Skip to main content
Log in

Population divergence in fish elemental phenotypes associated with trophic phenotypes and lake trophic state

  • Population ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Studies of ecological stoichiometry typically emphasize the role of interspecific variation in body elemental content and the effects of species or family identity. Recent work suggests substantial variation in body stoichiometry can also exist within species. The importance of this variation will depend on insights into its origins and consequences at various ecological scales, including the distribution of elemental phenotypes across landscapes and their role in nutrient recycling. We investigated whether trophic divergence can produce predictable patterns of elemental phenotypes among populations of an invasive fish, the white perch (Morone americana), and whether elemental phenotypes predict nutrient excretion. White perch populations exhibited a gradient of trophic phenotypes associated with landscape-scale variation in lake trophic state. Perch body chemistry varied considerably among lakes (from 0.09 for % C to 0.31-fold for % P) casting doubt on the assumption of homogenous elemental phenotypes. This variation was correlated with divergence in fish body shape and other trophic traits. Elemental phenotypes covaried (r 2 up to 0.84) with lake trophic state. This covariation likely arose in contemporary time since many of these perch populations were introduced in the last century and the trophic state in many of the lakes has changed in the past few decades. Nutrient excretion varied extensively among populations, but was not readily related to fish body chemistry or lake trophic state. This suggests that predictable patterns of fish body composition can arise quickly through trophic specialization to lake conditions, but such elemental phenotypes may not translate to altered nutrient recycling by fish.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Able K, Fahay M (1998) First year in the life of estuarine fishes in the middle Atlantic Bight. Rutgers University Press, New Brunswick

    Google Scholar 

  • Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42

    Google Scholar 

  • Allgeier JE, Wenger SJ, Rosemond AD, Schindler DE, Layman CA (2015) Metabolic theory and taxonomic identity predict nutrient recycling in a diverse food web. Proc Natl Acad Sci 112:E2640–E2647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • APHA (2005) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, Washington, D.C.

    Google Scholar 

  • Bassar RD, Marshall MC, López-Sepulcre A, Zandonà E, Auer SK, Travis J, Pringle CM, Flecker AS, Thomas SA, Fraser DF, Reznick DN (2010) Local adaptation in Trinidadian guppies alters ecosystem processes. Proc Natl Acad Sci USA 107:3616–3621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berner D, Adams DC, Grandchamp A-C, Hendry AP (2008) Natural selection drives patterns of lake-stream divergence in stickleback foraging morphology. J Evol Biol 21:1653–1665

    Article  CAS  PubMed  Google Scholar 

  • Blake R (2004) Fish functional design and swimming performance. J Fish Biol 65:1193–1222

    Article  Google Scholar 

  • Boros G, Sály P, Vanni MJ (2015) Ontogenetic variation in the body stoichiometry of two fish species. Oecologia 179:329–341

    Article  PubMed  Google Scholar 

  • Brown JH, Gupta VK, Li B-L, Milne BT, Restrepo C, West GB (2002) The fractal nature of nature: power laws, ecological complexity and biodiversity. Philosophical transactions of the Royal Society of London. Ser B Biol Sci 357:619–626

    Article  Google Scholar 

  • Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Article  Google Scholar 

  • Busch W-DN, Davies DH, Nepszy SJ (1977) Establishment of White Perch, Morone americana, in Lake Erie. J Fish Res Board Can 34:1039–1041

    Article  Google Scholar 

  • Carpenter SR, Kitchell JF (1996) The trophic cascade in lakes. Cambridge University Press, New York

    Google Scholar 

  • Dalton CM, Flecker AS (2014) Metabolic stoichiometry and the ecology of fear in Trinidadian guppies: consequences for life histories and stream ecosystems. Oecologia 176:691–701

    Article  PubMed  Google Scholar 

  • El-Sabaawi RW, Kohler TJ, Zandoná E, Travis J, Marshall MC, Thomas SA, Reznick DN, Walsh M, Gilliam JF, Pringle C, Flecker AS (2012a) Environmental and organismal predictors of intraspecific variation in the stoichiometry of a neotropical freshwater fish. PLoS One 7:e32713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Sabaawi RW, Zandonà E, Kohler TJ, Marshall MC, Moslemi JM, Travis J, López-Sepulcre A, Ferriére R, Pringle CM, Thomas SA, Reznick DN, Flecker AS (2012b) Widespread intraspecific organismal stoichiometry among populations of the Trinidadian guppy. Funct Ecol 26:666–676

