Stable oxygen and carbon isotope profiles in an invasive bivalve (Corbicula fluminea) in North Carolina watersheds

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Geochimica et Cosmochimica Acta 73 (2009) 3234–3247 www.elsevier.com/locate/gca

Stable oxygen and carbon isotope profiles in an invasive bivalve (Corbicula fluminea) in North Carolina watersheds John P. Bucci a,*, William J. Showers b, Bernie Genna b, Jay F. Levine a a

Aquatic Epidemiology and Conservation Laboratory, College of Veterinary Medicine, North Carolina State University, 4700 Hillsborough Street, Raleigh, NC 27606, USA b Department of Marine, Earth and Atmospheric Sciences, North Carolina State University, 2800 Faucette Drive, Jordan Hall, Raleigh, NC 27695, USA Received 16 May 2008; accepted in revised form 3 March 2009; available online 1 April 2009

Abstract The modern invasive bivalve Corbicula fluminea was collected in 2006 from three sites with different land uses located in a North Carolina River Basin. The primary objective was to describe the d18O and d13C profiles of C. fluminea shells under various land use conditions. An additional aim was to evaluate whether growth patterns of C. fluminea form seasonally. Annual shell growth patterns were measured from the umbo to the margin and co-varied with estimates of ambient water temperature, corresponding to seasonal variation. The C. fluminea growth patterns as translucent bands (slower growth) appeared to form during winter months and opaque bands (rapid growth) formed during summer. A mixed model analysis (ANOVA) showed a significant site level effect of d18O and d13C profiles examined among sites (F = 17.1; p = 0.003). A second model showed a borderline significant site effect among profiles with variability more pronounced at the urban site, Crabtree Creek (p = 0.085). Previous habitat assessment ratings and water chemistry measurements suggested that the urban site was more impacted by storm water runoff. Understanding d18O and d13CSHELL profiles and shell growth patterns of the invasive bivalve (C. fluminea) may help establish a framework for using these animals as biomonitors to record water temperature and nutrient pollution. Ó 2009 Elsevier Ltd. All rights reserved.

1. INTRODUCTION Monitoring the health of freshwater ecosystems has become increasingly important as land use changes supporting local economic and residential development contribute to increased nutrient input, release of domestic and industrial effluent, and storm water drainage (Howarth et al., 2002; Smith, 2003). As watersheds become adversely affected by poor water quality, bivalves serve as natural environmental sentinels of ecosystem health. Bivalve growth, survival and feeding patterns (Bucci et al., 2008) can serve as indicators of ecosystem integrity (Carlton and Geller, 1993; Baker et al., 1998; Gosling, 2003).

*

Corresponding author. E-mail address: [email protected] (J.P. Bucci).

0016-7037/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.gca.2009.03.023

The study of incremental growth of shells in relation to the location of seasonal growth lines (i.e., sclerochronology) depends on the fact that accretionary biogenic carbon is precipitated in oxygen isotope equilibrium with ambient water temperature (Urey, 1947; Clark, 1975; Grossman and Ku, 1986). To infer growth relationships, the sclerochronology technique has demonstrated that when either temperature or d18OWATER are constrained, precipitation of d18OSHELL values can be derived (Jones and Quitmyer, 1996; Stanczykowska and Lewandowski, 1996; Dettman et al., 1999; Dunca and Mutvei, 2001). Accretionary biogenic carbonate may be used to interpret annual variation in d18O and d13C values as seasonal changes in environmental conditions (Dettman and Lohmann, 1993; Patterson, 1998; Wurster and Patterson, 2001). Isotopic (d13C) signatures of accretionary carbon may be used to detect specific food sources (Tanaka et al., 1986; Patterson, 1999).

Stable oxygen and carbon isotope profiles in an invasive bivalve

As variations in shell d18O and d13C values are measured, a record of growth patterns and water quality conditions may signify ecosystem degradation (Surge et al., 2001; Scho¨ne et al., 2003; Dunca et al., 2005; Goewert et al., 2007). However, there is little stable isotope analysis of shell growth information on living invasive species such as Corbicula fluminea, which are ubiquitous across a range of water conditions. Native unionids are in decline throughout North America (Lydeard et al., 2004). Species have been extirpated from many areas, and their declining numbers heighten the need to select alternative species for environmental monitoring. The widespread invasive bivalve, C. fluminea is sympatric with many native bivalves, and abundant throughout the continental United States. As increased populations of invasive bivalves out compete native species for food and space, shell growth patterns may provide a useful means of monitoring habitat restoration efforts (Christian et al., 2004; Dettman et al., 2004; Weiss et al., 2002). The primary objective of the present study was to describe the d18O and d13C profiles of C. fluminea shells under various land use conditions. An additional aim was to evaluate whether growth patterns of C. fluminea form seasonally. Understanding d18O and d13CSHELL profiles and shell growth patterns of the invasive bivalve (C. fluminea) may help establish a framework for using these animals as biomonitors to record water temperature and nutrient pollution (Doherty, 1990; van der Schalie et al., 2001; Miller et al., 2005).

