Food web de-synchronization in England's largest lake: An assessment based on multiple phenological metrics

Global Change Biology

Volumn 19, Issue 12, 2013, Pages 3568-3580

  Thackeray, Stephen J ^a   Henrys, Peter A ^a   Feuchtmayr, Heidrun ^a   Jones, Ian D ^a   Maberly, Stephen C ^a   Winfield, Ian J ^a  

^a CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

Author keywords

Chlorophyll; Daphnia; Hierarchical models; Match mismatch; Perch; Phytoplankton; Temperature; Uncertainty; Windermere; Zooplankton

Indexed keywords

CHLOROPHYLL; CLIMATE CHANGE; CONCENTRATION (COMPOSITION); ECOSYSTEM FUNCTION; ENVIRONMENTAL ASSESSMENT; FOOD WEB; GLOBAL CHANGE; LAKE ECOSYSTEM; PHENOLOGY; PHYTOPLANKTON; SURVIVAL; TEMPERATURE EFFECT; UNCERTAINTY ANALYSIS; ZOOPLANKTON;

CUMBRIA; ENGLAND; UNITED KINGDOM; WINDERMERE;

DAPHNIA; PERCA FLUVIATILIS;

CHLOROPHYLL; CHLOROPHYLL A;

ANIMAL; ARTICLE; CLIMATE CHANGE; DAPHNIA; FOOD CHAIN; HIERARCHICAL MODELS; LAKE; MATCH-MISMATCH; PERCH; PHYSIOLOGY; PHYTOPLANKTON; SEASON; TEMPERATURE; UNCERTAINTY; UNITED KINGDOM; WINDERMERE; ZOOPLANKTON;

CHLOROPHYLL; DAPHNIA; HIERARCHICAL MODELS; MATCH-MISMATCH; PERCH; PHYTOPLANKTON; TEMPERATURE; UNCERTAINTY; WINDERMERE; ZOOPLANKTON;

ANIMALS; CHLOROPHYLL; CLIMATE CHANGE; DAPHNIA; ENGLAND; FOOD CHAIN; LAKES; PERCHES; PHYTOPLANKTON; SEASONS; TEMPERATURE; ZOOPLANKTON;

EID: 84887448700     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/gcb.12326     Document Type: Article

References (62)

