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Aug 14, 2009 - southwest of the intersection of Red Run Boulevard and. Owings Mills Boulevard (Baltimore County, Maryland). This pond was chosen for its ...
Arch Environ Contam Toxicol (2010) 58:325–331 DOI 10.1007/s00244-009-9373-0

Lethal and Sublethal Effects of Embryonic and Larval Exposure of Hyla versicolor to Stormwater Pond Sediments Adrianne B. Brand Æ Joel W. Snodgrass Æ Matthew T. Gallagher Æ Ryan E. Casey Æ Robin Van Meter

Received: 6 January 2009 / Accepted: 27 July 2009 / Published online: 14 August 2009 Ó Springer Science+Business Media, LLC 2009

Abstract Stormwater ponds are common features of modern stormwater management practices. Stormwater ponds often retain standing water for extended periods of time, develop vegetative characteristics similar to natural wetlands, and attract wildlife. However, because stormwater ponds are designed to capture pollutants, wildlife that utilize ponds might be exposed to pollutants and suffer toxicological effects. To investigate the toxicity of stormwater pond sediments to Hyla versicolor, an anuran commonly found using retention ponds for breeding, we exposed embryos and larvae to sediments in laboratory microcosms. Exposure to pond sediments reduced survival of embryos by *50% but did not affect larval survival. Larvae exposed to stormwater pond sediment developed significantly faster ( x ¼ 39 days compared to 42 days; p = 0.005) and were significantly larger at metamorphosis ( x ¼ 0:49 g compared to 0.36 g; p \ 0.001) than controls that were exposed to clean sand. Substantial amounts (712– 2215 mg/l) of chloride leached from pond sediments into the water column of treatment microcosms; subsequently, survival of embryos was negatively correlated (r2 = 0.50; p \ 0.001) with water conductivity during development. A. B. Brand  J. W. Snodgrass (&)  M. T. Gallagher Department of Biological Sciences, Towson University, 8000 York Road, Towson, MD 21252, USA e-mail: [email protected] R. E. Casey Department of Chemistry, Towson University, 8000 York Road, Towson, MD, 21252 R. Van Meter Marine, Estuarine, and Environment Science Graduate Program, University of Maryland Baltimore County, Center for Urban Environmental Research & Education, Baltimore, MD 21250, USA

Our results, along with the limited number of other toxicological studies of stormwater ponds, suggest that road salt contributes to the degradation of stormwater pond habitat quality for amphibian reproduction and that future research should focus on understanding interactions among road salts and other pollutants and stressors characteristic of urban environments.

As urban and suburban areas continue to expand, resource managers must modify the landscape to decrease the impact of human presence on our environment. Proper stormwater and runoff management from impervious surfaces is paramount, as mismanagement can lead to degradation and pollution of downstream water bodies as well as local flooding and property damage (US EPA 1993). One of the major components of stormwater management schemes are stormwater ponds, which are built to catch and store runoff and the wide range of pollutants that accumulate on impervious surfaces (e.g., roads, parking lots, rooftops) such as metals, road salts, and polycyclic aromatic hydrocarbons (PAHs; Davis et al. 2001; Marsalek 2003; Pitt et al. 1995; Van Metre and Mahler 2003). Impervious surfaces decrease infiltration during rain or snow events, increasing surface runoff to receiving waters (Dunne and Leopold 1978; Hopkinson and Day 1980). Stormwater ponds are designed to detain and store runoff in order to remove pollutants and decrease the volume of water entering nearby streams, rivers, and wetlands after a storm event (Novotny 1995; US EPA 1993). These ponds are common features in the modern urban landscape and are often colonized by plants and other wildlife in the area (Bishop et al. 2000a, 2000b; Scher and Thiery 2005).

