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Oecologia

, Volume 186, Issue 4, pp 1031–1041 | Cite as

Blinded by the light? Nearshore energy pathway coupling and relative predator biomass increase with reduced water transparency across lakes

  • Tyler D. TunneyEmail author
  • Kevin S. McCann
  • Lauren Jarvis
  • Nigel P. Lester
  • Brian J. Shuter
Community ecology – original research

Abstract

Habitat coupling is a concept that refers to consumer integration of resources derived from different habitats. This coupling unites fundamental food web pathways (e.g., cross-habitat trophic linkages) that mediate key ecological processes such as biomass flows, nutrient cycling, and stability. We consider the influence of water transparency, an important environmental driver in aquatic ecosystems, on habitat coupling by a light-sensitive predator, walleye (Sander vitreus), and its prey in 33 Canadian lakes. Our large-scale, across-lake study shows that the contribution of nearshore carbon (δ13C) relative to offshore carbon (δ13C) to walleye is higher in less transparent lakes. To a lesser degree, the contribution of nearshore carbon increased with a greater proportion of prey in nearshore compared to offshore habitats. Interestingly, water transparency and habitat coupling predict among-lake variation in walleye relative biomass. These findings support the idea that predator responses to changing conditions (e.g., water transparency) can fundamentally alter carbon pathways, and predator biomass, in aquatic ecosystems. Identifying environmental factors that influence habitat coupling is an important step toward understanding spatial food web structure in a changing world.

Keywords

Food webs Trophic interactions Environmental change Stable isotopes Water clarity Sander vitreus 

Notes

Acknowledgements

We thank biologists and technical staff at the OMNRF Broad-Scale Monitoring Program for assistance with sample collection. S. Sandstrom, K. Armstrong, and J. Wright were particularly helpful with logistics and offered sampling advice. We also acknowledge the efforts of A. Oulimette and R. Mixon (University of New Hampshire Stable Isotope Laboratory). Beren W. Robinson provided helpful comments on an early draft of the manuscript. We also acknowledge Leon Barmuta and anonymous reviewers for constructive comments. Helpful discussion included K.S.M. laboratory members. TDT acknowledges useful discussion with the ‘Bass-walleye group’ a collaboration between WDNR, USGS, and the Center for Limnology UW-Madison. Research was supported by grants from the Natural Sciences and Engineering Research Council of Canada (to B.J.S. and K.S.M.) and the Climate Change Program of the OMNRF. Additional support came through a Tier 2 Canada Research Chair held by K.S.M. Partial support from CFREF to KSM.

Author contributions

TDT, KSM, NPL and BJS conceived and designed the study. TDT and LJ collected field data and conducted lab work. TDT, LJ, NPL and BJS organized and analyzed data. TDT wrote the initial draft of the manuscript. All authors provided editorial advice.

Supplementary material

442_2017_4049_MOESM1_ESM.docx (1023 kb)
Supplementary material 1 (DOCX 1023 kb)

