Share This Article:

Habitat protection for sensitive species: Balancing species requirements and human constraints using bioindicators as examples

Abstract Full-Text HTML Download Download as PDF (Size:128KB) PP. 50-62
DOI: 10.4236/ns.2013.55A007    4,312 Downloads   6,031 Views   Citations


Vertebrates have particular habitat needs as a function of life cycle and reproductive stage. This paper uses four species as examples to illustrate a paradigm of environmental assessment that includes physical, biological, toxicological and human dimensions. Species used include Chinook salmon (Oncorhynchus tshawytscha), northern leopard frog (Rana pipiens), northern pine snake (Pituophis m. melanoleucus), and red knot (Calidris canutus rufa, a sandpiper). The life cycles of these species include reliance on habitats that are aquatic, terrestrial, aerial, or combinations of these. Two species (frog, snake) are sedentary and two (salmon, sandpiper) are long-distance migrants. While some measurement endpoints are similar for all species (reproductive success, longevity, contaminant loads), others vary depending upon life cycle and habitat. Salmon have a restricted breeding habitat requiring coarse sand, moderate current, and high oxygen levels for adequate egg incubation. Leopard frogs require still water of appropriate temperature for development of eggs. Pine snakes require sand compaction sufficient to sustain a nest burrow without collapsing, and full sun penetration to the sand to allow their eggs in underground nests to incubate and hatch. Red knots migrate to high Arctic tundra, but incubate their own eggs, so temperature is less of a constraint, but feedinging habitat is. These habitat differences suggest the measurement endpoints that are essential to assess habitat suitability and to manage habitats to achieve stable and sustainable populations. Habitat use and population stability have implications for human activities for some, but not all species. Salmon are important economically, recreationally, and as part of Native American culture and diet. Red knots are of interest to people mainly because of their long, intercontinental migrations and declining populations. Other measurement endpoints for these four species illustrate the differences and similarities in metrics necessary to assess habitat needs. The implications of these differences are discussed.

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

Burger, J. , Gochfeld, M. , Powers, C. , Niles, L. , Zappalorti, R. , Feinberg, J. and Clarke, J. (2013) Habitat protection for sensitive species: Balancing species requirements and human constraints using bioindicators as examples. Natural Science, 5, 50-62. doi: 10.4236/ns.2013.55A007.


[1] National Research Council (2008) Public participation in environmental assessment and decision making. National Academy Press, Washington DC.
[2] European Environment Agency (2003) Environmental indicators: Typology and use in reporting. EEA, Copenhagen.
[3] National Oceanic and Atmospheric Administration (2011) The Gulf of Mexico at a Glance. NOAA, Department of Commerce, Washington DC.
[4] Environmental Protection Agency (2009) Environmental justice: Compliance and environment.
[5] Burger, J. (2011) Stakeholders and scientists: Achieving implementable solutions to energy and environmental issues. Springer, New York. doi:10.1007/978-1-4419-8813-3
[6] FWS (United States Fish & Wildlife Service) (2012) Species profile: Chinook salmon.
[7] Narum, S.R., Hess, J.E. and Metala, A.P. (2010) Examining genetic lineages of Chinook Salmon in the Colombia River Basin. Transactions of the American Fisheries Society, 139, 1465-1477. doi:10.1577/T09-150.1
[8] Columbia River Inter-Tribal Fish Commission (2013) We are Salmon people.
[9] Environmental Protection Agency (2009) Columbia River Basin: State of the River Report for Toxics. EPA 910R-08-004.
[10] Oregon Hanford Waste Board (2002) River without waste: Recommendations for Protecting the Columbia River from Hanford Site Nuclear Waste. USDOE, Hanford.
