Thesis
Using Stable Isotope Analysis to Determine the Trophic Position of Salmon in the Diet of Western Pond Turtles
Anthropogenic effects on river systems create a challenging environment for the western pond turtle (Emys marmorata). Habitat loss from urbanization (Hays et al., 1999), agriculture (Germano and Bury, 2001), road mortalities (Ashley and Robinson, 1996; Gibbs and Schriver, 2002), increases in generalist predators (Browne and Hecnar, 2007; Steen and Gibbs, 2004) and competition with invasive species (Semenov, 2010; Thompson et al., 2010; Polo-Cavia et al., 2010) has led to E. marmorata being listed as a species of special concern in California, endangered in Washington, and threatened in Oregon (Gray, 1995).
Agriculture and urbanization have created an increasing demand for water in California, which has resulted in numerous dams and other water diversion structures being constructed (Bury and Germano, 2008). This type of habitat alteration changes flow and thermal regimes, reduces water quantity and quality and converts lotic to lentic water (Reese and Welsh, 1998a). Downstream habitat is altered through channelization, which eliminates the slow, shallow edge-water habitat that supports hatchling turtles (Reese, 1996; Holland and Bury, 1998), and reduces recruitment (Reese and Welsh, 1998b).
The effect salmon have on stream and riparian ecosystems is immense (Scheuerell et al., 2005; Bartz and Naiman, 2005; Zhang et al., 2003; Janetski et al., 2009). Salmon play a critical role in stream ecosystems by transferring marine derived nutrients (>95% of body weight accumulated in the ocean) to relatively nutrient poor streams (Gresh et al., 2000; Schindler et al., 2003). Incorporation of marine derived nutrients into the aquatic ecosystem can stimulate food web productivity by increasing primary productivity, which leads to higher prey availability (Cram et al., 2011). The increased food web productivity in turn benefits juvenile salmon on their migration to the ocean (Bilby et al., 1998; Wipfli et al., 2003) and loss of this resource has been shown to decrease their survival rate (Achord et al., 2003; Zabel et al., 2005). Western Pond turtles could also be benefiting from this influx of marine derived nutrients and stable isotope analysis can clarify this relationship.
The western pond turtle occupies a diverse variety of habitats including rivers, streams, lakes, ponds, and sewage treatment ponds (Holland, 1994; Bury, 1972; Polo-Cavia et al., 2009). Optimal habitat includes pools with emergent basking areas and various types of refugia such as undercut banks, submerged vegetation, logs, mud and large rocks (Ernst and Lovich, 2009). Western pond turtles eat a variety of foods and are opportunistic predators and scavengers (Bury, 1986). They have been observed eating aquatic insects, all life stages of frogs, crustaceans, snails, fish and duck carcasses, and various aquatic plants (Bury, 1986; Carr, 1952; Evenden, 1948; Holland, 1985, 1994; Pope, 1939). Diet between sexes and age classes differ in prey size and proportion, which may decrease intraspecific competition (Bury, 1986).
Stable isotope ratios of nitrogen (15N/14N) and carbon (13C/12C) in body tissues reflect diet since metabolic reactions select for lighter isotopes (Fry, 2006), which after being used, are excreted, leaving heavier isotopes to accumulate in tissues. Increases in trophic level from plant to herbivore to carnivore results in a larger ratio of heavy isotopes with each trophic level. Marine nutrient sources are enriched in 15N compared to terrestrial sources (Schoeninger et al., 1983) and provide a unique and easy to differentiate signature in turtle tissues. Analysis of isotopic signatures offers advantages over traditional methods such as observation of feeding behavior or gut content analysis because it requires very small (~1 mg) tissue samples for analysis and can be performed on museum specimens. Consequently, stable isotope analysis provides a non-invasive method of determining the trophic position of salmon in their diet.
In this study I will use stable isotope analysis to test the hypothesis that western pond turtles are using salmon as a food source and if so, what trophic position salmon occupy in their diet. Using morphometric and radiograph data I will also test the hypothesis that turtles in areas with salmon runs experience higher body condition and fecundity than turtles in areas without salmon runs. I will also be able to test museum specimens to determine if salmon has been a part of their diet in areas that have historically had salmon runs.
