Disentangling food quantity and quality effects in zooplankton response to P-enrichment and UV radiation

Limnology and Oceanography

Volumn 57, Issue 1, 2012, Pages 235-250

  Villar Argaiz, Manueal ^a   Bullejos, Francisco Jose ^a   Medina Sanchez, Juan Manuel ^a   Ramos Rodriguez, Eloísa ^a   Delgado Molina, Jose Antonio ^b   Carrillo, Presentación ^a,b  

^a UNIVERSITY OF GRANADA   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMASS; FATTY ACID; FOOD QUALITY; GROWTH CURVE; LAKE ECOSYSTEM; NUTRIENT; NUTRIENT ENRICHMENT; OLIGOTROPHIC ENVIRONMENT; PHOSPHORUS; PRISTINE ENVIRONMENT; SESTON; ULTRAVIOLET RADIATION; ZOOPLANKTON;

ANDALUCIA; BETIC CORDILLERA; MEDITERRANEAN REGION; SIERRA NEVADA [BETIC CORDILLERA]; SPAIN;

COPEPODA; DAPHNIA; DAPHNIA PULICARIA; KERATELLA COCHLEARIS; MIXODIAPTOMUS LACINIATUS; PULICARIA; ROTIFERA;

EID: 84869855951     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2012.57.1.0235     Document Type: Article

References (60)

