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Cue hierarchy in the foraging behaviour of the brackish cladoceran Daphniopsis australis

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Abstract

Zooplankton communities are an essential component of marine and freshwater food webs. However, there is still a relative lack of information on how these organisms behaviourally respond to a range of abiotic and biotic stressors. Specifically, the behaviour of the cladoceran Daphniopsis australis, a species endemic to South-eastern Australian saline lakes and ponds, is still unknown despite its potential role in the structure and function of inland water ecosystems. The swimming behaviour of males, parthenogenetic females and epiphial females was investigated under various conditions and combinations of food and conspecific cues. In the absence of cues, males displayed the most extensive swimming behaviour, exploring all areas of the container, and swimming in a series of relatively straight trajectories. In contrast, females typically exhibited a hop-and-sink motion characterised by the alternation between short bursts of swimming and sinking phases. Both females spent long periods near the bottom of the container, but epiphial females appeared to be more active than parthenogenetic ones that rarely made an excursion in the water column. In the presence of cues, males and females showed abilities to detect infochemicals from food and conspecifics, but exhibited specific behavioural strategies. Males essentially increased their swimming speed in the presence of food and/or conspecific infochemicals, and this increase was independent on the source of the cues, i.e. food, conspecific or a mixture of food and conspecifics. In contrast, females exhibited cue hierarchies that were related to their sexual status. Parthenogenetic females swam faster in the presence of food and a mixture of food and conspecific infochemicals than in the presence of cue from the opposite sex, which did not significantly differ from control observations conducted in the absence of cues. Epiphial females decreased their swimming speed in the presence of cues, with the most significant behavioural answers being driven by sex-related cues.

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References

  • Aladin N V. 1991. Salinity tolerance and morphology of the osmoregulation organs in Cladocera with special reference to Cladocera from the Aral Sea. Hydrobiologia, 225 (1): 291–299.

    Article  Google Scholar 

  • Aladin N V, Potts W T W. 1995. Osmoregulatory capacity of the Cladocera. J. Comp. Physiol. B., 164 (8): 671–683.

    Article  Google Scholar 

  • Banse K. 1995. Zooplankton: pivotal role in the controlof ocean production: I. Biomass and production. ICES J. Mar. Sci., 52 (3–4): 265–277.

    Article  Google Scholar 

  • Baylor E R, Smith F E. 1953. The orientation of Cladocera to polarized light. Am. Nat., 87 (833): 97–101.

    Article  Google Scholar 

  • Benzie J A H. 2005. The Genus Daphnia (Including Daphniopsis): Anomopoda: Daphniidae (Guides to the Identification of the Microinvertebrates of the Continental Waters of the World). Kenobi Productions, Ghent.

    Google Scholar 

  • Bledzki L A, Rybak J I. 2016. Freshwater Crustacean Zooplankton of Europe: Cladocera & Copepoda (Calanoida, Cyclopoida) Key to Species Identification, with Notes on Ecology, Distribution, Methods and Introduction to Data Analysis. Springer, New York. 918p.

    Book  Google Scholar 

  • Bownik A. 2017. Daphnia swimming behaviour as a biomarker in toxicity assessment: a review. Sci. Total Environ., 601–602: 194–205.

    Google Scholar 

  • Brancelj A, De Meester L, Spaak P. 2012. Cladocera: the Biology of Model Organisms: Proceedings of the Fourth International Symposium on Cladocera, Held in Postojna, Slovenia, 8–1. August 1996. Springer, New York. 303p.

    Google Scholar 

  • Brewer M C. 1998. Mating behaviours of Daphnia pulicaria, a cyclic parthenogen: comparisons with copepods. Philos. Trans. R oy. Soc. B: Biol. Sci., 353 (1369): 805–815.

    Article  Google Scholar 

  • Buskey E J. 1984. Swimming patterns as an indicator of the roles of copepod sensory systems in the recognition of food. Mar. Biol., 79(2): 165–175.

    Article  Google Scholar 

  • Campbell C E. 1994. Seasonal zooplankton fauna of salt evaporation basins in South Australia. Austr. J. Mar. Freshw. Res., 45 (2): 199–208.

