Response of phytoplankton in an alpine lake to inputs of dissolved organic matter through nutrient enrichment and trophic forcing

Limnology and Oceanography

Volumn 58, Issue 3, 2013, Pages 867-880

  Kissman, Carrie E H ^a,c   Williamson, Craig E ^a   Rose, Kevin C ^a,d   Saros, Jasmine E ^b  

^a MIAMI UNIVERSITY   (United States)

^b UNIVERSITY OF MAINE   (United States)

^c ST NORBERT COLLEGE   (United States)

^d SMITHSONIAN ENVIRONMENTAL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMASS; CLIMATE CHANGE; DIATOM; DISSOLVED ORGANIC MATTER; EPILIMNION; GLACIAL LAKE; GROWTH RATE; HYPOLIMNION; MICROCOSM; NUTRIENT ENRICHMENT; PEST OUTBREAK; PHYTOPLANKTON; TREELINE; TROPHIC CONDITIONS; ZOOPLANKTON;

EID: 84877741836     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2013.58.3.0867     Document Type: Article

References (53)

1. AMERICAN PUBLIC HEALTH ASSOCIATION. 2000. Standard methods for the examination of water and wastewater, 20th ed.
2. APHA BERGGREN, M., and OTHERS. 2010. Lake secondary production fueled by rapid transfer of low molecular weight organic carbon from terrestrial sources to aquatic consumers. Ecol. Lett. 13: 870-880, doi:10.1111/j.1461-0248.2010.01483.x
3. BRETT, M. T., M. J. KAINZ, S. J. TALPALE, and H. SESHAN. 2009. Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production. Proc. Natl. Acad. Sci. USA 106: 21197-21201, doi:10.1073/pnas.0904129106
4. CARPENTER, S. R., and OTHERS. 2005. Ecosystem subsidies: Terrestrial support of aquatic food webs from 13C addition to contrasting lakes. Ecology 86: 2737-2750, doi:10.1890/04-1282
5. CLERK, S., R. HALL, R. QUINLAN, and J. P. SMOL. 2000. Quantitative inferences of past hypolimnetic anoxia and nutrient levels from a Canadian Precambrian Shield lake. J. Paleolimnol. 23: 319-336, doi:10.1023/A:1008147127606
6. CLOW, D. W., C. RHOADES, J. BRIGGS, M. CALDWELL, and W. M. LEWIS. 2011. Responses of soil and water chemistry to mountain pine beetle induced tree mortality in Grand County, Colorado, USA. Appl. Geochem. 26: S174-S178, doi:10.1016/j.apgeochem.2011.03.096
7. COLE, J. J., S. R. CARPENTER, J. KITCHELL, M. L. PACE, C. T. SOLOMON, and B. WEIDEL. 2011. Strong evidence for terrestrial support of zooplankton in small lakes based on stable isotopes of carbon, nitrogen, and hydrogen. Proc. Natl. Acad. Sci. USA 108: 1975-1980, doi:10.1073/pnas.1012807108
8. COLE, J. J., S. R. CARPENTER, M. L. PACE, M. C. VAN DE BOGERT, J. L. KITCHELL, and J. R. HODGSON. 2006. Differential support of lake food webs by three types of terrestrial organic carbon. Ecol. Lett. 9: 558-568, doi:10.1111/j.1461-0248.2006.00898.x
9. COOKE, S. L., C. E. WILLIAMSON, B. R. HARGREAVES, and D. P. MORRIS. 2006a. Beneficial and detrimental interactive effects of dissolved organic matter and ultraviolet radiation on zooplankton in a transparent lake. Hydrobiologia 568: 15-28., doi:10.1007/s10750-005-0006-y
10. COOKE, S. L., C. E. WILLIAMSON, and J. E. SAROS. 2006b. How do temperature, dissolved organic matter and nutrients influence the response of Leptodiaptomus ashlandi to UV radiation in a subalpine lake? Freshw. Biol. 51: 1827-1837, doi:10.1111/j.1365-2427.2006.01618.x
11. CULVER, D. A., M. M. BOUCHERLE, D. J. BEAN, and J. W. FLETCHER. 1985. Biomass of freshwater crustacean zooplankton from length-weight regressions. Can. J. Fish. Aquat. Sci. 42: 1380-1390, doi:10.1139/f85-173
