Disproportionate importance of nearshore habitat for the food web of a deep oligotrophic lake
Stephanie E. Hampton A E , Steven C. Fradkin B , Peter R. Leavitt C and Elizabeth E. Rosenberger DA National Center for Ecological Analysis and Synthesis, 735 State St. Suite 300, University of California, Santa Barbara, CA 93101, USA.
B Olympic National Park, National Park Service, 600 East Park Avenue, Port Angeles, WA 98362, USA.
C University of Regina, Department of Biology, Regina, SK, S4S 0A2 Canada.
D Rocky Mountain Research Station, Boise Aquatic Sciences Lab, 322 East Front St. Suite 401, Boise, ID 83709, USA.
E Corresponding author. Email: hampton@nceas.ucsb.edu
Marine and Freshwater Research 62(4) 350-358 https://doi.org/10.1071/MF10229
Submitted: 29 August 2010 Accepted: 20 December 2010 Published: 28 April 2011
Abstract
In large deep oligotrophic lakes, multiple lines of evidence suggest that the shallow nearshore water provides disproportionately important feeding and breeding habitat for the whole-lake food web. We examined the trophic importance of the nearshore environment, human impacts nearshore, and several approaches to disturbance detection in a deep (190 m) oligotrophic lake with relatively modest residential development. In Lake Crescent, on the Olympic Peninsula of Washington (USA), stable isotope analysis demonstrated that apex salmonid predators derived more than 50% of their carbon from nearshore waters, even though this nearshore water accounted for only 2.5% of total lake volume. Unfortunately, it is this land–water interface that is initially degraded as shorelines are developed. We hypothesised that under these conditions of relatively modest disturbance, the effects of residential development would be strongly localised near to shore. Indeed, we found striking differences between developed and undeveloped sites in periphyton and associated organic matter, though there were no offshore signals of human impact in water nutrient analysis or paleolimnological investigations. Together, these results suggest that nearshore biological monitoring should be integrated in lake management plans to provide ‘early warning’ of potential food-web repercussions before pollution problems are evident in open water and comparatively intractable.
Additional keywords: habitat coupling, littoral zone, Oncorhynchus clarkii, Oncorhynchus mykiss, recreational fisheries, septic systems.
References
Aloi, J., Loeb, S., and Goldman, C. (1988). Temporal and spatial variability of the eulittoral epilithic periphyton, Lake Tahoe, California–Nevada. Journal of Freshwater Ecology 4, 401–410.| Temporal and spatial variability of the eulittoral epilithic periphyton, Lake Tahoe, California–Nevada.Crossref | GoogleScholarGoogle Scholar |
Andersson, E., and Brunberg, A. (2006). Inorganic nutrient acquisition in a shallow clearwater lake – dominance of benthic microbiota. Aquatic Sciences 68, 172–180.
| Inorganic nutrient acquisition in a shallow clearwater lake – dominance of benthic microbiota.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotVekt74%3D&md5=90f3fe811fa91b448f7924be6c7ca413CAS |
APHA (1998). ‘Standard Methods for the Examination of Water and Wastewater.’ (American Public Health Association: Washington, DC).
Arar, E., and Collins, G. (1997). Method 445.0: In vitro determination of chlorophyll a and pheophytin in marine and freshwater algae by fluorescence. National Exposure Research Laboratory Office of Research and Development U.S. Environmental Protection Agency Cincinnati, OH, USA.
Ask, J., Karlsson, J., Persson, L., Ask, P., Bystrom, P., et al. (2009). Whole-lake estimates of carbon flux through algae and bacteria in benthic and pelagic habitats of clear-water lakes. Ecology 90, 1923–1932.
| Whole-lake estimates of carbon flux through algae and bacteria in benthic and pelagic habitats of clear-water lakes.Crossref | GoogleScholarGoogle Scholar | 19694140PubMed |
Baker, B. (1998). Genetic analysis of two naturally spawning populations of Crescent lake cutthroat trout, Barnes Creek and Lyre River. Report of the Molecular Genetics Laboratory, Washington Department of Fish and Wildlife. Olympia, WA, USA. November 1998.
