Skip to main content
SpringerLink
Log in

Predator evasion in zooplankton is suppressed by polyunsaturated fatty acid limitation

  • Physiological ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Herbivorous zooplankton avoid size-selective predation by vertical migration to a deep, cold water refuge. Adaptation to low temperatures in planktonic poikilotherms depends on essential dietary lipids; the availability of these lipids often limits growth and reproduction of zooplankton. We hypothesized that limitation by essential lipids may affect habitat preferences and predator avoidance behavior in planktonic poikilotherms. We used a liposome supplementation technique to enrich the green alga Scenedesmus obliquus and the cyanobacterium Synecchococcus elongatus with the essential lipids, cholesterol and eicosapentaenoic acid (EPA), and an indoor system with a stratified water-column (plankton organ) to test whether the absence of these selected dietary lipids constrains predator avoidance (habitat preferences) in four species of the key-stone pelagic freshwater grazer Daphnia. We found that the capability of avoiding fish predation through habitat shift to the deeper and colder environment was suppressed in Daphnia unless the diet was supplemented with EPA; however, the availability of cholesterol did not affect habitat preferences of the tested taxa. Thus, their ability to access a predator-free refuge and the outcome of predator–prey interactions depends upon food quality (i.e. the availability of an essential fatty acid). Our results suggest that biochemical food quality limitation, a bottom–up factor, may affect the top–down control of herbivorous zooplankton.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arts MT, Ackman RG, Holub BJ (2001) “Essential fatty acids” in aquatic ecosystems: a crucial link between diet and human health and evolution. Can J Fish Aquat Sci 58:122–137

    Article  CAS  Google Scholar 

  • Becker C, Boersma M (2005) Differential effects of phosphorus and fatty acids on Daphnia magna growth and reproduction. Limnol Oceanogr 50:388–397. doi:10.4319/lo.2005.50.1.0388

    Article  CAS  Google Scholar 

  • Bernot RJ, Turner AM (2001) Predator identity and trait-mediated indirect effects in a littoral food web. Oecologia 129:139–146. doi:10.1007/s004420100705

    Article  Google Scholar 

  • Boriss H, Gabriel W (1988) Vertical migration in Daphnia: the role of phenotypic plasticity in the migration pattern for competing clones or species. Oikos 83:129–138

    Article  Google Scholar 

  • Brzeziński T (2010) Ecology of three sympatric Daphnia species and their hybrids. PhD. dissertation, University of Warsaw, Poland (in Polish, with English summary)

  • Cobelas MA, Lechado JZ (1989) Lipids in microalgae-a review. Biochem Grasas Aceites 40:118–145

    Google Scholar 

  • Cohen JH, Forward RB (2009) Zooplankton diel vertical migration—A review of proximate control. Oceanogr Mar Biol Annu Rev 47:77–109

    Google Scholar 

  • Cousyn C, De Meester L, Colbourne JK, Brendonck L, Verschuren D, Volckaert F (2001) Rapid, local adaptation of zooplankton behavior to changes in predation pressure in the absence of neutral genetic changes. Proc Natl Acad Sci USA 98:6256–6260

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Crockett EL (1998) Cholesterol function in plasma membranes from ectotherms: membrane specific roles in adaptation to temperature. Am Zool 38:291–304

    Article  CAS  Google Scholar 

  • Crockett EL, Hazel JR (1995) Cholesterol levels explain inverse compensation of membrane order in brush border but not homeoviscuous adaptation in basolateral membranes from intestinal epithelia of rainbow trout. J Exp Biol 198:1105–1113

    CAS  PubMed  Google Scholar 

  • Dawidowicz P, Loose C (1992) Metabolic costs during predator-induced diel vertical migration of Daphnia. Limnol Oceanogr 37:1589–1595

    Article  Google Scholar 

  • Dodson SI (1988) The ecological role of chemical stimuli for the zooplankton: predator-avoidance behavior in Daphnia. Limnol Oceanogr 33:1431–1439

    Article  Google Scholar 

  • Elser JJ, Fagan WF, Denne RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham S, McCauley E, Schutz KL, Siemann EH, Sterner RW (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580. doi:10.1038/35046058

    Article  CAS  PubMed  Google Scholar 

  • Farkas T (1979) Adaptation of fatty-acid compositions to temperature-a study on planktonic crustaceans. Comp Biochem Physiol 64B:71–76

    CAS  Google Scholar 

  • Flik B, Ringelberg J (1993) Influence of food availability on the initiation of diel vertical migration (DVM) in Lake Maarseveen. Arch Hydrobiol 39:57–65

    Google Scholar 

  • Fortin D, Beyer HL, Boyce MS, Smith DW, Duchesne T, Mao JS (2005) Wolves influence elk movements: behavior shapes a trophic cascade in Yellowstone National Park. Ecology 86:1320–1330

