Abstract
One of the central questions of ecological stoichiometry theory is to what extent animal species maintain constant elemental composition in their bodies. Although several recent studies demonstrate intraspecific variation in animal elemental composition, relatively little is known about ontogenetic changes in vertebrates, especially during early life stages. We studied the intraspecific and interspecific ontogenetic variation in the body stoichiometry of two fish species in two different orders; fathead minnow (Pimephales promelas) and sheepshead minnow (Cyprinodon variegatus), reared under controlled laboratory conditions. During ontogeny, we measured the chemical composition of fish bodies, including carbon (C), nitrogen (N), phosphorus (P), calcium (Ca), and ribonucleic acid (RNA) contents. We found that N and RNA contents were relatively high in early life stages and declined substantially during development. In contrast, body C and C:N ratios were relatively low in embryos, post-embryos and larvae, and increased remarkably thereafter. Concentrations and ratios of some elements (e.g., Ca, P, Ca:P) did not exhibit consistent ontogenetic trends, but fluctuated dynamically between consecutive developmental stages in both species. Specific growth rates correlated significantly with RNA contents in both species. Analyses of the relative importance of different P pools at each developmental stage revealed that RNA was a considerable P pool in post-embryos, while bone-associated P was the dominant body P pool in later stages. Our results suggest that the elemental composition of fish bodies changes considerably during ontogeny. Each ontogenetic stage has its own stoichiometric signature, but the timing, magnitude and direction of ontogenetic changes can vary substantially between taxa.
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Back JA, King RS (2013) Sex and size matter: ontogenetic patterns of nutrient content of aquatic insects. Freshwater Sci 32:837–848. doi:10.1899/12-181.1
Benstead JP, Hood JM, Whelan NV, Kendrick MR, Nelson D, Hanninen AF, Demi LM (2014) Coupling of dietary phosphorus and growth across diverse fish taxa: a meta-analysis of experimental aquaculture studies. Ecology 95:2768–2777. doi:10.1890/13-1859.1
Biro PA, Post JR, Abrahams MV (2005) Ontogeny of energy allocation reveals selective pressure promoting risk-taking behavior in young fish cohorts. Proc R Soc B: Biol Sci 272:1443–1448. doi:10.1098/rspb.2005.3096
Blessing JJ, Marshall JC, Balcombe SR (2010) Humane killing of fishes for scientific research: a comparison of two methods. J Fish Biol 76:2571–2577. doi:10.1111/j.1095-8649.2010.02633.x
Boros G, Tátrai I, György ÁI, Vári Á, Nagy SA (2009) Changes in internal phosphorus loading and fish population as possible causes of water quality decline in a shallow, biomanipulated lake. Int Rev Hydrobiol 94:326–337. doi:10.1002/iroh.200811090
Boros G, Jyväsjärvi J, Takács P, Mozsár A, Tátrai I, Søndergaard M, Jones RI (2012) Between-lake variation in the elemental composition of roach (Rutilus rutilus L.). Aquat Ecol 46:385–394. doi:10.1007/s10452-012-9402-3
Boros G, Takács P, Vanni MJ (2015) The fate of phosphorus in decomposing fish carcasses: a mesocosm experiment. Freshwater Biol 60:479–489. doi:10.1111/fwb.12483
Brown ME (1946) The growth of brown trout (Salmo trutta Linn.). I. Factors influencing the growth of trout fry. J Exp Biol 22:118–129
Buisson L, Blanc L, Grenouillet G (2008) Modelling stream fish species distribution in a river network: the relative effects of temperature versus physical factors. Ecol Freshwater Fish 17:244–257. doi:10.1111/j.1600-0633.2007.00276.x
Chidami S, Amyot M (2008) Fish decomposition in boreal lakes and biogeochemical implications. Limnol Oceanogr 53:1988–1996
