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Behavioural interseasonal adaptations in Daphnia pulicaria (Crustacea: Cladocera) as induced by predation infochemicals

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Abstract

A wide range of chemical signals have been demonstrated to affect the swimming behaviour of Daphnia, including molecules associated with predation threat. In this contribution, we investigate how the concomitant presence of kairomones from the predaceous fish Lepomis macrochirus and alarm pheromones from crushed conspecifics affect the small-scale swimming behaviour of Daphnia pulicaria. In particular, we studied both the light/dark and summer/winter variations in the swimming motion of the cladoceran in the presence and absence of these infochemicals, and related them to the limnology of the environment. At summertime temperature, in the presence of light and infochemicals D. pulicaria confined its motion to the first few centimetres of the observation vessel, expressing positive phototaxis. In all other conditions, instead, no significant difference in the time spent in the upper and lower parts of the chamber was recorded. The upward displacement of D. pulicaria recorded in our experiments deviates from the most traditionally accepted downward migration used to move into darker layers to avoid visual predation. Our results highlight additional behavioural mechanisms that might be efficiently exploited by D. pulicaria to contrast predation by L. macrochirus.

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References

  • Bernot RJ, Dodds WK, Quist MC, Guy CS (2006) Temperature and kairomone induced life history plasticity in coexisting Daphnia. Aquat Ecol 40:361–372. doi:10.1007/s10452-006-9035-5

    Article  Google Scholar 

  • Brewer MC, Coughlin JN (1996) Virtual plankton: a novel approach to the investigation of aquatic predator-prey interactions. In: Lenz PH, Hartline DK, Purcell JE, Macmillan DL (eds) Zooplankton: sensory ecology and physiology. Gordon and Breach, Amsterdam, pp 425–434

    Google Scholar 

  • Brönmark C, Hansson L-A (2005) The biology of lakes and ponds. Oxford University Press, Oxford

    Google Scholar 

  • Burks RL, Lodge DM, Jeppesen E, Lauridsen TL (2002) Diel horizontal migration of zooplankton: costs and benefits of inhabiting the littoral. Freshw Biol 47:343–365

    Article  Google Scholar 

  • Cabin RJ, Mitchell RJ (2000) To Bonferroni or not to Bonferroni: when and how are the questions. Bull Ecol Soc Am 81:246–248

    Google Scholar 

  • Castiglione P, Cencini M, Vulpiani A, Zambianchi E (1999) Transport in finite size systems: an exit time approach. Chaos 9:871–879

    Article  PubMed  Google Scholar 

  • Cerbin S, Kraak MHS, de Voogt P, Visser PM, Van Donk E (2010) Combined and single effects of pesticide carbaryl and toxic Microcystis aeruginosa on the life history of Daphnia pulicaria. Hydrobiologia 643:129–138

    Article  CAS  Google Scholar 

  • Coker RE (1939) The problem of cyclomorphosis in Daphnia. Q Rev Biol 14:137–148

    Article  Google Scholar 

  • Cole BJ (1995) Fractal time in animal behaviour: the movement activity of Drosophila. Anim Behav 50:1317–1324

    Article  Google Scholar 

  • de Bernardi R, Peters RH (1987) Why Daphnia? In: Peters RH, de Bernardi R (eds) Daphnia. Memorie dell’Istituto italiano di idrobiologia dott. Marco de Marchi, vol 45. Consiglio Nazionale delle Ricerche, Verbania-Pallanza, pp 353–366

    Google Scholar 

  • Dicke M, Sabelis MW (1988) Infochemical terminology: Based on cost-benefit analysis rather than origin of compounds? Funct Ecol 2:131–139

    Article  Google Scholar 

  • Dodson SI (1989) Predator-induced reaction norms. Bioscience 39:447–452

    Article  Google Scholar 

  • Dodson SI, Hanazato T (1995) Commentary on effects of anthropogenic and natural organic chemicals on development, swimming behavior, and reproduction of Daphnia, a key member of aquatic ecosystems. Environ Health Perspect 103:7–11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dodson SI, Hanazato T, Gorski PR (1995) Behavioral responses of Daphnia pulex exposed to carbaryl and Chaoborus kairomone. Environ Toxicol Chem 14:43–50

    Article  CAS  Google Scholar 

  • Dodson SI, Ryan S, Tollrien R, Lampert W (1997) Individual swimming behavior of Daphnia: effects of food, light and container size in four clones. J Plankton Res 19:1537–1552

