Abstract
Understanding how trait diversification alters ecosystem processes is an important goal for ecological and evolutionary studies. Ecological stoichiometry provides a framework for predicting how traits affect ecosystem function. The growth rate hypothesis of ecological stoichiometry links growth and phosphorus (P) body composition in taxa where nucleic acids are a significant pool of body P. In vertebrates, however, most of the P is bound within bone, and organisms with boney structures can vary in terms of the relative contributions of bones to body composition. Threespine stickleback populations have substantial variation in boney armour plating. Shaped by natural selection, this variation provides a model system to study the links between evolution of bone content, elemental body composition, and P excretion. We measure carbon:nitrogen:P body composition from stickleback populations that vary in armour phenotype. We develop a mechanistic mass-balance model to explore factors affecting P excretion, and measure P excretion from two populations with contrasting armour phenotypes. Completely armoured morphs have higher body %P but excrete more P per unit body mass than other morphs. The model suggests that such differences are driven by phenotypic differences in P intake as well as body %P composition. Our results show that while investment in boney traits alters the elemental composition of vertebrate bodies, excretion rates depend on how acquisition and assimilation traits covary with boney trait investment. These results also provide a stoichiometric hypothesis to explain the repeated loss of boney armour in threespine sticklebacks upon colonizing freshwater ecosystems.
Similar content being viewed by others
References
Aguirre WE, Bell MA (2012) Twenty years of body shape evolution in a threespine stickleback population adapting to a lake environment. Biol J Linn Soc 105:817–831
Allan JD, Castillo MM (2007) Stream ecology: structure and function of running waters. Springer, Berlin
Allen J, Wootton R (1982a) Age, growth and rate of food consumption in an upland population of the three-spined stickleback, Gasterosteus aculeatus L. J Fish Biol 21:95–105
Allen J, Wootton R (1982b) The effect of ration and temperature on the growth of the three-spined stickleback, Gasterosteus aculeatus L. J Fish Biol 20:409–422
Allen JR, Wootton RJ (1983) Rate of food consumption in a population of threespine sticklebacks, Gasterosteus aculeatus, estimated from the faecal production. Environ Biol Fish 8:157–162
Allen J, Wootton R (1984) Temporal patterns in diet and rate of food consumption of the three-spined stickleback (Gasterosteus aculeatus L.) in Llyn Frongoch, an upland Welsh lake. Freshwater Biol 14:335–346
Barrett RDH, Rogers SM, Schluter D (2008) Natural selection on a major armor gene in threespine stickleback. Science 322:255–257
Barrett RDH, Rogers SM, Schluter D (2009) Environment specific pleiotropy facilitates divergence at the Ectodysplasin locus in threespine stickleback. Evolution 63:2831–2837
Bassar RD et al (2010) Local adaptation in Trinidadian guppies alters ecosystem processes. Proc Natl Acad Sci USA 107:3616–3621. doi:10.1073/Pnas.0908023107
Bassar RD et al (2012) Direct and indirect ecosystem effects of evolutionary adaptation in the Trinidadian guppy (Poecilia reticulata). Am Nat 180:167–185
Bell MA (1981) Lateral plate polymorphism and ontogeny of the complete plate morph of threespine sticklebacks (Gasterosteus aculeatus). Evol 35(1):67–74
Bell MA, Aguirre WE, Buck NJ (2004) Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution 58:814–824
Boros G, Sály P, Vanni MJ (2015) Ontogenetic variation in the body stoichiometry of two fish species. Oecologia 179(2):1–13
Capps KA, Atkinson CA, Rugenski AT (2015) Consumer-driven nutrient dynamics in freshwater ecosystems: an introduction. Freshwater Biol 60:439–442
Cleveland A, Montgomery W (2003) Gut characteristics and assimilation efficiencies in two species of herbivorous damselfishes (Pomacentridae: Stegastes dorsopunicans and S. planifrons). Mar Biol 142:35–44
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
Dodds WK, Whiles MR (2010) Freshwater ecology. Elsevier, London
El-Sabaawi RW et al (2012) Widespread intraspecific organismal stoichiometry among populations of the Trinidadian guppy. Funct Ecol 26:666–676
El-Sabaawi RW et al (2015a) Intraspecific phenotypic differences in fish affect ecosystem processes as much as bottom-up factors. Oikos. doi:10.1111/oik.01769