[11] Dauble, D.D. and Watson, D.G. (1997) Status of fall Chinook salmon populations in the mid-Columbia River, 1948-1992. North American Journal of Fisheries Management, 17, 283-300. doi:10.1577/1548-8675(1997)017<0283:SOFCSP>2.3.CO;2
[12] Dauble, D.D., Hanrahan, T.P., Geist, D.R. and Parsley, M.J. (2003) Impacts of the Columbia River hydroelectric system on main-stem habitats of fall Chinook salmon. North American Journal of Fisheries Management, 23, 641-659. doi:10.1577/M02-013
[13] Hyun, S.-Y., Keefer, M.W., Fryer, J.D., Jepson, M.A., Sharma, R., Caudill, C.C., Whiteaker, J.M. and Naughton, G.P. (2012) Population-specific escapement of Columbia River fall Chinook salmon: Tradeoffs among estimation techniques. Fisheries Research, Vol. 129-130, pp. 82-93. doi:10.1016/j.fishres.2012.06.013
[14] Kostow, K. (2012) Strategies for reducing the ecological risks of hatchery programs: Case studies from the Pacific Northwest. Environmental Biology of Fishes, 94, 285-310. doi:10.1007/s10641-011-9868-1
[15] Fulton, L.A. (1968) Spawning areas and abundance of Chinook salmon (Oncorhynchus tshawytscha) in the Columbia River Basin—Past and present. US Fish and Wildlife Service, Special Scientific Report, Fisheries No. 571, Washington DC.
[16] Hess, M.A., Rabe, G.D., Vogel, J.L., Stephenson, J.J., Nelson, D.D. and Narum, S.R. (2012) Supportive breeding boosts natural population abundance with minimal negative impacts on fitness of a wild population of Chinook salmon. Molecular Ecology, 21, 5236-5250. doi:10.1111/mec.12046
[17] Chelan (Chelan County Public Utility) (2012) Mid-Columbia Salmon species.
[18] Landeen, D. and Pinkham, A. (1999) Salmon and his people. Quaternary Research, 62, 1-8.
[19] Hanrahan, T.P., Dauble, D.D. and Geist, D.R. (2004) An estimate of Chinook salmon (Oncorhynchus tshawytscha) spawning habitat and red capacity upstream of a migration barrier in the upper Columbia River. Canadian Journal of Fisheries and Aquaculture Science, 61, 23-33. doi:10.1139/f03-140
[20] Johnson, J., Johnson, T. and Copeland, T. (2012) Defining life histories of precocious male parr, minijack, and jack Chinook Salmon using scale patterns. Transactions of the American Fisheries Society, 141, 1545-1556. doi:10.1080/00028487.2012.705256
[21] Connor, W. P., Sneva, J.G., Tiffan, K.E., Steinhorst, R.K. and Ross, D. (2005) Two alternative juvenile life history types for fall Chinook salmon in the Snake River Basin. Transactions of the American Fisheries Society, 134, 291305. doi:10.1577/T03-131.1
[22] Dauble, D.D. and Geist, D.R. (2000) Comparison of mainstem spawning habitats for two populations of fall Chinook salmon in the Columbia River Basin. Regulated Rivers: Research & Management, 16, 345-361. doi:10.1002/1099-1646(200007/08)16:4<345::AID-RRR577>3.0.CO;2-R
[23] Sharma, R. and Quinn, T.P. (2012) Linkages between the life history type and migration pathways in freshwater and marine environments for Chinook salmon, Oncorhynchus tshawytscha. Acta Oecologica, 41, 1-13. doi:10.1016/j.actao.2012.03.002
[24] Hatten, J.R., Tiffan, K.F., Anglin, D.R., Haeseker, S.L., Skalicky, J.J. and Schaller, H. (2009) A spatial model to assess the effects of hydropower operations on Columbia River fall Chinook salmon spawning habitat. North American Journal of Fisheries Management, 29, 1379-1405. doi:10.1577/M08-053.1