    Article  Google Scholar 

  • Colbourne J K, Wilson C C, Hebert P D N. 2006. The systematics of Australian Daphnia and Daphniopsis (Crustacea: Cladocera): a shared phylogenetic history transformed by habitat–specific rates of evolution. Biol. J. Linn. Soc., 89 (3): 469–488.

    Article  Google Scholar 

  • Cowles T J. 2004. Planktonic layers: physical and biological interactions on the small scale. In: Seuront L, Strutton P G eds. Handbook of Scaling Methods in Aquatic Ecology: Measurements, Analysis, Simulation. CRC Press, Boca Raton, FL. p.31–49.

    Google Scholar 

  • DaS. Ferrã o Filho A, Da Costa S M, Ribeiro M G L, Azevedo S M F O. 2008. Effects of a saxitoxin–producer strain of Cylindrospermopsis raciborskii (cyanobacteria) on the swimming movements of cladocerans. Environ. Toxicol., 23 (2): 161–168.

    Article  Google Scholar 

  • Dees N D, Bahar S, Garcia R, Moss F. 2008. Patch exploitation in two dimensions: from Daphnia to simulated foragers. J. Theor. Biol., 252 (1): 69–76.

    Article  Google Scholar 

  • Delbare D, Dhert P. 1996. Cladocerans, nematodes and trochophora. In: Laverns P, Sorgeloos P eds. Manual on the Production and Use of Live Food for Aquaculture. Food and Agriculture Organization of United Nation, Rome.

    Google Scholar 

  • Dodson S I, Frey D G. 2001. Cladocera and other branchiopoda. In: Thorp J H, Covich A P eds. Ecology and Classification of North American Freshwater Invertebrates. 2 nd edn. Academic Press, San Diego. p.723–786.

  • Dodson S, Ramcharan C. 1991. Size–specific swimming behavior of Daphnia pulex. J. Plankton Res., 13 (6): 1 367–1 379.

    Article  Google Scholar 

  • Dusenbery D B. 1992. Sensory Ecology: How Organisms Acquire and Respond to Information. WH Freeman, New York.

    Google Scholar 

  • Garcia R, Moss F, Nihongi A, Strickler J R, Göller S, Erdmann U, Schimansky–Geier L, Sokolov I M. 2007. Optimal foraging by zooplankton within patches: the case of Daphnia. Mathem. Biosci., 207 (2): 165–188.

    Article  Google Scholar 

  • Hamza W, Ruggiu D. 2000. Swimming behaviour of Daphnia galeata × hyalina as a response to algal substances and to opaque colours. Int. Rev. Hydrobiol., 85 (2–3): 157–166.

    Article  Google Scholar 

  • Hann B J. 1986. Revision of the genus Daphniopsis Sars, 1903 (Cladocera: Daphniidae) and a description of Daphniopsis chilensis, new species, from South America. J. Crustacean Biol., 6 (2): 246–263.

    Article  Google Scholar 

  • Hebert P D, Wilson C C. 2000. Diversity of the genus Daphniopsis in the saline waters of Australia. Can. J. Zool., 78 (5): 794–808.

    Article  Google Scholar 

  • Hinow P, Nihongi A, Strickler J R. 2015. Statistical mechanics of zooplankton. PLoS One, 10 (8): e0135258.

    Article  Google Scholar 

  • Humphries N E, Weimerskirch H, Queiroz N, Southall E J, Sims D W. 2012. Foraging success of biological Lé vy flights recorded in situ. Proc. Natl. Acad. Sci. U. S. A., 109 (19): 7 169–7 174.

    Article  Google Scholar 

  • Ismail H N, Qin J G, Seuront L, Adams M. 2010b. Impacts of male and food density on female performance in the brackish cladoceran Daphniopsis australis. Hydrobiologia, 652 (1): 277–288.

    Article  Google Scholar 

  • Ismail H N, Qin J G, Seuront L. 2010a. Thermal and halo tolerance of a brackish cladoceran Daphniopsis australis (Sergeev & Williams). In: Martorino L, Puopolo K eds. New Oceanography Research Developments: Marine Chemistry, Ocean Floor Analyses and Marine Phytoplankton. Nova Science Publisher, New York. p.213–230.