    Article  Google Scholar 

  • Dzialowski AR, Lennon JT, O’Brien WJ, Smith VH (2003) Predator-induced phenotypic plasticity in the exotic cladoceran Daphnia lumholtzi. Freshw Biol 48:1593–1602. doi:10.1046/j.1365-2427.2003.01111.x

    Article  Google Scholar 

  • Ellerby DJ, Gerry SP (2011) Sympatric divergence and performance trade-offs of bluegill ecomorphs. Evol Ecol 38:422–433. doi:10.1007/s11692-011-9130-y

    Google Scholar 

  • Gerry SP, Vogelzang M, Ascher JM, Ellerby DJ (2013) Variation in the diet and feeding morphology of polyphenic Lepomis macrochirus. J Fish Biol 82:338–346. doi:10.1111/j.1095-8649.2012.03471.x

    Article  CAS  PubMed  Google Scholar 

  • Hansson L-A, Hylander S (2009) Effects of ultraviolet radiation on pigmentation, photoenzymatic repair, behavior, and community ecology of zooplankton. Photochem Photobiol Sci 8:1266–1275. doi:10.1039/b908825c

    Article  CAS  PubMed  Google Scholar 

  • Hansson L-A, Hylander S, Sommaruga R (2007) Escape from UV threats in zooplankton: a cocktail of behavior and protective pigmentation. Ecology 88:1932–1939

    Article  PubMed  Google Scholar 

  • Hebert PDN (1977) Niche overlap among species in the Daphnia carinata complex. J Anim Ecol 46:399–409

    Article  Google Scholar 

  • Hembre LK, Peterson LA (2012) Evolution of predator avoidance in a Daphnia population: evidence from the egg bank. Hydrobiologia 700:245–255. doi:10.1007/s10750-012-1234-6

    Article  Google Scholar 

  • Ingle D (1968) Spatial dimension of vision in fish. In: Ingle D (ed) The central nervous system and fish behavior. University of Chicago Press, Chicago, pp 51–94

    Google Scholar 

  • Jensen KH, Jakobsen PJ, Kleiven OT (1998) Fish kairomone regulation of internal swarm structure in Daphnia pulex (Cladocera: Crustacea). Hydrobiologia 368:123–127

    Article  Google Scholar 

  • Lammens EHRR, Boesewinkel-De Bruyn N, Hoogveld H, Van Donk E (1992) P-load, phytoplankton, zooplankton and fish stock in Loosdrecht Lake and Tjeukemeer: confounding effects of predation and food availability. Hydrobiologia 233:87–94. doi:10.1007/bf00016098

    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, Wolf HG (1986) Cyclomorphosis in Daphnia cucullata: morphometric and population genetic analyses. J Plankton Res 8:289–303

    Article  Google Scholar 

  • Larsson P, Lampert W (2012) Finding the optimal vertical distribution: behavioural responses of Daphnia pulicaria to gradients of environmental factors and the presence of fish. Freshw Biol 57:2514–2525

    Article  Google Scholar 

  • Lass S, Spaak P (2003) Chemically induced anti-predator defences in plankton: a review. Hydrobiologia 491:221–239

    Article  Google Scholar 

  • Lass S, Boersma M, Spaak P (2000) How do migrating daphnids cope with fish predation risk in the epilimnion under anoxic conditions in the hypolimnion? J Plankton Res 22:1411–1418

    Article  Google Scholar 

  • LTER NTL (1982) North Temperate Lakes LTER: Ice Duration—Trour Lake Area 1981—current. Center for Limnology; NTL LTER; Long Term Ecological Research Network. doi:10.6073/pasta/0afed3aec6e5638b05d7f99136fe88dd

  • LTER NTL (2012a) North Temperate Lakes LTER: Physical Limnology of Primary Study Lakes 1981—current. Center for Limnology; NTL LTER; Long Term Ecological Research Network. doi:10.6073/pasta/ad7bc75f05a723cd539824700b81641d

  • LTER NTL (2012b) North Temperate Lakes LTER: Secchi Disk Depth; Other Auxiliary Base Crew Sample Data 1981—current. Center for Limnology; NTL LTER; Long Term Ecological Research Network. doi:10.6073/pasta/81349f1e48cc3dd669c52ce5192a8b70

  • Mandelbrot BB (1967) How long is the coast of Britain? Statistical self-similarity and fractional dimension. Science 156:636–638

    Article  CAS  PubMed  Google Scholar 

  • McGill R, Tukey JW, Larsen WA (1978) Variations of box plots. Am Stat 32:12–16

    Google Scholar 

  • Meerhoff M, Fosalba C, Bruzzone C, Mazzeo N, Noordoven W, Jeppesen E (2006) An experimental study of habitat choice by Daphnia: plants signal danger more than refuge in subtropical lakes. Freshw Biol 51:1320–1330