1. Adrian R, Wilhelm S, Gerten D (2006) Life-history traits of lake plankton species may govern their phenological response to climate warming. Global Change Biology, 12, 652-661.
2. Askeyev OV, Sparks TH, Askeyev IV, Tishin DV, Tryjanowski P (2010) East versus West: contrasts in phenological patterns. Global Ecology and Biogeography, 19, 783-793.
3. Berger SA, Diehl S, Stibor H, Trommer G, Ruhenstroth M (2010) Water temperature and stratification depth independently shift cardinal events during plankton spring succession. Global Change Biology, 16, 1954-1965.
4. Both C, Van Asch M, Bijlsma RG, Van Den Burg AB, Visser ME (2009) Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? Journal of Animal Ecology, 78, 73-83.
5. Burthe S, Daunt F, Butler A et al. (2012) Phenological trends and trophic mismatch across multiple levels of a North Sea pelagic food web. Marine Ecology-Progress Series, 454, 119-133.
6. Craig JF (2000) Percid Fishes: Systematics, Ecology and Exploitation. Blackwell, Oxford.
7. Cushing DH (1990) Plankton production and year class strength in fish populations - an update of the match mismatch hypothesis. Advances in Marine Biology, 26, 249-293.
8. De Senerpont Domis LN, Mooij WM, Hulsmann S, Van Nes EH, Scheffer M (2007) Can overwintering versus diapausing strategy in Daphnia determine match-mismatch events in zooplankton-algae interactions? Oecologia, 150, 682-698.
9. Feuchtmayr H, Moss B, Harvey I, Moran R, Hatton K, Connor L, Atkinson D (2010) Differential effects of warming and nutrient loading on the timing and size of the spring zooplankton peak: an experimental approach with hypertrophic freshwater mesocosms. Journal of Plankton Research, 32, 1715-1725.
10. Feuchtmayr H, Thackeray SJ, Jones ID, De Ville M, Fletcher J, James B, Kelly J (2012) Spring phytoplankton phenology - are patterns and drivers of change consistent among lakes in the same climatological region? Freshwater Biology, 57, 331-344.
11. George DG (2012) The effect of nutrient enrichment and changes in the weather on the abundance of Daphnia in Esthwaite Water, Cumbria. Freshwater Biology, 57, 360-372.
12. George DG, Hewitt DP (1998) The influence of year-to-year changes in position of the Atlantic Gulf Stream on the biomass of zooplankton in Windermere North Basin, UK. In: Management of Lakes and Reservoirs During Global Climate Change (eds George DG, Jones JG, Punčochář P, Reynolds CS, Sutcliffe DW ), pp. 223-244, Kluwer Academic Publishers, Dordrecht, The Netherlands.
13. George DG, Reynolds CS (1997) Zooplankton-phytoplankton interactions: the case for refining methods, measurements and models. Aquatic Ecology, 31, 59-71.
14. George DG, Talling JF, Rigg E (2000) Factors influencing the temporal coherence of five lakes in the English Lake District. Freshwater Biology, 43, 449-461.
15. Gerten D, Adrian R (2000) Climate-driven changes in spring plankton dynamics and the sensitivity of shallow polymictic lakes to the North Atlantic Oscillation. Limnology and Oceanography, 45, 1058-1066.
16. Grace JB (2006) Structural Equation Modelling and Natural Systems. Cambridge University Press, UK.
17. Guisande C, Gliwicz ZM (1992) Egg size and clutch size in two Daphnia species growth at different food levels. Journal of Plankton Research, 14, 997-1007.
18. Guma'a SA (1978a) The food and feeding habits of young perch, Perca fluviatilis, in Windermere. Freshwater Biology, 8, 177-187.
19. Guma'a SA (1978b) The effects of temperature on the development and mortality of eggs of perch, Perca fluviatilis. Freshwater Biology, 8, 221-227.
20. Hall DJ (1964) An experimental approach to the dynamics of a natural population of Daphnia galeata mendotae. Ecology, 45, 94-112.
21. Hampton SE, Romare P, Seiler DE (2006) Environmentally controlled Daphnia spring increase with implications for sockeye salmon fry in Lake Washington, USA. Journal of Plankton Research, 28, 399-406.
22. Hutchinson GE (1957) A Treatise on Limnology. Volume 1: Geography, Physics and Chemistry. Chapman and Hall Ltd., London.
23. IPCC (2007) Summary for policymakers. In: Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds Parry ML, Canziani OF, Palutikof JP, Van der Linden PJ, Hanson CE), PP. 81-82. Cambridge University Press, Cambridge.
24. Jones ID, Winfield IJ, Carse F (2008) Assessment of long-term changes in habitat availability for Arctic charr (Salvelinus alpinus) in a temperate lake using oxygen profiles and hydroacoustic surveys. Freshwater Biology, 53, 393-402.
25. Lampert W (1978) A field study on the dependence of the fecndity of Daphnia spec. on food concentration. Oecologia, 36, 363-369.
26. Lampert W, Fleckner W, Rai H, Taylor BE (1986) Phytoplankton control by grazing zooplankton: a study on the spring clear-water phase. Limnology and Oceanography, 31, 478-490.
27. Lund JWG (1949) Studies on Asterionella I. The origin and nature of the cells producing seasonal maxima. Journal of Ecology, 37, 389-419.
28. Lunn DJ, Thomas A, Best N, Spiegelhalter D (2000) WinBUGS - a Bayesian modelling framework: concepts, structure and extensibility. Statistics and Computing, 10, 325-337.
29. Maberly SC, Elliott JA (2012) Insights from long-term studies in the Windermere catchment: external stressors, internal interactions and the structure and function of lake ecosystems. Freshwater Biology, 57, 233-243.
30. Mackereth FGH, Heron J, Talling JF (1978) Water Analysis: Some Revised Methods for Limnologists. Freshwater Biological Association, Ambleside.