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size from second to third order and dominant land use type varied from agriculture, forested to urban (Table 1). The NRB is the third largest river basin in North Carolina and is entirely located within the state. Land use type designations were based on land use land cover (LULC) calculated percentages. The sum of the area of each land use category for the different sites within a watershed were compiled using ArcinfoÒ GIS software (ESRI, 2004). Hydrologic units were defined on a 1:250,000 scale. The aerial extent of each land use type was summed for each site and the percentage of land use of the total area of the watershed was calculated. Point source data and basin assessment reports for the Neuse River Basin were also considered (Tables 1 and 2; NCDWQ, 2002). 2.2. Estimated d18OWATER values The d18OWATER values of ambient water were not measured, although estimated d18OWATER values at each study site were derived using an empirical temperature-fractionation equation (Jones et al., 1983; Dettman et al., 1999). Specifically, the Grossman and Ku (Grossman and Ku, 1986) equation was used to compare d18OWATER fluctuation across seasons with estimated water temperature (Tw °C) given measured d18OSHELL values. This equation has traditionally been used to evaluate the oxygen equilibrium relationship between estimated d18OSHELL values and water temperature, given measured d18OWATER values.

2. METHODS 2.1. Site and shell specimens Three live C. fluminea bivalve specimens of similar size class (15–20 mm) were collected in the spring of 2006 from sites in three different watersheds in the Neuse River Basin (NRB) (Fig. 1). The sites where the bivalve specimens were collected included creeks in an agricultural (Bear Creek; N 35°160 2900 W 77°470 4000 ), urban (Crabtree Creek; N 35° 490 7300 , W 78° 370 8600 ), and forested (Marks Creek; N 35° 420 3600 , W 78° 250 9500 ) land use type. The creeks ranged in

Table 1 Size and percent land use land cover (LULC) calculated within the watersheds for each site. Land use

Marks Creek

Bear Creek

Crabtree Creek

Size (sq. km) Urban Agricultural Woody/mixed Herbaceous Water Wetlands

74 2 28 63 0.8 0.8 4

153 3 67 24 0.7 0.7 5

240 30 1 55 11 0.9 1

Fig. 1. Study sites are marked by a black bulls-eye in the Neuse River Basin, North Carolina. Crabtree Ck = Urban; Marks Ck = Forested; Bear Ck = Agricultural. Small circles symbolize point sources.

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J.P. Bucci et al. / Geochimica et Cosmochimica Acta 73 (2009) 3234–3247

Table 2 Point and non-point sources proximal to study sites. NPDES = National pollutant discharge elimination system. Sites

NPDES large

NPDES small

Farm operations

Total

Bear Creek Marks Creek Crabtree Creek

0 0 1

0 1 10

14 0 3

14 1 14

Estimated water temperature (Tw °C) for each watershed, which closely tracks air temperature, was calculated from weekly averages of ambient air temperatures (Patterson, 1998). Air temperatures were measured at state operated weather stations proximal to bivalve collection sites (Scho¨ne et al., 2004). Air temperature data was used in the relationship between estimated water temperature, d18OWATER and aragonite d18OSHELL values across the life of the specimens: Results were given relative to Vienna Pee Dee Belemnite (VPDB) standard.
T w C ¼ 20:6  4:34 d18 OSHELL  d18 OWATER ð1Þ where d18OSHELL is the d18O (VPDB) of aragonitic shell (average value of the three specimens) and d18OWATER is the d18O value of the estimated water values. To generate a time chronology, each d18OSHELL value was consecutive in order of sample position and superimposed across a time scale. To align d18OSHELL values with estimated d18OWATER values, measured d18OSHELL values were assigned dates to individual measurement points by anchoring the increments of growth at or near the time of collection. The guide used for assignment of dates was the known location of harvest date of the shell related to the growth lines observed visually.

2.3. Micro-mill technique Corbicula fluminea shells are predominantly composed of biogenic aragonite material (Counts and Prezant, 1982; Fritz et al., 1990). Shell material was prepared for processing by mechanically removing the periostracum layer and only the prismatic layer was sampled (0.5 mm depth) along growth lines (Fig. 2). Shell growth record was constructed by sampling the outer prismatic layer and analyzing the carbonate component for d13C and d18O (Lowenstam and Weiner, 1989). The right valve from each organism was mounted to a computer-controlled micromilling stage. The Corbicula valves were particularly thin (0.7 mm). Each valve was homogenously sanded down to the outer prismatic layer, from the umbo to the ventral margin. A high-precision instrument consisting of a hand-held dental drill (carbide 0.6 lm) bit mounted under a binocular microscope was used to serial drill samples along the maximum growth axis, yielding 14–20 individual samples across 20 mm of shell growth. Samples were taken every 1–2 mm from the growing edge to the umbo. This method was a modification of previous micromill techniques (Wurster et al., 1999; Dettman and Lohmann, 1995). The velocity of the bit was controlled to prevent any alteration of the carbonate material during the sampling process. Care was taken to avoid mixing layers of carbonate of different age and mixing between the outer prismatic and inner nacreous layers. 2.4. Stable isotopes Carbonate samples were analyzed for d18O and d13C values. Carbonate powder (minimum sample mass was 20 lg) from each drilled sample was vacuum roasted for 1 h at 220 °C to remove any organic contaminates.

