, Volume 20, Issue 1, pp 29–38 | Cite as

Spatial heterogeneity in induced defense of Brachionus calyciflorus within a single lake caused by a bed of floating-leaved macrophyte Trapa species

  • Yurie OtakeEmail author
  • Maiko Kagami
  • Takeo Kuriyama
  • Takehito Yoshida
Special Feature Ecological and limnological bases for management of overgrown macrophytes


While induced defense of aquatic organisms against predators has been considerably studied by both laboratory and field research, our understanding is still limited about, for example, whether induced defense is variable between microhabitats within the same lake and how multiple predators influence induced defense in the natural environment. Here, we examined whether a rotifer species, Brachionus calyciflorus showed a different development degree of induced defenses against its predator Asplanchna and cyclopoid copepods between the microhabitats of a macrophyte bed consisting of Trapa species and open water. B. calyciflorus was more abundant and had larger posterolateral spines as a defensive trait in open water than in the Trapa bed. Asplanchna was more abundant in open water than in the Trapa bed, whereas cyclopoids were more abundant in the Trapa bed. Both of the predators significantly affected the development of the defense trait. The effect of Asplanchna on the defense trait was positive, whereas the effect of cyclopoids was negative. Thus, a spatial difference in the development degree of induced defense between the microhabitats occurred as the dense Trapa bed influenced the abundance of the two predators. The results also suggest that the induced defense of B. calyciflorus was effective in reducing the predation pressure from Asplanchna while B. calyciflorus was not able to avoid predation by cyclopoids in the Trapa bed.


Induced defense Brachionus calyciflorus Asplanchna Cyclopoid copepods Floating-leaved macrophyte Predator–prey interaction 



We thank Toshio Furota, Ryohei Makino, and members of the Laboratory of Aquatic Ecology of Toho University for their assistance with field sampling. We thank Norio Hayashi, Jun Nishihiro, Takashi Yamanouchi, Gen Morimoto and Junji Konuma for their suggestions and comments on this study. We also thank two reviewers and the editor for their constructive comments. This study was supported by JSPS KAKENHI (25281052, 26291088) and River Foundation (23-1251-011).

Supplementary material

10201_2017_534_MOESM1_ESM.docx (65 kb)
Supplementary material 1 (DOCX 65 kb)