Baker, B. (2000). Genetic analysis of Beardslee rainbow trout from Crescent Lake. Report of the Molecular Genetics Laboratory, Washington Department of Fish and Wildlife, Olympia, WA, USA.
Bowker, D., Wareham, M. T., and Learner, A. M. (1983). The selection and ingestion of epilithic algae by Nais elinguis (Oligochaeta : Naididae). Hydrobiologia 98, 171–178.
| The selection and ingestion of epilithic algae by Nais elinguis (Oligochaeta : Naididae).Crossref | GoogleScholarGoogle Scholar |
Brett, M., and Muller-Navarra, D. (1997). The role of highly unsaturated fatty acids in aquatic food web processes. Freshwater Biology 38, 483–499.
| The role of highly unsaturated fatty acids in aquatic food web processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmsFSkuw%3D%3D&md5=1d663edfabd1b4f00bb2774ba000c895CAS |
Bunting, L., Leavitt, P. R., Weidman, R. P., and Vinebrooke, R. D. (2010). Regulation of the nitrogen biogeochemistry of mountain lakes by subsidies of terrestrial dissolved organic matter and the implications for climate studies. Limnology and Oceanography 55, 333–345.
| Regulation of the nitrogen biogeochemistry of mountain lakes by subsidies of terrestrial dissolved organic matter and the implications for climate studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVSgurs%3D&md5=52fded2bb6c15b00878ecd4086babe83CAS |
Carpenter, S. R., Cole, J. J., Pace, M. L., Van de Bogert, M., Bade, D. L., et al. (2005). Ecosystem subsidies: terrestrial support of aquatic food webs from C-13 addition to contrasting lakes. Ecology 86, 2737–2750.
| Ecosystem subsidies: terrestrial support of aquatic food webs from C-13 addition to contrasting lakes.Crossref | GoogleScholarGoogle Scholar |
Cott, P. A., Sibley, P. K., Somers, W. M., Lilly, M. R., and Gordon, A. M. (2008). A review of water level fluctuations on aquatic biota with an emphasis on fishes in ice-covered lakes. Journal of the American Water Resources Association 44, 343–359.
| A review of water level fluctuations on aquatic biota with an emphasis on fishes in ice-covered lakes.Crossref | GoogleScholarGoogle Scholar |
Diehl, S. (1992). Fish predation and benthic community structure: the role of omnivory and habitat complexity. Ecology 73, 1646–1661.
| Fish predation and benthic community structure: the role of omnivory and habitat complexity.Crossref | GoogleScholarGoogle Scholar |
Dolson, R., McCann, K., Rooney, N., and Ridgway, M. (2009). Lake morphometry predicts the degree of habitat coupling by a mobile predator. Oikos 118, 1230–1238.
| Lake morphometry predicts the degree of habitat coupling by a mobile predator.Crossref | GoogleScholarGoogle Scholar |
Donohue, I., and Molinos, J. G. (2009). Impacts of increased sediment loads on the ecology of lakes. Biological Reviews of the Cambridge Philosophical Society 84, 517–531.
| Impacts of increased sediment loads on the ecology of lakes.Crossref | GoogleScholarGoogle Scholar | 19485985PubMed |
Fradkin, S. C. (2010). Long-term limnological monitoring of Lake Crescent: Data summary 2005–2010. NCCN Large Lowland Lakes Monitoring Report. Olympic National Park, National Park Service, Port Angeles, WA.
Francis, T., and Schindler, D. (2006). Degradation of littoral habitats by residential development: woody debris in lakes of the Pacific Northwest and Midwest, United States. Ambio 35, 274–280.
| Degradation of littoral habitats by residential development: woody debris in lakes of the Pacific Northwest and Midwest, United States.Crossref | GoogleScholarGoogle Scholar | 17240759PubMed |
Francis, T., and Schindler, D. (2009). Shoreline urbanization reduces terrestrial insect subsidies to fishes in North American lakes. Oikos 118, 1872–1882.
| Shoreline urbanization reduces terrestrial insect subsidies to fishes in North American lakes.Crossref | GoogleScholarGoogle Scholar |
Francis, T. B., Schindler, D. E., Fox, J. M., and Seminet-Reneau, E. (2007). Effects of urbanization on the dynamics of organic sediments in temperate lakes. Ecosystems 10, 1057–1068.