A Mechanically removed periostracum and outer prismatic layer before serial drill sampling

1 mm

B Outer Prismatic layer Nacreous layer

Umbo

Fig. 2. (A) Top view of Corbicula fluminea sampled from umbo to end of shell. (B) Composite photograph of shell cross section (not actual sample) illustrating translucent and opaque banding. Outer Prismatic layer Nacreous layer Umbo B.

Stable oxygen and carbon isotope profiles in an invasive bivalve

The samples were then reacted with 100% orthophosphoric acid in a Kiel Autocarbonate device (Thermoquest Finnegan MAT, Bremen, Germany) and the resultant CO2 gas is cryogenically purified and analyzed for d18O and d13C in a MAT 251 isotope ratio mass spectrometer (Thermoquest Finnigan MAT, Bremen, Germany). The isotope ratio results were expressed in standard delta (d) notation versus the VPDB standard where: 

 d18 O ¼ 18 O=16 O sample=ð18 O=16 OÞstandard  1  103 & ð2Þ Samples were run against an internal laboratory and external carbonate standards (NBS-18, 19, and 20) for isotopic analysis. Isotopic standard reproducibility was ±0.03 for d13C, and ±0.05 for d18O, during the period the shells were analyzed for isotopic analysis.

30

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2.5. Annual growth rate estimation The basis for sclerochronology involves the ability to identify shell growth increments and verify their annual periodicity. Temperature is considered a major factor controlling metabolic rates of bivalves, and hence shell growth rates (Claassen, 1998). If shell growth increments record the ambient water temperature conditions at or close to the time of collection, they can be used to estimate growth rates (Dettman et al., 1999; Goewert et al., 2007). Shell growth rates were calculated from samples (1 to 2 mm resolution) of shell deposition along the axis of growth and modeled after the technique used by Jones and Quitmyer (1996). Translucent and opaque refers to shell properties revealed using transmitted light, whereas dark versus light refers to shell growth patterns under reflected light. Low winter temperatures can inhibit growth, which produce a visible trans-

A

25

-2 -3 -4

20

10

-7

OWATER

-6

18

TwºC

-5 15

-8 5 -9 0

Bear Creek -5 30

B

25

-10 -11 -2 -3 -4

20

10

-7

OWATER

-6

18

TwºC

-5 15

-8 5 -9 0

-10

Marks Creek -5 30

C

25

-11 -2 -3 -4

20

10

-7

OWATER

-6

18

TwºC

-5 15

-8 5 -9 0

Crabtree Creek

-10 -11

5/ 1/ 04 7/ 1/ 04 9/ 1/ 0 11 4 /1 /0 4 1/ 1/ 05 3/ 1/ 05 5/ 1/ 05 7/ 1/ 05 9/ 1/ 0 11 5 /1 /0 5 1/ 1/ 06 3/ 1/ 06 5/ 1/ 06 7/ 1/ 06

-5

Fig. 3. Ambient water d18OWATER as estimated by Eq. (1) plotted across time. Triangles indicate Tw °C and diamonds d18OWATER.

J.P. Bucci et al. / Geochimica et Cosmochimica Acta 73 (2009) 3234–3247

2005

-2

Collected 5.18.06

-3

2004

-2

Direction of Growth

-3 -4

-5

-5

-6

-6

-7

-7

-8

-8

-9

-9

-10

-10

-11

-11

-12

-12

13

-4

18

BCk-1

2

-13

1

-14 -2

-3

-3

-4

-4

-5

-5

-6

-6

-7

-7

-8

-8

-9

-9

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-11

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-12

13

-14 -2

18

O (‰ VPDB)

-13

-13

BCk-2

-13

1.5

-14 -2

-14 -2

-3

-3

-4

-4

-5

-5

-6

-6

-7

-7

-8

-8 -9 -10

-11

-11

-12

-12

13

-9 -10

18

O (‰ VPDB)

C (‰ VPDB)

O (‰ VPDB)

provide an estimate of annual growth rate. A 2& (±0.5&) change in d18OSHELL values is the presumed seasonal range allowing for an annual growth rate comparison between watersheds (Dettman et al., 1999). Growth rates

C (‰ VPDB)

lucent growth increment or dark band during the coldest season (Jones and Quitmyer, 1996). Annual growth bands were observed along the distance to the end of shell axis along with the isotopic analyses to

C (‰ VPDB)

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-13

BCk-3

2

-13

1

-14

-14 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

Margin

Distance from End of Shell (mm)

Umbo

Fig. 4. The d18O and d13C profiles of three individual Corbicula fluminea sampled from the agricultural site (Bear Creek). Triangles represent d18O and filled circles represent d13C values. Gray bars at the bottom of each plot indicate the location of prominent translucent growth lines.