  1. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1–7. Accessed Sept 2015
  2. Bertani I, Leonardi S, Rossetti G (2013) Antipredator-induced trait changes in Brachionus and prey selectivity by Asplanchna in a large river under low-discharge conditions: evidence from a field study. Hydrobiologia 702:227–239CrossRefGoogle Scholar
  3. Black RW, Hairston NG (1983) Cyclomorphosis in Eubosmina longispina in a small North American pond. Hydrobiologia 102:61–67CrossRefGoogle Scholar
  4. Brandl Z (2005) Freshwater copepods and rotifers: predators and their prey. Hydrobiologia 546:475–489CrossRefGoogle Scholar
  5. Brönmark C, Lakowitz T, Hollander J (2011) Predator-induced morphological plasticity across local populations of a freshwater snail. PLoS One 6:e21773CrossRefGoogle Scholar
  6. Burks RL, Lodge DM, Jeppesen E, Lauridsen TL (2002) Diel horizontal migration of zooplankton: costs and benefits of inhabiting the littoral. Freshw Biol 47:343–365CrossRefGoogle Scholar
  7. Cardinale BJ, Brady VJ, Burton TM (1998) Changes in the abundance and diversity of coastal wetland fauna from the open water/macrophyte edge towards shore. Wetlands Ecol Manag 6:59–68CrossRefGoogle Scholar
  8. Chang KH, Hanazato T (2003a) Seasonal and reciprocal succession and cyclomorphosis of two Bosmina species (Cladocera, Crustacea) co-existing in a lake: their relationship with invertebrate predators. J Plankton Res 25:141–150CrossRefGoogle Scholar
  9. Chang KH, Hanazato T (2003b) Vulnerability of cladoceran species to predation by the copepod Mesocyclops leuckarti: laboratory observations on the behavioural interactions between predator and prey. Freshw Biol 48:476–484CrossRefGoogle Scholar
  10. Cyr H, Downing JA (1988) Empirical relationships of phytomacrofaunal abundance to plant biomass and macrophyte bed characteristics. Can J Fish Aquat Sci 45:976–984CrossRefGoogle Scholar
  11. Dahl J, Peckarsky BL (2002) Induced morphological defenses in the wild: predator effects on a mayfly, Drunella coloradensis. Ecology 83:1620–1634CrossRefGoogle Scholar
  12. Dahl J, Peckarsky BL (2003) Developmental responses to predation risk in morphologically defended mayflies. Oecologia 137:188–194CrossRefGoogle Scholar
  13. de Paggi SBJ, Muñoz S, Frau D, Paggi JC, Scarabotti P, Devercelli M, Meerhoff M (2012) Horizontal distribution of rotifers in a subtropical shallow lake (Paraná floodplain, Argentina). Fundam Appl Limnol Arch Hydrobiol 180:321–333CrossRefGoogle Scholar
  14. DeWitt TJ, Robinson BW, Wilson DS (2000) Functional diversity among predators of a freshwater snail imposes an adaptive trade-off for shell morphology. Evol Ecol Res 2:129–148Google Scholar
  15. Fairchild GW (1981) Movement and microdistribution of Sida crystallina and other littoral microcrustacea. Ecology 62:1341–1352CrossRefGoogle Scholar
  16. Fryer G (1957) The feeding mechanism of some freshwater cyclopoid copepods. J Zool 129:1–25Google Scholar
  17. Gilbert JJ (1966) Rotifer ecology and embryological induction. Science 151:1234–1237CrossRefGoogle Scholar
  18. Gilbert JJ (1967) Asplanchna and postero-lateral spine production in Brachionus calyciflorus. Arch Hydrobiol 64:1–62Google Scholar
  19. Gilbert JJ (1980) Further observations on developmental polymorphism and its evolution in the rotifer Brachionus calyciflorus. Freshw Biol 10:281–294CrossRefGoogle Scholar
  20. Gilbert JJ (2011) Induction of different defences by two enemies in the rotifer Keratella tropica: response priority and sensitivity to enemy density. Freshw Biol 56:926–938CrossRefGoogle Scholar
  21. Gilbert JJ (2013) The cost of predator-induced morphological defense in rotifers: experimental studies and synthesis. J Plankton Res 35:461–472CrossRefGoogle Scholar
  22. Gopheng M (1977) Food and feeding habits of Mesocyclops leuckarti (Claus) in Lake Kinneret (Israel). Freshw Biol 7:513–518CrossRefGoogle Scholar