  • Ismail H N, Qin J G, Seuront L. 2011a. Dietary responses of the brackish cladoceran Daphniopsis australis fed on different algal species. J. Exp. Mar. Biol. Ecol., 409 (1–2): 275–282.

    Article  Google Scholar 

  • Ismail H N, Qin J G, Seuront L. 2011b. Regulation of life history in the brackish cladoceran, Daphniopsis australis (Sergeev and Williams, 1985) by temperature and salinity. J. Plankton Res., 33 (5): 763–777.

    Article  Google Scholar 

  • Ismail H N, Qin J G, Seuront L. 2011c. The survival and reproductive performance of Daphniopsis australis (Cladocera: Daphniidae) in response to temperature changes. Jurnal Intelek, 6 (1): 70–76.

    Google Scholar 

  • Kiørboe T. 2008. A Mechanistic Approach to Plankton Ecology. Princeton University Press, Princeton.

    Google Scholar 

  • La G H, Choi J Y, Chang K H, Jang M H, Joo G J, Kim H W. 2014. Mating behavior of Daphnia: impacts of predation risk, food quantity, and reproductive phase of females. PLoS One, 9 (8): e104545.

    Article  Google Scholar 

  • Mergeay J, Declerck S, Verschuren D, De Meester L. 2006. Daphnia community analysis in shallow Kenyan lakes and ponds using dormant eggs in surface sediments. Freshw. Biol., 51 (3): 399–411.

    Article  Google Scholar 

  • Nihongi A, Ziarek J J, Nagai T, Uttieri M, Zambianchi E, Strickler J R. 2011. Daphnia pulicaria hijacked by Vibrio cholera: altered swimming behaviour and predation risk implications. In: Kattel G ed. Zooplankton and Phytoplankton: Types, Characteristics and Ecology. Nova Science Publishers, New York. p.181–192.

    Google Scholar 

  • Nihongi A, Ziarek J J, Uttieri M, Sandulli M, Zambianchi E, Strickler J R. 2016. Behavioural interseasonal adaptations in Daphnia pulicaria (Crustacea: Cladocera) as induced by predation infochemicals. Aquat. Ecol., 50 (4): 667–684.

    Article  Google Scholar 

  • O'Keefe T C, Brewer M C, Dodson S I. 1998. Swimming behavior of Daphnia: its role in determining predation risk. J. Plankton Res., 20 (5): 973–984.

    Article  Google Scholar 

  • Pyke J H. 1984. Optimal foraging theory: a critical review. Ann. Rev. Ecol. Syst., 15: 523–575.

    Article  Google Scholar 

  • Sars G O. 1903. On the crustacean fauna of Central Asia. 2. Cladocera. Ann. Mus. zool. Acad. Sci. St. Petersbourg, 8: 157–194.

    Google Scholar 

  • Schwartz S S, Hebert P D N. 1987. Breeding system of Daphniopsis ephemeralis: adaptations to a transient environment. Hydrobiologia, 145 (1): 195–200.

    Article  Google Scholar 

  • Sergeev V, Williams W D. 1985. Daphniopsis australis nov. sp. (Crustacea: Cladocera), a further daphniid in Australian salt lakes. Hydrobiologia, 120 (2): 119–128.

    Article  Google Scholar 

  • Seuront L, Brewer M C, Strickler J R. 2004c. Quantifying zooplankton swimming behavior: the question of scale. In: Seuront L, Strutton P G eds. Handbook of Scaling Methods in Aquatic Ecology: Measurement, Analysis, Simulation. CRC Press, Boca Raton. p.333–359.

    Google Scholar 

  • Seuront L, Schmitt F G, Brewer M C, Strickler J R, Souissi S. 2004b. From random walk to multifractal random walk in zooplankton swimming behavior. Zool. Stud., 43 (2): 498–510.

    Google Scholar 

  • Seuront L, Stanley H E. 2014. Anomalous diffusion and multifractality enhance mating encounters in the ocean. Proc. Natl. Acad. Sci. U. S. A., 111 (6): 2 206–2 211.

