pp 1–11 | Cite as

Phototactic behavior of native Daphnia in the presence of chemical cues from a non-native predator Bythotrephes

  • Emily L. KiehnauEmail author
  • Lawrence J. Weider
Behavioral ecology – original research


Chemical cues are used by many taxa to communicate within and among species. Behavioral defenses induced by predator cues are a mechanism by which prey species resist or avoid predator attack. This study examined the egg bank of native Daphnia species in a lake that has been invaded by Bythotrephes longimanus, an invertebrate zooplanktivore native to northern-central Europe and Asia (initial invasion 1994, population boom in 2009). Daphnia resting eggs from both pre- and post-B. longimanus invasion lake sediments were hatched and established as isofemale clonal lines. Phototactic behavior (a proxy for vertical migration behavior) was assessed in the presence and absence of B. longimanus cue. This was done to evaluate the hypothesis that the heavy predation imposed by B. longimanus would have been selected for Daphnia clones that are more negatively phototactic in the presence of B. longimanus cue, because B. longimanus is a visual predator. The behavior of the clones derived from pre-B. longimanus era resting eggs was not significantly different from the behavior of the clones from the post-B. longimanus era and exposure to predator cue did not affect the phototactic response of the clones. There was a significant difference in the phototactic behavior of the three Daphnia species tested (Daphnia ambigua, Daphnia mendotae, and Daphnia pulicaria). These results suggest that predation by B. longimanus is not the main factor that is influencing the phototactic behavior of Daphnia in the lake. Other factors such as fish predation may be playing a more significant role in this system.


Invasive species Inducible defenses Kairmones Vertical migration Zooplankton 



We thank Jake Walsh for his assistance in the collection of sediment cores and logistical support. We thank Rachel Hartnett, Rebecca Prather, Ellen Welti, Silvia Markova, Christian Brewer, and Katherine Hooker for assisting with setup of the phototactic assays. Kevin Kiehnau provided vital assistance in the collection of zooplankton samples. We thank Claire Curry for providing advice on the statistical analyses. We thank John Shurin and three anonymous reviewers for valuable comments on an earlier version of the manuscript. This work was supported by The University of Oklahoma Department of Biology Adams Scholarship Fund. This manuscript represents a portion of ELK’s doctoral dissertation at The University of Oklahoma.

Author contribution statement

ELK conceived and designed the experiment with input from LJW. ELK conducted the fieldwork. ELK and LJW processed sediments and conducted the laboratory experiments. ELK analyzed the data and drafted the manuscript. LJW provided conceptual advice and edited the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Animal rights statement

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

Supplementary material

442_2019_4461_MOESM1_ESM.pdf (322 kb)
Supplementary material 1 (PDF 323 kb)