1. Ahlgren, G., W. Goedkoop, H. Markensten, L. Sonesten, and M. BOBERG. 1997. Seasonal variations in food quality for pelagic and benthic invertebrates in Lake Erken-the role of fatty acids. Freshw. Biol. 38: 550-570, doi:10.1046/j.1365-2427. 1997.00219.x
2. American Public Health Association [APHA]. 1992. Standard methods for the examination of water and wastewater. Port City Press.
3. Ávila, A., and J. PeNuelas. 1999. Increasing frequency of Saharan rains over northeastern Spain and its ecological consequences. Sci. Total Environ. 228: 153-156, doi:10.1016/ S0048-9697(99)00041-8
4. Becker, C., and M. Boersma. 2003. Resource quality effects on life histories of Daphnia. Limnol. Oceanogr. 48: 700-706, doi:10.4319/lo.2003.48.2.0700
5. Boersma, M. 2000. The nutritional quality of P-limited algae for Daphnia. Limnol. Oceanogr. 45: 1157-1161, doi:10.4319/ lo.2000.45.5.1157
6. Boersma, M. and C. Kreutzer. 2002. Life at the edge: Is food quality really of minor importance at low quantities?. Ecology 83: 2552-2561, doi:10.1890/0012-9658(2002)083[2552:LATEIF] 2.0.C0;2
7. Boersma, M. and C. Kreutzer., C. Schops, and E. McCauley. 2001. Nutritional quality of seston for the freshwater herbivore Daphnia galeata X hyalina: Biochemical versus mineral limitations. Oecologia 129: 342-348.
8. Bullejos, F. J., P. Carrillo, M. Villar-Argaiz, and J. M. Medina-SAnchez. 2010. Roles of phosphorus and ultraviolet radiation in the strength of phytoplankton-zooplankton coupling in a Mediterranean high mountain lake. Limnol. Oceanog. 55: 2549-2562, doi:10.4319/lo.2010.55.6.2549
9. Burnham, K. P., and D. R. Anderson. 1998. Model selection and inference: A practical information-theoretic approach. Springer.
10. Carney, H. J., and J. J. Elser. 1990. Strength of zooplanktonphytoplankton coupling in relation to trophic state, p. 615-631. In M. Tilzer and C. Serruya [eds.], Large lakes: Ecological structure and function. Springer-Verlag.
11. Carrillo, P., J. A. Delgado-Molina, J. M. Medina-SAnchez, F. J. Bullejos, and M. Villar-Argaiz. 2008. Phosphorus inputs unmask negative effects of ultraviolet radiation on algae in a high mountain lake. Glob. Change Biol. 14: 423-439, doi:10.1111/j.1365-2486.2007.01496.x
12. Carrillo, P., J. A. Delgado-Molina, J. M. Medina-SAnchez, F. J. Bullejos, and M. Villar-Argaiz., J. M. Medina-SAnchez, and M. Villar-Argaiz. 2002. The interaction of phytoplankton and bacteria in a high mountain lake: Importance of the spectral composition of solar radiation. Limnol. Oceanogr. 47: 1294-1306, doi:10.4319/lo.2002.47.5.1294
13. Carrillo, P., J. A. Delgado-Molina, J. M. Medina-SAnchez, F. J. Bullejos, and M. Villar-Argaiz., J. M. Medina-SAnchez, and M. Villar-Argaiz., I. Reche, P. SAnchez-Castillo, and L. Cruz-Pizarro. 1995. Direct and indirect effects of grazing on the phytoplankton seasonal succession in an oligotrophic lake. J. Plankton Res. 17: 1363-1379, doi:10.1093/plankt/17.6.1363
14. Christie, W. W. 1982. A simple procedure for rapid transmethylation of glycerolipids and cholesteryl esters. J. Lipid Res. 23: 1072-1075.
15. Conde-Porcuna, J. M., and others. 2009. Modelos de funcionamiento de comunidades pelagicas en ecosistemas singulares (lagos de alta montaña del Parque Nacional de Sierra Nevada): Una herramienta para la conservación, p. 175-190. In L. Ramírez and B. Asensio [eds.], Proyectos de investigation en parques nacionales: 2005-08. Organismo Autónomo de Parques Nacionales, Spain, [Modelling pelagic communities in unique ecosystems (high mountain lakes of Sierra Nevada National Park): A tool for conservation.]
16. Cruz-Pizarro, L. 1981. Biomasa y production de Mixodiaptomus laciniatus (Copepoda, Calanoida) en el lago de La Caldera (Sierra Nevada, Granada), p. 115-124. In P. Narcis [ed.], I Actas del Primer Congreso Espaínol de Limnología.
17. Asociacion Espanola de Limnología, [Biomass and production of Mixodiaptomus laciniatus (Copepoda, Calanoida) in Lake La Caldera (Sierra Nevada, Granada).]
18. Delgado-Molina, J. A., P. Carrillo, J. M. Medina-SAnchez, M. Villar-Argaiz, and F. J. Bullejos. 2009. Interactive effects of phosphorus loads and ambient ultraviolet radiation on the algal community in a high-mountain lake. J. Plankton Res. 31: 619-634, doi:10.1093/plankt/fbp018