| Effects of urbanization on the dynamics of organic sediments in temperate lakes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlKrsrrE&md5=dc329b2947aed2885fc4f2cf529c4d12CAS |
Garrison, P., and Wakeman, R. (2000). Use of paleolimnology to document the effect of lake shoreland development on water quality. Journal of Paleolimnology 24, 369–393.
| Use of paleolimnology to document the effect of lake shoreland development on water quality.Crossref | GoogleScholarGoogle Scholar |
Glaz, P. N., Nozais, C., and Arseneault, D. (2009). Macroinvertebrates on coarse woody debris in the littoral zone of a boreal lake. Marine and Freshwater Research 60, 960–970.
| Macroinvertebrates on coarse woody debris in the littoral zone of a boreal lake.Crossref | GoogleScholarGoogle Scholar |
Hadwen, W., and Bunn, S. (2005). Food web response to low-level nutrient and 15N-tracer additions in the littoral zone of an oligotrophic dune lake. Limnology and Oceanography 504, 1096–1105.
| Food web response to low-level nutrient and 15N-tracer additions in the littoral zone of an oligotrophic dune lake.Crossref | GoogleScholarGoogle Scholar |
Hadwen, W., Bunn, S., Arthington, A., and Mosisch, T. (2005). Within-lake detection of the effects of tourist activities in the littoral zone of oligotrophic dune lakes. Aquatic Ecosystem Health & Management 8, 159–173.
| Within-lake detection of the effects of tourist activities in the littoral zone of oligotrophic dune lakes.Crossref | GoogleScholarGoogle Scholar |
Jacoby, J., Bouchard, D. D., and Patmont, C. (1991). Response of periphyton to nutrient enrichment in Lake Chelan, WA. Lake and Reservoir Management 7, 33–43.
| Response of periphyton to nutrient enrichment in Lake Chelan, WA.Crossref | GoogleScholarGoogle Scholar |
Jeppesen, E., Sondergaard, M., Jensen, J. P., Havens, K. E., Anneville, O., et al. (2005). Lake responses to reduced nutrient loading – an analysis of contemporary long-term data from 35 case studies. Freshwater Biology 50, 1747–1771.
| Lake responses to reduced nutrient loading – an analysis of contemporary long-term data from 35 case studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGqsbrL&md5=9e10b26809114b6fc3d61eceeccdb075CAS |
Jonsson, B., Jonsson, N., Hindar, K., Northcote, T., and Engen, S. (2008). Asymmetric competition drives lake use of coexisting salmonids. Oecologia 157, 553–560.
| Asymmetric competition drives lake use of coexisting salmonids.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cngtVGmtQ%3D%3D&md5=6669ec6b4861f53bd267fcad46afd274CAS | 18629544PubMed |
Lambert, D., Cattaneo, A., and Carignan, R. (2008). Periphyton as an early indicator of perturbation in recreational lakes. Canadian Journal of Fisheries and Aquatic Sciences 65, 258–265.
| Periphyton as an early indicator of perturbation in recreational lakes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktVWlsrs%3D&md5=86b331e86702b942bdb1e13f403819e5CAS |
Leavitt, P. R., and Hodgson, D. A. (2001). Sedimentary pigments. In ‘Tracking Environmental Change Using Lake Sediments’. (Eds J. P. Smol, H. J. B. Birks and W. M. Last.) pp. 295–325. (Kluwer Academic Publishers: Dordrecht.)
Leavitt, P. R., Brock, C. S., Ebel, C., and Patoine, A. (2006). Landscape-scale effects of urban nitrogen on a chain of freshwater lakes in central North America. Limnology and Oceanography 51, 2262–2277.
| Landscape-scale effects of urban nitrogen on a chain of freshwater lakes in central North America.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOju7bL&md5=5324354384e2eb5456c1b5cfa6619275CAS |
Lewin, W. C., Okun, N., and Mehner, T. (2004). Determinants of the distribution of juvenile fish in the littoral area of a shallow lake. Freshwater Biology 49, 410–424.
