Abstract
Recent work has indicated that stoichiometric food quality in terms of the carbon:phosphorus (C:P) ratio affects consumers whether the imbalance involves a deficit or an excess of nutrients; hence, organisms exist on a “stoichiometric knife edge”. While previous studies have focused primarily on autotroph–herbivore trophic transfer, nutritional imbalances may also affect the interactions between species at higher trophic levels. Since the foods of carnivores are normally stoichiometrically similar to the body compositions of those carnivores, they may be more severely affected than herbivores if imbalances become pronounced. We analysed the response of the predatory copepod Parabroteas sarsi to monospecific diet treatments consisting of high and low C:P prey items. These dietary treatments strongly affected the predator’s elemental composition and growth, although prey selection, excretion, egestion, and respiration rates were not affected. We suggest that, due to their low threshold elemental ratio and a narrow C:P stoichiometric knife edge, these predators are highly vulnerable to stoichiometric imbalances, whether an excess or a deficit of nutrients is involved. Our results demonstrating this high sensitivity to prey C:P ratio show that the stoichiometric knife edge may apply to not only herbivores but also higher trophic levels. Thus, predators such as P. sarsi, with a much narrower range of food quality, may also be strongly affected by fluctuations in the quality of their prey, with negative consequences for their secondary production.
Similar content being viewed by others
References
Andersen T, Hessen DO (1991) Carbon, nitrogen, and phosphorus content of freshwater zooplankton. Limnol Oceanogr 36:807–814
APHA (2005) Standard methods for the examination of water and wastewater. American Public Health Association, Washington, DC
Balseiro E, Souza MS, Modenutti B, Reissig M (2008) Living in transparent lakes: low food P:C ratio decreases antioxidant response to ultraviolet radiation in Daphnia. Limnol Oceanogr 53:2383–2390
Boersma M (2000) The nutritional quality of P limited algae for Daphnia. Limnol Oceanogr 45:1157–1161
Boersma M, Elser JJ (2006) Too much of a good thing: on stoichiometrically balanced diets and maximal growth. Ecology 87:1325–1330
Boersma M, Kreutzer C (2002) Life at the edge: is food quality really of minor importance at low quantities? Ecology 83:2552–2561
Boersma M, Aberle N, Hantzsche FM, Schoo KL, Wiltshire KH, Malzahn AM (2008) Nutritional limitation travels up the food chain. Int Rev Hydrobiol 93:479–488
Boersma M, Becker C, Malzahn AM, Vernooij S (2009) Food chain effects of nutrient limitation in primary producers. Mar Freshw Res 60:983–989
Bohonak AJ, Linde KVD (2004) RMA: software for reduced major axis regression, Java version. http://www.kimvdlinde.com/professional/rma.html
Brett MT, Muller-Navarra DC (1997) The role of highly unsaturated fatty acids in aquatic food web processes. Freshw Biol 38:483–499
Brett MT, Müller-Navarra DC, Persson J (2009) Crustacean zooplankton fatty acid composition. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, pp 115–146
Bullejos FJ, Carrillo P, Gorokhova E, Medina-Sánchez JM, Balseiro EG, Villar-Argaiz M (2014) Shifts in food quality for herbivorous consumer growth: multiple golden means in the life history. Ecology 95:1272–1284
Calbet A, Agustí S (1999) Latitudinal changes of copepod egg production rates in Atlantic waters: temperature and food availability as the main driving factors. Mar Ecol Prog Ser 181:155–162
Darchambeau F, Faerøvig PJ, Hessen DO (2003) How Daphnia copes with excess carbon in its food. Oecologia 136:336–346
DeMott WR, Gulati RD (1999) Phosphorus limitation in Daphnia: evidence from a long term study of three hypereutrophic Dutch lakes. Limnol Oceanogr 44:1557–1564