    Article  Google Scholar 

  • Seuront L, Vincent D. 2008. Increased seawater viscosity, Phaeocystis globosa spring bloom and Temora longicornis feeding and swimming behaviours. Mar. Ecol. Progr. Ser., 363: 131–145.

    Article  Google Scholar 

  • Seuront L, Yamazaki H, Souissi S. 2004a. Hydrodynamic disturbance and zooplankton swimming behavior. Zool. Stud., 43 (2): 376–387.

    Google Scholar 

  • Seuront L. 2006. Effect of salinity on the swimming behaviour of the estuarine calanoid copepod Eurytemora affinis. J. Plankton Res., 28 (9): 805–813.

    Article  Google Scholar 

  • Seuront L. 2011. Behavioral fractality in marine copepods: endogenous rhythms versus exogenous stressors. Phys. A: Stat. Mech. Appl., 39 0 (2): 250–256.

    Article  Google Scholar 

  • Seuront L. 2013. Chemical and hydromechanical components of mate–seeking behaviour in the calanoid copepod Eurytemora affinis. J. Plankton Res., 35 (4): 724–743.

    Article  Google Scholar 

  • Seuront L. 2015a. On uses, misuses and potential abuses of fractal analysis in zooplankton behavioral studies: a review, a critique and a few recommendations. Phys. A: Stat. Mech. Appl., 432: 410–434.

    Google Scholar 

  • Seuront L. 2015b. Copepods: Diversity, Habitat and Behavior. Nova Science Publishers, New York. 291p.

    Google Scholar 

  • Sims D W, Humphries N E, Bradford R W, Bruce B D. 2012. Lé vy flight and Brownian search patterns of a free–ranging predator reflect different prey field characteristics. J. Anim. Ecol., 81 (2): 432–442.

    Article  Google Scholar 

  • Timms B V. 2007. The biology of the saline lakes of central and eastern inland of Australia: a review with special reference to their biogeographical affinities. Hydrobiologia, 576 (1): 27–37.

    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, New York. p.309–312.

    Google Scholar 

  • Wickramarathna L N, Noss C, Lorke A. 2014. Hydrodynamic trails produced by Daphnia: size and energetics. PLoS One, 9 (3): e92383.

    Article  Google Scholar 

  • Woodson C B, Webster D R, Weissburg M J, Yen J. 2007. Cue hierarchy and foraging in calanoid copepods: ecological implications of oceanographic structure. Mar. Ecol. Progr. Ser., 330: 163–177.

    Article  Google Scholar 

  • Yen J, Sehn J K, Catton K, Kramer A, Sarnelle O. 2011. Pheromone trail following in three dimensions by the freshwater copepod Hesperodiaptomus shoshone. J. Plankton Res., 33 (6): 907–916.

    Article  Google Scholar 

  • Zar J H. 2010. Biostatistical Analysis. 5 th edn. Prentice–Hall, Upper Saddle River, NJ.

    Google Scholar 

  • Ziarek J J, Nihongi A, Nagai T, Uttieri M, Strickler J R. 2011. Seasonal adaptations of Daphnia pulicaria swimming behaviour: the effect of water temperature. Hydrobiologia, 661 (1): 317–327.

    Article  Google Scholar 

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Acknowledgement

This research was supported by an Honours Scholarship from Flinders University to C. McCloud, and an Australian Research Council’s Discovery Projects funding scheme (project DP0664681). Professor Seuront is the recipient of an Australian Professorial Fellowship (project DP0988554). This work is a contribution to the CPER research project CLIMIBIO. The authors thank the French Ministère de l’Enseignement Supérieur et de la Recherche, the Hauts de France Region and the European Funds for Regional Economical Development for their financial support to this project.

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McCloud, C.L., Ismail, H.N. & Seuront, L. Cue hierarchy in the foraging behaviour of the brackish cladoceran Daphniopsis australis. J. Ocean. Limnol. 36, 2050–2060 (2018). https://doi.org/10.1007/s00343-018-7335-y

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