    Article  Google Scholar 

  • El-Sabaawi RW, Travis J, Zandonà E, McIntyre PB, Reznick DN, Flecker A (2014) Intraspecific variability modulates interspecific variability in animal organismal stoichiometry. Ecol Evol 4:1505–1515

    Article  PubMed  PubMed Central  Google Scholar 

  • El-Sabaawi RW, Warbanski ML, Rudman SM, Hovel R, Matthews B (2016) Investment in boney defensive traits alters organismal stoichiometry and excretion in fish. Oecologia 181:1209–1220

    Article  PubMed  Google Scholar 

  • Elser J, Elser M, MacKay N, Carpenter S (1988) Zooplankton-mediated transitions between N-and P-limited algal growth. Limnol Oceanogr 33:1–14

    Article  CAS  Google Scholar 

  • Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison JF, Hobbie SE, Odell GM, Weider LW (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 3:540–550

    Article  Google Scholar 

  • Flecker AS, McIntyre PB, Moore JW, Anderson JT, Taylor BW, Hall RO Jr (2010) Migratory fishes as material and process subsidies in riverine ecosystems. Am Fish Soc Symp 73:559–592

    Google Scholar 

  • Fox JW (2007) The dynamics of top-down and bottom-up effects in food webs of varying prey diversity, composition, and productivity. Oikos 116:189–200

    Article  Google Scholar 

  • Frost PC, Stelzer RS, Lamberti GA, Elser JJ (2002) Ecological stoichiometry of trophic interactions in the benthos: understanding the role of C: N: P ratios in lentic and lotic habitats. J N Am Benthol Soc 21:515–528

    Article  Google Scholar 

  • Hall Jr RO, Koch BJ, Marshall MC, Taylor BW, Tronstad LM (2007) How body size mediates the role of animals in nutrient cycling in aquatic ecosystems. In: Hildrew AG, Edmonds-Brown R, Raffaelli D (eds) Body size: the structure and function of aquatic ecosystems. Cambridge University Press, New York, pp 286–305

  • Halliwell DB (2005) Introduced fish of maine. Maine Department of Environmental Protection, MAPB Series: Focus on Freshwater Biodiversity, Augusta

    Google Scholar 

  • Harmon LJ, Matthews B, Des Roches S, Chase JM, Shurin JB, Schluter D (2009) Evolutionary diversification in stickleback affects ecosystem functioning. Nature 458:1167–1170

    Article  CAS  PubMed  Google Scholar 

  • Hendrixson HA, Sterner RW, Kay AD (2007) Elemental stoichiometry of freshwater fishes in relation to phylogeny, allometry and ecology. J Fish Biol 70:121–140

    Article  Google Scholar 

  • Hergenrader GL, Bliss QP (1971) The white perch in Nebraska. Trans Am Fish Soc 100:734–738

    Article  Google Scholar 

  • Jeyasingh PD, Cothran RD, Tobler M (2014) Testing the ecological consequences of evolutionary change using elements. Ecol Evol 4:528–538

    Article  PubMed  PubMed Central  Google Scholar 

  • Kinnison MT, Hairston NG, Hendry AP (2015) Cryptic eco-evolutionary dynamics. Ann N Y Acad Sci 1360:120–144

    Article  PubMed  Google Scholar 

  • Knoll LB, McIntyre PB, Vanni MJ, Flecker AS (2009) Feedbacks of consumer nutrient recycling on producer biomass and stoichiometry: separating direct and indirect effects. Oikos 118:1732–1742

    Article  CAS  Google Scholar 

  • Layman CA, Allgeier JE, Rosemond AD, Dahlgren C, Yeager LA (2011) Marine fisheries declines viewed upside down: human impacts on consumer-driven nutrient recycling. Ecol Appl 21:343–349

    Article  PubMed  Google Scholar 

  • McIntyre PB, Flecker AS (2010) Ecological stoichiometry as an integrative framework in stream fish ecology. Am Fish Soc Symp 73:539–558