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However, wildlife that use stormwater ponds might be at risk of exposure to the pollutants that the ponds are designed to collect (Bishop et al. 2000a, 2000b; Campbell 1994). There are few studies on the toxicity of conditions in stormwater ponds, but wildlife that use the ponds are not always adversely affected (Bishop et al. 2000b; Casey et al. 2005; Karouna-Renier and Sparling 1997, 2001). Furthermore, the risk to wildlife might vary widely in a landscape, depending on pollutant inputs to ponds and accessibility by wildlife (Bishop et al. 2000a; Massal et al. 2007; Ostergaard et al. 2009; Simon et al. 2009). The use of stormwater ponds by wildlife is of concern for pond-breeding amphibians in particular. Pond-breeding amphibians gather at ponds and wetlands to mate and deposit their eggs, which hatch and develop in the aquatic environment until they metamorphose into terrestrial or semiaquatic juveniles. In fact, many species have been documented using stormwater ponds (Bascietto and Adams 1983; Bishop et al. 2000b; Ostergaard et al. 2009; Simon et al. 2009), but the ability of these ponds to serve as adequate habitats in maintaining local populations remains unclear. Moreover, the relative roles of breeding site degradation and loss of upland habitat on amphibian survival and distribution in suburban areas have received limited attention (Snodgrass et al. 2008). This study assesses the toxicity of stormwater pond sediments to embryonic and larval Gray Treefrogs (Hyla versicolor). We focused on H. versicolor because its abundance in stormwater ponds suggests an intermediate tolerance of pollutants that can accumulate in these ponds (Bishop et al. 2000a; Simon et al. 2009); Snodgrass et al. (2008) reported on a sensitive (Rana sylvatica) and a tolerant species (Bufo americanus) that experienced complete and no mortality, respectively, when exposed to sediment from a relatively polluted stormwater pond. Although a number of pollutants were detected in the sediments used by Snodgrass et al. (2008), they concluded that sodium chloride (NaCl) leached from pond sediments was most likely responsible for the lethal and sublethal effects they observed. Therefore, we expected H. versicolor to exhibit both lethal and sublethal responses to exposure to sediments from a relatively polluted pond and correlations among survival, sublethal effects, and Cl- concentrations in individual exposure bins.

Methods During the summer of 2007 we exposed H. versicolor embryos and larvae to stormwater pond sediments in microcosms in a greenhouse at Towson University, Maryland. To obtain embryos, we collected three amplexed pairs of H. versicolor from an uncontaminated wetland in

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Prince Georges County, Maryland, on June 6, 2007 and transported them back to the laboratory in 2-l plastic containers with water from the wetland. The pairs were allowed to oviposit overnight, and the eggs were assigned to experimental treatments within 24 h of fertilization. The experiment was set up in a randomized block design with two treatments: clean commercial sand as a control (n = 15) and stormwater pond sediment (n = 15). During late spring 2007 we used clean posthole diggers to collect *5 gal of surface sediment (i.e., top 10 cm) from a stormwater pond located northwest of Baltimore, just southwest of the intersection of Red Run Boulevard and Owings Mills Boulevard (Baltimore County, Maryland). This pond was chosen for its association with heavily traveled roadways and corresponding high levels of metals (Cr, Cu, Ni, Zn) and road salts (Casey et al. 2005). We transported pond sediments to Towson University in clean plastic buckets, where we homogenized the sediments before transferring them to treatment bins. We used 5.7-l plastic containers for each replicate, with 600 ml of sand or sediment and 2.8 l of aged tap water. We allowed containers 24 h to age prior to the addition of embryos. For the duration of the experiment, we changed half of the water volume every 4 days and otherwise maintained water levels at 2.8 l in all containers. For the duration of the experiment, we also measured pH, temperature, and specific conductance just before and after water changes. Because previous experiments suggested that road salts leached from pond sediments were the primary stressor in microcosms (Snodgrass et al. 2008), and ponds contaminated with road salts often show a strong vertical gradient of increasing Cl- concentrations with depth (Marsalek 2003), we collected 3 mL of water from the surface and bottom of all bins using clean syringes on the third day of the experiment (just as eggs were hatching). Use of syringes allowed us to collect water only associated with the top or bottom of the bins. Water samples were stored at 2°C until processed for Cl- levels using ion chromatography (IC; Dionex IC 25). All sample runs on the IC included replicates, blanks, and standards prepared from NIST-traceable commercial stock solutions (SPEX Certiprep). The eggs we collected were divided among bins such that each bin received 4 eggs from 3 different clutches, for a total of 12 eggs per container. Eggs were checked daily until all either hatched or died. We kept the surviving larvae in the containers until they reached Gosner stage 25 and began to feed (Gosner 1960). After the surviving larvae reached stage 25, we randomly selected one larva to remain in each bin for the rest of the experiment. Maintaining one larva per bin assured that growth and survival were not influenced by competitive interactions. Larvae were fed equal amounts of cooked spinach as needed throughout the