  1. Bates D, Kliegl R, Vasishth S, Baayen H (2015) Parsimonious mixed models. arXiv:1506.04967 (stat.ME)
  2. Beranek A (2012) An assessment of the long-term phenology and impact of Bythotrephes longimanus in Island Lake Reservoir, Minnesota, using sediment records. Master thesis, Department of Integrated Biosciences, University of Minnesota, Minneapolis, Minnesota, USA.
  3. Black AR, Dodson SI (2003) Ethanol: a better preservation technique for Daphnia. Limnol Oceanogr Methods 1:45–50. CrossRefGoogle Scholar
  4. Bollens SM, Frost BW (1991) Ovigerity, selective predation, and variable diel vertical migration in Euchaeta elongate (Copepoda: calanoida). Oecologia 87:155–161. CrossRefGoogle Scholar
  5. Boudreau SA, Yan ND (2003) The differing crustacean zooplankton communities of Canadian Shield lakes with and without the nonindigenous zooplanktivore Bythotrephes longimanus. Can J Fish Aquatic Sci 60:1307–1313. CrossRefGoogle Scholar
  6. Bourdeau PE, Pangle KL, Peacor SD (2011) The invasive predator Bythotrephes induces changes in the vertical distribution of native copepods in Lake Michigan. Biol Invasions 13:2533–2545. CrossRefGoogle Scholar
  7. Bourdeau PE, Pangle KL, Reed EM, Peacor SD (2013) Finely tuned response of native prey to an invasive predator in a freshwater system. Ecology 94:1449–1455. CrossRefGoogle Scholar
  8. Bourdeau PE, Pangle KL, Peacor SD (2015) Factors affecting the vertical distribution of the zooplankton assemblage in Lake Michigan: the role of the invasive predator Bythotrephes longimanus. J Great Lakes Res 41:115–124. CrossRefGoogle Scholar
  9. Brodin T, Johansson F (2002) Effects of predator-induced thinning and activity changes on life history in a damselfly. Oecologia 132:316–322. CrossRefGoogle Scholar
  10. Bungartz B, Branstrator DK (2003) Morphological changes in Daphnia mendotae in the chemical presence of Bythotrephes longimanus. Arch Hydrobiol 158:97–108. CrossRefGoogle Scholar
  11. Burks RL, Jeppesen E, Lodge DM (2001) Littoral zone structure as Daphnia refugia against fish predators. Limnol Oceanogr 46:230–237. CrossRefGoogle Scholar
  12. Burks RL, Lodge DM, Jeppesen E (2002) Diel horizontal migration of zooplankton: costs and benefits of inhabiting the littoral. Freshw Biol 47:343–365. CrossRefGoogle Scholar
  13. Cox JG, Lima SL (2006) Naiveté and an aquatic-terrestrial dichotomy in the effects of introduced predators. Trends Ecol Evol 21:674–680. CrossRefGoogle Scholar
  14. Davies J (1985) Evidence for a diurnal horizontal migration in Daphnia hyalina lacustris Sars. Hydrobiologia 120:103–105. CrossRefGoogle Scholar
  15. Dawidowics P, Loose CJ (1992) Metabolic costs during predator-induced diel vertical migration of Daphnia. Limnol Oceanogr 37:1589–1595. CrossRefGoogle Scholar
  16. De Meester L (1989) An estimation of the heritability of phototaxis in Daphnia magna Straus. Oecologia 78:142–144. CrossRefGoogle Scholar
  17. De Meester L (1991) An analysis of the phototactic behavior of Daphnia magna clones and their sexual descendants. Hydrobiologia 225:217–227. CrossRefGoogle Scholar
  18. De Meester L (1993) Genotype, fish-mediated chemical, and phototactic behavior in Daphnia magna. Ecology 74:1467–1474. CrossRefGoogle Scholar
  19. De Meester L (1996) Evolutionary potential and local genetic differentiation in a phenotypically plastic trait of a cyclical parthenogen, Daphnia magna. Evolution 50:1293–1298. CrossRefGoogle Scholar
  20. Decaestecker E, De Meester L, Ebert D (2002) In deep trouble: habitat selection constrained by multiples enemies in zooplankton. Proc Natl Acad Sci USA 99:5481–5485. CrossRefGoogle Scholar
  21. Dodson S (1988) The ecological role of chemical stimuli for the zooplankton: predator-avoidance behavior in Daphnia. Limnol Oceanogr 33:1431–1439. Google Scholar
  22. Dumont HJ, Miron I, D’Allasta V, Decraemer W, Claus C, Somers D (1973) Limnological aspects of some Moroccan Atlas lakes, with reference to some physical and chemical variables, the nature and distribution of the phyto- and zoo-plankton, including a note on possibilities for the development of an inland fishery. Int Rev Hydrobiol 58:33–60. CrossRefGoogle Scholar
  23. Fontaine JJ, Martin TE (2006) Parent birds assess nest predation risk and adjust their reproductive strategies. Ecol Lett 9:428–434. CrossRefGoogle Scholar
  24. Frisch D, Morton PK, Chowdhury PR, Culver BW, Colbourne JK, Weider LJ, Jeyasingh PD (2014) A millennial-scale chronicle of evolutionary responses to cultural eutrophication in Daphnia. Ecol Lett 17:360–368. CrossRefGoogle Scholar