    Google Scholar 

  • McIntyre PB, Flecker AS, Vanni MJ, Hood JM, Taylor BW, Thomas SA (2008) Fish distributions and nutrient cycling in streams: can fish create biogeochemical hotspots? Ecology 89:2335–2346

    Article  PubMed  Google Scholar 

  • Meyer J, Schultz E, Helfman G (1983) Fish schools: an asset to corals. Science (New York, NY) 256:1–3

    Google Scholar 

  • Moody EK, Corman JR, Elser JJ, Sabo JL (2015) Diet composition affects the rate and N:P ratio of fish excretion. Freshw Biol 60:456–465

    Article  CAS  Google Scholar 

  • Nilsson PA, Brönmark C (2000) Prey vulnerability to a gape-size limited predator: behavioural and morphological impacts on northern pike piscivory. Oikos 88:539–546

    Article  Google Scholar 

  • Palkovacs EP, Marshall MC, Lamphere BA, Lynch BR, Weese DJ, Fraser DF, Reznick DN, Pringle CM, Kinnison MT (2009) Experimental evaluation of evolution and coevolution as agents of ecosystem change in Trinidadian streams. Philosophical transactions of the Royal Society of London. Ser B Biol Sci 364:1617–1628

    Article  Google Scholar 

  • Post DM, Palkovacs EP (2009) Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play. Philosophical transactions of the Royal Society of London. Ser B Biol Sci 364:1629–1640

    Article  Google Scholar 

  • Post D, Taylor J, Kitchell J (1998) The role of migratory waterfowl as nutrient vectors in a managed wetland. Conserv Biol 12:910–920

    Article  Google Scholar 

  • Post DM, Palkovacs EP, Schielke EG, Dodson SI (2008) Intraspecific variation in a predator affects community structure and cascading trophic interactions. Ecology 89:2019–2032

    Article  PubMed  Google Scholar 

  • Ricker W (1992) Back-calculation of fish lengths based on proportionality between scale and length increments. Can J Fish Aquat Sci 49:1018–1026

    Article  Google Scholar 

  • Robinson BW, Wilson DS, Margosian AS, Lotito PT (1993) Ecological and morphological differentiation of pumpkinseed sunfish in lakes without bluegill sunfish. Evol Ecol 7:451–464

    Article  Google Scholar 

  • Rohlf FJ (2004) TpsDig. Version 2.0. Available at: http://life.bio.sunysb.edu/ee/rohlf/software.html. Department of Ecology and Evolution, SUNY, New York

  • Rohlf FJJ (2005) TpsRelw. Version 1.31. Available at: http://life.bio.sunysb.edu/ee/rohlf/software.html. Department of Ecology and Evolution, SUNY, New York

  • Schaus M, Vanni M, Wissing T, Bremigan M, Garvey J, Stein R (1997) Nitrogen and phosphorus excretion by detritivorous gizzard shad in a reservoir ecosystem. Limnol Oceanogr 42:1386–1397

    Article  CAS  Google Scholar 

  • Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford

    Google Scholar 

  • Sereda JM, Hudson JJ, Taylor WD, Demers E (2008) Fish as sources and sinks of nutrients in lakes. Freshw Biol 53:278–289

    CAS  Google Scholar 

  • Shackell NL, Frank KT, Fisher JAD, Petrie B, Leggett WC (2010) Decline in top predator body size and changing climate alter trophic structure in an oceanic ecosystem. Proc R Soc B Biol Sci 277:1353

    Article  Google Scholar 

  • Skulason S, Smith TB (1995) Resource polymorphisms in vertebrates. Trends Ecol Evol 10:366–370

    Article  CAS  PubMed  Google Scholar 

  • Stanley JG, Danie DS (1983) Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (North Atlantic)-white perch. FWS/OBS-82/II.7. National Coastal Ecosystems Team, Division of Biological Services, U.S. Fish and Wildlife Service, Washington, DC

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • Sterner RW, George NB (2000) Carbon, nitrogen, and phosphorus stoichiometry of cyprinid fishes. Ecology 81:127–140

    Article  Google Scholar 

  • Svanbäck R, Eklöv P (2002) Effects of habitat and food resources on morphology and ontogenetic growth trajectories in perch. Oecologia 131:61–70