  23. Grant JWG, Bayly IAE (1981) Predator induction of crests in morphs of the Daphnia carinata King complex. Limnol Oceanogr 26:201–218CrossRefGoogle Scholar
  24. Green J, Lan OB (1974) Asplanchna and the spines of Brachionus calyciflorus in two Javanese sewage ponds. Freshw Biol 4:223–226CrossRefGoogle Scholar
  25. Halbach U (1970) Die Ursachen der temporalvariation von Brachionus calyciflorus Pallas (Rotatoria). Oecologia 4:262–318CrossRefGoogle Scholar
  26. Hanazato T (1992) Population dynamics and cyclomorphosis of Bosmina longirostris in Lake Yunoko. Jpn J Limnol 53:13–25CrossRefGoogle Scholar
  27. Hanazato T, Arakawa T, Sakuma M, Chang KH, Okino T (2001) Zooplankton community in Lake Suwa: community structure and its role in the ecosystem (in Japanese with English abstract). Jpn J Limnol 62:151–167CrossRefGoogle Scholar
  28. Havel JE (1985) Cyclomorphosis of Daphnia pulex spined morphs. Limnol Oceanogr 30:853–861CrossRefGoogle Scholar
  29. Havel JE, Dodson SI (1984) Chaoborus predation on typical and spined morphs of Daphnia pulex: behavioral observations. Limnol Oceanogr 29:487–494CrossRefGoogle Scholar
  30. Havel JE, Dodson SI (1987) Reproductive costs of Chaoborus-induced polymorphism in Daphnia pulex. Hydrobiologia 150:273–281CrossRefGoogle Scholar
  31. Hebert PD, Grewe PM (1985) Chaoborus-induced shifts in the morphology of Daphnia ambigua. Limnol Oceanogr 30:1291–1297CrossRefGoogle Scholar
  32. Jamieson CD (1980) The predatory feeding of copepodid stages III to adult Mesocyclops leuckarti (Claus). In: Kerfoot WC (ed) Evolution and ecology of zooplankton communities. University Press of New England, Hanover, pp 518–533Google Scholar
  33. Kato Y, Nishihiro J, Yoshida T (2016) Floating-leaved macrophyte (Trapa japonica) drastically changes seasonal dynamics of a temperate lake ecosystem. Ecol Res 31:695–707CrossRefGoogle Scholar
  34. Kerfoot WC (1975) The divergence of adjacent populations. Ecology 56:1298–1313CrossRefGoogle Scholar
  35. Kerfoot WC (1977) Implications of copepod predation. Limnol Oceanogr 22:316–325CrossRefGoogle Scholar
  36. Kerfoot WC, Peterson C (1980) Predatory copepods and Bosmina: replacement cycles and further influences of predation upon prey reproduction. Ecology 61:417–431CrossRefGoogle Scholar
  37. Krueger DA, Dodson SI (1981) Embryological induction and predation ecology in Daphnia pulex. Limnol Oceanogr 26:219–223CrossRefGoogle Scholar
  38. Kuczyńska-Kippen N (2009) The spatial segregation of zooplankton communities with reference to land use and macrophytes in shallow Lake Wielkowiejskie (Poland). Int Rev Hydrobiol 94:267–281CrossRefGoogle Scholar
  39. Larsson P, Dodson SI (1993) Chemical communication in planktonic animals. Archiv Hydrobiol 129:129–155CrossRefGoogle Scholar
  40. Laurila A, Pakkasmaa S, Merilä J (2006) Population divergence in growth rate and antipredator defences in Rana arvalis. Oecologia 147:585–595CrossRefGoogle Scholar
  41. Lord H, Lagergren R, Svensson JE, Lundqvist N (2006) Sexual dimorphism in Bosmina: the role of morphology, drag, and swimming. Ecology 87:788–795CrossRefGoogle Scholar
  42. McQueen DJ (1969) Reduction of zooplankton standing stocks by predaceous Cyclops bicuspidatus thomasi in Marion Lake, British Columbia. J Fish Board Can 26:1605–1618CrossRefGoogle Scholar
  43. Meerhoff M, Iglesias C, De Mello FT, Clemente JM, Jensen E, Lauridsen TL, Jeppesen E (2007) Effects of habitat complexity on community structure and predator avoidance behaviour of littoral zooplankton in temperate versus subtropical shallow lakes. Freshw Biol 52:1009–1021CrossRefGoogle Scholar
  44. Parejko K, Dodson SI (1991) The evolutionary ecology of an antipredator reaction norm: Daphnia pulex and Chaoborus americanus. Evolution 45:1665–1674CrossRefGoogle Scholar
  45. Pasternak AF, Mikheev VN, Wanzenböck J (2006) How plankton copepods avoid fish predation: from individual responses to variations of the life cycle. J Ichthyol 46:S220–S226CrossRefGoogle Scholar