[25] Honea, J.M., Jorgensen, J.C., McClure, M.M., Cooney, T.D., Engie, K., Holzer, D.M. and Hilborn, R. (2009) Evaluating habitat effects on population status: Influence of habitat restoration on spring-run Chinook salmon. Freshwater Biology, 54, 1576-1592. doi:10.1111/j.1365-2427.2009.02208.x
[26] Geist, D.R., Jones, J., Murray, C.J. and Dauble, D.D. (2000) Suitability criteria analyzed at the spatial scale of redd clusters improved estimates of fall Chinook salmon (Oncorhynchus tshawytscha) spawning habitat use in the Hanford Reach, Columbia River. Canadian Journal of Fisheries and Aquatic Sciences, 57, 1636-1646. doi:10.1139/f00-101
[27] Geist, D.R. (2000) Hyporhelc discharge of river water into fall Chinook salmon spawning areas in the Hanford Reach, Columbia River. Canadian Journal of Fisheries and Aquatic Sciences, 57, 1647-1656. doi:10.1139/f00-102
[28] Donley, E.E., Naiman, R.J. and Marineau, M.D. (2012) Strategic planning for instream flow restoration: A case study of potential climate change impacts in the central Columbia River basin. Global Change Biology, 18, 30713086. doi:10.1111/j.1365-2486.2012.02773.x
[29] Regetz, J. (2003) Landscale-level constraints on recruitment of Chinook salmon (Oncorhynchus tshawytscha) in the Columbia River, USA. Aquatic Conservation: Marine and Freshwater Ecosystems, 13, 35-49. doi:10.1002/aqc.524
[30] Farag, A.M., Harper, D.D., Cleveland, L., Brumbaugh, W.G. and Little, E.E. (2006) The potential for chromium to affect the fertilization process of Chinook salmon (Oncorhynchus tshawytscha) in the Hanford Reach of the Columbia River, Washington, USA. Archives of Environmental Contamination and Toxicology, 50, 575-579. doi:10.1007/s00244-005-0010-2
[31] Good, T., McClure, M.M., Sandford, B.P., Barnas, K.A., Marsh, D.M., Ryan, B.A. and Casillas, E. (2007) Quantifying the effect of the Caspian tern predation on threatened and endangered Pacific salmon in the Columbia River estuary. Endangered Species Research, 3, 11-21. doi:10.3354/esr003011
[32] Stuart, S.C., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, A.S.L., Fishman, D.L. and Waller, R.W. (2004) Status and trends of amphibian declines and extinctions. Science, 306, 1783. doi:10.1126/science.1103538
[33] Ballie, J.E.M., Hilton-Tarylor, C. and Stuart, S.N. (2004) IUCN red list of threatened species: A global species assessment. IUCN Publications Services Unit, Cambridge. doi:10.2305/IUCN.CH.2005.3.en
[34] Blaustein, A.R., Wake, D.B. and Sousa, W.P. (1994) Amphibian declines: Judging stability, persistence, and susceptibility of populations to local and global extinctions. Conservation Biology, 8, 60-71. doi:10.1046/j.1523-1739.1994.08010060.x
[35] Hillis, D.M. (1988) Systematics of the Rana pipiens complex: Puzzle and paradigm. Annual review of Ecology and Systematics, 19, 39-63. doi:10.1146/
[36] Newman, C.E., Feinberg, J.A., Rissler, L.J., Burger, J. and Shaffer, H.B. (2012) A new species of leopard frog (Anura:Ranidae) from the urban northeastern US. Molecular Phylogenetics and Evolution, 63, 445-455.
[37] Lannoo, M. (2005) Amphibian declines: The conservation status of United States species. University of California Press, Berkeley.