References

  1. Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manag 74:1175–1178CrossRefGoogle Scholar
  2. Bartels P, Hirsch PE, Svanbäck R, Eklöv P (2012) Water transparency drives intra-population divergence in Eurasian perch (Perca fluviatilis). PLoS One 7:e43641CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bartels P, Hirsch PE, Svanbäck R, Eklöv P (2016) Dissolved organic carbon reduces habitat coupling by top predators in lake ecosystems. Ecosystems 19:955–967CrossRefGoogle Scholar
  4. Batt RD, Carpenter SR, Cole JJ, Pace ML, Johnson RA, Kurtzweil JT, Wilkinson GM (2015) Altered energy flow in the food web of an experimentally darkened lake. Ecosphere 6(3):33.  https://doi.org/10.1890/ES14-00241.1 CrossRefGoogle Scholar
  5. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  6. Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35CrossRefGoogle Scholar
  7. Crawley MJ (2013) The R book. 2nd edn. Wiley, ChichesterGoogle Scholar
  8. Dillon PJ, Rigler FH (1974) The phosphorus–chlorophyll relationship in lakes. Limnol Oceanogr 19:767–773CrossRefGoogle Scholar
  9. Dolson R, McCann K, Rooney N, Ridgway M (2009) Lake morphometry predicts the degree of habitat coupling by a mobile predator. Oikos 118:1230–1238CrossRefGoogle Scholar
  10. Einfalt LM, Grace EJ, Wahl DH (2012) Effects of simulated light intensity, habitat complexity and forage type on predator–prey interactions in walleye Sander vitreus. Ecol Freshw Fish 21:560–569CrossRefGoogle Scholar
  11. Eloranta AP, Kahilainen KK, Amundsen P-A, Knudsen R, Harrod C, Jones RI (2015) Lake size and fish diversity determine resource use and trophic position of a top predator in high-latitude lakes. Ecol Evol 5:1664–1675CrossRefPubMedPubMedCentralGoogle Scholar
  12. Finstad AG, Helland IP, Ugedal O, Hesthagen T, Hessen DO (2014) Unimodal response of fish yield to dissolved organic carbon. Ecol Lett 17:36–43CrossRefPubMedGoogle Scholar
  13. Graham MH (2003) Confronting multicollinearity in ecological multiple regression. Ecology 84:2809–2815CrossRefGoogle Scholar
  14. Gratton C, Donaldson J, Vander Zanden MJ (2008) Ecosystem linkages between lakes and the surrounding terrestrial landscape in northeast iceland. Ecosystems 11:764–774CrossRefGoogle Scholar
  15. Huxel GR, McCann K (1998) Food web stability: the influence of trophic flows across habitats. Am Nat 152:460–469CrossRefPubMedGoogle Scholar
  16. Huxel GR, McCann K, Polis GA (2002) Effects of partitioning allochthonous and autochthonous resources on food web stability. Ecol Res 17:419–432CrossRefGoogle Scholar
  17. Kalff J (2002) Limnology: inland water ecosystems. Prentice Hall, Upper Saddle River, N.J., USAGoogle Scholar
  18. Karlsson J, Byström P, Ask J, Ask P, Persson L, Jansson M (2009) Light limitation of nutrient-poor lake ecosystems. Nature 460:506–509CrossRefPubMedGoogle Scholar
  19. Keller W (2007) Implications of climate warming for Boreal Shield lakes: a review and synthesis. Environ Rev 15:99–112CrossRefGoogle Scholar
  20. Kelso JRM (1978) Diel rhythm in activity of walleye, Stizostedion vitreum vitreum. J Fish Biol 12:593–599CrossRefGoogle Scholar
  21. Lester NP, Dextrase AJ, Kushneriuk RS, Rawson MR, Ryan PA (2004) Light and temperature: key factors affecting walleye abundance and production. Trans Am Fish Soc 133:588–605CrossRefGoogle Scholar
  22. Locke BA (1990) Quality control data for the limnology section. Dorset Research Centre, Ontario Ministry of the Environment, Queen's Printer for Ontario, Ontario, CanadaGoogle Scholar
  23. Mazerolle MJ (2017) AICcmodavg: Model selection and multimodel inference based on (Q) AIC(c). R package version 2.1-1. https://cran.r-project.org/package=AICcmodavg
  24. McCann K (2007) Protecting biostructure. Nature 446:29CrossRefPubMedGoogle Scholar
  25. McCann KS (2012) Food webs. Princeton University Press, Princeton, N.J., USAGoogle Scholar
  26. McCann KS, Rassmussen JB, Umbanhower J (2005) The dynamics of spatially coupled food webs. Ecol Lett 8:513–523CrossRefPubMedGoogle Scholar
  27. McCauley DJ, Young HS, Dunbar RB, Estes JA, Semmens BX, Micheli F (2012) Assessing the effects of large mobile predators on ecosystem connectivity. Ecol Appl 22:1711–1717CrossRefPubMedGoogle Scholar
  28. Nakano S, Murakami M (2001) Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proc Natl Acad Sci 98:166–170CrossRefPubMedPubMedCentralGoogle Scholar
  29. Ontario Ministry of the Environment (1983) Handbook of analytical methods for environmental sampling. Ontario Ministry of the Environment, Queen's Printer for Ontario, Ontario, CanadaGoogle Scholar
  30. Polis G, Hurd S (1995) Extraordinarily high spider densities on islands flow of energy from the marine to terrestrial food webs and the absence of predation. PNAS 92:4382–4386CrossRefPubMedPubMedCentralGoogle Scholar