Literature Cited
Achord, S., P. S. Levin and R. W. Zabel. 2003. Density-Dependent Mortality in Pacific
Salmon: the Ghost of Impacts Past? Ecology Letters, 6: 335–342.
Ashley, E.P., and Robinson, J.T. 1996. Road mortality of amphibians, reptiles and other
wildlife on the Long Point Causeway, Lake Erie, Ontario. Canadian Field Naturalist,
110: 403–412.
Bartz, K. K. and R. J. Naiman. 2005. Effects of Salmon-Borne Nutrients on Riparian
Soils and Vegetation in Southwest Alaska. Ecosystems, 8: 529-545.
Bilby, R. E., B. R. Fransen, P. A. Bisson and J. K. Walter. 1998. Response of Juvenile
Coho Salmon (Oncorhynchus kisutch) and Steelhead (Oncorhynchus mykiss) to
the Addition of Salmon Cacasses to Two Streams in Southwestern Washington,
U.S.A. Canadian Journal of Fisheries and Aquatic Sciences, 55: 1909–1918.
Browne, C. L. and S. J. Hecnar. 2007. Species loss and shifting population structure of
freshwater turtles despite habitat protection. Biological Conservation, 138: 421-429.
Bury, R. B. 1972. Habits and Home Range of the Pacific Pond Turtle, Clemmys marmorata, in
a Stream Community. Ph.D. dissertation, University of California, Berkeley.
Bury, R. B. 1986. Feeding Ecology of the Turtle, Clemmys marmorata. Journal of
Herpetology, 20(4): 515-521.
Bury, R. B. and D. J. Germano. 2008. Actinemys marmorata (Baird and Girard 1852) –
western pond turtle, Pacific pond turtle. In: Rhodin, A.G.J., Pritchard, P.C.H., van Dijk,
P.P., Saumure, R.A., Buhlmann, K.A., and Iverson, J.B. (Eds.) Conservation Biology
of Freshwater Turtles and Tortoises: A Compilation Project of the IUCN/SSC Tortoise
and Freshwater Turtle Specialist Group. Chelonian Research Monographs No. 5, pp.
001.1-001.9.
Carr, A. F. Jr. 1952. Handbook of Turtles: The Turtles of the United States, Canada,
and Baja California. Comstock Publishing Association, Cornell University Press,
Ithaca, New York.
Cram, J. M., P. M. Kiffney, R. Klett, and R. L. Edmonds. 2011. Do Fall Additions of
Salmon Carcasses Benefit Food Webs in Experimental Streams? Hydrobiologia, 675:
197-209.
Ernst, C. H. and J. E. Lovich. 2009. Turtles of the United States and Canada. Baltimore (MD):
The Johns Hopkins University Press.
Evenden, F. G. Jr. 1948. Distribution of the Turtles of Western Oregon. Herpetologica, 4: 201-
204.
Fry B. 2006. Stable Isotope Ecology. New York (NY): Springer Science+Business Media, LLC.
Germano, D. J., R.B. Bury. 2001. Western pond turtles (Clemmys marmorata) in the Central
Valley of California: status and population structure. Transactions of the Western
Section of the Wildlife Society, 37: 22–36.
Gibbs, J. P., and W. G. Shriver. 2002. Estimating the Effects of Road Mortality on Turtle
Populations. Conservation Biology, 16(6): 1647-1652.
Gray, E. M., 1995. DNA Fingerprinting Reveals a Lack of Genetic Variation in Northern
Populations of the Western Pond Turtle (Clemmys marmorata). Conservation Biology,
9: 1244–1254.
Gresh T., J. Lichatowich, and P. Schoonmaker. 2000. An Estimation of Historic and Current
Levels of Salmon Production in the Northeast Pacific Ecosystem: Evidence of a
Nutrient Deficit in the Freshwater Systems of the Pacific Northwest. Fisheries,
25:15-21.
Hays, D. W., K. R. McAllister, S. A. Richardson, and D. W. Stinson. 1999. Washington State
Recovery Plan for the Western Pond Turtle. Washington Department of Fish and
Wildlife, Olympia.
Holland, D. C. and R. B. Bury. 1998. Clemmys marmorata (Baird and Girard 1852) Western
pond turtle. In P. C. Pritchard and A. G. Rhodin, (eds.) Conservation Biology of
Freshwater Turtles, Chelonian Research Monographs vol. II. In press.