Stable oxygen and carbon isotope profiles in an invasive bivalve

were estimated by counting back observed growth bands in millimeters divided by the number of isotopic samples from the date the animal was collected. 2.6. Statistical analyses Based on our initial hypothesis to test whether land use sites differed in mean d18OSHELL and d13CSHELL values, a mixed model (ANOVA) analysis was used (Model 1) where the difference (d18O to d13C) was the response, with a fixed location effect and a random, nested effect due to the individual bivalves (Singer, 1998; SAS, 2002). Additionally, we used a multiple comparison procedure (i.e., Tukey’s), which compared the location means to test the significance of the differences between sites. For each of the nine sample bivalves (three at each location), a second mixed model used the variance of the differences (d18O to d13C) as the response against land use site. A single factor ANOVA was used to test differences between the annual growth rates as estimated by d18O and d13C profiles and land use type (Scheiner and Gurevich, 2001). 3. RESULTS 3.1. Temperature and d18OWATER For all three sites, variation between estimated d18OWATER values and approximate water temperature was observed seasonally. Measured d18OSHELL values were used in conjunction with approximated temperature to determine estimated d18OWATER values. A graph of the d18OWATER values as calculated by Eq. (1) was plotted across a timeline for each specimen (Fig. 3). Locations of seasonal growth bands were estimated, allowing for the assignment of calendar years. The Bear Creek temperature ranged from 3 to 27 °C and d18OWATER varied from 9.4 to 3.6&. Marks Creek Tw °C ranged from 3 to 26 °C and d18OWATER varied from 9 to 4.2&. In April of 2005, there was an observed 0.6& shift in d18OWATER values from 7.4 to 6.8&. Values from Crabtree Creek Tw °C ranged from 1 to 27 °C and water d18O varied from 10 to 3.2&. 3.2. Profiles of d18OSHELL and d13CSHELL values The relationship between the d18OSHELL and d13CSHELL values for the 9 C. fluminea specimens was evaluated along the maximum growth line from the umbo to the shell margin. The values for all samples averaged a 2 to 3& range across the d18O and d13C values measured (Figs. 4–6). Although departures from this range were evident, most samples showed a sinusoidal pattern with seasonal variability. Results of Model (1) showed a significant site level effect among d18O and d13C profiles between land use categories (F = 17.1; p = 0.003) (Table 3). However, a post hoc multiple comparisons test (Tukey’s) showed that none of the three comparisons were significantly different at the 0.05 level, possibly due to low power associated with the small sample size. For the second model, the site level effect was

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marginally significant (p = 0.085). This may seem counter informative to the initial model, which has additional randomness embedded, compared to using only the mean differences in the mixed model. A post hoc test for Model (2) was used and the variances of the three sites showed that Crabtree Creek was more variable (0.99), compared to Bear Creek (0.25) and Marks Creek (0.34). So, the urban site had on average more variance than the other two, even though it was not significantly greater at the 0.05 level. The Crabtree Creek d18O and d13CSHELL profiles showed a seasonal pattern of less than 2 years of growth with more variability than the agricultural and forested samples. The Crabtree Creek d18O values ranged from 7.9 to 3.4& and the d13C values ranged from 12.3 to 6.9& (Fig. 6). The d13C values from CCk2 were inconsistent with d18O values between 5.1 mm and 9.8 mm from the margin to the umbo. The CCk3 d13C profile showed a departure from the d18O trend at approximately 12.2 mm from the growing edge. Also, there was a departure between d18O and d13C profiles at 5 mm for sample CCk1. Bear Creek d18O and d13C profiles showed a seasonal pattern of growth for approximately 2 years (Fig. 4). The d18O values ranged from 6.5 to 3.7& and the d13C values showed a higher degree of variability from 12.2 to 8.5&. In Marks Creek, less variability was observed between d18O and d13C values for MCk1 and MCk3 with more variability observed in MCk2 compared to MCk1 and MCk3 (Fig. 5). The d18O values from Marks Creek ranged from 6.9 to 4.0& and the d13CSHELL values ranged from 13.3 to 10&. A plateau with minor variation from August to September 2005 was observed for MCk2 with an average value of 4.5&. 3.3. Growth rates by site Considering the d18O and d13CSHELL profiles and seasonal variability, growth rates per year were estimated at all sites (Figs. 4–6). The calculated mean annual growth rates were not significantly different, although they were higher among agricultural (Bear Creek, 8.7 mmyr), and urban (Crabtree Creek, 8.2 mmyr) compared to forested (Marks Creek, 6.5 mmyr) sites (F = 3.4; p = 0.17; Table 4). Two yearly cycles were observed in both the d18O and d13C profiles for two of the Bear Creek samples and 3 yearly cycles were observed for two of the Marks Creek samples (Figs. 4 and 5). Crabtree Creek d18O and d13C profiles displayed 2 yearly cycles (Fig. 6). The estimated average age per sample was higher in the forested (3.5 yr) compared to the urban (2 yr) and agricultural (1.5 yr) site. The average length for the urban (16.4 mm) samples was longer compared to the agricultural (15.7 mm) and forested (15.4 mm) samples. 4. DISCUSSION 4.1. Temperature and d18OWATER The d18O of the unionid shell is controlled by the temperature as well as d18OWATER values in which it lives