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experiment, and we continued to observe the bins daily for survival and development until metamorphosis. When tadpoles showed signs of metamorphosis (i.e., reached Gosner stage 41) we placed a small piece of wood in the bins to allow metamorphosing individuals to leave the water. When metamorphosing individuals reached Gosner stage 42 we removed them from bins and placed them in small plastic containers lined with moistened paper towels until they completed tail resorption (i.e., Gosner stage 46), at which point we weighed them (i.e., size at metamorphosis) and determined the length of the developmental period (i.e., day to metamorphosis). We used repeated-measures analysis of variation (ANOVA) as executed in the PROC MIXED procedure of SAS to analyze differences in the temporal dynamics of temperature, pH, and conductivity. For all models, we used a compound symmetry variance-covariance matrix. We also used the MIXED procedure to compare Cl– concentrations between sand and pond treatments as well as the top and bottom of bins, and we included bin as a nested random effect in the model. We used the LIFETEST procedure of SAS to compare survival of embryos and larvae between the sand and pond treatments. We treated both life stages as censored data, and we used nonparametric log-rank tests to compare survival between treatments because survival functions were not exponential. To measure sublethal effects, we compared size at and days to metamorphosis between treatments for all surviving larvae. To compare size at metamorphosis, we used an ANCOVA model with days to metamorphosis as a covariate. Preliminary analyses indicated homogeneity of slopes, so no interaction term was included in the final analysis. To meet the assumption of homogeneity of variance in the model, we log(x ? 1)-transformed the data for size at metamorphosis. We used Fisher’s exact test to compare days to metamorphosis between treatments, as a large number of cells had frequencies less than 5. Finally, we used simple regression analyses to relate conductivity to Cl- concentrations. When lethal or sublethal effects were observed among bins containing pond sediments, we used simple correlation analyses to investigate relationships between effects and mean conductivity over the first 7 days of the experiment (embryo survival) or between effects and both mean conductivity over the first 7 days and the entire experiment (for larvae). Our simple regressions for conductivity and Cl- relationships can be used to convert conductivity to Cl- concentrations. We focused on mean conductivity over the first 7 days for embryos because all individuals completed embryo development in 7 days. For larvae we included both mean over the first 7 days and the entire experiment because stress

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during embryonic development might have effects on larval end points independent of larval exposure.