19. DeMott, W. R., R. D. Gulati, and E. Van Donk. 2001. Effects of dietary phosphorus deficiency on the abundance, phosphorus balance, and growth of Daphnia cucullata in three hypereutrophic Dutch lakes. Limnol. Oceanogr. 46: 1871-1880, doi:10.4319/lo.2001.46.8.1871
20. Elser, J. J., and others. 2005. Response of grazing snails to phosphorus enrichment of modern stromatolite microbial communities. Freshw. Biol. 50: 1826-1835, doi: 10.1111/ j.1365-2427.2005.01453.x
21. Elser, J. J., A. L. Peace, M. Kyle, M. Wojewodzic, M. L. McCrakin, T. Andersen, and D. O. Hessen. 2010. Atmospheric nitrogen deposition is associated with elevades phosphorus limitation of lake zooplankton. Ecol. Lett. 13: 1256-1261, doi:10.1111/j.1461-0248.2010.01519.x
22. Folch, J., M. Lees, and G. H. Sloane-Stanely. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226: 497-507.
23. Girotti, A. W. 2001. Photosensitized oxidation of membrane lipids: Reaction pathways, cytotoxic effects, and cytoprotec- tive mechanisms. J. Photochem. Photobiol. B. 63: 103-113, doi:10.1016/S1011-1344(01)00207-X
24. Gurevitch, J., and L. V. Hedges. 1993. Meta-analysis: Combining the results of independent experiments, p. 378-398. In S. M. Scheiner and J. Gurevitch [eds.], Design and analysis of ecological experiments. Chapman and Hall.
25. Hessen, D. O. 2008. Efficiency, energy and stoichiometry in pelagic food webs; reciprocal roles of food quality and food quantity. Freshw. Rev. 1: 43-57.
26. Intergovernmental Panel on Climate Change [IPCC]. 2007. Climate change 2007: The physical science basis-a contribution of Working Groups I to the Fourth Assessment Report of the intergovernmental Panel on Climate Change. Cambridge Univ. Press.
27. Lampert, W., and P. Muck. 1985. Multiple aspects of food limitation in zooplankton communities: The Daphnia-Eu- diaptomus example. Arch. Hydrobiol. 21: 311-322.
28. Leech, D. M., and C. E. Williamson. 2000. Is tolerance to UV radiation in zooplankton related to body size, taxon, or lake transparency? Ecol. Appl. 10:1530-1540, doi:10.1890/1051-0761(2000)010[1530:ITTURI]2.0.C0;2
29. Leu, E., P. J. Faerovig, and D. O. Hessen. 2006. UV effects on stoichiometry and PUFAs of Selenastrum capricornutum and the consequences for the grazer Daphnia magna. Freshw. Biol. 51: 2296-2308, doi:10.1111/j.1365-2427.2006.01651.x
30. MaraNon, E., and others. 2010. Degree of oligotrophy controls the response of microbial plankton to Saharan dust. Limnol. Oceanogr. 55: 2339-235210.4319/lo.2010.55.6.2339
31. Morales-Baquero, R., E. Pulido-Villena, and I. Reche. 2006. Atmospheric inputs of phosphorus and nitrogen to the southwest Mediterranean region: Biochemical response of high mountain lakes. Limnol. Oceanogr. 51: 830-837, doi:10.4319/lo.2006.51.2.0830
32. MÜller-Navarra, D. C. 1995. Biochemical versus mineral limitation in Daphnia. Limnol. Oceanogr. 40: 1209-1214, doi:10.4319/lo.1995.40.7.1209
33. MÜller-Navarra, D. C., M. T. Brett, A. M. Liston, and C. R. Goldman. 2000. A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 403: 74-77, doi:10.1038/47469
34. MÜller-Navarra, D. C., M. T. Brett, A. M. Liston, and C. R. Goldman., and W. Lampert. 1996. Seasonal patterns of food limitation in Daphnia galeata: Separating food quantity and food quality effects. J. Plankton Res. 18: 1137-1158, doi:10.1093/plankt/18.7.1137
35. Nuwer, M. L., B. W. Frost, and E. V. Armbrust. 2008. Population structure of the planktonic copepod Calanus pacificus in the North Pacific Ocean. Mar. Biol. 156: 107-115, doi:10.1007/s00227-008-1068-y
36. Park, S., M. T. Brett, D. C. MUller-Navarra, and C. R. Goldman. 2002. Essential fatty acid content and the phosphorus to carbon ratio in cultured algae as indicators of food quality for Daphnia. Freshw. Biol. 47: 1377-1390, doi:10.1046/j.1365-2427.2002.00870.x
37. Persson, J., M. T. Brett, T. Vrede, and J. L. Ravet. 2007. Food quantity and quality regulation of trophic transfer between primary producers and a keystone grazer (Daphnia) in pelagic freshwater food webs. Oikos 116: 1152-1163, doi: 10.1111/ j.0030-1299.2007.15639.x
38. Plath, K., and M. Boersma. 2001. Mineral limitation of zooplankton: Stoichiometric constraints and optimal foraging. Ecology 85: 1260-1269, doi:10.1890/0012-9658(2001)082 [1260:ML0ZSC]2.0.C0;2
39. Psenner, R. 1999. Living in a dusty world: Airbone dust as a key factor for alpine lakes. Water Air Soil Pollut. 112: 217-227, doi: 10.1023/A:1005082832499
