Terrestrial carbohydrates support freshwater zooplankton during phytoplankton deficiency

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Taipale, Sami J ^a,b   Galloway, Aaron W E ^c   Aalto, Sanni L ^d   Kahilainen, Kimmo K ^a   Strandberg, Ursula ^b,e   Kankaala, Paula ^b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c UNIVERSITY OF OREGON   (United States)

^d UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^e RYERSON UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; FATTY ACID; FRESH WATER;

ANIMAL; CARBOHYDRATE METABOLISM; CHEMISTRY; DAPHNIA; FOOD CHAIN; LAKE; PHYSIOLOGY; ZOOPLANKTON;

ANIMALS; CARBOHYDRATE METABOLISM; CARBOHYDRATES; DAPHNIA; FATTY ACIDS; FOOD CHAIN; FRESH WATER; LAKES; ZOOPLANKTON;

EID: 84982085631     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep30897     Document Type: Article

References (89)

1. Ackman, R. G. Characteristics of the fatty acid composition and biochemistry of some fresh-water fsh oils and lipids in comparison with marine oils and lipids. J. Com. Biochem. Physiol. 22, 907-922 (1967).
2. Arts, M. T., Brett, M. T. & Kainz, M. J. Lipids in Aquatic Ecosystems. Springer, New York (2009).
3. Hixson, S. M., Sharma, B., Kainz, M. J., Wacker, A. & Arts, M. T. Production, distribution, and abundance of long-chain omega-3 polyunsaturated fatty acids: a fundamental dichotomy between freshwater and terrestrial ecosystems. Environ. Rev. 23, 414-424 (2015).
4. Ahlgren, G., Gustafsson, I.-B. & Boberg, M. Fatty acid content and chemical composition of freshwater microalgae. J. Phycol. 28, 37-50 (1992).
5. Galloway, A. W. E., Britton-Simmons, K. H., Duggins, D. O., Gabrielson. P. W. & Brett, M. T. Fatty acid signatures diferentiate marine macrophytes at ordinal and family ranks. J. Phycol. 48, 956-965 (2012).
6. Taipale, S. J. et al. Fatty acid composition as biomarkers of freshwater microalgae: analysis of 37 strains of microalgae in 22 genera and in 7 classes. Aquat. Microb. Ecol. 71, 165-178 (2013).
7. Polis, G. A., Anderson, W. B. & Holt, R. D. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu. Rev. Ecol. Syst. 28, 289-316 (1997).
8. Bartels, P. et al. Reciprocal subsidies between freshwater and terrestrial ecosystem structure consumer resource dynamics. Ecology 93, 1173-1182 (2012).
9. Soininen, J., Bartels, P., Heino, J., Luoto, M. & Hillebrand, H. Toward more integrated ecosystem research in aquatic and terrestrial environments. BioScience 65, 174-182 (2015).
10. Wilder, S. M., Norris, M., Raymond, W. L., Raubenheimer, D. & Simpson, S. J. Arthropod food webs become increasingly lipid-limited at higher trophic levels. Ecol. Lett. 16, 895-902 (2013).
11. Monteith, D. T. et al. Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 22, 537-540 (2007).
12. Brett, M. T., Kainz, M. J., Taipale, S. J. & Seshan, H. Phytoplankton, not allochthonous carbon sustains herbivorous zooplankton production. Proc. Natl. Acad. Sci. USA 106, 21197-21201 (2009).
13. Kelly, P. T., Solomon, C. T., Weidel, B. C. & Jones, S. E. Terrestrial carbon is a resource, but not a subsidy, for lake zooplankton. Ecology 95, 1236-1242 (2014).
14. Solomon, C. T. et al. Ecosystem consequences of changing inputs of terrestrial dissolved organic matter to lakes: current knowledge and future challenges. Ecosystems 18, 376-389 (2015).
15. Kuijper, L. D. J., Anderson, T. R. & Kooijman, S. A. L. M. C and N gross growth efciencies of copepod egg production studied using a dynamic energy budget model. J. Plankton Res. 26, 213-226 (2004).
16. Arnould, J. P. Y., Green, J. A. & Rawlins, D. R. Fasting metabolism in Antarctic fur seal (Arctocephalus 23azelle) pups. Comp. Biochem. Physiol. A 129, 829-841 (2001).
17. Hiltunen, M., Strandberg, U., Taipale, S. J. & Kankaala, P. Taxonomic identity and phytoplankton diet afect fatty acid composition of zooplankton in large lakes with difering dissolved organic carbon concentration. Limnol. Oceanogr. 60, 303-317 (2015).