| Determinants of the distribution of juvenile fish in the littoral area of a shallow lake.Crossref | GoogleScholarGoogle Scholar |
Lewin, W., Arlinghaus, R., and Mehner, T. (2006). Documented and potential biological impacts of recreational fishing: Insights for management and conservation. Reviews in Fisheries Science 14, 305–367.
| Documented and potential biological impacts of recreational fishing: Insights for management and conservation.Crossref | GoogleScholarGoogle Scholar |
Loeb, S. L. (1981). An in situ method for measuring the primary productivity and standing crop of the epilithic periphyton community in lentic systems. Limnology and Oceanography 26, 394–399.
| An in situ method for measuring the primary productivity and standing crop of the epilithic periphyton community in lentic systems.Crossref | GoogleScholarGoogle Scholar |
Loeb, S., Reuter, J., and Goldman, C. (1983). Littoral zone production of oligotrophic lakes: the contributions of phytoplankton and periphyton. In ‘Periphyton of Freshwater Ecosystems’. (Ed. R. G. Wetzel.) pp. 161–167. (Dr. W. Junk Publishers: The Hague.)
MacIntyre, S., and Melack, J. (1995). Vertical and horizontal transport in lakes: linking littoral, benthic, and pelagic habitats. Journal of the North American Benthological Society 14, 599–615.
| Vertical and horizontal transport in lakes: linking littoral, benthic, and pelagic habitats.Crossref | GoogleScholarGoogle Scholar |
Marburg, A. E., Turner, M. G., and Kratz, T. K. (2006). Natural and anthropogenic variation in coarse wood among and within lakes. Journal of Ecology 94, 558–568.
| Natural and anthropogenic variation in coarse wood among and within lakes.Crossref | GoogleScholarGoogle Scholar |
McCauley, E., and Kalff, J. (1981). Empirical relationships between phytoplankton and zooplankton biomass in lakes. Canadian Journal of Fisheries and Aquatic Sciences 38, 458–463.
| Empirical relationships between phytoplankton and zooplankton biomass in lakes.Crossref | GoogleScholarGoogle Scholar |
Meyer, J., and Fradkin, S. C. (2002). Summary of fisheries and limnological data for Lake Crescent, Washington. Olympic National Park Report, National Park Service, Port Angeles, WA.
Moore, J. (1975). The role of algae in the diet of Asellus aquaticus L. and Gammarus pulex L. Journal of Animal Ecology 44, 719–730.
| The role of algae in the diet of Asellus aquaticus L. and Gammarus pulex L.Crossref | GoogleScholarGoogle Scholar |
Moore, J., Schindler, D. E., Scheuerell, M. D., Smith, D., and Frodge, A. J. (2003). Lake eutrophication at the urban fringe, Seattle region, USA. Ambio 32, 13–18.
| 12691486PubMed |
Mulholland, P., Tank, J. L., Sanzone, D. M., Wollheim, W. M., Peterson, B. J., et al. (2000). Nitrogen cycling in a forest stream determine by a 15 N tracer addition. Ecological Monographs 70, 471–493.
Nakano, S., and Murakami, M. (2001). Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proceedings of the National Academy of Sciences of the USA 98, 166–170.
| Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslKqsQ%3D%3D&md5=55b88ebbdedfeee79df1fc5728c0dc1aCAS | 11136253PubMed |
O’Connell, M., Dempson, J., and Power, M. (2005). Ecology and trophic relationships of the fishes of Gander Lake, a large, deep, oligotrophic lake in Newfoundland, Canada. International Review of Hydrobiology 90, 486–510.
| Ecology and trophic relationships of the fishes of Gander Lake, a large, deep, oligotrophic lake in Newfoundland, Canada.Crossref | GoogleScholarGoogle Scholar |
O’Toole, A., Hanson, K., and Cooke, S. (2009). The effect of shoreline recreational angling activities on aquatic and riparian habitat within an urban environment: implications for conservation and management. Environmental Management 44, 324–334.
| The effect of shoreline recreational angling activities on aquatic and riparian habitat within an urban environment: implications for conservation and management.Crossref | GoogleScholarGoogle Scholar | 19452206PubMed |
Phillips, D. L., Newsome, S. D., and Gregg, J. W. (2005). Combining sources in stable isotope mixing models: alternative methods. Oecologia 144, 520–527.
| Combining sources in stable isotope mixing models: alternative methods.Crossref | GoogleScholarGoogle Scholar | 15711995PubMed |
Pierce, B. (1984). The trouts of Lake Crescent. M.Sc. Thesis, Colorado State University, Fort Collins.
