratification beginning in early spring, and maximum surface temperatures in midsummer (Jassby et al. 2003). Although well known for its clear waters, clarity has been decreasing since the late 1960s, with a current annual mean Secchi depth of approximately 20 m (Winder et al., 2009). Lake Tahoe's annual pelagic primary production has shown a more than 4.5-fold increase in 40 y (Chandra et al. 2005), and it remains a low-nutrient lake (Winder & Hunter 2008) with a change from N limitation to N/P colimitation during the early 1980s (Goldman et al. 1993). Littoral zone temperatures range from ~6.0[degrees]C in winter months and to 21.0[degrees]C in midsummer.

Four sites with established C. fluminea populations were sampled: Lakeside, Marla Bay, and Nevada Beach each at a depth of 5 m, and Nevada Beach at a depth of 20 m (hereafter referred to as LS5, MB5, NV5, and NV20). A benthic sampling and visual evaluation of Lake Tahoe shows that C. fluminea are largely restricted to the southeastern and southern littoral zones (Wittmann & Chandra, unpubl.). At Lakeside, there is a wide, shallow shelf with approximately 1.3 km from shoreline to the greatest depth of 5 m before dropping off to deeper depths. The bottom substrate here is nearly equal amounts of medium sand (0.50-0.30 mm) and very fine sand (0.062 mm), with the small remainder in the range of fine cobble (64 mm) to clay (<0.003 mm), as determined by the Wentworth particle size distribution (Brakensiek et al. 1979, Gordon et al. 2004). Marla Bay is approximately 1.5 km wide with a maximum depth of 5 m before a steep drop toward profundal depths at the edge of the bay, approximately 0.50 km from the shoreline. At Nevada Beach the bottom extends approximately 110 m from the shoreline to a depth of 5 m, followed by a slope to greater depths. The substrate is dominated by medium sand (0.50-0.30 mm) at both Marla Bay (>50%) and Nevada Beach (>75%), with the remaining particle sizes ranging from very fine gravel (4.00 mm) to very fine sand.

Field Collection

We collected C. fluminea using a Petite Ponar grab (area, 225 [cm.sup.2]) biweekly from May through August (late spring to summer) and monthly from September through November (fall) 2010. Lake water was collected near the water-substrate interface using a Van Dorn sampler and measured for in situ temperature using a hobbyist digital thermometer (Coralife ESU Digital Thermometer). In situ point measurements for temperature were validated against a continuous temperature data logger that indicated a clear relationship among the measurements to describe seasonal patterns in temperature (Denton, unpubl. data). TOC in the overlying lake water was analyzed with an elemental analyzer (Shimadzu TNPC-4110C). SPOM was gathered from a thin scraping of the surface sediment ([less than or equal to] 1 cm in depth) obtained from the Petite Ponar sample, and measured as loss on ignition (Froelich 1980). Environmental conditions were analyzed by a 1-way ANOVA for temperature and TOC for site and date independently, and 2-way ANOVA analyzed SPOM by site by date, and a pairwise difference was determined with Tukey's HSD post hoc analysis.

All C. fluminea samples were held in 18-L field buckets with sediment and lake water, stored at ~10.0[degrees]C, and processed in the laboratory within 24 h of collection. Samples were elutriated in the laboratory and sieved through 90-[micro]m mesh to retain the smallest individual clams and to calculate abundance (measured as clams per square meter) for each sampling period and location. Ali grabs were combined into 1 sample per site per date; therefore, variations in dates by individual sites were not determined.

Reproductive Effort

To quantify eggs and developed fertilized larval forms (hereafter referred to as veligers), we dissected the gills of approximately 40 clams (shell length, 13 [+ or -] 1 mm) per site across sampling dates. Clams between 11 mm and 19 mm were dissected occasionally when the target size class was not met completely. Clams were measured for shell length with digital calipers to the nearest 0.01 mm prior to dissection. Ctenidia were squash mounted and examined under 100X magnification light microscopy (Morton 1977, Britton & Morton 1982). Developmental stages were determined based on the descriptions from Kraemer & Galloway (1986). Because these data were determined to be distributed nonnormally (Anderson-Darling normality test), they were [log.sub.10] transformed and analyzed by a 2-way ANOVA of site by date. Pairwise differences were determined with a Tukey HSD post hoc analysis. Mean values and standard error with sample size are reported. All statistical analyses were performed using SAS 9.2 (SAS Institute, Inc., Cary, NC) and Minitab 15.1 (Minitab, Inc., State College, PA).