Results Although temperature fluctuated significantly throughout the experiment (range: 23–32°C; F1,28 = 1155.5; p \ 0.001) and differed significantly between sediment and sand bins (F1,28 = 5.35; p = 0.028), the difference between sediment and sand bins was slight and not biologically significant; over the entire experiment the mean temperature for sand and sediment bins was 27.2°C (SE = 0.07) and 27.4°C (SE = 0.07), respectively. Conductivity in bins containing pond sediments reached a mean peak of 3694 lS/cm (SE = 355) in the first several days of the experiment and then declined to a mean of 968 lS/cm (SE = 33) by the end of the experiment; the maximum recorded conductivity in a bin containing pond sediment was 5150 lS/cm. In contrast, conductivity in bins containing clean sand averaged 345 lS/cm (SE = 3) was relatively constant throughout the experiment and never exceeded 500 lS/cm. Because of the changes in conductivity throughout the experiment in the sediment treatment, both the main effects of sediment (F1,28 = 955.6; p \ 0.001) and the interaction between sediment and time were significant in the repeatedmeasures model (F8,205 = 220.84; p \ 0.001). In keeping with the difference in conductivity, variation in pH also differed significantly between bins containing sand and pond sediments. However, as with temperature, these differences did not appear to be biologically significant, as pH averaged 8.6 (SE = 0.02) and 8.4 (SE = 0.02) in sand and pond sediment bins, respectively. Differences in conductivity between treatments appeared to be due mainly to road salt inputs, as Cl- was significantly elevated in bins containing pond sediments, particularly in bottom waters (F1,28 = 16.4; p \ 0.001 for the interaction term in the model). Bins containing clean sand had mean Cl- concentrations of 86.2 mg/L (SE = 1.5) and 88.5 mg/L (SE = 1.7) in top and bottom waters, respectively. In contrast, mean Cl- in the top and bottom waters from bins containing pond sediments was 895.5 mg/L (SE = 26.8) and 1157.9 mg/L (SE = 65.5), respectively. Surprisingly, there was little correlation between surface and bottom water Cl- concentrations among bins containing pond sediment (r = 0.29; p = 0.286). The slope of the relationship between conductivity and Cl- concentration at the top of the water column (conductivity = 315.27 ? 1.61 Cl-; r2 = 0.97; p \ 0.001) was smaller than the slope of the relationship between Cl- concentration at the bottom of the water

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column and conductivity (conductivity = 412.19 ? 2.99 Cl-; r2 = 0.93; p \ 0.001). The majority of mortality among embryos and tadpoles exposed to sediment occurred just after hatching, but before embryos reached Gosner stage 25 (Fig. 1). Eggs took 3–4 days to hatch and all surviving embryos reached Gosner stage 25 in 7 days. Survival of H. versicolor embryos was significantly different between sediment (44%) and control bins (99%; p = \ 0.001). However, survival of larvae after reaching Gosner stage 25 was high overall (93%) and did not differ significantly between treatments (p = 0.224). The survival of embryos was negatively correlated with mean conductivity over the first 7 days of the experiment (r = -0.71; n = 15; p \ 0.001; Fig 2). Fig. 3 Mean days to and size at metamorphosis of Gray Treefrogs exposed to clean sand and sediment from a stormwater retention pond in Baltimore County, Maryland. Error bars are ±1 SE

Fig. 1 Survival of Gray Treefrog embryos (Gosner stage 1 to 25) over the first 8 days of exposure to clean sand or sediment from a stormwater retention pond in Baltimore County, Maryland. Proportion surviving and SE bars were estimated from survival functions using the PCRO LIFETEST procedure of SAS

For embryos that did survive to Gosner stage 25 there were unexpected sublethal effects of exposure to pond sediments. In fact, larvae in sediment bins completed metamorphosis faster and at a larger size than those in control treatments. Larvae in control bins took an average of 3 days longer to metamorphose and were 27% smaller than those in sediment treatments (Fig. 3). The differences in size at metamorphosis and days to metamorphosis between sand and pond treatments were significant (F1,23 = 37.09, p \ 0.001 and p = 0.005, respectively). As might be expected with declining conductivities throughout the experiment, size at metamorphosis among the pond treatments was negatively correlated with mean conductivity over the first 7 days of the experiment (r = -0.57; n = 12, p = 0.034) but not mean conductivity over the entire experiment (r = -0.35, n = 12, p = 0.218). Among pond treatments there was no relationship between days to metamorphosis and mean conductivity over the first 7 days of the experiment (r = -0.43, n = 12, p = 0.125) or over the entire experiment (r = -0.06, p = 0.842).