  25. Fuchs B, Zimmermann B, Wabakken P, Bornstein S, Månsson J, Evans AL, Liberg O, Sand H, Kindberg J, Ågren EO, Arnemo JM (2016) Sarcoptic mange in the Scandinavian wolf Canis lupus population. BMC Vet Res 12:156–167. CrossRefGoogle Scholar
  26. Gillis MK, Walsh MR (2017) Rapid evolution mitigates the ecological consequences of an invasive species (Bythotrephes longimanus) in lakes in Wisconsin. Proc Biol Sci 284:20170814. CrossRefGoogle Scholar
  27. Hembre LK, Peterson LA (2013) Evolution of predator avoidance in a Daphnia population: evidence from the egg bank. Hydrobiologia 700:245–255. CrossRefGoogle Scholar
  28. Huntley M, Brooks ER (1982) Effects of age and food availability on diel vertical migration of Calanus pacificus. Mar Biol 71:23–31. CrossRefGoogle Scholar
  29. Jokela A, Arnott SE, Beisner BE (2013) Influence of light on the foraging impact of an introduced predatory cladoceran, Bythotrephes longimanus. Freshw Biol 58:1946–1957. CrossRefGoogle Scholar
  30. Kerfoot WC, Weider LJ (2004) Experimental paleoecology (resurrection ecology): chasing Van Valen’s Red Queen hypothesis. Limnol Oceanogr 49:1300–1316. CrossRefGoogle Scholar
  31. Kerfoot WC, Robbins JA, Weider LJ (1999) A new approach to historical reconstruction: combining descriptive and experimental paleolimnology. Limnol Oceanogr 44:1232–1247. CrossRefGoogle Scholar
  32. 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. CrossRefGoogle Scholar
  33. Kim N, Yan ND (2010) Methods for rearing the invasive zooplankter Bythotrephes in the laboratory. Limnol Oceanogr Methods 8:552–561. CrossRefGoogle Scholar
  34. Kvam OV, Kleiven OT (1995) Diel horizontal migration and swarm formation in Daphnia in response to Chaoborus. Hydrobiologia 307:177–184. CrossRefGoogle Scholar
  35. Laforsch C, Beccara L, Tollrian R (2006) Inducible defenses: the relevance of chemical alarm cues in Daphnia. Limnol Oceanogr 51:1466–1472. CrossRefGoogle Scholar
  36. Lampert W (1989) The adaptive significance of diel vertical migration of zooplankton. Funct Ecol 3:21–27. CrossRefGoogle Scholar
  37. Lampert W (2011) Daphnia: development of a model organism in ecology and evolution. In: Kinne O (eds) Excellence in ecology: book 21. International ecology institute, Oldendorf/Luhe, GermanyGoogle Scholar
  38. Lauridsen TL, Buenk I (1996) Diel changes in the horizontal distribution of zooplankton in the littoral zone of two shallow eutrophic lakes. Arch Hydrobiol 137:161–176. Google Scholar
  39. Leibold MA (1991) Trophic interactions and habitat segregation between competing Daphnia species. Oecologia 86:510–520. CrossRefGoogle Scholar
  40. Leibold M, Tessier AJ (1991) Contrasting patterns of body size for Daphnia species that segregate by habitat. Oecologia 869:342–348. CrossRefGoogle Scholar
  41. Loose CJ, Dawidowics P (1994) Trade-offs in diel vertical migration by zooplankton: the costs of predator avoidance. Ecology 75:2255–2263. CrossRefGoogle Scholar
  42. Michels H, Amsinck SL, Jeppesen E, De Meester L (2007) Interclonal variation in diel horizontal migration behavior of the water flea Daphnia magna—searching for a signature of adaptive evolution. Hydrobiologia 594:117–129. CrossRefGoogle Scholar
  43. Muirhead J, Sprules WG (2003) Reaction distance of Bythotrephes longimanus, encounter rate and index of prey risk for Harp Lake, Ontario. Freshw Biol 48:135–146. CrossRefGoogle Scholar
  44. North Temperate Lakes Long-Term Ecological Research, NSF (2001a) North temperate lakes LTER: fish abundance 1981-current [Database].
  45. North Temperate Lakes Long-Term Ecological Research, NSF (2001b) North temperate lakes LTER: physical limnology of primary study lakes 1981-current [Database].
  46. North Temperate Lakes Long-Term Ecological Research, NSF (2001c) North temperate lakes LTER: zooplankton—Madison lakes area 1976–1994 [Database].
  47. North Temperate Lakes Long-Term Ecological Research, NSF (2001d) North temperate lakes LTER: zooplankton—Madison lakes area 1997-current [Database].
  48. Pangle KL, Peacor SD (2006) Non-lethal effect of the invasive predator Bythotrephes longimanus on Daphnia mendotae. Freshw Biol 51:1070–1078. CrossRefGoogle Scholar
  49. Pangle KL, Peacor SD (2009) Light-dependent predation by the invertebrate planktivore Bythotrephes longimanus. Can J Fish Aquatic Sci 66:1748–1757. CrossRefGoogle Scholar
  50. Pangle KL, Peacor SD, Johannsson OE (2007) Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate. Ecology 88:402–412. CrossRefGoogle Scholar
  51. Pasch B, Bolker BM, Phelps SM (2013) Interspecific dominance via vocal interactions mediates altitudinal zonation in neotropical singing mice. Am Nat 182:E161–E173. CrossRefGoogle Scholar