12. DANIELSDOTTIR, M. G., M. T. BRETT, and G. B. ARHONDITSIS. 2007. Phytoplankton food quality control of planktonic food web processes. Hydrobiologia 589: 29-41, doi:10.1007/s10750-007-0714-6
13. DEMOTT, W. R., and A. J. TESSIER. 2002. Stoichiometric constraints vs. algal defenses: Testing mechanisms of zooplankton food limitation. Ecology 83: 3426-3433, doi:10.1890/0012-9658(2002)083[3426:SCVADT]2.0.CO;2
14. FAITHFULL, C., M. HUSS, T. VREDE, J. KARLSSON, and A.-K. BERGSTROM. 2012. Transfer of bacterial production based on labile carbon to higher trophic levels in an oligotrophic pelagic system. Can. J. Fish. Aquat. Sci. 69: 85-93, doi:10.1139/f2011-142
15. FAITHFULL, C., M. HUSS, T. VREDE, and A.-K. Bergström. 2011. Bottom-up carbon subsidies and top-down predation pressure interact to affect aquatic food web structure. Oikos 120: 311-320, doi:10.1111/j.1600-0706.2010.18683.x
16. FEE, E. J., R. E. HECKY, S. E. M. KASIAN, and D. R. CRUIKSHANK. 1996. Effects of lake size, water clarity, and climatic variability on mixing depths in Canadian Shield lakes. Limnol. Oceanogr. 41: 912-920, doi:10.4319/lo.1996.41.5.0912
17. FRANCIS, T. B., D. E. SCHINDLER, G. W. HOLTGRIEVE, E. R. LARSON, M. D. SCHEUERELL, B. X. SEMMENS, and E. J. WARD. 2011. Habitat structure determines resource use by zooplankton in temperate lakes. Ecol. Lett. 14: 364-372, doi:10.1111/j.1461-0248.2011.01597.x
18. FROST, P. C., C. T. CHERRIER, J. H. LARSON, S. BRIDGHAM, and G. A. LAMBERTI. 2007. Effects of dissolved organic matter and ultraviolet radiation on the accrual, stoichiometry and algal taxonomy of stream periphyton. Freshw. Biol. 52: 319-330, doi:10.1111/j.1365-2427.2006.01696.x
19. GRANELI, E., P. CARLSSON, and C. LEGRAND. 1999. The role of C, N and P in dissolved and particulate organic matter as a nutrient source for phytoplankton growth, including toxic species. Aquat. Ecol. 33: 17-27, doi:10.1023/A:1009925515059
20. HARSCH, M. A., P. E. HULME, M. S. MCGLONE, and R. P. DUNCAN. 2009. Are treelines advancing? A global metaanalysis of treeline response to climate warming. Ecol. Lett. 12: 1040-1049, doi:10.1111/j.1461-0248.2009.01355.x
21. INTERLANDI, S. J., S. S. KILHAM, and E. C. THERIOT. 1999. Responses of phytoplankton to varied resource availability in large lakes of the greater Yellowstone ecosystem. Limnol. Oceanogr. 44: 668-682, doi:10.4319/lo.1999.44.3.0668
22. KAGAMI, M., N. R. HELMSING, and E. VAN DONK. 2011. Parasitic chytrids could promote copepod survival by mediating material transfer from inedible diatoms. Hydrobiologia 659: 49-54, doi:10.1007/s10750-010-0274-z
23. KAGAMI, M., B. W. IBELINGS, A. DE BRUIN, and E. VAN DONK. 2005. Vulnerability of Asterionella formosa to Daphnia grazing: The impact of a fungal parasite. Verh. Int. Ver. Limnol. 29: 350-354.
24. KAGAMI, M., T. YOSHIDA, T. B. GURUNG, and J. URABE. 2002. Direct and indirect effects of zooplankton on algal composition in in situ grazing experiments. Oecologia 133: 356-363, doi:10.1007/s00442-002-1035-0
25. KLUG, J. L. 2002. Positive and negative effects of allochthonous dissolved organic matter and inorganic nutrients on phytoplankton growth. Can. J. Fish. Aquat. Sci. 59: 85-95, doi:10.1139/f01-194