Holland, D. C. 1985. Clemmys marmorata (Western Pond Turtle): Feeding. Herpetological
Review, 19: 87-88.
Holland, D. C. 1994. Final report on the western pond turtle project. Report, prepared for
Wildlife Diversity Division, Oregon Department of Fish and Wildlife, Portland.
Janetski, J. J., D. T. Chaloner, S. D. Tiegs, and G. A. Lamberti, 2009. Pacific Salmon Effects
on Stream Ecosystems: a Quantitative Synthesis. Oecologia, 159: 583-595.
Polo-Cavia, N., P. Lopez, and J. Martin. 2010. Competitive Interactions During Basking
Between Native and Invasive Freshwater Turtle Species. Biological Invasions, 12:
2141-2152.
Polo-Cavia, N., T. Engstrom P. Lopez, and J. Martin. 2009. Body Condition does not Predict
Immunocompetence of Western Pond Turtles in Altered Versus Natural Habitats.
Animal Conservation, 13(3): 256-264.
Pope, C. H. 1939. Turtles of the United States and Canada. Alfred A. Knopf, New York.
Reese, D. A. 1996. Comparative Demography and Habitat Use of Western Pond Turtles in
Northern California: the Effects of Damming and Related Alterations. Unpublished
Ph.D. Dissertation. University of California, Berkeley.
Reese, D. A. and H. H. Welsh. 1998a. Comparative Demography of Clemmys marmorata
Populations in the Trinity River of California in the Context of Dam-Induced Alterations.
Journal of Herpetology, 4: 505-515.
Reese, D. A. and H. H. Welsh. 1998b. Habitat Use by Western Pond Turtles in the Trinity
River, California. Journal of Wildlife Management, 62: 842-853.
Scheuerell, M. D., P. S. Levin, R. W. Zabel, J. G. Williams and B. L. Sanderson. 2005. A
New Perspective on the Importance of Marine-Derived Nutrients to Threatened Stocks
of Pacific Salmon (Oncorhynchus spp.). Canadian Journal of Fisheries and Aquatic
Sciences, 62: 961-964.
Schindler, D. E., M. D. Scheuerell, J. W. Moore, S.M. Gende, T.B. Francis, and W. J. Palen.
2003. Pacific Salmon and the Ecology of Coastal Ecosystems. Frontiers in Ecology
and the Envorionment, 1: 31–37.
Schoeninger, M. J., M. J. DeNiro, and H. Tauber. 1983. Stable Nitrogen Isotope Ratios of
Bone Collagen Reflect Marine and Terrestrial Components of Prehistoric Human Diet.
Science, 220:1381-1383.
Semenov, D. V. 2010. Slider Turtle, Trachemys scripta elegans, as Invasion Threat (Reptilia;
Testudines). Russian Journal of Biological Invasions, 1(4): 296-300.
Steen, D.A. and J. P. Gibbs. 2004. Effect of Roads on the Structure of Freshwater Turtle
Populations. Conservation Biology, 18(4):1143-1148.
Thomson, R. C., P. Q. Spinks, and H. B. Shaffer. 2010. Distribution and Abundance of
Invasive Red-Eared Sliders (Trachemys scripta elegans) in California's Sacramento
River Basin and Possible Impacts on Native Western Pond Turtles (Emys marmorata).
Chelonian Conservation and Biology, 9(2): 297-302.
Wipfli, M.S., J. P. Hudson, J. P. Caouette and D. T. Chaloner. 2003. Marine Subsidies in
Freshwater Ecosystems: Salmon Carcasses Increase the Growth Rates of Stream-
Resident Salmonids. Transactions of the American Fisheries Society, 132: 371-381.
Zabel, R.W., M. D. Scheuerell, M. M. McClure and J. G. Williams. 2006. The Interplay
Chinook Salmon. Conservation Biology, 20(1): 190-200.
Zhang, Y., J. N. Negishi, J. S. Richardson and R. Kolodziejczyk. 2003. Impacts of Marine-
Derived Nutrients on Ecosystem Functioning. Proceedings of the Royal Society of
London B, 270: 2117-2123.