    Article  Google Scholar 

  • Ger KA, Hansson L-A, Lürling M (2014) Understanding cyanobacteria-zooplankton interactions in a more eutrophic world. Freshwat Biol 59:1783–1798. doi:10.1111/fwb.12393

    Article  Google Scholar 

  • Gliwicz ZM (1986) Predation and the evolution of vertical migration in zooplankton. Nature 320:746–748. doi:10.1038/320746a0

    Article  Google Scholar 

  • Gliwicz ZM (1990) Food thresholds and body size in cladocerans. Nature 343:638–640. doi:10.1038/343638a0

    Article  Google Scholar 

  • Gliwicz ZM (2003) Between hazards of starvation and risk of predation: the ecology of offshore animals. In: Kinne O (ed) Excellence of ecology, part 12. International Ecology Institute, Oldendorf

    Google Scholar 

  • Guillard RR (1975) Cultures of phytoplankton for feeding of marine invertebrates. Culture of marine invertebrate animals. Plenum, New York, pp 29–60

    Chapter  Google Scholar 

  • Gurr MP, Harwood JL (1991) Lipid biochemistry—An introduction, 4th edn. Chapman and Hall, London

    Google Scholar 

  • Hansson LA, Hylander S (2009) Size-structured risk assessments govern Daphnia migration. Proc R Soc Lond B 276:331–336. doi:10.1098/rspb.2008.1088

    Article  Google Scholar 

  • Hartwich M, Martin-Creuzburg D, Rothhaupt K-O, Wacker A (2012) Oligotrophication of a large, deep lake alters food quantity and quality constraints at the primary producer–consumer interface. Oikos 121:1702–1712

    Article  CAS  Google Scholar 

  • Hassett RP, Crockett EL (2009) Habitat temperature is an important determinant of cholesterol contents in copepods. J Exp Biol 212:71–77

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Haupt F, Stockenreiter M, Baumgarten M, Boersma M, Stibor H (2009) Daphnia diel vertical migration: implications beyond zooplankton. J Plankton Res 31:515–524. doi:10.1093/plankt/fbp003

    Article  Google Scholar 

  • Hays GC (2003) A review of the adaptive significance and ecosystem consequences of zooplankton diel vertical migrations. Hydrobiologia 503:163–170. doi:10.1023/B:HYDR.0000008476.23617.b0

    Article  Google Scholar 

  • Hazel JR (1995) Thermal adaptation in biological membranes—is homeoviscous adaptation the explanation. Annu Rev Physiol 57:19–42. doi:10.1146/annurev.ph.57.030195.000315

    Article  CAS  PubMed  Google Scholar 

  • Hazel JR, Williams EE (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167–227. doi:10.1016/0163-7827(90)90002-3

    Article  CAS  PubMed  Google Scholar 

  • Heath MR, Speirs DC, Steele JH (2014) Understanding patterns and processes in models of trophic cascades. Ecol Lett 17:101–114

    Article  PubMed Central  PubMed  Google Scholar 

  • Jöhnk KD, Huisman J, Sharples J, Sommeijer B, Visser PM, Stroom JM (2008) Summer heatwaves promote blooms of harmful cyanobacteria. Glob Change Biol 14:495–512. doi:10.1111/j.1365-2486.2007.01510.x

    Article  Google Scholar 

  • Lampert W (1989) The adaptive significance of diel vertical migration of zooplankton. Funct Ecol 3:21–27

    Article  Google Scholar 

  • Lampert W (1991) The dynamics of Daphnia in a shallow lake. Verh Intern Ver Limnol 24:795–798

    Google Scholar 

  • Lampert W, Taylor BE (1985) Zooplankton grazing in a eutrophic lake: implications of diel vertical migration. Ecology 66:68–82. doi:10.2307/1941307

    Article  Google Scholar 

  • Lampert W, McCauley E, Manly BFJ (2003) Trade-offs in the vertical distribution of zooplankton: ideal free distribution with costs? Proc R Soc Lond B 270:765–773. doi:10.1098/rspb.2002.2291

    Article  Google Scholar 

  • Loose CJ, Dawidowicz P (1994) Trade-offs in diel vertical migration by zooplankton: the costs of predator avoidance. Ecology 75:2255–2263. doi:10.2307/1940881

    Article  Google Scholar 

  • Luttbeg B, Kerby JC (2005) Are scared prey as good as dead? Trends Ecol Evol 20:416–418

    Article  PubMed  Google Scholar 

  • Manzur T, Vidal F, Pantoja JF, Fernández M, Navarrete SA (2014) Behavioural and physiological responses of limpet prey to a seastar predator and their transmission to basal trophic levels. J Anim Ecol 83:923–933. doi:10.1111/1365-2656.12199

