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Cercopagis pengoi and Mysis spp. alter their feeding rate and prey selection under predation risk of herring (Clupea harengus membras)

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Abstract

The anti-predator behaviour of Baltic crustacean planktivores was studied in feeding experiments under predation pressure of herring. The experiments were conducted with pelagic mysids: Mysis mixta and Mysis relicta, and with Cercopagis pengoi, a non-indigenous cladoceran, which invaded the Baltic Sea in 1992. Zooplankton was offered as prey. Two kinds of experiments were performed in the absence and presence of chemical predator cues: (1) two-prey experiments with prey, which have poor or good escape responses and all three planktivores and (2) natural prey experiments with mysids in natural zooplankton assemblages. The results showed that all three species reacted to the chemical cue of herring by decreasing their feeding rate and altering prey selection. C. pengoi selected easily captured prey (rotifers) in two-prey experiments under predation risk while selection for any prey was evident in mysids in natural prey experiments only in the absence of predator cues. This indicates that planktivores have different anti-predator strategies, which are modified by their own prey capture abilities. C. pengoi was a very efficient predator on small prey with size-specific prey consumption rate 5 to 18 times the rate of mysids. Results show that the studied planktivores are capable of adjusting their feeding behaviour to decrease their conspicuousness in order to increase survival under predation risk. Further, results support the view that C. pengoi has adapted well to the Baltic ecosystem, sharing food niche with pelagic mysids and most probably having a strong influence on the whole pelagic food web.

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References

  • Aneer G (1980) Estimates of feeding pressure on pelagic and benthic organisms by Baltic herring (Clupea harengus v. membras L.). Ophelia 1:265–275

    Google Scholar 

  • Antsulevich A, Välipakka P (2000) Cercopagis pengoi—new important food object of the Baltic herring in the Gulf of Finland. Int Rev Hydrobiol 85:609–619

    Article  Google Scholar 

  • Bielecka L, Zmijewska MI, Szymborska A (2000) A new predatory cladoceran Cercopagis (Cercopagis) pengoi (Ostroumov 1891) in the Gulf of Gdansk. Oceanologia 42:371–374

    Google Scholar 

  • Branstrator D (1995) Ecological interactions between Bythotrephes cederstroemi and Leptodora kindtii and the implications for species replacement in Lake Michigan. J Great Lakes Res 21:670–679

    Google Scholar 

  • Brönmark C, Hansson L-A (2000) Chemical communication in aquatic systems: an introduction. Oikos 88:103–109

    Article  Google Scholar 

  • Browman HI, Kruse S, O’Brien WJ (1989) Foraging behavior of the predaceous cladoceran, Leptodora kindtii, and escape responses of their prey. J Plankton Res 11:1075–1088

    Google Scholar 

  • Bushnoe TM, Warner DM, Rudstam LG, Mills EL (2003) Cercopagis pengoi as a new prey item for alewife (Alosa pseudoharengus) and rainbow smelt (Osmerus mordax) in Lake Ontario. J Great Lakes Res 29:205–212

    Google Scholar 

  • Cooper SD, Goldman CR (1980) Opossum shrimp (Mysis relicta) predation on zooplankton. Can J Fish Aquat Sci 37:909–919

    Google Scholar 

  • Cristescu MEA, Hebert PDN (2002) Phylogeny and adaptive radiation in the Onychopoda (Crustacea, Cladocera): evidence from multiple gene sequences. J Evol Biol 15:838–849

    Article  CAS  Google Scholar 

  • Diehl S (1988) Foraging efficiency of three freshwater fishes: effects of structural complexity and light. Oikos 53:207–214

    Google Scholar 

  • Drenner RW, Strickler JR, O’Brien WJ (1978) Capture probability: the role of zooplankter escape in the selective feeding of planktivorous fish. J Fish Res Bd Can 35:1370–1373

    Google Scholar 

  • Eggers DM (1977) The nature of prey selection by planktivorous fish. Ecology 58:46–59

    Article  Google Scholar 

  • Eklöv P, Diehl S (1994) Piscivore efficiency and refuging prey: the importance of predator search mode. Oecologia 98:344–353

    Article  Google Scholar 

  • Flinkman J, Vuorinen I, Aro E (1992) Planktivorous Baltic herring (Clupea harengus) prey selectively on reproducing copepods and cladocerans. Can J Fish Aquat Sci 49:73–77