    Article  Google Scholar 

  • Miner JG, Stein RA (1993) Interactive influence of turbidity and light on larval bluegill (Lepomis macrochirus) foraging. Can J Fish Aquat Sci 50:781–788. doi:10.1139/f93-090

    Article  Google Scholar 

  • Mittelbach GG (1984) Predation and resource partitioning in two sunfishes (Centrarchidae). Ecology 65:499–513

    Article  Google Scholar 

  • Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405

    Article  Google Scholar 

  • Nakagawa S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15:1044–1045. doi:10.1093/beheco/arh107

    Article  Google Scholar 

  • Nihongi A, Ziarek J, Nagai T, Uttieri M, Zambianchi E, Strickler JR (2011) Daphnia pulicaria hijacked by Vibrio cholerae: altered swimming behaviour and predation risk implications. In: Kattel G (ed) Zooplankton and phytoplankton: types, characteristics and ecology. Nova Science Publishers Inc, New York, pp 181–192

    Google Scholar 

  • Ohman MD, Frost BW, Cohen EB (1983) Reverse diel vertical migration: an escape from invertebrate predators. Science 220:1404–1407

    Article  CAS  PubMed  Google Scholar 

  • O’Keefe TC, Brewer MC, Dodson SI (1998) Swimming behavior of Daphnia: its role in determining predation risk. J Plankton Res 20:973–984

    Article  Google Scholar 

  • Oram E, Spitze K (2013) Depth selection by Daphnia pulex in response to Chaoborus kairomone. Freshw Biol 58:409–415

    Article  Google Scholar 

  • Pestana JLT, Baird DJ, Soares AMVM (2013) Predator threat assessment in Daphnia magna: the role of kairomones versus conspecific alarm cues. Mar Fresh Res 64:679–686. doi:10.1071/mf13043

    Article  Google Scholar 

  • Pietrzak B, Pijanowska J, Dawidowicz P (in press) The effect of temperature and kairomone on Daphnia escape ability: a simple bioassay. Hydrobiologia. doi:10.1007/s10750-015-2539-z

  • Pijanowska J (1997) Alarm signals in Daphnia? Oecologia 112:12–16. doi:10.1007/s004420050277

    Article  Google Scholar 

  • Pijanowska J, Kloc M (2004) Daphnia response to predation threat involves heat-shock proteins and the actin and tubulin cytoskeleton. Genesis 38:81–86. doi:10.1002/gene.20000

    Article  CAS  PubMed  Google Scholar 

  • Pijanowska J, Kowalczewski A (1997) Predators can induce swarming behaviour and locomotory responses in Daphnia. Freshw Biol 37:649–656. doi:10.1046/j.1365-2427.1997.00192.x

    Article  Google Scholar 

  • Ringelberg J, Van Gool E (1998) Do bacteria, not fish, produce ‘fish kairomone’? J Plankton Res 20:1847–1852

    Article  Google Scholar 

  • Ryan S, Dodson SI (1998) Seasonal analysis of Daphnia pulicaria swimming behavior. Hydrobiologia 384:111–118

    Article  Google Scholar 

  • Sakwińska O (1998) Plasticity of Daphnia magna life history traits in response to temperature and information about a predator. Freshw Biol 39:681–687

    Article  Google Scholar 

  • Schwarzenberger A, Courts C, von Elert E (2009) Target gene approaches: gene expression in Daphnia magna exposed to predator-borne kairomones or to microcystin-producing and microcystin-free Microcystis aeruginosa. BMC Genom 10:527. doi:10.1186/1471-2164-10-527

    Article  CAS  Google Scholar 

  • Seuront L, Brewer MC, Strickler JR (2004a) Quantifying zooplankton swimming behavior: the question of scale. In: Seuront L, Strutton PG (eds) Handbook of scaling methods in aquatic ecology—measurements, analysis, simulation. CRC Press, Boca Raton, pp 333–359

    Google Scholar 

  • Seuront L, Yamazaki H, Souissi S (2004b) Hydrodynamic disturbance and zooplankton swimming behaviour. Zool Stud 43:376–387

    Google Scholar 

  • Slusarczyk M, Ochocka A, Biecek P (2013) Prevalence of kairomone-induced diapause in Daphnia magna from habitats with and without fish. Hydrobiologia 715:225–232. doi:10.1007/s10750-013-1552-3

    Article  Google Scholar 

  • Smith KC, Macagno ER (1990) UV photoreceptors in the compound eye of Daphnia magna (Crustacea, Branchiopoda). A fourth spectral class in single ommatidia. J Comp Physiol A 166:597–606