    Article  PubMed  Google Scholar 

  • Martin-Creuzburg D, Von Elert E, Hoffmann KH (2008) Nutritional constraints at the cyanobacteria-Daphnia interface: the role of essential lipids. Limnol Oceanogr 53:456–468

    Article  Google Scholar 

  • Martin-Creuzburg D, Sperfeld E, Wacker A (2009) Colimitation of a freshwater herbivore by sterols and polyunsaturated fatty acids. Proc R Soc Lond B 276:1805–1814

    Article  CAS  Google Scholar 

  • Martin-Creuzburg D, Wacker A, Ziese C, Kainz MJ (2012) Dietary lipid quality affects temperature-mediated reaction norms of a freshwater key herbivore. Oecologia 168:901–912. doi:10.1007/s00442-011-2155-1

    Article  PubMed  Google Scholar 

  • Masclaux H, Bec A, Kainz MJ, Desvilettes Ch, Jouve I, Bourdier G (2009) Combined effects of food quality and temperature on somatic growth and reproduction of two freshwater cladocerans. Limnol Oceanogr 54:1323–1332. doi:10.4319/lo.2009.54.4.1323

    Article  Google Scholar 

  • Mehner T, Benndorf J, Kasprzak P, Koschel R (2002) Biomanipulation of lake ecosystems: succesful applications and expanding complexity in the underlying science. Freshw Biol 47:2453–2465

    Article  Google Scholar 

  • Müller-Navarra DC (1995) Evidence that a highly unsaturated fatty acid limits Daphnia growth in nature. Arch Hydrobiol 132:297–307

    Google Scholar 

  • Müller-Navarra DC, Brett MT, Liston AM, Goldman CR (2000) A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 403:74–77. doi:10.1038/47469

    Article  PubMed  Google Scholar 

  • Müller-Navarra DC, Brett MT, Park S, Chandra S, Ballantyne AP, Zorita E, Goldman CR (2004) Unsaturated fatty acid content in seston and tropho-dynamic coupling in lakes. Nature 427:69–72. doi:10.1038/nature02210

    Article  PubMed  Google Scholar 

  • Pace ML, Cole JJ, Carpenter SR, Kitchell JF (1999) Trophic cascades revealed in diverse ecosystems. Trends Ecol Evol 14:483–488

    Article  PubMed  Google Scholar 

  • Perrow MR, Meijer M-L, Dawidowicz P (1997) Biomanipulation in shallow lakes: state of the art. Hydrobiologia 342(343):355–365

    Article  Google Scholar 

  • Persson J, Brett MT, Vrede T, Ravet JL (2007) Food quantity and quality regulation of trophic transfer between primary producers and a keystone grazer (Daphnia) in pelagic freshwater food webs. Oikos 116:1152–1163. doi:10.1111/j.0030-1299.2007.15639.x

    Article  Google Scholar 

  • Petersen SO, Holmstrup M (2000) Temperature effects on lipid composition of the earthworms Lumbricus rubellus and Eisenia nordenskioeldi. Soil Biol Biochem 32:1787–1791

    Article  CAS  Google Scholar 

  • Petersen SO, Klug MJ (1994) Effects of sieving, storage, and incubation temperature on the phospholipid fatty acid profile of a soil microbial community. Appl Environ Microbiol 60:242–2430

    Google Scholar 

  • Pond DW, Tarling GA (2011) Phase transition of wax esters adjust buoyancy in diapausing Calanoides acutus. Limnol Oceanogr 56:1310–1318

    Article  CAS  Google Scholar 

  • Ravet JL, Brett MT, Müller-Navarra DC (2003) A test of the role of polyunsaturated fatty acids in phytoplankton food quality for Daphnia using liposome supplementation. Limnol Oceanogr 48:1938–1947

    Article  CAS  Google Scholar 

  • Reichwaldt ES, Stibor H (2005) The impact of diel vertical migration of Daphnia on phytoplankton dynamics. Oecologia 146:50–56. doi:10.1007/s00442-005-0176-3

    Article  PubMed  Google Scholar 

  • Sakwinska O, Dawidowicz P (2005) Life history strategy and depth selection behavior as alternative antipredator defenses among natural Daphnia hyalina populations. Limnol Oceanogr 50:1284–1289. doi:10.4319/lo.2005.50.4.1284

    Article  Google Scholar 

  • Schlechtriem C, Arts MT, Zellmer ID (2006) Effect of temperature on the fatty acid composition and temporal trajectories of fatty acids in fasting Daphnia pulex (Crustacea, Cladocera). Lipids 41:397–400

    Article  CAS  PubMed  Google Scholar 

  • Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–156

    Article  Google Scholar 

  • Smyntek PM, Teece MA, Schulz KL, Storch AJ (2008) Taxonomic differences in the essential fatty acid composition of groups of freshwater zooplankton relate to reproductive demands and generation time. Freshwat Biol 53:1768–1782