Dickman EM, Newell JM, Gonzalez MJ, Vanni MJ (2008) Light, nutrients, and food-chain length constrain planktonic energy transfer efficiency across multiple trophic levels. Proc Natl Acad Sci USA 105:18408–18412
Elser JJ et al (2005) Response of grazing snails to phosphorus enrichment of modern stromatolitic microbial communities. Freshw Biol 50:1826–1835
Frost PC et al (2006) Threshold elemental ratios of carbon and phosphorus in aquatic consumers. Ecol Lett 9:774–779
Hall SR, Leibold MA, Lytle DA, Smith VH (2004) Stoichiometry and planktonic grazer composition over gradients of light, nutrients, and predation risk. Ecology 85:2291–2301
Hay S, Kiørboe T, Matthews A (1991) Zooplankton biomass and production in the North Sea during the autumn circulation experiment, October 1987–March 1988. Cont Shelf Res 11:1453–1476
He X, Wang WX (2006) Releases of ingested phytoplankton carbon by Daphnia magna. Freshw Biol 51:649–665
He X, Wang WX (2008) Stoichiometric regulation of carbon and phosphorus in P-deficient Daphnia magna. Limnol Oceanogr 53:244–254
Hessen DO, Elser JJ, Sterner RW, Urabe J (2013) Ecological stoichiometry: an elementary approach using basic principles. Limnol Oceanogr 58:2219–2236
Hewson-Hughes AK, Hewson-Hughes VL, Miller AT, Hall SR, Simpson SJ, Raubenheimer D (2011) Geometric analysis of macronutrient selection in the adult domestic cat, Felis catus. J Exp Biol 214:1039–1051
Hirst A, Lampitt R (1998) Towards a global model of in situ weight-specific growth in marine planktonic copepods. Mar Biol 132:247–257
Hirst A, McKinnon A (2001) Does egg production represent adult female copepod growth? A call to account for body weight changes. Mar Ecol Progr Ser 223:179–199
Jensen K et al. (2012) Optimal foraging for specific nutrients in predatory beetles. Proc R Soc B 279:2212–2218
Kagata H, Ohgushi T (2007) Carbon–nitrogen stoichiometry in the tritrophic food chain willow, leaf beetle, and predatory ladybird beetle. Ecol Res 22:671–677
Kilham SS, Kreeger DA, Lynn SG, Goulden CE, Herrera L (1998) COMBO—a defined freshwater culture medium for algae and zooplankton. Hydrobiologia 377:147–159
Kiørboe T, Nielsen TG (1994) Regulation of zooplankton biomass and production in a temperate, coastal ecosystem. 1. Copepods Limnol Oceanogr 39:493–507
Lampert W, Bohrer R (1984) Effect of food availability on the respiratory quotient of Daphnia magna. Comp Biochem Physiol A Physiol 78:221–223
Laspoumaderes C, Modenutti B, Balseiro E (2010) Herbivory versus omnivory: linking homeostasis and elemental imbalance in copepod development. J Plankton Res 32:1573–1582
Laspoumaderes C, Modenutti B, Souza MS, Navarro MB, Cuassolo F, Balseiro E (2013) Glacier melting and stoichiometric implications for lake community structure: zooplankton species distributions across a natural light gradient. Global Change Biol 19:316–326
Malzahn AM, Aberle N, Clemmesen C, Boersma M (2007) Nutrient limitation of primary producers affects planktivorous fish condition. Limnol Oceanogr 52:2062–2071
Marshall SM, Orr AP (1972) The biology of a marine copepod Calanus finmarchicus (Gunnerus). Springer, Berlin
Mayntz D, Toft S, Vollrath F (2003) Effects of prey quality and availability on the life history of a trap-building predator. Oikos 101:631–638
Mayntz D, Raubenheimer D, Salomon M, Toft S, Simpson SJ (2005) Nutrient-specific foraging in invertebrate predators. Science 307:111–113
McKinnon A (1996) Growth and development in the subtropical copepod Acrocalanus gibber. Limnol Oceanogr 41:1438–1447
Morehouse RL, Dzialowski AR, Jeyasingh PD (2013) Impacts of excessive dietary phosphorus on zebra mussels. Hydrobiologia 707:73–80
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
Plath K, Boersma M (2001) Mineral limitation of zooplankton: stoichiometric constraints and optimal foraging. Ecology 82:1260–1269
