Skip to main content
SpringerLink
Log in

Sublethal toxicity of untreated and treated stormwater Zn concentrations on the foraging behaviour of Paratya australiensis (Decapoda: Atyidae)

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Aquatic organisms use chemical cues to perform key ecological behaviours such as locating food. Anthropogenic pollutants have the potential to disrupt these behaviours by down-regulating chemoreception. Urban stormwater runoff is a major source of metal pollution, particularly Zn, and is a leading contributor to the degradation of receiving waters. Consequently, significant remedial efforts have focused on using constructed stormwater wetlands to reduce pollutant loads. However, no studies have examined the efficacy of water quality improvements on ecologically relevant behaviours in aquatic biota. We conducted controlled laboratory experiments to test whether untreated (100 and 400 µg L−1) and treated (40 µg L−1) stormwater Zn concentrations observed in constructed wetlands interfere with the foraging behaviour of the glass shrimp (Paratya australiensis). The ability of shrimp to perceive, approach and search for a chemoattractant source was used to assess foraging behaviour. Abnormal foraging behaviour was observed in shrimp exposed to Zn at untreated stormwater concentrations. The strongest change relative to the control was observed for perception, which decreased by more than 80 and 60 % in the 400 µg Zn L−1 and 100 µg Zn L−1 groups, respectively. The behaviour of shrimp exposed to Zn concentrations measured in treated stormwater did not differ from the controls. The results suggest that the reduction of stormwater Zn concentrations via wetland treatment can prevent abnormal contamination-induced behaviours in shrimp, leading to improved aquatic ecosystem health. This study also highlights the subtle, but biologically significant impacts arising from sublethal exposures of Zn, and emphasise the utility of behavioural toxicology. The behavioural test used here is a simple and effective approach that could be incorporated into studies assessing the efficacy of stormwater treatment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ache B, Case J (1969) An analysis of antennular chemoreception in two commensal shrimps of the genus betaeus. Physiol Zool 42(4):361–371

    CAS  Google Scholar 

  • Atema J (1977) Functional separation of smell and taste in fish and crustacea. In: LeMagnen J, MacLeod P (eds) Olfaction and taste, vol 6. Information Retrieval, London, pp 165–174

    Google Scholar 

  • Baldwin DH, Sandahl JF, Labenia JS, Scholz NL (2003) Sublethal effects of copper on coho salmon: impacts on nonoverlapping receptor pathways in the peripheral olfactory nervous system. Environ Toxicol Chem 22(10):2266–2274. doi:10.1897/02-428

    Article  CAS  Google Scholar 

  • Barbieri E, Doi SA (2011) The effects of different temperature and salinity levels on the acute toxicity of zinc in the Pink Shrimp (Farfantepenaeus paulensis). Mar Freshw Behav Physiol 44(4):251–263. doi:10.1080/10236244.2011.617606

    Article  CAS  Google Scholar 

  • Benvenuti S, Ioale P, Gagliardo A, Bonadonna F (1992) Effects of zinc sulfate-induced anosmia on homing behavior of pigeons. Comp Biochem Phys A 103(3):519–526. doi:10.1016/0300-9629(92)90281-t

    Article  Google Scholar 

  • Birch GF, Matthai C, Fazeli MS, Suh J (2004) Efficiency of a constructed wetland in removing contaminants from stormwater. Wetlands 24(2):459–466. doi:10.1672/0277-5212(2004)024[0459:eoacwi]2.0.co;2

  • Birch GF, Fazeli MS, Niatthai C (2005) Efficiency of an infiltration basin in removing contaminants from urban stormwater. Environ Monit Assess 101(1–3):23–38

    CAS  Google Scholar 

  • Blaxter JHS, Hallers-Tjabbes CCT (1992) The effect of pollutants on sensory systems and behaviour of aquatic animals. Neth J Aquat Ecol 26(1):43–58. doi:10.1007/bf02298027

    Article  CAS  Google Scholar 

  • Blinova NK, Cherkashin SA (2012) The olfactory system of crustaceans as a model for ecologo-toxicological studies. J Evol Biochem Phys+ 48(2):155–165. doi:10.1134/s0022093012020053

    Article  CAS  Google Scholar 

  • Bool JD, Witcomb K, Kydd E, Brown C (2011) Learned recognition and avoidance of invasive mosquitofish by the shrimp Paratya australiensis. Mar Freshw Res 62(10):1230–1236. doi:10.1071/mf11140

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Buskey EJ (1984) Swimming pattern as an indicator of the roles of copepod sensory systems in the recognition of food. Mar Biol 79(2):165–175. doi:10.1007/bf00951825

    Article  Google Scholar 

  • Butler R, Roddie BD, Mainstone CP (1990) The effects of sewage sludge on two life-history stages of Mytilus edulis. Chem Ecol 4(4):211–219. doi:10.1080/02757549008035235

    Article  Google Scholar 

  • Chu KH, Lau PY (1994) Effects of diazinon, malathion, and paraquat on the behavioral response of the shrimp Metapenaeus ensis to chemoattractants. Bull Environ Contam Toxicol 53:127–133