Anthropogenic effects on river systems create a challenging environment for the western pond turtle (Emys marmorata). Habitat loss from urbanization (Hays et al., 1999), agriculture (Germano and Bury, 2001), road mortalities (Ashley and Robinson, 1996; Gibbs and Schriver, 2002), increases in generalist predators (Browne and Hecnar, 2007; Steen and Gibbs, 2004) and competition with invasive species (Semenov, 2010; Thompson et al., 2010; Polo-Cavia et al., 2010) has led to E. marmorata being listed as a species of special concern in California, endangered in Washington, and threatened in Oregon (Gray, 1995).
Agriculture and urbanization have created an increasing demand for water in California, which has resulted in numerous dams and other water diversion structures being constructed (Bury and Germano, 2008). This type of habitat alteration changes flow and thermal regimes, reduces water quantity and quality and converts lotic to lentic water (Reese and Welsh, 1998a). Downstream habitat is altered through channelization, which eliminates the slow, shallow edge-water habitat that supports hatchling turtles (Reese, 1996; Holland and Bury, 1998), and reduces recruitment (Reese and Welsh, 1998b).
The effect salmon have on stream and riparian ecosystems is immense (Scheuerell et al., 2005; Bartz and Naiman, 2005; Zhang et al., 2003; Janetski et al., 2009). Salmon play a critical role in stream ecosystems by transferring marine derived nutrients (>95% of body weight accumulated in the ocean) to relatively nutrient poor streams (Gresh et al., 2000; Schindler et al., 2003). Incorporation of marine derived nutrients into the aquatic ecosystem can stimulate food web productivity by increasing primary productivity, which leads to higher prey availability (Cram et al., 2011). The increased food web productivity in turn benefits juvenile salmon on their migration to the ocean (Bilby et al., 1998; Wipfli et al., 2003) and loss of this resource has been shown to decrease their survival rate (Achord et al., 2003; Zabel et al., 2005). Western Pond turtles could also be benefiting from this influx of marine derived nutrients and stable isotope analysis can clarify this relationship.
The western pond turtle occupies a diverse variety of habitats including rivers, streams, lakes, ponds, and sewage treatment ponds (Holland, 1994; Bury, 1972; Polo-Cavia et al., 2009). Optimal habitat includes pools with emergent basking areas and various types of refugia such as undercut banks, submerged vegetation, logs, mud and large rocks (Ernst and Lovich, 2009). Western pond turtles eat a variety of foods and are opportunistic predators and scavengers (Bury, 1986). They have been observed eating aquatic insects, all life stages of frogs, crustaceans, snails, fish and duck carcasses, and various aquatic plants (Bury, 1986; Carr, 1952; Evenden, 1948; Holland, 1985, 1994; Pope, 1939). Diet between sexes and age classes differ in prey size and proportion, which may decrease intraspecific competition (Bury, 1986).
Stable isotope ratios of nitrogen (15N/14N) and carbon (13C/12C) in body tissues reflect diet since metabolic reactions select for lighter isotopes (Fry, 2006), which after being used, are excreted, leaving heavier isotopes to accumulate in tissues. Increases in trophic level from plant to herbivore to carnivore results in a larger ratio of heavy isotopes with each trophic level. Marine nutrient sources are enriched in 15N compared to terrestrial sources (Schoeninger et al., 1983) and provide a unique and easy to differentiate signature in turtle tissues. Analysis of isotopic signatures offers advantages over traditional methods such as observation of feeding behavior or gut content analysis because it requires very small (~1 mg) tissue samples for analysis and can be performed on museum specimens. Consequently, stable isotope analysis provides a non-invasive method of determining the trophic position of salmon in their diet.
In this study I will use stable isotope analysis to test the hypothesis that western pond turtles are using salmon as a food source and if so, what trophic position salmon occupy in their diet. Using morphometric and radiograph data I will also test the hypothesis that turtles in areas with salmon runs experience higher body condition and fecundity than turtles in areas without salmon runs. I will also be able to test museum specimens to determine if salmon has been a part of their diet in areas that have historically had salmon runs.
Literature Cited
Achord, S., P. S. Levin and R. W. Zabel. 2003. Density-Dependent Mortality in Pacific
Salmon: the Ghost of Impacts Past? Ecology Letters, 6: 335–342.