26. LURLING, M. 2003. Effects of microcystin-free and microcystin containing strains of the cyanobacterium Microcystis aeruginosa on growth of the grazer Daphnia magna. Environ. Toxicol. 18: 202-211, doi:10.1002/tox.10115
27. MATTHEWS, B., and A. MAZUMDER. 2006. Habitat specialization and the exploitation of allochthonous carbon by zooplankton. Ecology 87: 2800-2812, doi:10.1890/0012-9658(2006)87[2800:HSATEO]2.0.CO;2
28. MCKNIGHT, D. M., R. HARNISH, R. L. WERSHAW, J. S. BARON and S. SCHIFF. 1997. Chemical characteristics of particulate, colloidal and dissolved organic material in Loch Vale watershed, Rocky Mountain National Park. Biogeochemistry 36: 99-124, doi:10.1023/A:1005783812730
29. MILBRINK, G., M. L. KRUSE, and J. BENGTSSON. 2003. Competitive ability and life history strategies in four species of Daphnia: D. obtusa, D. magna, D. pulex and D. longispina. Arch. Hydrobiol. 157: 433-453, doi:10.1127/0003-9136/2003/0157-0433
30. MONTEITH, D. T., and OTHERS. 2007. Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450: 537-541, doi:10.1038/nature06316
31. PACE, M. L., and OTHERS. 2004. Whole lake carbon-13 additions reveal terrestrial support of aquatic food webs. Nature 427: 240-243, doi:10.1038/nature02227
32. PACE, M. L., and OTHERS. 2007. Does terrestrial organic carbon subsidize the planktonic food web in a clear-water lake? Limnol. Oceanogr. 52: 2177-2189, doi:10.4319/lo.2007.52.5.2177
33. RAFFA, K. F., B. H. AUKEMA, B. J. BENTZ, A. L. CARROLL, J. A. HICKE, M. G. TURNER, and W. H. ROMME. 2008. Cross-scale drivers of natural disturbances prone to anthropogenic amplification: The dynamics of bark beetle eruptions. BioScience 58: 501-517, doi:10.1641/B580607
34. RAMSTACK, J. M., S. C. FRITZ, D. R. ENGSTROM, and S. A. HEISKARY. 2003. The application of a diatom-based transfer function to evaluate regional water-quality trends in Minnesota since 1970. J. Paleolimnol. 29: 79-94, doi:10.1023/A:1022869205291
35. REID, J. W., and C. E. WILLIAMSON. 2010. Copepoda, p. 915-944. In J. H. Thorp and A. P. Covich [eds.], Ecology and classification of North American freshwater invertebrates. Academic Press.
36. ROMAN, M. R., and P. A. RUBLEE. 1980. Containment effects in copepod grazing experiments: A plea to end the black box approach. Limnol. Oceanogr. 25: 982-990, doi:10.4319/lo.1980.25.6.0982
37. ROSE, K. C., C. E. WILLIAMSON, J. E. SAROS, R. SOMMARUGA, and J. M. FISCHER. 2009. Differences in UV transparency and thermal structure between alpine and subalpine lakes: Implications for organisms. Photochem. Photobiol. Sci. 8: 1244-1256, doi:10.1039/b905616e
38. ROUSH, W., J. S. MUNROE, and D. B. FAGRE. 2007. Development of a spatial analysis method using ground-based repeat photography to detect changes in the alpine treeline ecotone, Glacier National Park, Montana, U.S.A. Arct. Antarct. Alp. Res. 39: 297-308, doi:10.1657/1523-0430(2007)39[297:DOASAM]2.0.CO;2
39. SANCLEMENTS, M. D., G. P. OELSNER, D. M. MCKNIGHT, J. L. STODDARD, and S. J. NELSON. 2012. New insights into the source of decadal increases of dissolved organic matter (DOM) in acid-sensitive lakes of the Northeastern U.S. Environ. Sci. Technol. 46: 3212-3219, doi:10.1021/es204321x
40. SANDERS, R. W., C. E. WILLIAMSON, P. L. STUTZMAN, R. E. MOELLER, C. E. GOULDEN, and R. AOKI-GOLDSMITH. 1996. Reproductive success of "herbivorous" zooplankton fed algal and nonalgal food resources. Limnol. Oceanogr. 41: 1295-1305, doi:10.4319/lo.1996.41.6.1295