J.P. Bucci et al. / Geochimica et Cosmochimica Acta 73 (2009) 3234–3247 2005

2004

-2

Direction of growth

-3

Collected 3-22-06

-4

-4

-5

-5

-6

-6

-7

-7

-8

-8 -9 -10

-11

-11

-12

-12

13

-9 -10

18

MCk-1

3

2

-13

1

-14 -2

-3

-3

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-7

-7

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-8

-9

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-11

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-12

13

-14 -2

18

O (‰ VPDB)

-13

-13

3

2

1

MCk-2

-13

-14 -2

-14 -2

-3

-3

-4

-4

-5

-5

-6

-6

-7

-7

-8

-8 -9 -10

-11

-11

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-12

13

-9 -10

18

O (‰ VPDB)

C (‰ VPDB)

O (‰ VPDB)

-3

2006

C (‰ VPDB)

-2

C (‰ VPDB)

3240

-13 -14

MCk-3

1.5

-13

-14 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18

Distance from End of Shell (mm) Fig. 5. The d18O and d13C profil es of three individual Corbicula fluminea sampled from the forested site (Marks Creek). Triangles represent d18O and filled circles represent d13C values. Gray bars at the bottom of each plot indicate the location of prominent translucent growth lines.

(Thebault et al., 2007; Dettman et al., 1999; Schone et al., 2004), where cold temperature corresponds to higher d18O values and warm temperature corresponds to lower d18O

values (Jones and Quitmyer, 1996). We estimated d18OWA18 TER values seasonally from measured d OSHELL values and air temperature documented in three North Carolina

Stable oxygen and carbon isotope profiles in an invasive bivalve 2005

-2

Direction of growth

-3

-3

-4

-4

-5

-5

-6 -7

-6

Collected 6-17-06

-7 -8

-9

-9

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13

-8

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2

1

CCk-1

-14 -2

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CCk-2 -14 -2

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O (‰ VPDB)

-14 -2

-13 -14

2

1

CCk-3

C (‰ VPDB)

O (‰ VPDB)

-14 -2

-13

C (‰ VPDB)

-13

13

O (‰ VPDB)

2004

C (‰ VPDB)

-2 2006

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-13

-14 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 Margin Umbo Distance from End of Shell (mm)

Fig. 6. The d18O and d13C profiles of three individual Corbicula fluminea sampled from the urban site (Crabtree Creek). Triangles represent d18O and filled circles represent d13C values. Gray bars indicate location of prominent translucent bands.

streams with different land use conditions using an equilibrium fractionation equation (Grossman and Ku, 1986). The study results support the claim that isotope values of arago-

nite sampled from a modern freshwater bivalve may be influenced by winter/summer temperature variation (Wurster and Patterson, 2001).

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J.P. Bucci et al. / Geochimica et Cosmochimica Acta 73 (2009) 3234–3247

Table 3 The isotopic data (d13C and d18O profiles) for C. fluminea collected from each study site and used in the mixed model ANOVA. EOS = End of shell. Sample

EOS (mm)

d13C

d18O

Sample

EOS (mm)

d13C

d18O

Sample

EOS (mm)

d13C

d18O

BCk1-1 BCk1-2 BCk1-3 BCk1-4 BCk1-5 BCk1-6 BCk1-7 BCk1-8 BCk1-9 BCk110 BCk111 BCk111 BCk112 BCk113 BCk114 BCk115 BCk116 BCk117 BCk118 BCk21 BCk22 BCk23 BCk24 BCk25 BCk26 BCk27 BCk28 BCk29 BCk210 BCk211 BCk212 BCk213 BCk214 BCk215 BCk216 BCk217 BCk31 BCk32 BCk33 BCk34 BCk35 BCk36 BCk37 BCk38 BCk39 BCk310 BCk311 BCk312 BCk313 BCk314 BCk315 BCk316

1 1.5 1.8 2.2 2.8 3.6 4.2 5.2 6.2 7.4 8.4 9.5 10.6 11.2 12 12.8 14 14.7 15.7 1 2.3 3 4.4 4.9 5.5 6.5 7.8 8.4 9 9.6 10.3 10.7 11.2 12.1 13.9 15 0.8 2.2 3 4 5 6 7.4 8.6 9.8 10.8 11.9 13 14.2 15 16 16.5

10.0 10.9 12.0 10.6 11.8 10.7 12.1 9.6 11.0 10.9 11.0 11.0 11.9 10.7 11.6 9.4 10.5 10.3 10.5 11.7 11.3 11.1 9.8 8.7 10.1 11.2 10.7 11.3 12.2 11.6 11.7 11.7 12.3 11.9 11.1 10.3 9.7 11.8 11.3 9.5 10.3 11.4 11.5 11.1 11.1 11.1 10.6 9.8 9.7 10.1 10.4 10.3

4.2 5.0 6.5 4.1 5.5 5.7 5.9 3.7 4.9 5.6 5.6 5.5 5.9 5.2 5.2 3.8 5.4 5.0 5.0 5.8 5.9 6.0 4.7 4.1 4.5 5.2 6.2 6.0 6.3 6.0 6.0 5.4 5.6 4.8 5.0 4.9 4.1 5.9 5.8 4.3 5.8 6.2 6.2 5.6 5.5 5.4 5.0 4.8 4.8 4.9 5.4 5.4