[38] Daszak, P., Scott, D.E., Kilpatrick, A.M., Faggioni, C., Gibbons, J.W. and Porter, D. (2005) Amphibian population declines at Savannah River Site are linked to climate not chytridiomycosis. Ecology, 86, 3232-3237. doi:10.1890/05-0598
[39] Clarkson, R.W. and Rorabaugh, J.C. (1989) Status of leopard frogs (Rana pipiens complex) in Arizona and southeastern California. Southwestern Naturalist, 34, 531-538. doi:10.2307/3671513
[40] Rorabaugh, J.C. (2005) Rana pipiens schreber, 1782, northern leopard frog. In: Lannoo, M., Ed., Amphibian Declines: The Conservation Status of United States Species, University of California Press, Berkeley, 570-577.
[41] Woodhams, D.C., Hyatt, A.D., Boyle, D.G. and RollinsSmith, L.A. (2008) The northern leopard frog Rana pipiens is a widespread reservoir species harboring Batrachochytrium dendrobatidis in North America. Herpetological Review, 39, 66-68.
[42] Wagner, G. (1997) Status of the northern leopard frog (Rana pipiens) in Alberta. Wildlife Status Report, No. 9, Alberta Environmental Protection, Edmonton.
[43] Hoffman, E.A., Schueler, F.W. and Blouin, M.S. (2004) Effective population sizes and temporal stability of genetic structure in Rana pipiens, the northern leopard frog. Evolution, 58, 2536-2545.
[44] Merrell, D.J. (1968) A comparison of the estimated size and the “effective size” of breeding populations of the leopard frog, Rana pipiens. Evolution, 22, 274-283. doi:10.2307/2406526
[45] Moore, J.A. (1949) Geographic variation of adaptive characters in Rana pipiens. Evolution, 3, 1-24. doi:10.2307/2405448
[46] Ultsch, G.R., Bradford, D.F. and Freda, J. (1999) Physiology: Coping with the environment. In: McDiarmid, R.W. and Altig, R., Eds., Tadpoles: The Biology of Anuran Larvae, University of Chicago Press, Berkeley, 189214.
[47] Hecnar, S.J. and M’Closkey, R.T. (1997) The effects of predatory fish on amphibian species richness and distribution. Biological Conservation, 79, 123-131. doi:10.1016/S0006-3207(96)00113-9
[48] Relyea, R.A. (2004) Synergistic impacts of malathion and predatory stress on six species of North American tadpoles. Environmental Toxicology and Chemistry, 23, 10801084. doi:10.1897/03-259
[49] Relyea, R.A. (2009) A cocktail of contaminants: How mixtures of pesticides at low concentrations affect aquatic communities. Oecologia, 159, 363-376. doi:10.1007/s00442-008-1213-9
[50] Gross, J.A., Chen, T.-H. and Karasov, W.H. (2007) Lethal and sublethal effects of chronic cadmium exposure on northern leopard frog (Rana pipiens) tadpoles. Environmental Toxicology and Chemistry, 26, 1192-1197. doi:10.1897/06-479R.1
[51] Daszak, P., Berger, L., Cunningham, A.A., Hyatt, A.D., Green, D.E. and Speare, R. (1999) Emerging infectious diseases and amphibian population declines. Emerging Infectious Diseases, 5, 735-748. doi:10.3201/eid0506.990601
[52] Gerald, G.W., Bailey, M.A. and Holmes, N.J. (2006) Habitat utilization of pituophis melanoleucus on Arnold Air Force Base in middle Tennessee. Southwestern Naturalist, 5, 253-264. doi:10.1656/1528-7092(2006)5[253:HUOPMM]2.0.CO;2
[53] Golden, D.M., Winkler, P., Woerner, P., Fowles, G., Pitts, W. and Jenkins, D. (2009) Status assessment of the Northern Pine Snake (Pituophis m melanoleucus) in New Jersey: An evaluation of trends and threats. New Jersey Department of Environmental Protection, Trenton.
[54] Burger, J. and Zappalorti, R.T. (2011) The northern pine snake (Pituophis melanoleucus): Its life history, behavior, and conservation. Nova Science, New York.