  31. Polis G, Strong D (1996) Food web complexity and community dynamics. Am Nat 147:813–846CrossRefGoogle Scholar
  32. Polis G, Anderson W, Holt R (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316CrossRefGoogle Scholar
  33. Post DM, Conners ME, Goldberg DS (2000) Prey preference by a top predator and the stability of linked food chains. Ecology 81:8–14CrossRefGoogle Scholar
  34. Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189CrossRefPubMedGoogle Scholar
  35. Pringle RM, Fox-Dobbs K (2008) Coupling of canopy and understory food webs by ground-dwelling predators. Ecol Lett 11:1328–1337CrossRefPubMedGoogle Scholar
  36. R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
  37. Robillard MM, Fox MG (2006) Historical changes in abundance and community structure of warmwater piscivore communities associated with changes in water clarity, nutrients, and temperature. Can J Fish Aquat Sci 63:798–809CrossRefGoogle Scholar
  38. Rooney N, McCann K, Gellner G, Moore JC (2006) Structural asymmetry and the stability of diverse food webs. Nature 442:265–269CrossRefPubMedGoogle Scholar
  39. Ryder RA (1977) Effects of ambient light variations on behavior of yearling, subadult, and adult walleyes (Stizostedion vitreum vitreum). J Fish Board Can 34:1481–1491CrossRefGoogle Scholar
  40. Sandstrom S, Rawson M, Lester N (2013) Manual of instructions for broad-scale fish community monitoring; using North American (NA1) and Ontario Small Mesh (ON2) Gillnets. (No. Version 2013.2). Ontario Ministry of Natural Resources, Queen’s printer for Ontario, Peterborough, ON, CanadaGoogle Scholar
  41. Scheu S (2001) Plants and generalist predators as links between the below-ground and above-ground system. Basic Appl Ecol 2:3–13CrossRefGoogle Scholar
  42. Schindler DW (1977) Evolution of phosphorus limitation in lakes. Science 195:260–262CrossRefPubMedGoogle Scholar
  43. Schindler DE, Scheuerell MD (2002) Habitat coupling in lake ecosystems. Oikos 98:177–189CrossRefGoogle Scholar
  44. Stasko AD, Johnston TA, Gunn JM (2015) Effects of water clarity and other environmental factors on trophic niches of two sympatric piscivores. Freshw Biol 60:1459–1474CrossRefGoogle Scholar
  45. Tunney TD, McCann KS, Lester NP, Shuter BJ (2012) Food web expansion and contraction in response to changing environmental conditions. Nat Commun 3:1105CrossRefPubMedGoogle Scholar
  46. Tunney TD, McCann K, Lester N, Shuter B (2014) Effects of differential warming on complex communities. PNAS 111:8077–8082CrossRefPubMedPubMedCentralGoogle Scholar
  47. Vadeboncoeur Y, Vander Zanden MJ, Lodge DM (2002) Putting the lake back together: reintegrating benthic pathways into lake food web models: lake ecologists tend to focus their research on pelagic energy pathways, but, from algae to fish, benthic organisms form an integral part of lake food webs. BioScience 52(1):44–54.  https://doi.org/10.1641/0006-3568(2002)052[0044:PTLBTR]2.0.CO;2 CrossRefGoogle Scholar
  48. Vandenbyllaardt L, Ward FJ, Braekevelt CR, McIntyre DB (1991) Relationships between turbidity, piscivory, and development of the retina in juvenile walleyes. Trans Am Fish Soc 120:382–390CrossRefGoogle Scholar
  49. Vander Zanden MJ, Vadeboncoeur Y (2002) Fishes as integrators of of benthic and pelagic food webs in lakes. Ecology 83:2152–2161CrossRefGoogle Scholar
  50. Vander Zanden MJ, Casselman J, Rasmussen J (1999) Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401:464–467CrossRefGoogle Scholar
  51. Vander Zanden MJ, Clayton MK, Moody EK, Solomon CT, Weidel BC, Pond DW (2015) Stable isotope turnover and half-life in animal tissues: a literature synthesis. PLOS ONE 10(1):e0116182CrossRefPubMedPubMedCentralGoogle Scholar
  52. Weidel BC, Carpenter SR, Kitchell JF, Vander Zanden MJ (2011) Rates and components of carbon turnover in fish muscle: insights from bioenergetics models and a whole-lake 13C addition. Can J Fish Aquat Sci 68:387–399CrossRefGoogle Scholar
  53. Wolkovich EM, Allesina S, Cottingham KL, Moore JC, Sandin SA, de Mazancourt C (2014) Linking the green and brown worlds: the prevalence and effect of multichannel feeding in food webs. Ecology 95:3376–3386CrossRefGoogle Scholar
  54. Ziegler JP, Solomon CT, Finney BP, Gregory-Eaves I (2015) Macrophyte biomass predicts food chain length in shallow lakes. Ecosphere 6(1):5.  https://doi.org/10.1890/ES14-00158.1 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Center for LimnologyUniversity of Wisconsin-MadisonMadisonUSA
  2. 2.Department of Integrative BiologyUniversity of GuelphGuelphCanada
  3. 3.Aquatic Research and Development SectionOntario Ministry of Natural ResourcesPeterboroughCanada
  4. 4.Department of Ecology and EvolutionUniversity of TorontoTorontoCanada
  5. 5.Fisheries and Oceans Canada, Gulf Fisheries CentreMonctonCanada

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