RESULTS

Environmental Conditions

At all sites, temperatures were less than 8.0[degrees]C on May 11, with the greatest increase in temperature from June 16-28 (Fig. 1). Seasonal high temperatures were recorded at each site on July 20. A temporary decrease in temperatures on August 30 was associated with a cold front that passed through the Tahoe basin at that time. Temperatures were significantly different over dates (P < 0.0001) but not sites (P = 0.659). TOC concentrations were not significantly different among sites (P = 0.549). Mean concentrations ([+ or -]SE) across all dates (n = 10) at each site were 10.7 [+ or -] 0.5 mg/L (LS5), 10.7 [+ or -] 0.4 mg/L (MB5), 10.9 [+ or -] 0.5 mg/L (NV5), and 10.7 [+ or -] 0.5 mg/L (NV20). There was a significant site-by-date interaction in SPOM (P < 0.0001). A Tukey post hoc analysis determined that LS5 (6.8 [+ or -] 3.3 [micro]g/mg) and NV20 (6.1 [+ or -] 4.4 [micro]g/mg) had greater concentrations of SPOM than MB5 (4.6 [+ or -] 2.9 [micro]g/mg) and NV5 (3.6 [+ or -] 1.1 [micro]g/mg) during the season (Fig. 2).

Reproductive Activity

A total of 1,875 clams were dissected to determine their reproductive status and activity throughout the course of the sampling period. The mean shell length at each site during the entire sampling period was 13.68 [+ or -] 1.3 mm (LS5, n = 461), 13.33 [+ or -] 0.7 mm (MB5, n = 479), 13.91 [+ or -] 1.0 mm (NV5, n = 478), and 13.74 [+ or -] 1.2 mm (NV20, n = 457). Eggs were present in the demibranches on all sampling dates from May 11 to November 5 (Fig. 3). Egg abundances observed had a significant site-by-date interaction (P < 0.0001), and a Tukey post hoc analysis determined that the greatest abundance occurred on August 30. Veligers were detected in the middle to end of summer and occurred in low abundance on August 16, and were in high abundance on August 30 and September 13. These sampling dates were +27, +41, and +55 days after the critical temperature threshold needed to initiate a spawning of brooding veligers (King et al. 1986, Kraemer & Galloway 1986). There was a significant site-by-date interaction of brooding veliger abundance, and a Tukey post hoc analysis showed that August 30, September 13, and October 8 had the greatest abundance of veligers present, and the veliger abundance at shallow locations was significantly greater than NV20 (P < 0.0001). Across all 3 shallow sites, there were similar levels of reproductive effort, with a mean veliger abundance per clam ([+ or -]SE) of 10 [+ or -] 2 (n = 603), with ranges of 286 [+ or -] 28 (n = 25 for clams with [greater than or equal to ] 100 veligers) and 20 [+ or -] 2 (n = 78 for clams with <100 veligers), and 498 clams had no veligers present in samples from mid August through early November. NV20 had a mean abundance of 3 [+ or -] 1 veligers across 4 clams, with 196 clams having no veligers present in samples during the same period

[FIGURE 1 OMITTED]

Population Structure

Overall population abundance was significantly different by site over all sampling dates (P = 0.0013), with abundance at NV20 (2,541 [+ or -] 291 clams/[m.sup.2]) significantly greater than the shallow sites (Fig. 4). The distribution of C. fluminea was heterogeneous along the bottom at each site. Across sites for all sampling dates, there was a significant difference in the number of grabs obtained to meet the needs of dissection (P = 0.0014), with LS5 requiring the greatest number of samples over the dates (9 [+ or -] 3 grabs per date), MB5 and NV5 requiring fewer but nearly equal numbers of grabs (7 [+ or -] 2 and 7 [+ or -] 1 grabs per date, respectively), and NV20 requiring the fewest (5 [+ or -] 2 grabs per date, n = 12; SD is noted because SE values were less than 1). Size class distribution of C. fluminea by site suggests differences in population structure (Fig. 4). Size class distributions in LS5 were variable, but no one size class (or group of size classes) dominated the population structure throughout the sampling season. Size classes between 13 mm and 17 mm represented a majority of the populations in MB5, with clams occasionally reaching a shell length of 22 mm. Shell lengths of [less than or equal to] 4 mm were absent from these samplings. At NV5, the [less than or equal to] 4-mm size class was present in all samplings with very low presence during June 16 and November 5. The 13-17 mm-size class was large throughout the sampling dates, and clams disappeared from the population after 22 mm. The [less than or equal to] 4-mm size class at NV20 was present on June 16 and September 13. For a majority of the other samplings, this size class was completely absent, with a minimal presence on August 2, October 8, and November 5. As in the other locations, the largest size class was the 13-17-mm group.