MCk11 MCk12 MCk13 MCk14 MCk15 MCk16 MCk17 MCk18 MCk19 MCk110 MCk111 MCk112 MCk113 MCk114 MCk115 MCk116 MCk14 MCk117 MCk118 MCk21 MCk22 MCk23 MCk24 MCk25 MCk26 MCk27 MCk28 MCk29 MCk210 MCk211 MCk212 MCk213 MCk214 MCk215 MCk216 MCk31 MCk32 MCk33 MCk34 MCk35 MCk36 MCk37 MCk38 MCk39 MCk310 MCk311 MCk312

1 2 3 4 4.5 5.5 6 7 7.5 8 9 10 11 13 14 15 15.7 16.5 17 1 1.8 2.7 3.2 4 5 6 7 8 9 10 12 13 14.5 15.5 17 1 2 3 4.2 5.1 6 6.9 8.2 9.1 10 11 12.2

10.2 11.9 10.8 10.0 11.8 13.1 12.3 11.4 10.6 11.9 13.2 13.3 12.6 10.2 11.4 12.1 12.6 12.2 11.8 11.2 11.0 12.6 11.7 10.9 13.1 11.8 11.1 12.6 12.5 12.4 11.7 10.5 11.6 11.4 11.5 12.9 11.9 11.0 11.2 11.2 11.8 11.8 12.6 12.6 12.5 11.8 11.4

5.0 6.0 5.4 4.6 4.9 6.3 5.7 5.2 4.6 5.3 6.5 6.9 6.1 5.1 5.0 4.9 5.2 5.0 5.4 5.5 5.8 6.0 5.5 4.9 6.8 5.9 4.9 5.1 5.0 4.8 4.8 4.0 4.9 5.0 4.8 6.1 6.0 5.4 4.9 5.1 5.2 5.9 6.2 6.7 6.4 5.7 4.9

CCk11 CCk12 CCk13 CCk14 CCk15 CCk16 CCk17 CCk18 CCk19 CCk110 CCk111 CCk112 CCk113 CCk114 CCk115 CCk116 CCk117 CCk21 CCk22 CCk23 CCk24 CCk25 CCk26 CCk27 CCk28 CCk29 CCk210 CCk211 CCk212 CCk213 CCk214 CCk215 CCk216 CCk217 CCk218 CCk219 CCk31 CCk32 CCk33 CCk34 CCk35 CCk36 CCk37 CCk38 CCk39 CCk310 CCk311 CCk312 CCk313 CCk314 CCk315 CCk316

1 1.5 2 2.8 3.2 4.1 5 5.5 6.1 7 7.6 8.3 9.3 10.5 11.4 12.9 13.6 1 2 2.7 3.5 4.3 5 5.6 6.7 7.6 8.7 9.7 10.8 11.8 12.6 14.7 15.2 16.3 17.5 19 1 2 3 4.3 5 6 6.8 7.8 9 10 11.2 12.5 13.8 15 16 16.5

10.9 10.4 10.1 10.4 10.8 12.3 11.5 10.7 12.2 11.8 11.1 10.4 9.9 11.2 11.2 10.9 11.5 11.2 10.4 11.6 11.4 11.9 11.8 10.4 11.9 11.6 11.5 10.0 11.3 11.6 11.8 11.9 10.9 11.6 10.7 10.4 11.4 10.0 10.6 10.5 11.6 10.7 10.9 12.2 12.2 11.5 10.6 6.9 11.4 10.8 10.7 10.9

4.5 4.4 3.8 3.4 3.6 4.9 4.9 5.2 6.1 5.8 5.3 5.7 4.9 6.3 7.5 7.9 7.7 4.8 4.3 5.4 5.8 5.6 5.9 6.3 6.0 7.4 6.8 5.0 5.1 5.3 5.4 5.7 5.2 5.7 5.0 4.0 6.1 4.5 4.5 3.6 5.5 4.9 5.5 6.2 6.1 5.8 4.3 4.3 5.8 5.8 5.4 5.7

In Crabtree Creek, the fluctuation in response to temperature changes observed in d18OWATER values was higher (6.8&) compared to other two study sites and similar first order systems (Kendall and Coplen, 1998). Discharge from storm water runoff may have influenced temperature and d18OWATER values (Dettman et al., 2004). It is thought that

urban catchments experience more rapid discharge with rain events due to the higher percentage of impervious surfaces (Rose and Peters, 2001). Seasonal fluctuation in d18OWATER values from urban stream sites in North Carolina have been shown to vary from 4 to 6 & (Kendall and Coplen, 1998). Dettman et al. (1999) reported a 4.7& range in d18OWATER

Stable oxygen and carbon isotope profiles in an invasive bivalve Table 4 Mean annual shell growth rates (mmyr) of three C. fluminea individuals by site. Mean growth rate equals length of shell divided by observed yearly growth cycles. Average length (umbo to end of shell) is also calculated. Date collected