    Article  CAS  PubMed  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W. H Freeman and Company, New York

    Google Scholar 

  • Sokal RR, Rohlf FJ (2009) Introduction to biostatistics, 2nd edn. Dover Publications, Mineola, New York

    Google Scholar 

  • Sommer U, Gliwicz ZM, Lampert W, Duncan A (1986) The PEG-model of seasonal succession of planktonic events in fresh waters. Arch Hydrobiol 106:433–471

    Google Scholar 

  • Spaak P, Boersma M (1997) Tail spine length in the Daphnia galeata complex: costs and benefits of induction by fish. Aquat Ecol 31:89–98. doi:10.1023/A:1009935100804

    Article  Google Scholar 

  • Stirling G (1995) Daphnia behaviour as a bioassay of fish presence of predation. Funct Ecol 9:778–784. doi:10.2307/2390252

    Article  Google Scholar 

  • Swaffar SM, O’Brien WJ (1996) Spines of Daphnia lumholtzi create feeding difficulties for juvenile bluegill sunfish (Lepomis macrochirus). J Plankton Res 18:1055–1061

    Article  Google Scholar 

  • Szulkin M, Dawidowicz P, Dodson SI (2006) Behavioural uniformity as a response to cues of predation risk. Anim Behav 71:1013–1019

    Article  Google Scholar 

  • Tavşanoğlu ÜN, Çakiroğlu AI, Erdoğan Ş, Meerhoff M, Jeppesen E, Beklioglu M (2012) Sediments, not plants, offer the preferred refuge for Daphnia against fish predation in Mediterranean shallow lakes: an experimental demonstration. Freshw Biol 57:795–802

    Article  Google Scholar 

  • Tiselius P, Hansen B, Jonsson P, Kiørboe T, Nielsen TG, Piontkovski S, Saiz E (1995) Can we use laboratory-reared copepods for experiments? A comparison of feeding behaviour and reproduction between a field and a laboratory population of Acartia tonsa. ICES J Mar Sci 52:369–376

    Article  Google Scholar 

  • Tucker AJ, Williamson CE, Rose KC, Oris JT, Connelly SJ, Olson MH, Mitchell DL (2010) Ultraviolet radiation affects invasibility of lake ecosystems by warm-water fish. Ecology 91:882–890. doi:10.1890/09-0554.1

    Article  PubMed  Google Scholar 

  • Tukey JW (1977) Exploratory data analysis. Addison-Wesley, Reading

    Google Scholar 

  • Uttieri M, Zambianchi E (2012) On the fractal characterisation of zooplankton motion: applications and perspectives. In: Mitchell EW, Murray SR (eds) Classification and application of fractals: new research. Nova Science Publishers Inc, New York, pp 113–129

    Google Scholar 

  • Uttieri M, Mazzocchi MG, Nihongi A, Ribera d’Alcalà M, Strickler JR, Zambianchi E (2004) Lagrangian description of zooplankton swimming trajectories. J Plankton Res 26:99–105. doi:10.1093/plankt/fbg116

    Article  Google Scholar 

  • Uttieri M, Zambianchi E, Strickler JR, Mazzocchi MG (2005) Fractal characterization of three-dimensional zooplankton swimming trajectories. Ecol Model 185:51–63

    Article  Google Scholar 

  • Uttieri M, Cianelli D, Zambianchi E (2013) Behaviour-dependent predation risk in swimming zooplankters. Zool Stud 52:32. doi:10.1186/1810-522X-52-32

    Article  Google Scholar 

  • Uttieri M, Sandulli R, Spezie G, Zambianchi E (2014) From small to large scale: a review of the swimming behaviour of Daphnia. In: El-Doma M (ed) Daphnia: Biology and mathematics perspectives. Nova Science Publishers Inc, New York, pp 309–322

    Google Scholar 

  • Van Gool E, Ringelberg J (1995) Swimming of Daphnia galeata × hyalina in response to changing light intensities: influence of food availability and predator kairomone. Mar Fresh Behav Physiol 26:259–265

    Article  Google Scholar 

  • Van Gool E, Ringelberg J (1997) The effect of accelerations in light increase on the phototactic downward swimming of Daphnia and the relevance to diel vertical migration. J Plankton Res 19:2041–2050

    Article  Google Scholar 

  • Van Gool E, Ringelberg J (1998) Light-induced migration behaviour of Daphnia modified by food and predator kairomones. Anim Behav 56:741–747

    Article  Google Scholar 

  • Van Gool E, Ringelberg J (2002) Relationship between fish kairomone concentration in a lake and phototactic swimming by Daphnia. J Plankton Res 27:713–721