Discussion

Fig. 2 Relationship between the proportion of Gray Treefrog embryos surviving 8 days of exposure to sediments from a stormwater pond in Baltimore County, Maryland and maximum conductivity of the water in the exposure bins over the same period. The line is a simple linear regression (y = 2.2562–0.0004x; r2 = 0.50; p \ 0.001)

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Our results add to a growing literature that suggests pollutants are limiting factors for wildlife use of stormwater management ponds (Bishop et al. 2000a, 2000b; Collins and Russell 2009; Snodgrass et al. 2008). Snodgrass et al. (2008) reported complete mortality of Wood Frog (R. sylvatica) embryos and near-complete survival of American Toad (B. americanus) embryos and larvae when exposed to sediments from the same pond used in the current experiment. In surveys of amphibian use of stormwater ponds and other

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wetland systems in eastern North America, Wood Frogs are reported as rare, whereas American Toads are common (Bascietto and Adams 1983; Bishop et al. 2000a; Hecnar and M’Closkey 1997; Krutson et al. 1999; Massal et al. 2007; Simon et al. 2009), suggesting that Wood Frogs are less tolerant of disturbances associated with urban and suburban conditions than American Toads. These same studies report Gray Treefrogs as being more common than Wood Frogs but less common than American Toads in urban landscapes, suggesting that the response of Gray Treefrogs to pollutants from a stormwater pond should be intermediate to the response of a sensitive and a tolerant species. This was, in fact, the case as overall survival of Gray Treefrog embryos and larvae was * 48%, whereas survival of Wood Frogs and American Toads was 0% and * 85%, respectively (Snodgrass et al. 2008). Calling males and tadpoles of both American Toads and Gray Treefrogs have been observed at the wetland where sediments were collected for these experiments (Massal et al. 2007), but Wood Frogs have not been seen at the wetland, despite occurring at other wetlands within 1 km of the study site. Moreover, studies have reported negative relationships between amphibian occurrence and pollutant conditions in stormwater ponds (Simon et al. 2009). Therefore, it appears that pollutant conditions play at least a partial role in determining use of stormwater ponds by amphibians. A number of pollutants are known to accumulate in stormwater pond sediments and might be partially or completely responsible for the toxic effects that we observed among Gray Treefrog embryos. Previous analyses of sediment from the pond used in this experiment documented elevated metal levels, particularly Zn, Cu, and Cr (Casey et al. 2005; Snodgrass et al. 2008), but levels of metals never exceeded consensus-based probability effects thresholds for sediment (MacDonald et al. 2000). Polychlorinated biphenyls (PCBs) and polycyclic aromatic hydrocarbons (PAHs) have been reported as exceeding Ontario provincial sediment quality guidelines lowest effect levels in some Canadian stormwater ponds (Bishop et al. 2000b). We were unable to measure PCBs or PAHs as part of this project, so we are unable to assess their potential contribution to the observed toxic effects. However, PCBs and PAHs might act as endocrine disruptors (Malcon and Shore 2003) or have other adverse effects on amphibian development and survival (e.g., Bryer et al. 2006; Hatch and Burton 1998) and should be included in future studies. We did document a negative relationship between embryo survival and conductivity in water from bins containing pond sediments. In cold climates, road salts used as road deicers during winter months are known to elevate salinities in both natural wetlands in close proximity to roads (Karraker et al. 2008) as well as in stormwater ponds that directly receive runoff from roads (Marsalek 2003). Although studies have