[55] Burger, J., Zappalorit, R.T., Gochfeld, M. and DeVito, E. (2007) Effects of off-road vehicles on reproductive success of pine snakes (Pituophus melanoleucus) in the New Jersey pinelands. Urban Ecosystems, 10, 275-284. doi:10.1007/s11252-007-0022-y
[56] Burger, J. (1998) Effects of incubation temperature on behavior of hatchling pine snakes: Implications for survival. Behavioral Ecology and Sociobiology, 43, 11-18. doi:10.1007/s002650050461
[57] Burger, J. and Zappalorti, R.T. (1992) Philopatry and nesting phenology of pine snakes Pituophis melanoleucus in the New Jersey Pine Barrens. Behavioral Ecology and Sociobiology, 30, 331-326. doi:10.1007/BF00170599
[58] Burger, J., Zappalorti, R.T., Gochfeld, M., Boarman, W.I., Caffrey, M., Doig, M., Garber, S.D., Lauro, B., Mikovsky, M., Safina, C. and Saliva, J. (1988) Hiber-nacula and summer den sites of pine snakes (Pituophis melanoleucus) in the New Jersey Pine Barrens. Journal of Herpetology, 22, 425-433. doi:10.2307/1564337
[59] Burger, J., Zappalorti, R.T., Dowdell, J., Georgiadis, T., Hill, J. and Gochfeld, M. (1992) Subterranean predation on pine snakes (Pituophis melanoleucus). Journal of Herpetology, 26, 259-263. doi:10.2307/1564879
[60] Burger, J. and Zappalorti, R.T. (1989) Habitat use by pine snakes (Pituophis melanoleucus) in the New Jersey Pine Barrens: Individual and sexual variation. Journal of Herpetology, 23, 68-73. doi:10.2307/1564318
[61] Baker, A.J., Gonzalez, P.M., Piersma, T., Niles, L.J., de Lima Serrano do Nascimento, I., Atkinson, P.W., Clark, N.A., Minton, C.D.T., Peck, M.K. and Aarts, G. (2004) Rapid population decline in red knots: Fitness consequences of decreased refuelling rates and late arrival in Delaware Bay. Proceedings of the Royal Society of London, Series B, 271, 875-882. doi:10.1098/rspb.2003.2663
[62] Niles, L.J., Sitters, H.P., Dey, A.D., Atkinson, P.W., Baker, A.J., Bennett, K.A., Carmona, R., Clark, K.E., Clark, N.A., Espoz, C., González, P.M., Harrington, B.A., Hernández, D.E., Kalasz, K.S., Lathrop, R.G., Matus, R.N., Minton, C.D.T., Morrison, R.I.G., Peck, M.K., Pitts, W., Robinson, R.A. and Serrano, I.L. (2008) Status of the red knot (Calidris canutus rufa) in the western hemisphere. Studies in Avian Biology, 36, 185 p.
[63] Morrison, R.I.G., Ross, R.K. and Niles, L.J. (2004) Decline sin wintering populations of red knots in southern South America. The Condor, 106, 60-76. doi:10.1650/7372
[64] Niles, L., Burger, J., Porter, R.R., Dey, A.D., Minton, C.D.T., Gonzalez, P.M., Baker, A.J., Fox, J.W. and Gordon, C. (2010) First results using light level geolocators to track red knots in the western hemisphere show rapid and long intercontinental flights and new details of migration paths. Wader Study Group Bulletin, 117, 1-8.