    Google Scholar 

  • Flinkman J, Aro E, Vuorinen I, Viitasalo M (1998) Changes in northern Baltic zooplankton and herring nutrition from 1980s to 1990s: top–down and bottom–up processes at work. Mar Ecol Prog Ser 65:127–136

    Google Scholar 

  • Gerritsen J (1984) Size efficiency reconsidered: a general foraging model for free-swimming aquatic animals. Am Nat 123:450–467

    Article  Google Scholar 

  • Gerritsen J, Strickler JR (1977) Encounter probabilities and community structure in zooplankton: a mathematical model. J Fish Res Bd Can 34:73–82

    Google Scholar 

  • Gismervik I, Andersen T (1997) Prey switching by Acartia clausi: experimental evidence and implications of intraguild predation assessed by a model. Mar Ecol Prog Ser 157:247–259

    Google Scholar 

  • Greene CG (1986) Patterns of prey selection: implications of predator foraging tactics. Am Nat 128:824–839

    Article  Google Scholar 

  • Gorokhova E, Aladin N, Dumont HJ (2000) Further expansion of the genus Cercopagis (Crustacea, Branchiopoda, Onychopoda) in the Baltic Sea, with notes on the taxa present and their ecology. Hydrobiol 429:207–218

    Article  Google Scholar 

  • Gorokhova E, Fagerberg T, Hansson S (2004) Predation by herring (Clupea harengus) and sprat (Sprattus sprattus) on Cercopagis pengoi in a western Baltic Sea bay. ICES J Mar Sci 61:959–965

    Article  Google Scholar 

  • Gorokhova E, Hansson S, Höglander H, Andersen CM (2005) Stable isotopes show food web changes after invasion by the predatory cladoceran Cercopagis pengoi in a Baltic Sea bay. Oecologia 143:251–259

    Article  PubMed  Google Scholar 

  • Hamrén U, Hansson S (1999) A mysid shrimp (Mysis mixta) is able to detect the odour of its predator (Clupea harengus). Ophelia 51:187–191

    Google Scholar 

  • Hansson S, De Stasio BT, Gorokhova E, Mohammadian MA (2001) Ratio-dependent functional responses—tests with the zooplanktivore Mysis mxta. Mar Ecol Prog Ser 216:181–189

    Google Scholar 

  • Hirvonen H, Ranta E, Piironen J, Laurila A, Peuhkuri N (2000) Behavioural responses of naive Arctic charr young to chemical cues from salmonid and non-salmonid fish. Oikos 88:191–199

    Article  Google Scholar 

  • Hughes RN (1980) Optimal foraging theory in the marine context. Oceanogr Mar Biol Annu Rev 18:423–481

    Google Scholar 

  • Koski M, Viitasalo M, Kuosa H (1999) Seasonal development of mesozooplankton biomass and production on the SW coast of Finland. Ophelia 50:69–91

    Google Scholar 

  • Kotta J, Simm M, Kotta I, Kanošina I, Kallaste K, Raid T (2004) Factors controlling long-term changes of the eutrophicated ecosystem of Pärnu bay, Gulf of Riga. Hydrobiol 514:259–268

    Article  Google Scholar 

  • Krylov P, Panov V (1998) Resting eggs in the life cycle of Cercopagis pengoi, a recent invader of the Baltic Sea. Arch Hydrobiol Spec Issues Adv Limnol 52:383–392

    Google Scholar 

  • Krylov PI, Bychenkov DE, Panov VE, Rodionova NV, Telesh IV (1999) Distribution and seasonal dynamics of the Ponto-Caspian invader, Cercopagis pengoi (Crustacea, Cladocera) in the Neva Estuary (Gulf of Finland). Hydrobiol 393:227–232

    Article  Google Scholar 

  • Landry MR (1981) Switching between herbivory and carnivory by the planktonic marine copepod Calanus pacificus. Mar Biol 65:77–82

    Article  Google Scholar 

  • Laxson CL, McPhedran KN, Makarewicz JC, Telesh IV, MacIsaac HJ (2003) Effects of the non-indigenous cladoceran Cercopagis pengoi on the lower food web of Lake Ontario. Freshwat Biol 48:2094–2106

    Article  CAS  Google Scholar 

  • Lehman JT, Cáceres CE (1993) Food-web responses to species invasion by a predatory invertebrate: Bythotrephes in Lake Michigan. Limnol Oceanogr 38:879–891