18. Jensen, K. et al. Optimal foraging for specifc nutrients in predatory beetles. Proc. Biol. Sci. 7, 2212-2218 (2012).
19. Romano, M. D., Piatt, J. F. & Roby, D. D. Testing the junk-food hypothesis on marine birds: efects of prey type on growth and development. J. Waterbird Soc. 29, 407-524 (2006).
20. Trites, A. W. & Donnelly, C. P. The decline of Stellar sea lions Eumetopias jubatus in Alaska: a review of the nutritional stress hypothesis. Mamm. Rev. 33, 3-28 (2003).
21. 13C addition to contrasting lakes. Ecology 86, 2737-2750 (2005).
22. Karlsson, J. et al. Terrestrial organic matter support of lake food webs: Evidence from lake metabolism and stable hydrogen isotopes of consumers. Limnol Oceanogr 57, 1042-1048 (2012).
23. Jardine, T. D. et al. Reconciling the role of organic matter pathways in aquatic food webs by measuring multiple tracers in individuals. Ecology 96, 3257-3269 (2015).
24. Xenopoulos, M. A. et al. Regional comparisons of watershed determinants of dissolved organic carbon from the Upper Great Lakes region and selected regions globally. Limnol. Oceanogr. 48, 2321-2334 (2003).
25. Mattsson, T. et al. Export of dissolved organic matter in relation to land use along a European climatic gradient. Sci. Tot. Environ. 407, 1967-1976 (2009).
26. 13C in freshwater. Limnol. Oceanogr. Methods 6, 51-53 (2008).
27. Solomon, C. T. et al. Terrestrial, benthic, and pelagic resource use in lakes: results from a three-isotope Bayesian mixing model. Ecology 92, 1115-1125 (2011).
28. Hondula, K. L., Pace, M. L., Cole, J. J. & Batt, R. D. Hydrogen isotope discrimination in aquatic primary producers: Implications for aquatic food web studies. Aquat. Sci. 76, 217-229 (2014).
29. Hayes, J. M. Fractionation of carbon and hydrogen isotopes in biosynthetic processes. In: Stable isotope geochemistry. Reviews in mineralogy and geochemistry. (eds Valley, J. W. & Cole, D. R.), 225-278 (Mineralogical Society of America, Washington, DC, 2001).
30. Münster, U. Concentrations and fuxes of organic carbon substrates in the aquatic environment. Antonie Van Leeuwenhoek 63, 243-274 (1993).
31. Koehler, B., von Wachenfeldt, E., Kothawala, D. & Tranvik, L. J. Reactivity continuum of dissolved organic carbon decomposition in lake water. J. Geophys. Res.-Biogeo. 117, G01024 (2012).
32. Søndergaard, M. & Middelboe, M. A cross-system analysis of labile dissolved organic carbon, Mar. Ecol. Prog. Ser. 118, 283-294 (1995).
33. Hulatt, C. J. et al. Bioavailability and radiocarbon age of fluvial dissolved organic matter (DOM) from a northern peatland-dominated catchment: efect of land-use change. Aquat. Sci. 76, 393-404 (2014).
34. Jansson, M., Persson, L., De Roos, A. M., Jones, R. I. & Tranvik, L. J. Terrestrial carbon and intraspecifc size variation shape lake ecosystems. Trends Ecol. Evol. 22, 316-322 (2007).
35. Brendelberger, H. Filter mesh size of cladocerans predicts retention efciency for bacteria. Limnol. Oceanogr 36, 884-894 (1991).
36. Jurgens, K. Impact of Daphnia on planktonic microbial food webs-A review. Mar. Microb. Food Webs 8, 295-324 (1994).
37. Taipale, S. J., Brett, M. T., Pulkkinen, K. & Kainz, M. J. The influence of bacteria dominated diets on Daphnia magna somatic growth, reproduction and lipid composition. Fems Microbiol. Ecol. 82, 50-62 (2012).
38. Taipale, S. J. et al. Difering Daphnia magna assimilation efciencies for terrestrial, bacterial and algal carbon and fatty acids. Ecology 95, 563-576 (2014).
39. Scharnweber, K. J. et al. Whole-lake experiments reveal the fate of terrestrial particulate organic carbon in benthic food webs of shallow lakes. Ecology 95, 1496-1505 (2014).
40. Taylor, B. R., Parkinson, D. & Parsons, W. F. J. Nitrogen and lignin content as predictors of litter decay rates. A microcosm test. Ecology 70, 97-104 (1989).
41. Taipa le, S. J., Kainz, M. J. & Brett, M. T. A low ω-3:ω-6 ratio in D aphni a indicates terrestrial resource ut ilization and po or nutritional condition. J. Plankton Res 37, 596-610 (2015).