El-Sabaawi RW, Marshall MC, Bassar RD, Lopez-Sepulcre A, Palkovacs EP, Dalton CM (2015b) Assessing the effects of life history evolution on nutrient recycling: from experiments to the field. Freshwater Biol 60:590–601
Elser JJ, Urabe J (1999) The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology 80:735–751
Elser JJ, Dobberfuhl DR, MacKay NA, Schampel JH (1996) Organism size, life history, and N:P stoichiometry. Bioscience 46:674–684
Elser JJ, O’Brien WJ, Dobberfuhl DR, Dowling TE (2000) The evolution of ecosystem processes: growth rate and elemental stoichiometry of a key herbivore in temperate and arctic habitats. J Evol Biol 13:845–853
Elser JJ et al (2003) Growth rate-stoichiometry couplings in diverse biota. Ecol Lett 6:936–943. doi:10.1046/J.1461-0248.2003.00518.X
Frost PC et al (2006) Threshold elemental ratios of carbon and phosphorus in aquatic consumers. Ecol Lett 9:774–779. doi:10.1111/J.1461-0248.2006.00919.X
Gillooly JF et al (2005) The metabolic basis of whole-organism RNA and phosphorus content. Proc Natl Acad Sci USA 102:11923–11927. doi:10.1073/Pnas.0504756102
Griffiths D (2006) The direct contribution of fish to lake phosphorus cycles. Ecol Freshwater Fish 15:86–95
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
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
Hendry AP, Peichel CL, Matthews B, Boughman JW, Nosil P (2013) Stickleback research: the now and the next. Evol Ecol Res 15:111–141
Hevesy G (1945) Rate of renewal of the fish skeleton. Acta Physiol Scand 9:234–247
Hood JM, Vanni MJ, Flecker AS (2005) Nutrient recycling by two phosphorus-rich grazing catfish: the potential for phosphorus-limitation of fish growth. Oecologia 146:247–257
Jeyasingh PD, Cothran RD, Tobler M (2014) Testing the ecological consequences of evolutionary change using elements. Ecol Evol 4:528–538
Karasov WH, Douglas AE (2013) Comparative digestive physiology. Compr Physiol
Kay AD, Ashton IW, Gorokhova E, Kerkhoff AJ, Liess A, Litchman E (2005) Toward a stoichiometric framework for evolutionary biology. Oikos 109:6–17
Kiørboe T (2013) Zooplankton body composition. Limnol Oceanogr 58:1843–1850
Kraft CE (1992) Estimates of phosphorus and nitrogen cycling by fish using a bioenergetics approach. Can J Fish Aquat Sci 49:2596–2604
Lassuy DR (1984) Diet, intestinal morphology, and nitrogen assimilation efficiency in the damselfish, Stegastes lividus, in Guam. Environ Biol Fish 10:183–193
Leaver SD, Reimchen TE (2012) Abrupt changes in defence and trophic morphology of the giant threespine stickleback (Gasterosteus sp.) following colonization of a vacant habitat. Biol J Linn Soc 107:494–509
Marchinko KB (2009) Predation’s role in repeated phenotypic and genetic divergence of armor in threespine stickleback. Evolution 63:127–138
Matthews B, Marchinko KB, Bolnick DI, Mazumder A (2010) Specialization of trophic position and habitat use by sticklebacks in an adaptive radiation. Ecology 91:1025–1034
Matthews B et al (2011) Toward an integration of evolutionary biology and ecosystem science. Ecol Lett 14:690–701
McIntyre PB, Flecker AS (2010) Ecological stoichiometry as in integrative framework in stream fish ecology. Am Fish Soc Symp 73:539–558
McIntyre PB, Jones LE, Flecker AS, Vanni MJ (2007) Fish extinctions alter nutrient recycling in tropical freshwaters. Proc Natl Acad Sci USA 104:4461–4466. doi:10.1073/Pnas.0608148104
McManamay RA, Webster JR, Valett HM, Dolloff CA (2010) Does diet influence consumer nutrient cycling? Macroinvertebrate and fish excretion in streams. J N Am Benthol Soc 30:84–102
McPhail JD (1992) Ecology and evolution of sympatric sticklebacks (Gasterosteus): evidence for a species-pair in Paxton Lake, Texada Island, British Columbia. Can J Zool 70:361–369
McPhail JD (2007) Freshwater fishes of British Columbia. University of Alberta, Alberta
Morinville GR, Rasmussen JB (2003) Early juvenile bioenergetic differences between anadromous and resident brook trout (Salvelinus fontinalis). Can J Fish Aquat Sci 60:401–410
Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis, 1st edn. Pergamon, New York
Persson J, Fink P, Goto A, Hood JM, Jonas J, Kato S (2010) To be or not to be what you eat: regulation of stoichiometric homeostasis among autotrophs and heterotrophs. Oikos 119:741–751. doi:10.1111/J.1600-0706.2009.18545.X
Pilati A, Vanni MJ (2007) Ontogeny, diet shifts, and nutrient stoichiometry in fish. Oikos 116:1663–1674. doi:10.1111/J.2007.0030-1299.15970.X