    Article  Google Scholar 

  • Leppäkoski E, Olenin S (2000) Non-native species and rates of spread: lessons from the Brackish Baltic Sea. Biol Invasions 2:151–163

    Article  Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  • Lindén E, Lehtiniemi M, Viitasalo M (2003) Predator avoidance behaviour of Baltic littoral mysids Neomysis integer and Praunus flexuosus. Mar Biol 143:845–850

    Article  Google Scholar 

  • MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:603–609

    Article  Google Scholar 

  • Merilaita S (2001) Habitat heterogeneity, predation and gene flow: colour polymorphism in the isopod, Idotea baltica. Evol Ecol 15:103–116

    Article  Google Scholar 

  • Mohammadian MA, Hansson S, De Stasio BT (1997) Are marine planktonic invertebrates food limited? The functional response of Mysis mixta (Crustacea, Mysidacea) in the Baltic Sea. Mar Ecol Prog Ser 150:113–119

    Google Scholar 

  • Möllmann C, Kornilovs G, Fetter M, Köster FW (2004): Feeding ecology of central Baltic Sea herring and sprat. J Fish Biol 65:1563–1581

    Article  Google Scholar 

  • Mordukhai-Boltovskoi PhD, Rivier IK (1971) A brief survey of the ecology and biology of the Caspian Polyphemoidea. Mar Biol 8:160–169

    Article  Google Scholar 

  • Murtaugh PA (1981) Size-selective predation on Daphnia by Neomysis mercedis. Ecology 62:894–900

    Article  Google Scholar 

  • O’Brien WJ (1986) Planktivory by freshwater fish: thrust and parry in the pelagia. In: Kerfoot WC, Sih A (eds) Predation. Direct and indirect impacts on aquatic communities. University press of New England, Hanover, pp 3–16

    Google Scholar 

  • Ojaveer H, Lumberg A (1995) On the role of Cercopagis (Cercopagis) pengoi (Ostroumov) in Pärnu Bay and the NE part of the Gulf of Riga ecosystem. Proc Estonian Acad Sci Ecol 5:20–25

    Google Scholar 

  • Ojaveer H, Simm H, Lankov I (2004) Population dynamics and ecological impact of the non-indigenous Cercopagis pengoi in the Gulf of Riga (Baltic Sea). Hydrobiol 522:261–269

    Article  Google Scholar 

  • Pastorok RA (1981) Prey vulnerability and size selection by Chaoborus larvae. Ecology 62:1311–1324

    Article  Google Scholar 

  • Pearre S (1982) Estimating prey preference by predators: uses of various indices, and a proposal of another based on χ2. Can J Fish Aquat Sci 39:914–923

    Google Scholar 

  • Peltonen H, Vinni M, Lappalainen A, Pönni J (2004) Spatial distribution patterns of herring (Clupea harengus L.), sprat (Sprattus sprattus L.) and the three-spined stickleback (Gasterosteus aculeatus L.) in the Gulf of Finland, Baltic Sea. ICES J Mar Sci 61:966–971

    Article  Google Scholar 

  • Persson L (1991) Behavioural response to predators reverses the outcome of competition between prey species. Behav Ecol Sociobiol 28:101–105

    Article  Google Scholar 

  • Pertola S, Koski M, Viitasalo M (2002) Stoichiometry of mesozooplankton in N- and P-limited areas of the Baltic Sea. Mar Biol 140:425–434

    Article  Google Scholar 

  • Rudstam LG, Hansson S (1990) On the ecology of Mysis mixta (Crustacea, Mysidacea) in a coastal area of the northern Baltic proper. Ann Zool Fenn 27:259–263

    Google Scholar 

  • Rudstam LG, Danielsson K, Hansson S, Johansson S (1989) Diel vertical migration and feeding patterns of Mysis mixta (Crustacea, Mysidacea) in the Baltic Sea. Mar Biol 101:43–52

    Article  Google Scholar 

  • Rudstam LG, Hansson S, Johansson S, Larsson U (1992) Dynamics of planktivory in a coastal area of the northern Baltic Sea. Mar Ecol Prog Ser 80:159–173

    Google Scholar 

  • Salemaa H, Vuorinen I, Välipakka P (1990) The distribution and abundance of Mysis populations in the Baltic Sea. Ann Zool Fenn 27:253–257