42. Wenzel, A., Bergstrom, A. K., Jansson, M. & Vrede, T. Poor direct exploitation of terrestrial particulate organic material from peat layers by Daphnia galeata. Can. J. Fish Aquat. Sci. 69, 1870-1880 (2012).
43. Galloway, A. W. E. et al. Diet specifc biomarkers show that high-quality phytoplankton fuels herbivorous zooplankton in large boreal lakes. Freshw. Biol. 59, 1902-1915 (2014).
44. Kankaala, P. et al. Impacts of added dissolved organic carbon on boreal freshwater pelagic metabolism and food webs in mesocosm experiments. Fundam. Appl. Limnol. 177, 161-176 (2010).
45. McMeans, B. C., Koussoroplis, A.-M., Arts, M. T. & Kainz, M. J. Terrestrial dissolved organic matter supports growth and reproduction of Daphnia magna when algae are limiting. J. Plankton Res. 37, 1201-1209 (2015).
46. Cole, J. J. et al. 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 (2011).
47. Rautio, M., Mariash, H. & Forsström, L. Seasonal shifts between autochthonous and allochthonous carbon contributions to zooplankton diets in a subarctic lake. Limnol. Oceanogr. 56, 1513-1524 (2011).
48. Mohamed, M. N. & Taylor, W. D. Relative contribution of autochthonous and allochthonous carbon to limnetic zooplankton: A new cross-system approach. Fund. Appl. Limnol. 175, 113-124 (2009).
49. 15N) of lake phytoplankton. Freshwater Biol. 51, 807-822 (2006).
50. 13C values of distinct phytoplankton taxa. Ecosphere, in press (2016).
51. Brett, M. T. & Müller-Navarra, D. C. The role of highly unsaturated fatty acids in aquatic food web processes. Freshwater Biol. 38, 483-499 (1997).
52. Martin-Creuzburg, D. & Von Elert, E. "Ecological signifcance of sterols in aquatic food webs", In Lipids in Aquatic Ecosystems, (eds Arts, M. T., Brett, M. T. & Kainz, M. J.), 25-42 (Springer, New York, 2009).
53. Cole, J. J. et al. Diferential support of lake food webs by three types of terrestrial organic carbon. Ecol. Lett. 9, 558-568 (2006).
54. Simon, M., Cho, B. C. & Azam F. signifcance of bacterial biomass in lakes and the ocean: comparisons to phytoplankton biomass and biogeochemical implications. Mar. Ecol. Prog. Ser. 86, 103-110 (1992).
55. Kankaala, P., Lopez Bellido, J., Ojala, A., Tulonen, T. & Jones, R. I. Variable production by diferent pelagic energy mobilizers in boreal lakes. Ecosystems 16, 1152-1164 (2013).
56. del Giorgio, P. A. & Cole, J. J. Bacterial growth efciency in natural aquatic systems. Annu. Rev. Ecol. Syst. 29, 503-541 (1998).
57. Berggren, M., Laudon, H. & Jansson, M. Aging of allochthonous organic carbon regulates bacterial production in unproductive boreal lakes. Limnol. Oceanogr. 54, 133-1342 (2009).
58. Véra, A., Desvilettes, C., Bec, A. & Bourdier, G. Fatty acid composition of freshwater heterotrophic fagellates: an experimental study. Aquat. Microb. Ecol. 25, 271-279 (2001).
59. Blomquist, P., M. Jansson, S. Drakare, A.-K. Bergström & L. Brydsten. Effects of additions of DOC on pelagic biota in a clearwater system: Results from a whole lake experiment in northern Sweden. Microb. Ecol. 42, 383-394 (2001).
60. 13C addition reveals seasonal shifts in zooplankton diet. Ecology 89, 463-474 (2008).
61. Schilder, J. et al. The stable carbon isotope composition of Daphnia ephippia in small temperate lakes rEffects in-methane availability. Limnol. Oceanogr. 60, 1064-1075 (2015).
62. 4 emissions. J. Geophys. Res. 113, G02024 (2008).
63. Carpenter, S. R., Cole, J. J., Pace, M. L. & Wilkinson, G. M. Response of plankton to nutrients, planktivory and terrestrial organic matter: a model analysis of whole-lake experiments. Ecol. Lett. 19, 230-239 (2016).
64. Jones, R. I. The influence of humic substances on lacustrine planktonic food-chains. Hydrobiologia 229, 73-91 (1992).
65. Trane, J. E., Hessen, D. O. & Andersen, T. The absorption of light in lakes: negative impact of dissolved organic carbon on primary productivity. Ecosystems 17, 1040-1052 (2014).