  52. Pijanowska J (1997) Alarm signals in Daphnia? Oecologia 112:12–16. CrossRefGoogle Scholar
  53. Pijanowska J, Kowalczewski A (1997a) Cues from injured Daphnia and from cyclopoids feeding on Daphnia can modify life histories of conspecifics. Hydrobiologia 350:99–103. CrossRefGoogle Scholar
  54. Pijanowska J, Kowalczewski A (1997b) Predators can induce swarming behavior and locomotory responses in Daphnia. Freshw Biol 37:649–656. CrossRefGoogle Scholar
  55. Pijanowska J, Dawidowicz P, Weider LJ (2006) Predator-induced escape response in Daphnia. Arch Hydrobiol 167:77–87. CrossRefGoogle Scholar
  56. R Core Team (2019) R: a language and environment for statistical computing R foundation for statistical computing, Vienna.
  57. Rabus M, Waterkeyn A, Van Pottelbergh N, Brendonck L, Laforsch C (2012) Interclonal variation, effectiveness and long-term implications of Triops-induced morphological defences in Daphnia magna Strauss. J Plankton Res 34:152–160. CrossRefGoogle Scholar
  58. Ringelberg J (1964) The positively phototactic reaction of Daphnia magna Straus—a contribution to the understanding of diurnal migration. J Sea Res 2:319–406. CrossRefGoogle Scholar
  59. Ringelberg J (1991) Enhancement of the phototactic behavior in Daphnia by a chemical mediated by juvenile perch (Perca fluviatilis). J Plankton Res 12:17–25. CrossRefGoogle Scholar
  60. Runyon JB, Mescher MC, De Moraes CM (2006) Volatile chemical cues guide host location and host selection by parasitic plants. Science 313:1964–1967. CrossRefGoogle Scholar
  61. Schulz KL, Yurista PM (1999) Implications of an invertebrate predator’s (Bythotrephes cederstroemi) atypical effects on a pelagic zooplankton community. Hydrobiologia 380:179–193. CrossRefGoogle Scholar
  62. Stoks R, Govaert L, Pauwels K, Jansen B, De Meester L (2015) Resurrecting complexity: the interplay of plasticity and rapid evolution in the multiple trait response to strong changes in predation pressure in the water flea Daphnia magna. Ecol Lett 19:180–190. CrossRefGoogle Scholar
  63. Strauss SY, Lau JA, Carroll SP (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett 9:357–374. CrossRefGoogle Scholar
  64. Timms RM, Moss B (1984) Prevention of growth of potentially dense phytoplankton populations by zooplankton grazing in the presence of zooplanktivorous fish in a freshwater wetland ecosystem. Limnol Oceanogr 29:472–486. CrossRefGoogle Scholar
  65. Tollrian R (1995) Predator-induced morphological defenses: costs, life history shifts, and maternal effects in Daphnia pulex. Ecology 76:1691–1705. CrossRefGoogle Scholar
  66. Tollrian R, Leese F (2010) Ecological genomics: steps towards unraveling genetic basis of inducible defenses in Daphnia. BMC Biol 8:51. CrossRefGoogle Scholar
  67. Torres CW, Brandt M, Tsutsui ND (2007) The role of cuticular hydrocarbons as chemical cues for nestmate recognition in the invasive Argentine ant (Linepithema humile). Insectes Soc 54:336–373. CrossRefGoogle Scholar
  68. Trussell GC, Nicklin MO (2002) Cue sensitivity, inducible defense, and trade-offs in a marine snail. Ecology 83:1635–1647.;2 CrossRefGoogle Scholar
  69. von Frisch K (1942) Über einen Schreckstoff der Fischhaut und seine biologische Bedeutung. Z Vgl Physiol 291:46–145. CrossRefGoogle Scholar
  70. Vuorinen I, Rajasilta M, Salo J (1983) Selective predation and habitat shift in a copepod species—support for the predation hypothesis. Oecologia 59:62–64. CrossRefGoogle Scholar
  71. Walsh JR, Carpenter S, Vander Zanden J (2016a) Invasive species triggers a massive loss of ecosystem services through a trophic cascade. Proc Natl Acad Sci USA 113:4081–4085. CrossRefGoogle Scholar
  72. Walsh JR, Munoz SE, Vander Zanden MJ (2016b) Outbreak of an undetected invasive species triggered by a climate anomaly. Ecosphere 7:e01628. CrossRefGoogle Scholar
  73. Weider LJ (1984) Spatial heterogeneity of Daphnia genotypes: vertical migration and habitat partitioning. Limnol Oceanogr 29:225–235. CrossRefGoogle Scholar
  74. Wisconsin Department of Natural Resources (2018) Bureau of fisheries management. Fish stocking summary [Database].
  75. Yan ND, Leung B, Lewis MA, Peacor SD (2011) The spread, establishment and impacts of the spiny water flea, Bythotrephes longimanus, in temperate North America: a synopsis of the special issue. Biol Invasions 13:2423–2432. CrossRefGoogle Scholar
  76. Zaret TM, Suffern JS (1976) Vertical migration of zooplankton as a predator avoidance mechanism. Limnol Oceanogr 21:804–813. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Graduate Program in Ecology and Evolutionary Biology, Department of BiologyUniversity of OklahomaNormanUSA

Personalised recommendations