Reimchen T (1980) Spine deficiency and polymorphism in a population of Gasterosteus aculeatus: an adaptation to predators? Can J Zool 58:1232–1244
Reimchen TE (1994) Predators and morphological evolution in threespine stickleback. In: Bell M, Foster S (eds) The evolutionary biology of the threespine stickleback. Oxford University Press, pp 240–276
Rowan DJ, Rasmussen JB (1996) Measuring the bioenergetic cost of fish activity in situ using a globally dispersed radiotracer (137Cs). Can J Fish Aquat Sci 53:734–745
Rudman SM et al. (2015) Adaptive genetic variation mediates bottom-up and top-down control in an aquatic ecosystem. In: Proceedings of the Royal Society B, vol 282. The Royal Society, p 20151234
Rundle HD, Nagel L, Boughman JW, Schluter D (2000) Natural selection and parallel speciation in sympatric sticklebacks. Science 287:306–308
Saimoto RK (1993) Life history of marine threespine stickleback in Oyster Lagoon, British Columbia MSc, University of British Columbia
Schindler DE, Eby LA (1997) Stoichiometry of fishes and their prey: implications for nutrient recycling. Ecology 78:1816–1831
Schluter D (1993) Adaptive radiation in sticklebacks: size, shape, and habitat use efficiency. Ecology 74(3):699–709
Schoener TW (2011) The newest synthesis: understanding the interplay of evolutionary and ecological dynamics. Science 331:426–429
Sereda JM, Hudson JJ, McLoughlin PD (2008) General empirical models for predicting the release of nutrients by fish, with a comparison between detritivores and non-detritivores. Freshwater Biol 53:2133–2144
Snyder RJ (1991) Migration and life histories of the threespine stickleback: evidence for adaptive variation in growth rate between populations. Environ Biol Fish 31:381–388
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
Taylor BW, Flecker AS, Hall RO (2006) Loss of a harvested fish species disrupts carbon flow in a diverse tropical river. Science 313:833–836
Thompson JN (1998) Rapid evolution as an ecological process. Trends Ecol Evol 13:329–332
Torres LE, Vanni MJ (2007) Stoichiometry of nutrient excretion by fish: interspecific variation in a hypereutrophic lake. Oikos 116:259–270
Tudorache C, Blust R, De Boeck G (2007) Swimming capacity and energetics of migrating and non-migrating morphs of three-spined stickleback Gasterosteus aculeatus L. and their ecological implications. J Fish Biol 71:1448–1456
Vamosi SM (1996) Postmating isolation mechanisms between sympatric populations of three-spined sticklebacks. University of British Columbia, BC
Vamosi SM, Schluter D (2004) Character shifts in the defensive armor of sympatric sticklebacks. Evolution 58:376–385
Vanni MJ (2002) Nutrient cycling by animals in freshwater ecosystems. Annu Rev Ecol Syst 33:341–370
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
Waters TF (1977) Secondary production in inland waters. Adv Ecol Res 10:91–164
Wetzel RG (2001) Limnology: lake and river ecosystems, 3rd edn. Academic Press, San Diego
Wootton RJ (1976) The biology of the sticklebacks. Academic Press, London
Wootton RJ (1984) A functional biology of sticklebacks. University of California Press, California
Wootton RJ (1994) Energy allocation in the threespine stickleback. In: Bell M, Foster S (eds) The evolutionary biology of the threespine stickleback. Oxford University Press, pp 114–143
Wooton RJ (1998) Ecology of Teleost Fishes. 2nd edn. Kulwer Academic Publishers, Netherlands
Zuur AF (2009) Mixed effects models and extensions in ecology with R. Springer, Berlin
Acknowledgments
The authors thank Katie Peichel, Andrew Hendry, and two anonymous reviewers for their comments on this paper. This research was supported by a Natural Sciences and Engineering Research Council of Canada Discovery grant to R. El-Sabaawi and a Natural Sciences and Engineering Research Council of Canada Undergraduate Student Research Award fellowship to M. Warbanski.
Author contribution statement
R. E. S. conceived the study and wrote the manuscript. R. E. S., M. L. W., S. R., R. H., and B. M. collected the samples, analyzed the data, and provided editorial feedback.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Ken Spitze.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
El-Sabaawi, R.W., Warbanski, M.L., Rudman, S.M. et al. Investment in boney defensive traits alters organismal stoichiometry and excretion in fish. Oecologia 181, 1209–1220 (2016). https://doi.org/10.1007/s00442-016-3599-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-016-3599-0