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. doi:10.1007/s00442-014-3084-6
Davis JA, Boyd CE (1978) Concentrations of selected elements and ash in bluegill (Lepomis macrochirus) and certain other freshwater fish. Trans Am Fish Soc 107:862–867. doi:10.1577/1548-8659(1978)107<862:COSEAA>2.0.CO;2
Deegan LA (1986) Changes in body composition and morphology of young-of-the-year gulf menhaden, Brevoortia patronus Goode, in Fourleague Bay, Louisiana. J Fish Biol 29:403–415. doi:10.1111/j.1095-8649.1986.tb04956.x
El–Sabaawi RW, Zandona E, Kohler TJ, Marshall MC, Moslemi JM, Travis J, Lopez–Sepulcre A, Ferriére R, Pringle CM, Thomas SA, Reznick DN, Flecker AS (2012a) Widespread intraspecific organismal stoichiometry among populations of the Trinidadian guppy. Funct Ecol 26:666–676. doi:10.1111/j.1365-2435.2012.01974.x
El–Sabaawi RW, Kohler TJ, Zandoná E, Travis J, Marshall MC, Thomas SA, Reznick DN, Walsh M, Gilliam JF, Pringle C, Flecker AS (2012b) Environmental and organismal predictors of intraspecific variation in the stoichiometry of a Neotropical freshwater fish. PLoS One 7:1–12. doi:10.1371/journal.pone.0032713
Elser JJ, Dobberfuhl D, MacKay NA, Schampel JH (1996) Organism size, life history, and N: P stoichiometry: towards a unified view of cellular and ecosystem processes. Bioscience 46:674–684. doi:10.2307/1312897
Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie S, Fagan W, Schade J, Hood J, Sterner RW (2003) Growth rate—stoichiometry couplings in diverse biota. Ecol Lett 6:936–943. doi:10.1046/j.1461-0248.2003.00518.x
Fagan KA, Koops MA, Arts MT, Power M (2011) Assessing the utility of C: N ratios for predicting lipid content in fishes. Can J Fish Aquat Sci 68:374–385. doi:10.1139/F10-119
Gillooly J, Allen AP, Brown JH, Elser JJ, Martinez del Rio C, Savage VM, West GB, Woodruff WH, Woods HA (2005) The metabolic basis of whole-organism RNA and phosphorus content. Proc Natl Acad Sci USA 102:11923–11927. doi:10.1073/pnas.0504756102
Guisan A, Edwards TC Jr, Hasti T (2002) Generalized linear and generalized additive models in studies of species distributions: setting the scene. Ecol Model 157:89–100. doi:10.1016/S0304-3800(02)00204-1
Hastie TJ, Tibshirani RJ (1990) Generalized additive models. Chapman and Hall/CRC, Boca Raton
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. doi:10.1111/j.1095-8649.2006.01280.x
Hood JM, Sterner RW (2010) Diet mixing: do animals integrate growth or resources across temporal heterogeneity? Am Nat 176:651–663. doi:10.1086/656489
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. doi:10.1002/bimj.200810425
Kitchell JF, Koonce JF, Tennis PS (1975) Phosphorus flux through fishes. Verh Int Verein Limnol 19:2478–2484
Kooijman SALM (2000) Dynamic energy and mass budgets in biological systems, 2nd edn. Cambridge University Press, Cambridge
Kraft CE (1992) Estimates of phosphorus and nitrogen cycling by fish using a bioenergetics approach. Can J Fish Aquat Sci 49:2596–2604. doi:10.1139/f92-287
Lewis WM, Wurtsbaugh WA (2008) Control of lacustrine phytoplankton by nutrients: erosion of the phosphorus paradigm. Int Rev Hydrobiol 93:446–465. doi:10.1002/iroh.200811065
Lorenzen K (2000) Allometry of natural mortality as a basis for assessing optimal release size in fish-stocking programmes. Can J Fish Aquat Sci 57:2374–2381. doi:10.1139/f00-215
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. doi:10.1890/07-1552.1
Nakazawa T (2011) The ontogenetic stoichiometric bottleneck stabilizes herbivore–autotroph dynamics. Ecol Res 26:209–216. doi:10.1007/s11284-010-0752-9
Pangle KL, Sutton TM (2005) Temporal changes in the relationship between condition indices and proximate composition of juvenile Coregonus artedi. J Fish Biol 66:1060–1072. doi:10.1111/j.0022-1112.2005.00660.x