[65] Withers, K. (2002) Shorebird use of coastal wetlands and barrier island habitat in the Gulf of Mexico. Science World Journal, 2, 514-536. doi:10.1100/tsw.2002.112
[66] Niles, L.J., Bart, J., Sitters, H.P., Dey, A.D., Clark, K.E., Atkinson, P.W., Baker, A.J., Bennet, K.A., Kalasz, K.S., Clark, N.A., Clark, N.A., Clark, J., Gillings, S., Gates, A.S., Gonzalez, P.M., Hernandez, D.E., Minton, C.T., Morrison, R.I., Porter, R.R., Ross, R.K. and Veitch, C.R. (2009) Effects of horseshoe crab harvest in delaware bay on red knots: Are harvest restrictions working? Bioscience, 59, 153-164. doi:10.1525/bio.2009.59.2.8
[67] Morrison, R.I.G., Davidson, N.C. and Wilson, J.R. (2007) Survival of the fattest: Body stores on migration and survival in red knots, Calidris canutus islandica. Journal of Avian Biology, 38, 479-487.
[68] Burger, J., Gordon, C., Niles, L.J., Newman, J., Forcey, G. and Vlietstra, L. (2011) Risk evaluation for federally listed (roseate tern, piping plover) or candidate (red knot) bird species of in offshore waters: A first step for managing the potential impacts of wind facility development on the Atlantic Outer Continental Shelf. Renewable Energy, 36, 338-351. doi:10.1016/j.renene.2010.06.048
[69] Galbraith, H, Jones, R., Park, R., Clough, J, HerrodJulius, S., Harrington, B. and Page, G. (2002) Global climate change and sea level rise: Potential losses of intertidal habitat for shorebirds. Waterbirds, 25, 173-183.
[70] Burger, J. and Niles, L.J. (2012) Shorebirds and stakeholders: Effects of beach closure and human activities on shorebirds at a New Jersey coastal beach. Urban Ecosystems, published on line. doi:10.1007/s11252-012-0269-9
[71] Maxted, A.M., Luttrell, M.P., Goekjian, V.H., Brown, J.D., Niles, L.J., Dey, A.D., Kalasz, K.S., Swayne, D.E. and Stallknecht, D.E. (2012) Avian influenza virus infection dynamics in shorebird hosts. Journal of Wildlife Diseases, 48, 322-335.
[72] Burger, J., Carlucci, S.A., Jeitner, C.W. and Niles, L. (2007) Habitat choice, disturbance, and management of foraging shorebirds and gulls at a migratory stopover. Journal of Coastal Research, 23, 1159-1166. doi:10.2112/04-0393.1
[73] Goss-Custard, J.D., Triplet, P., Sueur, R. and West, A.D. (2006) Critical thresholds of disturbance by people and raptors in foraging wading birds. Biological Conservation, 127, 88-97. doi:10.1016/j.biocon.2005.07.015
[74] Butler, V.L. and O’Connor, J.E. (2004) 9000 years of salmon fishing on the Columbia River, North America. Quaternary Research, 62, 1-8. doi:10.1016/j.yqres.2004.03.002
[75] Thompson, W.L. and Lee, D.C. (2002) A two-stage information approach to modeling landscape-level attributes and maximum recruitment of Chinook salmon in the Columbia River basin. Natural Resource Modeling, 2, 227-257.
[76] Tiffan, K.F., Clark, L.O., Garland, R.D. and Rondorf, D. (2006) Variables influencing the presence of subyearling fall chinook salmon in shoreline habitats of the Hanford Reach, Columbia River. North American Journal of Fisheries Management, 26, 351-360. doi:10.1577/M04-161.1
[77] deGroot, R.S., Wilson, M.A. and Boumans, R.M.J. (2002) A typology for the classification, description and valuation of ecosystem functions, goods, and services. Ecological Economics, 41, 393-408. doi:10.1016/S0921-8009(02)00089-7
[78] Burger, J. (2006) Bioindicators: Types, development and use in ecological assessment and research. Environmental Bioindicators, 1, 22-30. doi:10.1080/15555270590966483
[79] Heink, U. and Kowarik, I. (2010) What are indicators? On the definition of indicators in ecology and environmental planning. Ecological Indicators, 10, 584-593. doi:10.1016/j.ecolind.2009.09.009

comments powered by Disqus

Copyright © 2018 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.