Environ Monit Assess DOI 10.1007/s10661-009-0847-3 Mercury contamination in three species of anuran amphibians from the Cache Creek Watershed, California, USA Roger L. Hothem · Mark R. Jennings · John J. Crayon Received: 24 November 2008 / Accepted: 10 March 2009 © U.S. Government 2009 Abstract Fish and wildlife may bioaccumulate had mean Hg concentrations greater than the US mercury (Hg) to levels that adversely affect re- Environmental Protection Agency’s tissue residue production, growth, and survival. Sources of Hg criterion for fish (0.3 μg/g). Of the bullfrog tissues within the Cache Creek Watershed in northern analyzed, the liver had the highest concentrations California have been identified, and concentra- of both total Hg and methyl mercury. Total Hg in tions of Hg in invertebrates and fish have been carcasses of bullfrogs was highly correlated with documented. However, bioaccumulation of Hg by total Hg in leg muscle, the tissue most often con- amphibians has not been evaluated. In this study, sumed by humans. adult and juvenile American bullfrogs (Lithobates catesbeianus) and foothill yellow-legged frogs Keywords Amphibians · Bioaccumulation · (Rana boylii), adult Northern Pacific treefrogs American bullfrog · Cache Creek · California · (Pseudacris regilla), and larval bullfrogs were col- Foothill yellow-legged frog · Lithobates lected and analyzed for total Hg. One or more catesbeianus · Mercury · Northern Pacific species of amphibians from 40% of the 35 sites treefrog · Pseudacris regilla · Rana boylii R. L. Hothem (B) J. J. Crayon Western Ecological Research Center, Western Ecological Research Center, US Geological Survey, Dixon Field Station, US Geological Survey, Davis Field Station, 6924 Tremont Road, Dixon, CA 95620, USA Davis, CA 95616, USA e-mail: [email protected] e-mail: [email protected] Present Address: M. R. Jennings M. R. Jennings US Geological Survey, Piedras Blancas Field Station, Rana Resources, P.O. Box 70, San Simeon, CA, 93452, USA P.O. Box 2185, Davis, e-mail: [email protected] CA 95617-2185, USA M. R. Jennings Present Address: Department of Herpetology, J. J. Crayon California Academy of Sciences, California Department of Fish and Game, Golden Gate Park, San Francisco, 78078 Country Club Drive, Bermuda Dunes, CA 94118, USA CA 92203, USA Environ Monit Assess Introduction (Central Valley Regional Water Quality Control Board 2003). Domagalski (2001) reported high Amphibians may be adversely affected by expo- concentrations of Hg in both water and streambed sure to environmental mercury (Hg), especially sediments in the Cache Creek Watershed. Stud- in its more bioavailable form, methylmercury ies conducted by the California Regional Water (MeHg). As shown in laboratory studies with Quality Control Board during 1996–1998 con- southern leopard frog (Rana sphenocephala)lar- firmed that Cache Creek was a major source of vae, amphibian development may be adversely Hg to the Sacramento–San Joaquin River Delta affected and survival through metamorphosis may and San Francisco Bay Estuary (Foe and Croyle be decreased by dietary Hg (Unrine et al. 2004). 1998). Sources of Hg in the Cache Creek Wa- Other effects may include impaired reproduction, tershed include geothermal springs, agricultural growth inhibition, behavioral modification, and runoff, erosion of naturally Hg-enriched soils, and various sublethal effects (Zillioux et al. 1993). atmospheric deposition, but the majority of the Of Hg, cadmium, copper, manganese, and zinc, Hg exported from the watershed originates from Jayaprakash and Madhyastha (1987) found that historic Hg mining operations in the upper water- Hg was the most toxic to larval ornate narrow- shed (Foe and Croyle 1998). mouthed toads (Microhyla ornata). Teratogenic Information on the concentrations of Hg in wa- and lethal effects of Hg have also been docu- ter, sediments (Foe and Croyle 1998; Domagalski mented for other larval amphibians (Dial 1976; 2001; Domagalski et al. 2004), invertebrates Chang et al. 1974; Punzo 1993). In addition to (Slotton et al. 1997), and fish (Slotton et al. 1995) being at risk for Hg toxicity themselves, amphib- from the Cache Creek Watershed have helped ians may play a role in the transport of Hg from define the sources of Hg in the watershed and the the aquatic to the terrestrial environment as well magnitude of its contamination. However, more as the conversion of elemental Hg to the more information on Hg concentrations in the upper bioavailable MeHg (Unrine et al. 2007). trophic levels, especially amphibians, is needed. There is growing evidence that some amphibi- Amphibians may be useful indicators of metal ans are declining or have disappeared from signifi- contamination (Cooke 1981), especially where fish cant parts of their historical ranges in the western cannot survive. They bioaccumulate and are par- USA (Blaustein et al. 1994; Jennings 1995; Fisher ticularly