    Article  Google Scholar 

  • Van Gool E, Ringelberg J (2003) What goes down must come up: symmetry in light-induced migration behaviour of Daphnia. Hydrobiologia 491:301–307

    Article  Google Scholar 

  • Vinyard GL, O’Brien WJ (1976) Effects of light and turbidity on the reactive distance of bluegill (Lepomis macrochirus). Can J Fish Aquat Sci 33:2845–2849. doi:10.1139/f76-342

    Google Scholar 

  • von Frisch K (1942) Über einen Schreckstoff der Fischhaut und seine biologische Bedeutung. Z Vergl Physiol 29:46–145. doi:10.1007/bf00304445

    Article  Google Scholar 

  • Weber A, Van Noordwijk A (2002) Swimming behaviour of Daphnia clones: differentiation through predator infochemicals. J Plankton Res 24:1335–1348

    Article  CAS  Google Scholar 

  • Weiss L, Laforsch C, Tollrian R (2012) The taste of predation and the defences of prey. In: Brönmark C, Hansson L-A (eds) Chemical ecology in aquatic systems. Oxford University Press, Oxford, pp 111–126

    Chapter  Google Scholar 

  • Weiss LC, Leimann J, Tollrian R (2015) Predator-induced defences in Daphnia longicephala: location of kairomone receptors and timeline of sensitive phases to trait formation. J Exp Biol 218:2918–2926. doi:10.1242/jeb.124552

    Article  PubMed  PubMed Central  Google Scholar 

  • Williamson CE, Hargreaves BR, Orr PS, Lovera PA (1999) Does UV play a role in changes in predation and zooplankton community structure in acidified lakes? Limnol Oceanogr 44:774–783

    Article  CAS  Google Scholar 

  • Wojtal-Frankiewicz A, Frankiewicz P, Jurczak T, Grennan J, McCarthy TK (2010) Comparison of fish and phantom midge influence on cladocerans diel vertical migration in a dual basin lake. Aquat Ecol 44:243–254. doi:10.1007/s10452-009-9280-5

    Article  CAS  Google Scholar 

  • Wright SP (1992) Adjusted P-values for simultaneous inference. Biometrics 48:1005–1013

    Article  Google Scholar 

  • Ziarek JJ, Nihongi A, Nagai T, Uttieri M, Strickler JR (2011) Seasonal adaptations of Daphnia pulicaria swimming behaviour: the effect of water temperature. Hydrobiologia 661:317–327. doi:10.1007/s10750-010-0540-0

    Article  Google Scholar 

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Acknowledgments

The research of M. U. was supported by the MOKA project (Modelling and Observation of zooplanKtonic orgAnisms; ID: RBFR10VF6M) financed by the Italian Ministry of Education, University and Research. The authors gratefully acknowledge the use of the following data sets: Physical Limnology of the North Temperate Lakes Primary Study—Secchi disk depth—Ice duration, North Temperate Lakes Long Term Ecological Research programme (http://lter.limnology.wisc.edu), NSF, Emily Stanley and Aaron Stephenson, Center for Limnology, University of Wisconsin-Madison. The authors are thankful to two anonymous Reviewers for stimulating comments on a previous version of the manuscript, and T. Nagai for useful discussion. The generous donation of the VidAna software by M. Hofmann (University of Bonn) is acknowledged. M.U. wishes to single out P. Licandro for support in statistical analysis, and M. Pottek for the realisation of the MOKA cartoon.

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Authors and Affiliations

  1. School of Freshwater Sciences, University of Wisconsin-Milwaukee, 600 E. Greenfield Avenue, Milwaukee, WI, 53204, USA

    Ai Nihongi & J. Rudi Strickler

  2. Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, 240 Longwood Avenue, Boston, MA, 02115, USA

    Joshua J. Ziarek

  3. Department of Science and Technology, University of Naples “Parthenope”, Centro Direzionale di Napoli – Isola C4, 80143, Naples, Italy

    Marco Uttieri, Roberto Sandulli & Enrico Zambianchi

  4. CoNISMa, Piazzale Flaminio 9, 00196, Rome, Italy

    Marco Uttieri & Enrico Zambianchi

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  1. Ai Nihongi
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Correspondence to Marco Uttieri.

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Nihongi, A., Ziarek, J.J., Uttieri, M. et al. Behavioural interseasonal adaptations in Daphnia pulicaria (Crustacea: Cladocera) as induced by predation infochemicals. Aquat Ecol 50, 667–684 (2016). https://doi.org/10.1007/s10452-016-9585-0

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