Probst, W. N., Stoll, S., Peters, L., Fischer, P., and Eckmann, R. (2009). Lake water level increase during spring affects the breeding success of bream Abramis brama (L.). Hydrobiologia 632, 211–224.
| Lake water level increase during spring affects the breeding success of bream Abramis brama (L.).Crossref | GoogleScholarGoogle Scholar |
Reynolds, C. (2008). A changing paradigm of pelagic food webs. International Review of Hydrobiology 93, 517–531.
| A changing paradigm of pelagic food webs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVGgt7nF&md5=baea434203b597e65d41d1dc453c19b1CAS |
Rosenberger, E. E., Hampton, S. E., Fradkin, S. C., and Kennedy, B. P. (2008). Effects of shoreline development on the nearshore environment in large deep oligotrophic lakes. Freshwater Biology 53, 1673–1691.
| Effects of shoreline development on the nearshore environment in large deep oligotrophic lakes.Crossref | GoogleScholarGoogle Scholar |
Sass, G. G., Gille, C. M., Hinke, J. T., and Kitchell, J. F. (2006). Whole-lake influences of littoral structural complexity and prey body morphology on fish predator–prey interactions. Ecology Freshwater Fish 15, 301–308.
| Whole-lake influences of littoral structural complexity and prey body morphology on fish predator–prey interactions.Crossref | GoogleScholarGoogle Scholar |
Savage, C., Leavitt, P., and Elmgren, R. (2004). Distribution and retention of effluent nitrogen in surface sediments of a coastal bay. Limnology and Oceanography 49, 1503–1511.
| Distribution and retention of effluent nitrogen in surface sediments of a coastal bay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVWqs7k%3D&md5=9805eaa7ffa3367cc158950bc88f2ea3CAS |
Schindler, D. W., and Scheuerell, M. (2002). Habitat coupling in lake ecosystems. Oikos 98, 177–189.
| Habitat coupling in lake ecosystems.Crossref | GoogleScholarGoogle Scholar |
Seminet-Reneau, E. (2007). Effects of shoreline development on the nearshore environment of a large deep nutrient-poor lake (Lake Crescent, USA). M.Sc. Thesis, College of Natural Resources. University of Idaho, Moscow, ID.
Strayer, D., and Findlay, S. (2010). Ecology of freshwater shore zones. Aquatic Sciences 72, 127–163.
| Ecology of freshwater shore zones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXit1agurw%3D&md5=9674145a98442c2896476a2db7865514CAS |
Tabor, R. W. (1975). ‘Guide to the Geology of Olympic National Park.’ (University of Washington Press: Seattle).
Threlkeld, S. T. (1994). Benthic–pelagic interactions in shallow-water columns – an experimentalist’s perspective. Hydrobiologia 275, 293–300.
| Benthic–pelagic interactions in shallow-water columns – an experimentalist’s perspective.Crossref | GoogleScholarGoogle Scholar |
Vadeboncoeur, Y., Vander Zanden, M. J., and Lodge, A. D. (2002). Putting the lake back together: reintegrating benthic pathways into lake food web models. BioScience 52, 44–54.
| Putting the lake back together: reintegrating benthic pathways into lake food web models.Crossref | GoogleScholarGoogle Scholar |
Vadeboncoeur, Y., Peterson, G., Vander Zanden, M. J., and Kalff, J. (2008). Benthic algal production across lake size gradients: interactions among morphometry, nutrients, and light. Ecology 89, 2542–2552.
| Benthic algal production across lake size gradients: interactions among morphometry, nutrients, and light.Crossref | GoogleScholarGoogle Scholar | 18831175PubMed |
Vander Zanden, M. J., and Vadeboncoeur, Y. (2002). Fishes as integrators of benthic and pelagic food webs in lakes. Ecology 83, 2152–2161.
| Fishes as integrators of benthic and pelagic food webs in lakes.Crossref | GoogleScholarGoogle Scholar |