Parmenter RR, Lamarra VA (1991) Nutrient cycling in a freshwater marsh—the decomposition of fish and waterfowl carrion. Limnol Oceanogr 36:976–987. doi:10.4319/lo.1991.36.5.0976
Pilati A, Vanni MJ (2007) Ontogeny, diet shifts, and nutrient stoichiometry in fish. Oikos 116:1663–1674. doi:10.1111/j.0030-1299.2007.15970.x
Post JR, Parkinson EA (2001) Energy allocation strategy in young fish: allometry and survival. Ecology 82:1040–1051. doi:10.1890/0012-9658(2001)082[1040:EASIYF]2.0.CO;2
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.r-project.org/. Accessed 3 Apr 2013
Rønsholdt B (1995) Effect of size/age and feed composition on body composition and phosphorus content of rainbow trout Oncorhynchus mykiss. Water Sci Technol 31:175–183. doi:10.1016/0273-1223(95)00437-R
Schmera D, Baur B, Erös T (2012) Does functional redundancy of communities provide insurance against human disturbances? An analysis using regional-scale stream invertebrate data. Hydrobiologia 693:183–194. doi:10.1007/s10750-012-1107-z
Sereda JM, Hudson JJ, Taylor WD, Demers E (2008) Fish as sources and sinks of nutrients in lakes. Freshwater Biol 53:278–289. doi:10.1111/j.1365-2427.2007.01891.x
Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton
Sterner RW, George NB (2000) Carbon, nitrogen and phosphorus stoichiometry of cyprinid fishes. Ecology 81:127–140. doi:10.1890/0012-9658(2000)081[0127:CNAPSO]2.0.CO;2
Sullam KE, Dalton CM, Russel JA, Kilham SS, El-Sabaawi R, German DP, Flecker AS (2015) Changes in digestive traits and body nutritional composition accommodate a trophic niche shift in Trinidadian guppies. Oecologia 177:245–257. doi:10.1007/s00442-014-3158-5
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. doi:10.1139/f00-062
Tarvainen M, Sarvala J, Helminen H (2002) The role of phosphorus release by roach [Rutilus rutilus (L.)] in the water quality changes of a biomanipulated lake. Freshwater Biol 47:2325–2336. doi:10.1046/j.1365-2427.2002.00992.x
Van Aerle R, Runnals TJ, Tyler CR (2004) Ontogeny of gonadal sex development relative to growth in fathead minnow. J Fish Biol 64:355–369. doi:10.1111/j.0022-1112.2004.00296.x
Vanni MJ (2002) Nutrient cycling by animals in freshwater ecosystems. Annu Rev Ecol Syst 33:341–370. doi:10.1146/annurev.ecolsys.33.010802.150519
Vanni MJ, Boros G, McIntyre PB (2013) When are fish sources versus sinks of nutrients in lake ecosystems? Ecology 94:2195–2206. doi:10.1890/12-1559.1
Vrede T, Dobberfuhl DR, Kooijman SALM, Elser JJ (2004) Fundamental connections among organism C:N:P stoichiometry, macromolecular composition and growth. Ecology 85:1217–1229. doi:10.1890/02-0249
Vrede T, Drakare S, Eklöv P, Hein A, Liess A, Olsson J, Persson J, Quevedo M, Stabo R, Svenback R (2011) Ecological stoichiometry of Eurasian perch–intraspecific variation due to size, habitat and diet. Oikos 120:886–896. doi:10.1111/j.1600-0706.2010.18939.x
Wood SN (2006) Generalized additive models: an introduction with R. Chapman and Hall/CRC, Boca Raton
Acknowledgments
The Rosztoczy Foundation supported Gergely Boros by providing a postdoctoral fellowship to conduct research at Miami University. We acknowledge the support of National Science Foundation grant DEB 0743192. We thank E. Mette, L. Porter, Z. Alley, A. Kiss and A. Morgan for assistance in the lab, and Miami University Animal Care Facility and Center for Bioinformatics and Functional Genomics staff for technical support.
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Communicated by Joel Trexler.
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Boros, G., Sály, P. & Vanni, M.J. Ontogenetic variation in the body stoichiometry of two fish species. Oecologia 179, 329–341 (2015). https://doi.org/10.1007/s00442-015-3349-8
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DOI: https://doi.org/10.1007/s00442-015-3349-8