31. Menzel A, Sparks TH, Estrella N et al. (2006) European phenological response to climate change matches the warming pattern. Global Change Biology, 12, 1969-1976.
32. Miller-Rushing AJ, Inouye DW, Primack RB (2008) How well do first flowering dates measure plant responses to climate change? The effects of population size and sampling frequency. Journal of Ecology, 96, 1289-1296.
33. Mills CA, Hurley MA (1990) Long-term studies on the Windermere populations of perch (Perca fluviatilis), pike (Esox lucius) and Arctic charr (Salvelinus alpinus). Freshwater Biology, 23, 119-136.
34. Munro IG, White RWG (1975) Comparison of the influence of temperature on the egg development and growth of Daphnia longispina O.F. Müller (Crustacea:cladocera) from two habitats in Southern England. Oecologia, 20, 157-165.
35. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421, 37-42.
36. Paxton CGM, Winfield IJ, Fletcher JM, George DG, Hewitt DP (2004) Biotic and abiotic influences on the recruitment of perch (Perca fluviatilis) in Windermere, U.K. Journal of Fish Biology, 65, 1622-1642.
37. Pinheiro J, Bates D, Debroy S, Sarkar D, R Development Core Team (2010) Nlme: Linear and Nonlinear Mixed Effects Models. R Package Version 3.1-97.
38. R Development Core Team (2011) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. Available at: http://www.R-project.org/ (accessed October 2012).
39. Ramsbottom AE (1976) Depth Charts of the Cumbrian Lakes. Freshwater Biological Association, Titus Wilson & Son Ltd., Kendal.
40. Reynolds CS (1989) Physical determinants of phytoplankton succession. In: Plankton Ecology (ed Sommer U), pp. 9-56. Brock-Springer, Madison.
41. Reynolds CS (1990) Temporal scales of variability in pelagic environments and the response of phytoplankton. Freshwater Biology, 23, 25-53.
42. Reynolds CS (1997) Successional development, energetics and diversity in planktonic communities. In: Biodiversity: An Ecological Perspective (eds Abe T, Levin SR, Higashi M), pp. 167-202. Springer, New york.
43. Reynolds CS (2006) Ecology of Phytoplankton. Cambridge University Press, Cambridge.
44. Reynolds CS, Irish AE (2000) The Phytoplankton of Windermere (English Lake District). Freshwater Biological Association, Ambleside.
45. Rolinski S, Horn H, Petzoldt T, Paul L (2007) Identifying cardinal dates in phytoplankton time series to enable the analysis of long-term trends. Oecologia, 153, 997-1008.
46. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature, 421, 57-60.
47. Roy DB, Sparks TH (2000) Phenology of British butterflies and climate change. Global Change Biology, 6, 407-416.
48. Schalau K, Rinke K, Straile D, Peeters F (2008) Temperature is the key factor explaining interannual variability of Daphnia development in spring: a modelling study. Oecologia, 157, 531-543.
49. Scheffer M, Rinaldi S, Kuznetsov YA, Van Nes EH (1997) Seasonal dynamics of Daphnia and algae explained as a periodically forced predator-prey system. Oikos, 80, 519-532.
50. Talling JF (1974) Photosynthetic pigments. General outline of spectrophotometric methods; specific procedures. In: A Manual on Methods for Measuring Primary Productivity in Aquatic Environments (ed. Vollenweider RA), pp. 22-26. Blackwell Scientific Publications, Oxford.
51. Talling JF (2002) Phytoplankton-zooplankton seasonal timing and the "clear-water" phase in some English lakes. Freshwater Biology, 48, 39-52.
52. Thackeray SJ, Jones ID, Maberly SC (2008) Long-term change in the phenology of spring phytoplankton: species-specific responses to nutrient enrichment and climatic change. Journal of Ecology, 96, 523-535.
53. Thackeray SJ, Sparks TH, Frederiksen M et al. (2010) Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Global Change Biology, 16, 3304-3313.
54. Thackeray SJ, Henrys PA, Jones ID, Feuchtmayr H (2012) Eight decades of phenological change for a freshwater cladoceran: what are the consequences of our definition of seasonal timing? Freshwater Biology, 57, 345-359.
55. Vanni MJ, Temte J (1990) Seasonal patterns of grazing and nutrient limitation of phytoplankton in a eutrophic lake. Limnology and Oceanography, 35, 697-709.
56. Vijverberg J (1980) Effect of temperature in laboratory studies on development and growth of Cladocera and Copepoda from Tjeukemeer, The Netherlands. Freshwater Biology, 10, 317-340.
57. Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proceedings of the Royal Society of London Series B-Biological Sciences, 272, 2561-2569.
58. Visser ME, Holleman LJM, Gienapp P (2006) Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird. Oecologia, 147, 164-172.
59. Weetman D, Atkinson D (2004) Evaluation of alternative hypotheses to explain temperature-induced life history shifts in Daphnia. Journal of Plankton Research, 26, 107-116.
60. Winder M, Schindler DE (2004) Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology, 85, 2100-2106.
61. Winfield IJ, Fletcher JM, James JB (2008) The Arctic charr (Salvelinus alpinus) populations of Windermere, U.K.: population trends associated with eutrophication, climate change and increased abundance of roach (Rutilus rutilus). Environmental Biology of Fishes, 83, 25-35.
62. Wood SN, Augustin NH (2002) GAMs with integrated model selection using penalized regression splines and applications to environmental modelling. Ecological Modelling, 157, 157-177.