sensitive to metals, have obligate aquatic and Shaffer 1996). The role of contaminants in larval stages, and sometimes spend their entire life these declines is unclear (Cory et al. 1970; Hayes cycle in a given pond or reach of a stream. and Jennings 1986; Jennings 1988), but contami- This study of Hg bioaccumulation in amphib- nants may be affecting species in specific areas ians was part of a larger study conducted in coop- (Davidson et al. 2001; Davidson 2002; Sparling eration with the US Fish and Wildlife Service et al. 2001). Of most concern in the Cache Creek that evaluated Hg bioaccumulation by macro- Watershed is the effect of Hg on the native foothill invertebrates, amphibians, fish, and insectivorous yellow-legged frog (Rana boylii), a California spe- birds from the Cache Creek Watershed. In this cies of special concern (Jennings and Hayes 1994). paper, we focus on an evaluation of Hg in three The Cache Creek Watershed, located within species of amphibians. The objectives of this part the North Coast Range of California (Fig. 1), is of the study were to: (1) quantify Hg bioaccu- an area with abundant geologic sources of Hg mulation in larval, juvenile, and adult amphibians and a long history of Hg contamination (Rytuba inhabiting the watershed, (2) relate Hg bioaccu- 2000). Waterways in the Cache Creek Watershed mulation by these amphibians to sources of Hg listed as impaired by Hg contamination by Section within the watershed, and (3) evaluate Hg and 303(d) of the Clean Water Act include: lower MeHg concentrations in various tissues of Amer- Cache Creek, Clear Lake, Davis Creek Reservoir, ican bullfrogs (Lithobates catesbeianus) collected Harley Gulch, Bear Creek, and Sulphur Creek from the watershed. Environ Monit Assess Reference Sites: 19 – TURKEYRN 1 – EFMIDDCR Canyon Sites: 2 – BRIMROAD 20 – BEAR>CCR 3 – SPNISHCR 21 – BEAR>H2O Upstream of Mines: 22 – BEARTHOM 4 – BEARHAMI 23 – CCR>BEAR Mine Sites: 24 – CCRHASWL 5 – ABBOTTDR 25 – CCRBUCKI 6 – BEAR<SUL 26 – CCR<BEAR 7 – DACR>DCR 27 – GRIZZLCR 8 – DACR<DCR 28 – TOM>BEAR 9 – DACR>CCR Valley Sites: 10 – DACRRESV 29 – CCRESPAR 11 – HARGULDS 30 – CCRGUIND 12 – HARGULLO 31 – CCR94BBR 13 – HARGUL20 32 – CCR<R102 14 – SCR>BEAR 33 – CCRBASIN 15 – SCR>WLHS 34 – VFYWAEAS 16 – SCR<WLHS 35 – VFYWAWES 17 – SCREASTF 18 – SCRWESTF Fig. 1 Sites, by region, within the Cache Creek Watershed between reference and mine (BEARHAMI) indicated by sampled for amphibians during 1997–1998. Reference sites a star, and Valley sites indicated by an open circle. Samples indicated by a blackened square, Mine sites indicated by collected per site and per year are listed in Table 1 a bulls eye, Canyon sites indicated by a triangle,thesite Materials and methods Creek, Mill Creek at Brim Road, and North Fork of Cache Creek at Spanish Creek (Fig. 1). Spe- Study area cific study sites within these reaches were selected based on current knowledge of Hg contamina- The 2,950-km2 Cache Creek Watershed is located tion, accessibility, and the presence of appropriate in the North Coast Range of California, about study organisms. 130 km north of San Francisco (Fig. 1). The wa- For geographic comparison of Hg concentra- tershed is primarily located in Lake, Colusa, and tions, the study area was classified into four major Yolo counties, but extends into parts of Napa, regions based primarily on proximity to Hg mine Mendocino, and Sonoma counties. Study sites on sites and stream gradient (Table 1 and Fig. 1). the main stem of Cache Creek ranged from Buck Uniform atmospheric deposition of Hg was as- Island downstream to the Yolo Basin Wildlife sumed throughout the watershed and was not Area and included sites on Bear Creek, Sulphur considered in the analyses. The three reference Creek, Harley Gulch, Davis Creek, Grizzly Creek, sites were located from 13.6 to 50.2 km from the and three references sites: East Fork of Middle nearest mine site in the upper reaches of the Environ Monit Assess Table 1 Collection sites, by region, and numbers of American bullfrogs (BULL), foothill yellow-legged frogs (FYLF), and northern Pacific treefrogs (PATR) collected from the Cache Creek Watershed, 1997–1998 (map key refers to Fig. 1) Map key Site description Site code Latitude Longitude Samples collected (1997/1998) BULL FYLF PATR Reference sites 1 East Fork Middle Creek EFMIDDCR 39◦1509 N 122◦5700 WU/Na 3/N U/N 2 Mill Creek above Brim BRIMROAD 39◦0945 N 122◦2659 W 3/5 3/U U/U Road 3 Spanish Creek SPNISHCR 39◦1017 N 122◦3705 W U/N 3/U U/N Total samples from reference sites 3/5 9/0 0/0 Site above mines 4 Bear Creek at Hamilton BEARHAMI 39◦0324 N 122◦2441 W6/Nb 3/N 3/N Canyon Total samples from above mine site 6/0 3/0 3/0 Mine sites 5 Abbott Mine Drain ABBOTTDR 39◦0056 N 122◦2628 W N/U N/1 N/U 6 Bear Creek below Sulphur BEAR<SUL 39◦0222 N 122◦2428 W6/Nb 3/N 3/N Creek 7 Davis Creek above Davis DACR>DCR 38◦5149 N 122◦2213 W6/Nc 3/N 3/N Creek Res.