Raubenheimer D, Simpson S (1993) The geometry of compensatory feeding in the locust. Anim Behav 45:953–964
Raubenheimer D, Simpson S (1999) Integrating nutrition: a geometrical approach. In: Simpson SJ, Mordue AJ, Hardie J (eds) Proceedings of the 10th International Symposium on Insect–Plant Relationships. Springer, Dordrecht, pp 67–82
Raubenheimer D, Simpson S (2003) Nutrient balancing in grasshoppers: behavioural and physiological correlates of dietary breadth. J Exp Biol 206:1669–1681
Raubenheimer D, Mayntz D, Simpson SJ, Tøft S (2007) Nutrient-specific compensation following diapause in a predator: implications for intraguild predation. Ecology 88:2598–2608
Richardson AJ, Verheye HM (1999) Growth rates of copepods in the southern Benguela upwelling system: the interplay between body size and food. Limnol Oceanogr 44:382–392
Sabat P, Lagos JA, Bozinovic F (1999) Test of the adaptive modulation hypothesis in rodents: dietary flexibility and enzyme plasticity. Comp Biochem Physiol A 123:83–87
Schmidt JM, Sebastian P, Wilder SM, Rypstra AL (2012) The nutritional content of prey affects the foraging of a generalist arthropod predator. PLoS One 7:e49223
Schoo KL, Aberle N, Malzahn AM, Boersma M (2010) Does the nutrient stoichiometry of primary producers affect the secondary consumer Pleurobrachia pileus? Aquat Ecol 44:233–242
Schoo KL, Aberle N, Malzahn AM, Boersma M (2012a) Food quality affects secondary consumers even at low quantities: an experimental test with larval European lobster. PLoS One 7:e33550
Schoo KL, Malzahn AM, Krause E, Boersma M (2012b) Increased carbon dioxide availability alters phytoplankton stoichiometry and affects carbon cycling and growth of a marine planktonic herbivore. Mar Biol 160:2145–2155
Simpson S, Raubenheimer D (1996) Feeding behaviour, sensory physiology and nutrient feedback: a unifying model. Entomol Exp Appl 80:55–64
Simpson SJ, Raubenheimer D (2012) The nature of nutrition: a unifying framework. Aust J Zool 59:350–368
Simpson SJ, Raubenheimer D, Charleston MA, Clissold FJ (2010) Modelling nutritional interactions: from individuals to communities. Trends Ecol Evol 25:53–60
Sterner RW, Elser JJ (2002) Ecological stoichiometry.The biology of elements from molecules to the biosphere. Princeton University Press, Princeton
Swalethorp R et al (2011) Grazing, egg production, and biochemical evidence of differences in the life strategies of Calanus finmarchicus, C. glacialis and C. hyperboreus in Disko Bay, western Greenland. Mar Ecol Progr Ser 429:125–144
Tao L, Hunter MD (2012) Does anthropogenic nitrogen deposition induce phosphorus limitation in herbivorous insects? Global Change Biol 18:1843–1853
Vega MP (1999) Life-stage differences in the diet of Parabroteas sarsi (Daday) (Copepoda, Calanoida): a field study. Limnologica 29:186–190
Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev Camb Philos Soc 81:259–291
Wilder SM, Mayntz D, Toft S, Rypstra AL, Pilati A, Vanni MJ (2010) Intraspecific variation in prey quality: a comparison of nutrient presence in prey and nutrient extraction by predators. Oikos 119:350–358
Acknowledgments
This work was supported by the Fondo Nacional de Ciencia y Técnica PICT 2011-2240, PICT2012-1168 and Universidad Nacional del Comahue B-163. JJE acknowledges the support of the US National Science Foundation (DMS-0920744) and the Fulbright Foundation. We are also grateful to two reviewers and the editor for their constructive comments. CL is a CONICET fellowship and EB and BM are CONICET researchers.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Robert O. Hall.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Laspoumaderes, C., Modenutti, B., Elser, J.J. et al. Does the stoichiometric carbon:phosphorus knife edge apply for predaceous copepods?. Oecologia 178, 557–569 (2015). https://doi.org/10.1007/s00442-014-3155-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-014-3155-8