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

DISCUSSION

In Lake Tahoe, C. fluminea in Lake Tahoe is univoltine, with reproduction in the late summer and low abundance of brooding veligers. There was a longer than expected delay between threshold temperatures for required reproduction based on previously published literature and empirical observations of brooding veligers made during dissections. Given that oogenesis occurs independent of temperature (Kraemer & Galloway 1986), we expected eggs to be present during all dissections. Because spermatogenesis and fertilization require minimum temperature thresholds to be met (10.0[degrees]C and 14.0[degrees]C, respectively), brooding veligers should not have been present until temperatures were at least 14[degrees]C for 10 consecutive degree-days (Kraemer & Galloway 1986). Temperatures across all shallow sampling sites reached this threshold by July 20, with a mean of 19.7 [+ or -] 0.4[degrees]C. A typical cycle of initial fertilization, larval maturity, to release of veligers is 6-14 days (Kraemer & Galloway 1986), with release occurring at least 16.0[degrees]C. In other systems, C. fluminea are observed to be bivoltine, with the first spawn occurring in late spring to early summer, and resuming in late summer. This pattern has been attributed to metabolic declines resulting from temperature increases greater than 27.5[degrees]C (Aldridge & McMahon 1978, M outhon 2001a). When spawning did occur in Lake Tahoe after a 4-wk delay, the overall abundance of veligers observed in the shallow sites (10 [+ or -] 2 veligers per clam) was much lower than the veliger abundance observed in more productive reservoir or riverine ecosystems. In these ecosystems, veliger reproductive efforts range from 588 to 735/clam per day in spring and fall (Aldridge & McMahon 1978) and 1,800 to 1,200/clam per day from late June and early October, respectively (Doherty et al. 1987). Recent studies have shown that Lake Tahoe's surface waters are warming at a faster rate than ambient air temperatures (Schneider et al. 2009, Coats 2010). In the future, this increase in water temperatures may expand the spawning potential of C. fluminea to an earlier initiation of reproductive development, and a longer fertilization and release period. It is unlikely, however, that a bivoltine spawning event will occur in Lake Tahoe because current temperature warming forecasts for the nearshore do not suggest an increase in temperature that would stop and reinitiate spawning, as found in warmer ecosystems. Alternatively, warming of the lake in the winter prior to the spawning cycle could enhance the reproductive success of C. fluminea (Weitere et al. 2009).

[FIGURE 4 OMITTED]

In other systems, food availability has been observed to be a significant contributor to spawning events of C. fluminea to meet the energetic demand of brooding (Mouthon 2001b). Corbicula fluminea brood veligers within the inner demibranches of the gills, which have secretory cells believed to provide nutrients to developing embryos (Britton & Morton 1982, Doherty et al. 1987). Although other studies reported chlorophyll a concentrations in systems with successful C. fluminea populations ranging from 3 to 100 [micro]g/L (Cohen et al. 1984, Mouthon 2001b, Mouthon & Parghentanian 2004), chlorophyll a concentrations in Lake Tahoe range from 0.5-1.5 [micro]g/L (TERC 2010). These low concentrations could limit C. fluminea growth and could reduce nourishment for brooding embryos. TOC at the water-substrate interface suggests similarly low food concentrations from this source. Although there were significant site-by-date differences for SPOM, overall reproductive effort was not significantly different among the sites, suggesting that variable concentrations of SPOM and TOC are not predictors of the fecundity of C. fluminea in Lake Tahoe. Further investigation of food availability--in particular, food quality--is needed to understand its role in Lake Tahoe clam reproductive effort with respect to water temperature.