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reported comparative toxicity information for Wood Frogs and American Toads (Collins and Russell 2009), no studies have investigated salt toxicity to Gray Treefrogs. In keeping with tolerances based on occurrence in urban areas, Wood Frog larvae appear to be approximately twice as sensitive to NaCl compared to American Toad larvae (96-h LC50 of 1721 mg/l Cl- and 3926 mg/L Cl-, respectively; Collins and Russell 2009). Conductivity in the bins with sediment suggested that 50% mortality of newly hatched Gray Treefrog embryos occurred at about 1050 mg/L Cl- (when relationships between conductivity and survival and Clconcentrations and conductivity are used), considerably lower than 96-h LC50 values reported for larval Wood Frogs and American Toads. Although most of the mortality we observed among embryos took place within a time frame (4 days) comparable to those used in the 96-h LC50 test with larvae, our experiment focused on both embryos and larvae and included sediments with a complex mixture of contaminants. Embryos and early larval stages (before Gosner stage 25) might be particularly sensitive to salts, as salts interfere with the uptake of water and expansion of perivitelline space necessary for normal development of the embryo (Padhye and Ghate 1992), and development of osmoregulatory abilities might still be occurring just after hatching. Moreover, interactions between salt and other contaminants are possible. For example, metals can disrupt the Na? ion regulation (Brooks and Mills 2003; Sola et al. 1995) and might exacerbate the effects of road salt contamination. Although a substantial decline in conductivity occurred during our experiment due to water changes, the water chemistry was typical of field conditions in salt-impacted stormwater ponds of the Baltimore/Washington DC metropolitan area. In ponds associated with high-traffic roadways, conductivities usually increase rapidly during December or January, following the first substantial snow event of the season. Conductivities remain elevated until March or April, when they start to steadily decline through August or September (Casey and Lev, unpublished data). The breeding season of Gray Treefrogs is prolonged, lasting from April through July or August in Maryland (Fellers 1979). Therefore, frogs breeding on June 6, the date of the start of our experiment, would have most likely experienced declining conductivities during their embryonic and larval development, and conductivities at the pond of sediment collection were similar or slightly higher than bin conductivities throughout the experiment. Ultimately, declines in conductivity might have resulted in our observation of lethal effects mainly among embryos and the unexpected sublethal effects among larvae. Sublethal effects were not in the direction expected, with exposure to pond sediments resulting in slightly quicker development and larger size at metamorphosis. Similarly, Brown Treefrog (Litoria ewingii) larvae exposed

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to NaCl via synthetic sea salt also showed patterns of increased size and shortened time to metamorphosis (Chinathamby et al. 2006). As individuals that are larger in size at metamorphosis have increased survival and recruitment to the adult population (Breven 1990; Smith 1987), some of the population effects of mortality among embryos might be offset by increased fitness of adults. Although it is unclear why larvae might develop faster and metamorphose at a larger size when exposed to elevated ion levels, it might be related to the cost of osmoregulation. Other aquatic organisms, such as fish, exhibit the lowest resting metabolic rates when in solutions that are isotonic with their body fluids (Boeuf and Payan 2001). However, wetlands where Gray Treefrogs normally breed have relatively low ionic concentrations, and their occupation by larvae might carry a cost of osmoregulation, as excess water is actively removed from the organism. Alternatively, in hypertonic solutions, the conservation of water would carry a cost. Ultimately, in solutions that are isotonic with regard to body fluids, larvae might have more energy to dedicate to growth. Hormesis—enhanced performance after contaminant exposure—was suggested as a possible mechanism for these effects. Other plausible explanations might include feeding stimulation due to increased ion concentration or a change in the quality of algal resources in ways that promote growth. Overall, our results, along with those of others, indicate that the response of amphibian embryos to stormwater pond sediment is complicated and dependent on developmental stage. Road salts appear to be interacting with other pollutants in stormwater ponds to determine their habitat value and the structure of amphibian communities using ponds. Because amphibians are able to detect and respond to salt concentrations (Davenport and Huat 1997; Hillyard 1999; Hillyard et al. 2007), placement of eggs in saltcontaminated water might represent an unrealistic exposure scenario; in this case, the occurrence of eggs and larvae would be restricted to a narrower range of salinities than actually tolerated by the organisms under laboratory conditions, such as observed by Viertel (1999) for R. temporaria. Therefore, future studies that investigate the toxicity of pond sediments across multiple ponds and that relate the findings to the distribution of amphibians in the field will be most informative. Acknowledgment This project was supported by a Maryland Water Resources Institute grant.

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