40. Quinn, G., and M. Keough. 2002. Experimental design and data analysis for biologists. Cambridge Univ. Press.
41. Ramos-Rodrsguez, E., and J. M. Conde-Porcuna. 2003. Nutrient limitation on a planktonic rotifer: Life history consequences and starvation resistance. Limnol. Oceanogr. 48: 933-938, doi:10.4319/lo.2003.48.2.0933
42. Ravet, J. L., and M. T. Brett. 2006. Phytoplankton essential fatty acid and phosphorus content constraints on Daphnia somatic growth and reproduction. Limnol. Oceanogr. 51: 2438-2452, doi:10.4319/lo.2006.51.5.2438
43. Ridame, C., and C. Guieu. 2002. Saharan input of phosphate to the oligotrophic water of the open western Mediterranean Sea. Limnol. Oceanogr. 47: 856-869, doi:10.4319/lo.2002.47. 3.0856
44. Romare, P., D. E. Schindler, M. D. Scheuerell, J. M. Scheuerell, A. H. Litt, and J. H. Shepherd. 2005. Variation in spatial and temporal gradients in zooplankton spring development: The effect of climatic factors. Freshw. Biol. 50: 1007-1021, doi:10.1111/j.1365-2427.2005.01386.x
45. Rosenberg, M. S., D. C. Adams, and J. Gurevitch. 2000. MetaWin: Statistical software for Meta-Analysis.
46. Santese, M., F. De Tomasi, and M. R. Perrone. 2007. Moderate Resolution Imaging Spectroradiometer (MODIS) and Aerosol Robotic Network (AERoNET) retrievals during dust outbreaks over the Mediterranean. J. Geophys. Res. D.: Atmos. 112: D18201, doi:10.1029/2007JD008482
47. Sommer, U., Z. M. Gliwicz, W. Lampert, and A. Duncan. 1986. The PEG-model of seasonal succession of planktonic events in fresh waters. Arch. Hydrobiol. 106: 433-471.
48. StatSoft. 1997. Statistica for Windows, release 7.1. StatSoft.
49. Stearns, S. C. 1992. The evolution of life histories. Oxford Univ. Press.
50. Stemberger, R., and J. J. Gilbert. 1985. Body size, food concentration, and population growth in planktonic rotifers. Ecology 66: 1151-1159, doi:10.2307/1939167
51. Sterner, R. W., and J. J. Elser. 2002. Ecological stoichiometry: The biology of elements from molecules to the biosphere. Princeton Univ. Press.
52. Sterner, R. W., and J. J. Elser., and K. I. Schulz. 1998. Zooplankton nutrition: Recent progress and a reality check. Aquat. Ecol. 32: 261-279, doi:10.1023/A:1009949400573
53. Stross, R. G. 1966. Light and temperature requirements for diapause development and realease in Daphnia. Ecology 47: 368-374, doi:10.2307/1932977
54. Urabe, J., M. Kyle, W. Makino, T. Toshida, T. Andersen, and J. J. Elser. 2002. Reduced light increases herbivore production due to stoichiometric effects of light/nutrient balance. Ecology 83: 619-627, doi:10.1890/0012-9658(2002)083 [0619:RLIHPD]2.0.CO;2
55. Villar-Argaiz, M., J. M. Medina-SAnchez, F. J. Bullejos, J. A. Delgado-Molina, O. RuIz-PErez, J. C. Navarro, and P. Carrillo. 2009. UV radiation and phosphorus interact to influence the biochemical composition of phytoplankton. Freshw. Biol. 54: 1233-1245, doi:10.1111/j.1365-2427. 2009.02170.x
56. Villar-Argaiz, M., J. M. Medina-SAnchez, F. J. Bullejos, J. A. Delgado-Molina, O. RuIz-PErez, J. C. Navarro, and P. Carrillo., and P. Carrillo. 2001. Inter- and intrannual variability in the phytoplankton community of a high mountain lake: The influence of external (atmospheric) and internal (recycled) sources of phosphorus. Freshw. Biol. 46: 1017-1034, doi:10.1046/j.1365-2427.2001.00734.x
57. Villar-Argaiz, M., J. M. Medina-SAnchez, F. J. Bullejos, J. A. Delgado-Molina, O. RuIz-PErez, J. C. Navarro, and P. Carrillo., and P. Carrillo., and. 2002. Microbial plankton response to contrasting climatic conditions: Insights from community structure, productivity and fraction stoichiometry. Aquat. Microb. Ecol. 29: 253-266, doi:10.3354/ame029253
58. Wacker, A., and E. von Elert. 2001. Polyunsaturated fatty acids: Evidence for non-substitutable biochemical resources in Daphnia galeata. Ecology 82: 2507-2520.
59. Williamson, C. E., P. J. Neale, G. Grad, H. J. De Lange, and B. R. Hargreaves. 2001. Beneficial and detrimental effects of UV on aquatic organisms: Implications of spectral variation. Ecol. Appl. 11: 1843-1857, doi:10.1890/1051-0761(2001)011[1843:BADE0U]2.0.C0;2
60. Zhao, J., M. Ramin, V. Cheng, and G. B. Arhonditsis. 2008. Plankton community patterns across a trophic gradient: The role of zooplankton functional groups. Ecol. Modell. 213: 417-436, doi:10.1016/j.ecolmodel.2008.01.016