In determining the similarities, if any, of reproductive effort between the shallow- and deep-water populations, an interesting observation is the low count of veligers seen in dissections from NV20, the deeper water site. Veligers were found on only 1 sampling date (August 30), with just 13 veligers seen in 4 clams. However, this site has the highest overall abundance among sites, with significant increases in observed abundance in the late summer. Population size structure at this site indicated an increase in abundance is toward the larger size classes (>13 mm) rather than recruitment of juveniles (<4 mm; Fig. 4). This suggests that deep-water populations are not reproductively active, and therefore are potentially a sink of clams rather than a source. If this is the case, clams would have had to be transported from the shallow depths to these deeper populations. Movement of clams to this deeper region may occur in 2 ways. One documented means of dispersal for C. fluminea is via floatation. Prezant and Chalermwat (1984) found that clams up to 14 mm, when exposed to a current of 10-20 cm/sec, would push off the substrate with their foot while extending both siphons. They excrete a long mucus thread that allows them to be lifted and carried in the water column until the current subsides. This current is typically not found in the nearshore of lakes. Another possibility is that wind-driven waves creating high-energy turbulence may transport clams from shallow depths to deeper locations. Redjah et al. (2010) found that the clam Mya arenaria, up to 20 mm, was displaced when subjected to turbulence in a level experimental flume with a high wave-current flow. In addition, in a sandy substrate similar to the NV5 and NV20 sampling sites, St-Onge and Miron (2007) found that between 40-90% of M. arenaria were eroded (transported) at stream velocities of 29-35 cm/s. With an approximate horizontal distance of 60 m between the 5-m and 20-m depth at Nevada Beach, an estimated slope of 18 deg, and documented populations of clams at 10 m and 15 m (unpublished samplings for 2008 and 2009), it is conceivable that high-energy turbulence resulting from internal lake currents and other physical waves could transport both juvenile dispersers and adult clams along the slope to deeper depths.

Throughout the 2010 sampling period, the juvenile size class (<4 mm) appeared sporadically across all sites and was probably a result of carryover from reproduction in 2009. Unlike other systems that show a pyramid-shape size class population structure, with less than 4 mm as the dominating the population (Hall 1984, Mouthon & Parghentanian 2004), the Lake Tahoe population contained more individuals in the 10-17 mm size classes, with a sharp decline in abundance of larger individuals in the range of 19-23 mm. Joy (1985) reported no shell growth for C. fluminea for water temperatures between 0[degrees]C and 13.0[degrees]C. Given that newly released veligers are 0.2 mm, and depending on the previous season's release period, it is conceivable that the 2009 spawn would appear as a new size class the following midsummer 2010. Temperatures in this study were less than 13.0[degrees]C by November; therefore, juveniles spawned in the 2010 season would likely not experience shell growth until May 2011 or June 2011.

ACKNOWLEDGMENTS

Gratitude is acknowledged to the anonymous reviewers whose comments enhanced this paper. In addition, we gratefully acknowledge funding provided by the Nevada Division of State Lands and the Southern Nevada Public Lands Management Act to S. C., M. W., G. S., and J. E. R. Invaluable field and laboratory support was provided by members of the University of Nevada, Reno, Aquatic Ecosystems Laboratory (Joseph Sullivan, Rob Bolduc, Christine Ngai, John Umek, Jessica Rasmussen, Robert Barnes, and Alex Denton) and the University of California, Davis, Tahoe Environmental Research Center (Raph Townsend, Katie Webb). The support of Jim Moore of California Fish and Game in assisting our understanding of the gonadal structures of bivalves is greatly appreciated. The review of dissection photographs by Marvin Galloway, Francis Parchas, and David Aldridge were an essential component of this study. Participants of the 2009 Tahoe Baikal Institute's Summer Environmental Exchange were instrumental in refining the preliminary methodology for this study.

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MARIANNE E. DENTON, (1)* SUDEEP CHANDRA, (1) MARION E. WITTMANN, (3)([dagger]) JOHN REUTER (3) AND JEFFREY G. BAGULEY (2)

(1) Aquatic Ecosystems Analysis Laboratory, Department of Natural Resources and Environmental Science, University of Nevada, 1664 N. Virginia Street, MS 186, Reno, NV, 89512; (2) Department of Biology, University of Nevada, 1664 N. Virginia Street, MS 314, Reno, NV 89557; (3) Tahoe Environmental Research Center, University of California, One Shields Avenue, Davis, CA, 95616

* Corresponding author. E-mail: mariannedenton@sbcglobal.net

([dagger]) Current address: Department of Biological Sciences, University of Notre Dame. Galvin Life Sciences Building, Notre Dame, IN 46556

DOI: 10.2983/035.031.0118
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