66. Guillard, R. R. L. & Lorenzen, C. J. Yellow-green algae with chlorophyllide. J. Phycol. 8, 10-14 (1972).
67. Watanabe, M. M., Kawachi, M., Hiroki, M. & Kasai F. (eds.) NIES Collection List of Strains: Microalgae and Protozoa. 6th edition. National Institute for Environmental Studies, Environment Agency, Japan, pp 167 (2000).
68. Guillard, R. R. L. Culture of phytoplankton for feeding marine invertebrates. In: Culture of Marine Invertebrate Animals. (eds Smith, W. L. & Chantey, M. H.), 29-60 (Plenum Publishers, 1975).
69. Brett, M. T. Resource quality Effects on Daphnia longispina ofspring ftness. J. Plankton Res. 15, 403-412 (1993).
70. Lampert, W. Feeding and nutrition in Daphnia. In Daphnia. (eds Peters, R. H. & de Bernardi, R.), 143-192 (Memorie dell'Istituto Italiana di Idrobiologia, 1987).
71. Taipale, S. J., Hiltunen, M., Vuorio, K. & Peltomaa, E. Suitability of phytosterols alongside fatty acids as chemotaxonomic biomarkers for phytoplankton. Frontiers in Plant Science 7, 212 (2016).
72. Sluiter, A. et al. Determination of structural carbohydrates and lignin in biomass. NREL Laboratory Analytical Procedure NREL/TP-510-42618. Golden, CO. National Renewable Energy Laboratory (2008).
73. Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers P. A. & Smith, F. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28, 350-356 (1956).
74. Lourenco, S. O. et al. Distribution of intracellular nitrogen in marine microalgae: Calculation of new nitrogen-to-protein conversion factors. Eur. J. Phycol. 39, 17-32 (2004).
75. Postel, L., Fock, H. & Hagen, W. Biomass and Abundance. In: ICES zooplankton methodology manual. (eds Harris, R. P. et al.), 83-192 (Academic Press, London, 2000).
76. Calvo-Flores, F. G., Dobado, J. A., García, J. I. & Martin-Martinez, F. J. Lignin and Lignans as Renewable Raw Materials: Chemistry, Technology and Applications. (John Wiley & Sons Ltd, 2015)
77. Phillips, D. L. & Gregg, J. W. Uncertainty in source partitioning using stable isotopes. Oecologia 127, 171-179 (2001).
78. von Bertalanfy, L. A quantitative theory of organic growth. Hum. Biol. 10, 181-213 (1938).
79. Sperfeld, E. & Wacker, A. Temperature-and cholesterol-induced changes in eicosapentaenoic acid limitation of Daphnia magna determined by a promising method to estimate growth saturation thresholds. Limnol. Oceanogr. 56, 1273-1284 (2011).
80. Arvola, L. Spectrophotometric determination of chlorophyll a and phaeopigments in ethanol extractions. Ann. Bot. Fenn. 18, 221-227 (1981).
81. Galloway, A. W. E. et al. A fatty acid based Bayesian approach for inferring diet in aquatic consumers. PloS ONE 10, e0129723 (2015).
82. Moore, J. W. & Semmens, B. X. Incorporating uncertainty and prior information into stable isotope mixing models. Ecol. Lett. 11, 470-480 (2008).
83. Parnell, A. C., Inger, R., Bearhop, S. & Jackson, A. L. Source partitioning using stable isotopes: coping with too much variation. PloS ONE 5, e9672 (2010).
84. Strandberg, U. et al. Inferring heterogeneous phytoplankton composition with a fatty acid mixing model. Ecosphere 6, doi: 10.1890/ES14-00382.1 (2015).
85. Zwart, B. et al. Typical freshwater bacteria: an analysis of available 16S rRNA gene sequencing from plankton of lakes and rivers. Aquat. Microb. Ecol. 28, 141-155.
86. Taipale, S. J., Jones, R. I. & Tiirola, M. Vertical diversity of bacteria in an oxygen-stratifed humic lake, evaluated using DNA and phospholipid analyses. Aquat. Microb. Ecol. 55, 1-16 (2009).
87. Galloway, A. W. E. & Winder, M. Partitioning the relative importance of phylogeny and environmental conditions on phytoplankton fatty acids. PLoS One 10, e0130053 (2015).
88. Dalsgaard, J., John, M. St., Kattner, G., Müller-Navarra, D. C. & Hagen, W. Fatty acid trophic markers in the pelagic marine food environment. Adv. Mar. Biol. 46, 226-340 (2003).
89. Development Core Team. R: A language and environment for statistical computing. R Foundataion for Statistical Computing, Vienna, Austria (2016).