    Article  Google Scholar 

  • Tanner DK, Brazner JC, Brady VJ (2000) Factors influencing carbon, nitrogen, and phosphorus content of fish from a Lake Superior coastal wetland. Can J Fish Aquat Sci 57:1243–1251

    Article  CAS  Google Scholar 

  • Taylor EB (1999) Species pairs of north temperate freshwater fishes: evolution, taxonomy, and conservation. Rev Fish Biol Fish 9:299–324

    Article  Google Scholar 

  • Torres LE, Vanni MJ (2007) Stoichiometry of nutrient excretion by fish: interspecific variation in a hypereutrophic lake. Oikos 116:259–270

    Article  CAS  Google Scholar 

  • Tuckett QM, Simon KS, Saros JE, Halliwell DB, Kinnison MT (2013) Fish trophic divergence along a lake productivity gradient revealed by historic patterns of invasion and eutrophication. Freshw Biol 58:2517–2531

    Article  Google Scholar 

  • Tuckett QM, Simon KS, Saros JE, Coghlan SMJ, Kinnison MT (2015) Biomass versus biodiversity: the relative contribution of population attributes to consumer nutrient loading in aquatic systems. Evol Ecol Res 16:705–723

    Google Scholar 

  • Turesson H, Brönmark C (2007) Predator-prey encounter rates in freshwater piscivores: effects of prey density and water transparency. Oecologia 153:281–290

    Article  PubMed  Google Scholar 

  • Vanni MJ (2002) Nutrient cycling by animals in freshwater ecosystems. Annu Rev Ecol Syst 33:341–370

    Article  Google Scholar 

  • Vanni MJ, Flecker AS, Hood JM, Headworth JL (2002) Stoichiometry of nutrient recycling by vertebrates in a tropical stream: linking species identity and ecosystem processes. Ecol Lett 5:285–293

    Article  Google Scholar 

  • Vanni MJ, Bowling AM, Dickman EM, Hale RS, Higgins KA, Horgan MJ, Knoll LB, Renwick WH, Stein RA (2006) Nutrient cycling by fish supports relatively more primary production as lake productivity increases. Ecology 87:1696–1709

    Article  PubMed  Google Scholar 

  • Vanni M, Boros G, McIntyre P (2013) When are fish sources vs. sinks of nutrients in lake ecosystems? Ecology 94:2195–2206

    Article  PubMed  Google Scholar 

  • Vrede T, Drakare S, Eklöv P, Hein A, Liess A, Olsson J, Persson J, Quevedo M, Stabo HR, Svanbäck R (2011) Ecological stoichiometry of Eurasian perch—intraspecific variation due to size, habitat and diet. Oikos 120:886–896

    Article  Google Scholar 

  • Webb PW (1978) Fast-start performance and body form in seven species of teleost fish. J Exp Biol 74:311–326

    Google Scholar 

  • Webb PW (1984) Body form, locomotion and foraging in aquatic vertebrates. Integr Comp Biol 24:107–120

    Google Scholar 

  • Whiles MR, Huryn AD, Taylor BW, Reeve JD (2009) Influence of handling stress and fasting on estimates of ammonium excretion by tadpoles and fish: recommendations for designing excretion experiments. Limnol Oceanogr: Method 7:1–7

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Many people contributed to this project including Dennis Anderson, Joe Dembeck, Joe Glowa, David Halliwell, John Reynolds and Wes Wright. This project was funded in part by the U.S. Environmental Protection Agency (EPA) under Section 319 of the Clean Water Act. This publication has not been formally reviewed by the EPA and the views expressed are solely those of the authors. Additional support was provided by the Maine Agricultural and Forest Experiment Station (Contribution # 3499) and the National Science Foundation through a Doctoral Dissertation Improvement Grant (DEB 1011267).

Author contribution statement

QMT, MTK, JES and KSS designed the experiments. QMT and KSS performed the experiments. QMT analyzed the data. QMT, MTK, JES and KSS wrote the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Quenton M. Tuckett.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Additional information

Communicated by Craig A. Layman.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tuckett, Q.M., Kinnison, M.T., Saros, J.E. et al. Population divergence in fish elemental phenotypes associated with trophic phenotypes and lake trophic state. Oecologia 182, 765–778 (2016). https://doi.org/10.1007/s00442-016-3714-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-016-3714-2

Keywords

Navigation