    Google Scholar 

  • Savino JF, Stein RA (1989) Behavioural interactions between fish predators and their prey: effects of plant density. Anim Behav 37:311–321

    Article  Google Scholar 

  • Thetmeyer H, Kils U (1995) To see and not to be seen: the visibility of predator and prey with respect to feeding behaviour. Mar Ecol Prog Ser 126:1–8

    Google Scholar 

  • Thiel R (1996) The impact of fish predation on the zooplankton community in a southern Baltic bay. Limnologica 26:123–137

    Google Scholar 

  • Torgersen T (2003) Proximate causes for anti-predatory feeding suppression by zooplankton during the day: reduction of contrast or motion—ingestion or clearance? J Plankton Res 25:565–571

    Article  Google Scholar 

  • Uitto A, Gorokhova E, Välipakka P (1999) Distribution of the non-indigenous Cercopagis pengoi in the coastal waters of the eastern Gulf of Finland. ICES J Mar Science 56(Suppl):49–57

    Article  Google Scholar 

  • Viherluoto M, Viitasalo M (2001a) Effect of light on the feeding rates of pelagic and littoral mysid shrimps: a trade-off between feeding success and predation avoidance. J Exp Mar Biol Ecol 261:237–244

    Article  PubMed  Google Scholar 

  • Viherluoto M, Viitasalo M (2001b) Temporal variability in functional responses and prey selectivity of the pelagic mysid, Mysis mixta, in natural prey assemblages. Mar Biol 138:575–583

    Article  Google Scholar 

  • Viherluoto M, Kuosa H, Flinkman J, Viitasalo M (2000) Food utilisation of pelagic mysids, Mysis mixta and M. relicta, during their growing season in the northern Baltic Sea. Mar Biol 136:553–559

    Article  Google Scholar 

  • Viitasalo M, Rautio M (1998) Zooplanktivory by Praunus flexuosus (Crustacea: Mysidacea): functional responses and prey selection in relation to prey escape responses. Mar Ecol Prog Ser 174:77–87

    Google Scholar 

  • Viitasalo M, Vuorinen I, Saesmaa S (1995) Mesozooplankton dynamics in the northern Baltic Sea: implications of variations in hydrography and climate. J Plankton Res 17:1857–1878

    Google Scholar 

  • Viitasalo M, Kiørboe T, Flinkman J, Pedersen LW, Visser AW (1998) Predation vulnerability of planktonic copepods: consequences of predator foraging strategies and prey sensory abilities. Mar Ecol Prog Ser 175:129–145

    Google Scholar 

  • Viitasalo M, Flinkman J, Viherluoto M (2001) Zooplanktivory in the Baltic Sea: a comparison of prey selectivity by Clupea harengus and Mysis mixta, with reference to prey escape reactions. Mar Ecol Prog Ser 216:191–200

    Google Scholar 

  • Weldon PJ (1990) Responses by vertebrates to chemicals by predators. In: MacDonald DW, Muller-Schwartz D, Silverstein RM (eds) Chemical signals in vertebrates. Plenum Press, New York, pp 500–521

    Google Scholar 

  • Zaret TM, Suffern JS (1976) Vertical migration in zooplankton as a predator avoidance mechanism. Limnol Oceanogr 21:804–813

    Article  Google Scholar 

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Acknowledgements

We want to thank the crew of R/V Aranda for help in plankton sampling, E. Lahdes and S. Sopanen for guidance in C. pengoi handling and E. Gorokhova, L. Karjala, M. Karjalainen, E. Lahdes and two anonymous reviewers for fruitful comments on the manuscript. The study was financed by the Academy of Finland project # 203799 (ML) and Walter and Andrée de Nottbeck Foundation (EL).

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  1. Finnish Institute of Marine Research, P.O. Box 2, 00561, Helsinki, Finland

    Maiju Lehtiniemi & Eveliina Lindén

  2. Tvärminne Zoological Station, J. A. Palménin tie 260, 10900, Hanko, Finland

    Eveliina Lindén

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  1. Maiju Lehtiniemi
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  2. Eveliina Lindén
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Correspondence to Maiju Lehtiniemi.

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Communicated by M. Kühl, Helsingør

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Lehtiniemi, M., Lindén, E. Cercopagis pengoi and Mysis spp. alter their feeding rate and prey selection under predation risk of herring (Clupea harengus membras). Mar Biol 149, 845–854 (2006). https://doi.org/10.1007/s00227-006-0243-2

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