Ashley, E.P., and Robinson, J.T. 1996. Road mortality of amphibians, reptiles and other
wildlife on the Long Point Causeway, Lake Erie, Ontario. Canadian Field Naturalist,
110: 403–412.
Bartz, K. K. and R. J. Naiman. 2005. Effects of Salmon-Borne Nutrients on Riparian
Soils and Vegetation in Southwest Alaska. Ecosystems, 8: 529-545.
Bilby, R. E., B. R. Fransen, P. A. Bisson and J. K. Walter. 1998. Response of Juvenile
Coho Salmon (Oncorhynchus kisutch) and Steelhead (Oncorhynchus mykiss) to
the Addition of Salmon Cacasses to Two Streams in Southwestern Washington,
U.S.A. Canadian Journal of Fisheries and Aquatic Sciences, 55: 1909–1918.
Browne, C. L. and S. J. Hecnar. 2007. Species loss and shifting population structure of
freshwater turtles despite habitat protection. Biological Conservation, 138: 421-429.
Bury, R. B. 1972. Habits and Home Range of the Pacific Pond Turtle, Clemmys marmorata, in
a Stream Community. Ph.D. dissertation, University of California, Berkeley.
Bury, R. B. 1986. Feeding Ecology of the Turtle, Clemmys marmorata. Journal of
Herpetology, 20(4): 515-521.
Bury, R. B. and D. J. Germano. 2008. Actinemys marmorata (Baird and Girard 1852) –
western pond turtle, Pacific pond turtle. In: Rhodin, A.G.J., Pritchard, P.C.H., van Dijk,
P.P., Saumure, R.A., Buhlmann, K.A., and Iverson, J.B. (Eds.) Conservation Biology
of Freshwater Turtles and Tortoises: A Compilation Project of the IUCN/SSC Tortoise
and Freshwater Turtle Specialist Group. Chelonian Research Monographs No. 5, pp.
001.1-001.9.
Carr, A. F. Jr. 1952. Handbook of Turtles: The Turtles of the United States, Canada,
and Baja California. Comstock Publishing Association, Cornell University Press,
Ithaca, New York.
Cram, J. M., P. M. Kiffney, R. Klett, and R. L. Edmonds. 2011. Do Fall Additions of
Salmon Carcasses Benefit Food Webs in Experimental Streams? Hydrobiologia, 675:
197-209.
Ernst, C. H. and J. E. Lovich. 2009. Turtles of the United States and Canada. Baltimore (MD):
The Johns Hopkins University Press.
Evenden, F. G. Jr. 1948. Distribution of the Turtles of Western Oregon. Herpetologica, 4: 201-
204.
Fry B. 2006. Stable Isotope Ecology. New York (NY): Springer Science+Business Media, LLC.
Germano, D. J., R.B. Bury. 2001. Western pond turtles (Clemmys marmorata) in the Central
Valley of California: status and population structure. Transactions of the Western
Section of the Wildlife Society, 37: 22–36.
Gibbs, J. P., and W. G. Shriver. 2002. Estimating the Effects of Road Mortality on Turtle
Populations. Conservation Biology, 16(6): 1647-1652.
Gray, E. M., 1995. DNA Fingerprinting Reveals a Lack of Genetic Variation in Northern
Populations of the Western Pond Turtle (Clemmys marmorata). Conservation Biology,
9: 1244–1254.
Gresh T., J. Lichatowich, and P. Schoonmaker. 2000. An Estimation of Historic and Current
Levels of Salmon Production in the Northeast Pacific Ecosystem: Evidence of a
Nutrient Deficit in the Freshwater Systems of the Pacific Northwest. Fisheries,
25:15-21.
Hays, D. W., K. R. McAllister, S. A. Richardson, and D. W. Stinson. 1999. Washington State
Recovery Plan for the Western Pond Turtle. Washington Department of Fish and
Wildlife, Olympia.
Holland, D. C. and R. B. Bury. 1998. Clemmys marmorata (Baird and Girard 1852) Western
pond turtle. In P. C. Pritchard and A. G. Rhodin, (eds.) Conservation Biology of
Freshwater Turtles, Chelonian Research Monographs vol. II. In press.