Agriculture Bear Creek

Urban Crabtree Creek

Forested Marks Creek

5-18-06 3-22-06 6-17-06

15.7/2 = 7.9 15/1.5 = 10 16.5/ 2 = 8.25 8.7 ± 1.1 15.7

13.6/2 = 6.8 19/2 = 9.5 16.5/2 = 8.25

17/3 = 5.7 17/3 = 5.7 12.2/ 1.5 = 8.1 6.5 ± 1.4 15.4

Mean (mmyr) Average length (mm)

8.2 ± 1.4 16.4

in a first order creek where the water temperature varied from 2 to 26 °C. Future measurements of temperature and d18OWATER values may explain this discrepancy. During early to mid July, Bear Creek d18OWATER values decreased approximately 1–1.5& lower than the previous point, although temperature values decreased as well (Fig. 3a). The USGS discharge data showed three discharge peaks of 400–590 cfs during this time period (USGS, 2005). Minor departures in estimated d18OWATER values may be explained by rainstorms and subsequent discharge events (Gat, 1987), which likely increase turbidity and the flow of nutrients through suspension. However, these explanations need further examination with consistent measurement of hydrological parameters such as discharge. The isotopic fractionation relationship described by Grossman and Ku (Grossman and Ku, 1986) has enabled scientists to evaluate ecologically based questions related to shell growth (Kaandorp et al., 2003; Ricken et al., 2003). However, continuous d18OWATER values are needed to examine these equilibrium relationships (Tevesz et al., 1996; Dunca et al., 2005). Regions that are affected by a combination of sources such as nutrient contamination and storm water runoff are considered variable mixers (Miles et al., 2000), and may influence d18O and d13CSHELL profiles. 4.2. Growth patterns In the present study, the consistency with which translucent bands corresponded with winter (at the highest d18O values recorded) and opaque bands with summer growth suggests that C. fluminea growth patterns vary with estimated d18OWATER values. Furthermore, C. fluminea growth patterns coincided with seasonal sinusoidal curves (Dettman and Lohmann, 1993); Negus, 1996). Prior sclerochronogical studies demonstrated that growth-band formation corresponds with ambient water temperature and d18OWATER values (Jones et al., 1983). Similar to results with freshwater bivalves by Dettman et al. (1999), C. fluminea d18O profiles depicted shifts in values of 2 to 3&, which were supported by both d18O of ambient water and d13CSHELL values (Figs. 2–4). The observed prominent growth-band formation supports previous studies that freshwater bivalve growth is

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markedly slower during colder temperatures (Jones et al., 1989; Anthony et al., 2001). Growth arrest lines (i.e., Haversine lines) were also observed in vertebrate bones during extended periods of arrested growth (Ogden, 1984). However, disturbance bands, which are considered different than annual lines, can occur with large storm events when surface water temperatures are reduced (Krantz et al., 1987; Negus, 1996). The C. fluminea growth pattern reflected those previously documented in freshwater unionids (Lampsilis cardium) from an Iowa River and from marine bivalves (M. mercenaria) collected from higher latitudes (Rhode Island, USA) (Peterson et al., 1985; Wurster and Patterson, 2001; Goewert et al., 2007). At higher latitudes, Joy (1985) found that C. fluminea cessate growth at water temperatures below 10 °C. Colder winter temperatures, common at higher latitudes are associated with translucent band increments and probably reflect periods of slower shell growth (Veinott and Cornett, 1996; Goodwin et al., 2001). 4.3. d18O and d13CSHELL profiles and land use Although growth-band formation appeared to vary seasonally, variability between d18O and d13CSHELL profiles at the urban site suggests that factors associated with land use water quality may have influenced results. Previous research has shown that consistency between these profiles may be less predictable since poor water quality (e.g., excess nitrogen input, turbidity, and dissolved oxygen) can have detrimental effects on shell growth (Rhoads and Morse, 1971; Dunca et al., 2005). Supporting the initial hypothesis, the results suggested that a site level effect exists between d18O and d13CSHELL profiles and sites with different land use conditions (Model 1). Model 2 showed that higher variability was observed in Crabtree Creek (0.99), even though this result was not statistically significant at the 0.05 level (p = 0.085). This lack of significance may be influenced by the small sample size (3 specimens per site). A larger sample may have revealed more of a differentiation among the three locations (Gillikin et al., 2005). However, more study is needed to examine whether C. fluminea d18O and d13CSHELL profiles collected from urban watersheds should be used as an indicator of ambient water temperature records both historically and in the future. An important driver of variation in isotopic composition of freshwater communities is nutrient pollution, which includes the anthropogenic influx of nitrogenous compounds (Allan, 1995). Previously measured water chemistry parameters measured across study sites from June 2000 to 2003 suggested that total nitrate as well as d15N values of nitrate were significantly higher in the agricultural compared to the urban and forested sites (p < 0.05) (Bucci, 2006). However, the apparent higher nitrate concentrations in ambient water may not have influenced the consistency in isotope profiles in the agricultural site. In the present study, the land use immediately surrounding the Marks Creek site was predominantly forested (Table 1). The Marks Creek site had ‘acceptable’ habitat quality ratings, lower nutrient inputs and turbidity with a higher diversity of fish (23 of 28 known species) (NCDENR, 2006). In comparison, a wide range of turbid-