    Article  CAS  Google Scholar 

  • Sperfeld E, Wacker A (2009) Effects of temperature and dietary sterol availability on growth and cholesterol allocation of the aquatic keystone species Daphnia. J Exp Biol 212:3051–3059. doi:10.1242/jeb.031401

    Article  CAS  PubMed  Google Scholar 

  • Sperfeld E, Wacker A (2011) Temperature- and cholesterol-induced changes in eicosapentaenoic acid limitation of Daphnia magna determined by a promising method to estimate growth saturation thresholds. Limnol Oceanogr 56:1273–1284

    Article  CAS  Google Scholar 

  • Sperfeld E, Wacker A (2012) Temperature affects the limitation of Daphnia magna by eicosapentaenoic acid, and the fatty acid composition of body tissue and eggs. Freshwat Biol 57:497–508. doi:10.1111/j.1365-2427.2011.02719.x

    Article  CAS  Google Scholar 

  • Stich HB, Lampert W (1981) Predator evasion as an explanation of diurnal vertical migration by zooplankton. Nature 293:396–398. doi:10.1038/293396a0

    Article  Google Scholar 

  • Van Dooremalen C, Berg MP, Ellers J (2013) Acclimation responses to temperature vary with vertical stratification: implications for vulnerability of soil-dwelling species to extreme temperature events. Glob Change Biol 19:975–984. doi:10.1111/gcb.12081

    Article  Google Scholar 

  • Viarengo AR, Accomando R, Roma G, Benati U, Damonte G, Orunesu M (1994) Differences in lipid composition of cell membranes from Antarctic and Mediterranean scallops. Comp Biochem Physiol B 109:579–584

    Google Scholar 

  • Von Elert E (2002) Determination of limiting polyunsaturated fatty acids in Daphnia galeata using a new method to enrich food algae with single fatty acids. Limnol Oceanogr 47:1764–1773. doi:10.4319/lo.2002.47.6.1764

    Article  Google Scholar 

  • Von Elert E, Jüttner F (1997) Phosphorus limitation not light controls the exudation of allelopathic compounds by Trichormus doliolum. Limnol Oceanogr 42:1796–1802

    Article  Google Scholar 

  • Von Elert E, Wolffrom T (2001) Supplementation of cyanobacterial food with polyunsaturated fatty acids does not improve growth of Daphnia. Limnol Oceanogr 46:1552–1558. doi:10.4319/lo.2001.46.6.1552

    Article  Google Scholar 

  • Von Elert E, Martin-Creuzburg D, Le Coz JR (2003) Absence of sterols constrains carbon transfer between cyanobacteria and a freshwater herbivore (Daphnia galeata). Proc R Soc Lond B 270:1209–1214. doi:10.1098/rspb.2003.2357

    Article  Google Scholar 

  • Wacker A, Von Elert E (2001) Polyunsaturated fatty acids: evidence for non-substitutable biochemical resources in Daphnia galeata. Ecology 82:2507–2520. doi:10.1890/0012-9658(2001)082[2507:PFAEFN]2.0.CO;2

  • Watson SB, McCauley E, Downing JA (1997) Patterns in phytoplankton taxonomic composition across temperate lakes of differing nutrient status. Limnol Oceanogr 42:487–495

    Article  Google Scholar 

  • Weers PM, Siewertsen MK, Gulati RD (1997) Is the fatty acids composition of Daphnia galeata determined by the fatty acid composition of the ingested diet? Freshwat Biol 38:731–738

    Article  CAS  Google Scholar 

  • Winder M, Boersma M, Spaak P (2003) On the cost of vertical migration: are feeding conditions really worse at greater depths? Freshwat Biol 48:383–393

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by a stipend from Deutscher Akademischer Auslandsdienst (DAAD) to T.B. The authors declare no conflict of interests. We thank to Maarten Boersma and anonymous reviewers for their valuable comments, and to Frederic Bartlett for linguistic help.

Author contribution statement

T.B. and E.v.E. worked together to design the experiments. T.B. performed the experiments and analysed the data. T.B. and E.v.E. wrote the paper.

Author information

Authors and Affiliations

  1. Aquatic Chemical Ecology, Zoological Institute, University of Köln, Zülpicher Str. 47b, 50674, Cologne, Germany

    Tomasz Brzeziński & Eric von Elert

Authors
  1. Tomasz Brzeziński
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eric von Elert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tomasz Brzeziński.

Ethics declarations

Ethical approval

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

Additional information

Communicated by Maarten Boersma.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 117 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brzeziński, T., von Elert, E. Predator evasion in zooplankton is suppressed by polyunsaturated fatty acid limitation. Oecologia 179, 687–697 (2015). https://doi.org/10.1007/s00442-015-3405-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3405-4

Keywords

Search

Navigation