41. SAROS, J. E., S. J. INTERLANDI, S. DOYLE, T. MICHEL, and C. E. WILLIAMSON. 2005a. Are the deep chlorophyll maxima in alpine lakes primarily induced by nutrient availability, not UV avoidance? Arct. Antarct. Alp. Res. 37: 557-563, doi:10.1657/1523-0430(2005)037[0557:ATDCMI]2.0.CO;2
42. SAROS, J. E., S. J. INTERLANDI, A. P. WOLFE, and D. R. ENGSTROM. 2003. Recent changes in the diatom community structure of lakes in the BeartoothMountain Range, U.S.A. Arct. Antarct. Alp. Res. 35: 18-23, doi:10.1657/1523-0430(2003)035[0018:RCITDC]2.0.CO;2
43. SAROS, J. E., T. J. MICHEL, S. J. INTERLANDI, and A. P. WOLFE. 2005b. Resource requirements of Asterionella formosa and Fragilaria crotonensis in oligotrophic alpine lakes: Implications for recent phytoplankton community reorganizations. Can. J. Fish. Aquat. Sci. 62: 1681-1689, doi:10.1139/f05-077
44. SAROS, J. E., and OTHERS. 2010. Melting alpine glaciers enrich highelevation lakes with reactive nitrogen. Environ. Sci. Technol. 44: 4891-4896, doi:10.1021/es100147j
45. SCOTT, C. E., J. E. SAROS, C. E. WILLIAMSON, S. C. PETERS, and D. L. MITCHELL. 2009. Effects of nutrients and dissolved organic matter on the response of phytoplankton to ultraviolet radiation: Experimental comparison in spring versus summer. Hydrobiologia 619: 155-166, doi:10.1007/s10750-008-9608-5
46. SHURIN, J. B., and OTHERS. 2010. Environmental stability and lake zooplankton diversity-contrasting effects of chemical and thermal variability. Ecol. Lett. 13: 453-463, doi:10.1111/j.1461-0248.2009.01438.x
47. SOMMARUGA, R., R. PSENNER, E. SCHAFFERER, K. A. KOINIG, and S. SOMMARUGA-WOGRATH. 1999. Dissolved organic carbon concentration and phytoplankton biomass in high-mountain lakes of the Austrian Alps: Potential effect of climatic warming on UV underwater attenuation. Arct. Antarct. Alp. Res. 31: 247-253, doi:10.2307/1552253
48. VINEBROOKE, R. D., and P. R. LEAVITT. 1998. Direct and interactive effects of allochthonous dissolved organic matter, inorganic nutrients, and ultraviolet radiation on an alpine littoral food web. Limnol. Oceanogr. 43: 1065-1081, doi:10.4319/lo.1998.43.6.1065
49. WEYHENMEYER, G. A., and J. KARLSSON. 2009. Nonlinear response of dissolved organic carbon concentrations in boreal lakes to increasing temperatures. Limnol. Oceanogr. 54: 2513-2519, doi:10.4319/lo.2009.54.6_part_2.2513
50. WILLIAMSON, C. E., W. DODDS, T. K. KRATZ, and M. A. PALMER. 2008. Lakes and streams as sentinels of environmental change in terrestrial and atmospheric processes. Front. Ecol. Environ. 6: 247-254, doi:10.1890/070140
51. WILLIAMSON, C. E., D. P. MORRIS, M. L. PACE, and O. G. OLSON. 1999. Dissolved organic carbon and nutrients as regulators of lake ecosystems: Resurrection of a more integrated paradigm. Limnol. Oceanogr. 44: 795-803, doi:10.4319/lo.1999.44.3_part_2.0795
52. WILLIAMSON, C. E., C. SALM, S. L. COOKE, and J. E. SAROS. 2010. How do UV radiation, temperature, and zooplankton influence the dynamics of alpine phytoplankton communities? Hydrobiologia 648: 73-81, doi:10.1007/s10750-010-0147-5
53. WILLIAMSON, C. E., J. E. SAROS, W. F. VINCENT, and J. P. SMOL. 2009. Lakes and reservoirs as sentinels, integrators, and regulators of climate change. Limnol. Oceanogr. 54: 2273-2282, doi:10.4319/lo.2009.54.6_part_2.2273