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ity values has been observed in the watershed that includes the Crabtree Creek site and peak to chronic levels have frequently approached standard limits. The visible land cover at the Crabtree Creek site was predominantly commercial and received wastewater from the large urban center of Raleigh, North Carolina. Therefore, the role of nutrient loading and turbidity on d13C values may affect shell growth and explain the variability observed between d18OSHELL and d13CSHELL profiles in this site. However, our study would have benefited from a more complete set of water chemistry parameters (i.e., discharge, dissolved oxygen) needed to evaluate these relationships further. The isotopic variability between d18OSHELL and 13 d CSHELL profiles observed in our study may represent sensitivity in the pattern of carbonate secretion to shell metabolic and kinetic affects (Tanaka et al., 1986; Lorrain et al., 2004). These vital effects can produce variability between d18OSHELL and d13CSHELL profiles and have been suggested in studies of biogenic carbonate (von Grafenstein et al., 1999; McConnaughey, 2003). These fractionation effects are preserved in the carbonate material because precipitation of carbonate from dissolved inorganic carbon (DIC) is more rapid than equilibration with the surrounding fluid (Craig, 1953; Adkins et al., 2003). During ‘kinetic effects’, a proportion of ambient DIC is produced from molecular CO2, which is produced from hydroxylation and produces d13CSHELL values similar to DIC (Heikoop et al., 2000). Metabolic CO2 effects may also be an important factor controlling the d13CSHELL values of biologically precipitated carbonates (Veinott and Cornett, 1996; Furla et al., 2000). Although the isotopic composition of metabolic carbon may be modified by biologic processes, it is cited as a likely source of d13C depleted carbon in shells (Geist et al., 2005). Observable differences in the Crabtree Creek d13C profile to seasonal trends may be a result of the incorporation of metabolic CO2 that affect respiration, which preferentially adds or removes d13C and depletes CO2 from the inorganic carbon reservoir during calcification (Auclair et al., 2004). If the contribution of metabolic CO2 was negligible, kinetic effects may explain apparent variability between d18O and d13C profiles in Crabtree Creek. Isotopic records from aquatic organisms suggest that shell carbonate forms in equilibrium with the host water, with little biologic or vital effect on stable isotope fractionation (Grossman and Ku, 1986). 4.4. Shell growth rates The association between nutrient source input and the uptake by bivalve consumers has been previously documented (McClelland et al., 1997; McKinney et al., 2002; Gustafson et al., 2007). Bivalves are semi-infaunal consumers and changes in nutrient loading and food source quality (i.e., algal and particulate matter) may have affected C. fluminea growth rates (Bayne and Newell, 1983); Craig, 1994; Gosling, 2003). The estimated higher growth rates in the agricultural (8.7 ± 1.1 mmyr) and urban compared to the forested (8.2 ± 1.4 mmyr) (6.5 ± 1.4 mmyr) sites may be related to the higher nitrate values observed in the agricultural and urban watersheds.

If water quality is a predictor of suspended particulate food sources, then nutrient impacted watersheds may affect shell growth as previously shown in specimens of U. crassus from a eutrophicated River in Soodla, Estonia (Mutvei et al., 1996). Similarly, lower food source quality (i.e., suspended detritus) found in urbanized streams may affect macroinvertebrate growth (Tenore et al., 1982; Lenat and Crawford, 1994). The consumption of these sources may have produced the isotopic variability between d18O and d13C profiles in Crabtree Creek. Therefore, considering differences in nutrient input across sites, a potential link between shell growth rates and food quality is plausible (Fry and Allen, 2003). However, the degree of influence of food quality on bivalve growth rates continues to be debated (Christian et al., 2004; Kendall et al., 2001; Raikow and Hamilton, 2001). Another important factor to consider is how Corbicula fluminea compared to native species assimilate (i.e., pedal vs. filter) food particles in impacted watersheds (Boltovskoy et al., 1995; Hakencamp and Palmer, 1999). Baker and Levinton (Baker and Levinton, 2003) showed that the invasive bivalve, Dreissena polymorpha has the ability to preferentially select nutritious food particles regardless of high turbidity conditions. Thus, C. fluminea may possess an increased level of tolerance to poor water quality when exposed to higher turbidity and decreased food quality (Williams et al., 1993; Michener and Shell, 1994; Huxel et al., 2002; Cherry et al., 2005; Bucci et al., 2008). Although progress is being made, sclerochronology methods to reconstruct nutrient pollution history have yet to be proven effective for several species of bivalves. Future studies should examine higher resolution d18O and d13CSHELL values in C. fluminea in combination with tissue d15N and d13C values to reconstruct vital effects. Ideally, these studies should be long-term and prospective in design, with specific cohorts of sentinel animals being deployed with the concurrent collection of water quality data. ACKNOWLEDGMENTS This research was supported in part by a state governmental grant to the Stable Isotope Laboratory at North Carolina State University. The authors would like to thank Dr. Donna Surge, Ann Goewert and Tracy Fenger at the University of North Carolina, Chapel Hill for the use of their Sclerochronology laboratory as well as their insightful comments during manuscript preparation. We thank Dr. Dickey, Joy Smith and Jamila Mathias as well as Tony Szempruch for their valuable contributions.

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