Holland, D. C. 1985. Clemmys marmorata (Western Pond Turtle): Feeding. Herpetological
Review, 19: 87-88.
Holland, D. C. 1994. Final report on the western pond turtle project. Report, prepared for
Wildlife Diversity Division, Oregon Department of Fish and Wildlife, Portland.
Janetski, J. J., D. T. Chaloner, S. D. Tiegs, and G. A. Lamberti, 2009. Pacific Salmon Effects
on Stream Ecosystems: a Quantitative Synthesis. Oecologia, 159: 583-595.
Polo-Cavia, N., P. Lopez, and J. Martin. 2010. Competitive Interactions During Basking
Between Native and Invasive Freshwater Turtle Species. Biological Invasions, 12:
2141-2152.
Polo-Cavia, N., T. Engstrom P. Lopez, and J. Martin. 2009. Body Condition does not Predict
Immunocompetence of Western Pond Turtles in Altered Versus Natural Habitats.
Animal Conservation, 13(3): 256-264.
Pope, C. H. 1939. Turtles of the United States and Canada. Alfred A. Knopf, New York.
Reese, D. A. 1996. Comparative Demography and Habitat Use of Western Pond Turtles in
Northern California: the Effects of Damming and Related Alterations. Unpublished
Ph.D. Dissertation. University of California, Berkeley.
Reese, D. A. and H. H. Welsh. 1998a. Comparative Demography of Clemmys marmorata
Populations in the Trinity River of California in the Context of Dam-Induced Alterations.
Journal of Herpetology, 4: 505-515.
Reese, D. A. and H. H. Welsh. 1998b. Habitat Use by Western Pond Turtles in the Trinity
River, California. Journal of Wildlife Management, 62: 842-853.
Scheuerell, M. D., P. S. Levin, R. W. Zabel, J. G. Williams and B. L. Sanderson. 2005. A
New Perspective on the Importance of Marine-Derived Nutrients to Threatened Stocks
of Pacific Salmon (Oncorhynchus spp.). Canadian Journal of Fisheries and Aquatic
Sciences, 62: 961-964.
Schindler, D. E., M. D. Scheuerell, J. W. Moore, S.M. Gende, T.B. Francis, and W. J. Palen.
2003. Pacific Salmon and the Ecology of Coastal Ecosystems. Frontiers in Ecology
and the Envorionment, 1: 31–37.
Schoeninger, M. J., M. J. DeNiro, and H. Tauber. 1983. Stable Nitrogen Isotope Ratios of
Bone Collagen Reflect Marine and Terrestrial Components of Prehistoric Human Diet.
Science, 220:1381-1383.
Semenov, D. V. 2010. Slider Turtle, Trachemys scripta elegans, as Invasion Threat (Reptilia;
Testudines). Russian Journal of Biological Invasions, 1(4): 296-300.
Steen, D.A. and J. P. Gibbs. 2004. Effect of Roads on the Structure of Freshwater Turtle
Populations. Conservation Biology, 18(4):1143-1148.
Thomson, R. C., P. Q. Spinks, and H. B. Shaffer. 2010. Distribution and Abundance of
Invasive Red-Eared Sliders (Trachemys scripta elegans) in California's Sacramento
River Basin and Possible Impacts on Native Western Pond Turtles (Emys marmorata).
Chelonian Conservation and Biology, 9(2): 297-302.
Wipfli, M.S., J. P. Hudson, J. P. Caouette and D. T. Chaloner. 2003. Marine Subsidies in
Freshwater Ecosystems: Salmon Carcasses Increase the Growth Rates of Stream-
Resident Salmonids. Transactions of the American Fisheries Society, 132: 371-381.
Zabel, R.W., M. D. Scheuerell, M. M. McClure and J. G. Williams. 2006. The Interplay
- Between Climate Variability and Density Dependence in the Population Viability
Chinook Salmon. Conservation Biology, 20(1): 190-200.
Zhang, Y., J. N. Negishi, J. S. Richardson and R. Kolodziejczyk. 2003. Impacts of Marine-
Derived Nutrients on Ecosystem Functioning. Proceedings of the Royal Society of
London B, 270: 2117-2123.
Background
I did my undergraduate work at Cal Poly San Luis Obispo, where I received a BS in Animal Science.