  46. Preißler K (1977) Do rotifers show “avoidance of the shore”? Oecologia 27:253–260CrossRefGoogle Scholar
  47. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed Sept 2015
  48. Relyea RA (2002) Local population differences in phenotypic plasticity: predator-induced changes in wood frog tadpoles. Ecol Monogr 72:77–93CrossRefGoogle Scholar
  49. Richter-Boix A, Llorente GA, Montori A (2007) A comparative study of predator-induced phenotype in tadpoles across a pond permanency gradient. Hydrobiologia 583:43–56CrossRefGoogle Scholar
  50. Sakamoto M (2012) Flexible response to environmental change: phenotypic plasticity (in Japanese). In: The ecological society of Japan (ed) Frontier of freshwater ecology. Kyoritsu Syuppan, Tokyo, pp 23–33Google Scholar
  51. Sakamoto M, Hanazato T (2008) Antennule shape and body size of Bosmina: key factors determining its vulnerability to predacious Copepoda. Limnology 9:27–34CrossRefGoogle Scholar
  52. Stemberger RS (1990) Food limitation, spination, and reproduction in Brachionus calyciflorus. Limnol Oceanogr 35:33–44CrossRefGoogle Scholar
  53. Strickler JR (1975) Intra- and interspecific information flow among planktonic copepods: receptors. Internationale Vereinigung fuer Theoretische und Angewandte Limnologie Verhandlungen 19:2951–2958Google Scholar
  54. Strickler JR, Bal AK (1973) Setae of the first antennae of the copepod Cyclops scutifer (Sars): their structure and importance. Proc Natl Acad Sci 70:2656–2659CrossRefGoogle Scholar
  55. Tatrai I, Herzig A (1995) Effect of habitat structure on the feeding efficiency of young stages of razor fish (Pelecus cultratus (L.)): an experimental approach. Hydrobiologia 299:75–81CrossRefGoogle Scholar
  56. Tollrian R (1993) Neckteeth formation in Daphnia pulex as an example of continuous phenotypic plasticity: morphological effects of Chaoborus kairomone concentration and their quantification. J Plankton Res 15:1309–1318CrossRefGoogle Scholar
  57. Tollrian R (1995) Predator-induced morphological defenses: costs, life history shifts, and maternal effects in Daphnia pulex. Ecology 76:1691–1705CrossRefGoogle Scholar
  58. Tollrian R, Dodson SI (1999) Inducible defences in cladocera: constraints, costs, and multipredator environments. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, pp 177–202Google Scholar
  59. Tollrian R, Harvell CD (eds) (1999a) The ecology and evolution of inducible defenses. Princeton University Press, PrincetonGoogle Scholar
  60. Tollrian R, Harvell CD (1999b) The evolution of inducible defenses: current ideas. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, pp 306–321Google Scholar
  61. Trussell GC, Smith LD (2000) Induced defenses in response to an invading crab predator: an explanation of historical and geographic phenotypic change. Proc Natl Acad Sci 97:2123–2127CrossRefGoogle Scholar
  62. Urabe J, Akai H, Yashiro K (1990) Change of plankton phase in Lake Inba and Lake Tega (in Japanese). Bull Biol Soc Chiba 40:14–20Google Scholar
  63. Whiteside MC, Williams JB, White CP (1978) Seasonal abundance and pattern of chydorid, Cladocera in mud and vegetative habitats. Ecology 59:1177–1188CrossRefGoogle Scholar
  64. Zagarese HE, Marinone MC (1992) Induction and inhibition of spine development in the rotifer Keratella tropica. Freshw Biol 28:289–300CrossRefGoogle Scholar

Copyright information

© The Japanese Society of Limnology 2017

Authors and Affiliations

  • Yurie Otake
    • 1
    • 2
    Email author
  • Maiko Kagami
    • 1
  • Takeo Kuriyama
    • 1
    • 3
  • Takehito Yoshida
    • 2
  1. 1.Department of Environmental Science, Faculty of ScienceToho UniversityFunabashiJapan
  2. 2.Department of General Systems StudiesUniversity of TokyoMeguroJapan
  3. 3.Institute of Natural and Environmental SciencesUniversity of HyogoTanbaJapan

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