    Article  CAS  Google Scholar 

  • Daly HR, Campbell IC, Hart BT (1990) Copper toxicity to Paratya australiensis: I. Influence of nitrilotriacetic acid and glycine. Environ Toxicol Chem 9(8):997–1006. doi:10.1002/etc.5620090805

  • Denoel M, Bichot M, Ficetola GF, Delcourt J, Ylieff M, Kestemont P, Poncin P (2010) Cumulative effects of road de-icing salt on amphibian behavior. Aquat Toxicol 99(2):275–280. doi:10.1016/j.aquatox.2010.05.007

    Article  CAS  Google Scholar 

  • Fleeger JW, Carman KR, Nisbet RM (2003) Indirect effects of contaminants in aquatic ecosystems. Sci Total Environ 317:207–233

    Article  CAS  Google Scholar 

  • Gemmell P (1978) Feeding habits and structure of the gut of the Australian freshwater prawn Paratya australiensis Kemp (Crustacean, Caridea, Atyidae). Proc Linn Soc NSW 103:210–216

    Google Scholar 

  • Gerhardt A (1995) Monitoring behavioural responses to metals in Gammarus pulex (L) (Crustacea) with impedance conversion. Environ Sci Pollut Res 2(1):15–23. doi:10.1007/bf02987506

    Article  CAS  Google Scholar 

  • Hare L (1992) Aquatic insects and trace metals: bioavailability, bioaccumulation, and toxicity. Crit Rev Toxicol 22(5–6):327–369. doi:10.3109/10408449209146312

  • Harpaz S, Kahan D, Galun R (1987) Variability in feeding behaviour of the Malaysian prawn Macrobrachium rosenbergii (de Man) during the molt cycle (Decapoda, Caridea). Crustaceana 52:53–60

    Article  Google Scholar 

  • Heugens EHW, Hendricks AJ, Dekker T, Straalen NMV, Admiraal W (2001) A review of the effects of multiple stressors on aquatic organisms and analysis of uncertainty factors for use in risk assessment. Crit Rev Toxicol 31(3):247–284

    Article  CAS  Google Scholar 

  • Hickey CW, Pyle E (2001) Derivation of water quality guideline values for heavy metals using a risk-based methodology: an approach for New Zealand. Australas J Ecotoxicol 7:137–156

    CAS  Google Scholar 

  • Hindley JPR (1975) The detection, location and recognition of food by juvenile banana prawns, Penaeus merquiensis (de Man). Mar Freshw Behav Physiol 45(6):193–210

    Article  Google Scholar 

  • Hose GC, Wilson SP (2005) Toxicity of endosulfan to Paratya australiensis Kemp (Decapoda : Atyidae) and Jappa kutera Harker (Ephemeroptera : Leptophlebiidae) in field-based tests. Bull Environ Contam Toxicol 75(5):882–889. doi:10.1007/s00128-005-0832-7

    Article  CAS  Google Scholar 

  • Hunter K, Pyle G (2004) Morphological response of Daphnia pulex to Chapborus americanus kairomone in the presence and absence of metals. Environ Toxicol Chem 23(5):1311–1316

    Article  CAS  Google Scholar 

  • Kumar A, Doan H, Barnes M, Chapman JC, Kookana RS (2010) Response and recovery of acetylcholinesterase activity in freshwater shrimp, Paratya australiensis (Decapoda: Atyidae) exposed to selected anti-cholinesterase insecticides. Ecotoxicol Environ Saf 73(7):1503–1510. doi:10.1016/j.ecoenv.2010.07.016

    Article  CAS  Google Scholar 

  • Long ER, Hong CB, Severn CG (2001) Relationships between acute sediment toxicity in laboratory tests and abundance and diversity of benthic infauna in marine sediments: a review. Environ Toxicol Chem 20(1):46–60. doi:10.1897/1551-5028(2001)020<0046:rbasti>2.0.co;2

    Article  CAS  Google Scholar 

  • Lurling M, Scheffer M (2007) Info-disruption: pollution and the transfer of chemical information between organisms. Trends Ecol Evol 22(7):374–379. doi:10.1016/j.tree.2007.04.002

    Article  Google Scholar 

  • Makepeace DK, Smith DW, Stanley SJ (1995) Urban stormwater quality-summary of contaminant data. Crit Rev Environ Sci Technol 25(2):93–139

    Article  CAS  Google Scholar 

  • Malaviya P, Singh A (2012) Constructed wetlands for management of urban stormwater runoff. Crit Rev Environ Sci Technol 42(20):2153–2214. doi:10.1080/10643389.2011.574107

    Article  CAS  Google Scholar 

  • Maltby L (1994) Stress, shredders and streams: using Gammarus energetics to assess water quality. In: Sutcliffce DW (ed) Water quality & stress indicators in marine and freshwater systems: linking levels of organisation vol 4, vol 3. Freshwater Biological Association, Ambleside, pp 98–110

    Google Scholar 

  • Maltby L, Naylor C (1990) Preliminary observations on the ecological relevance of the Gammarus ‘scope for growth’ assay: effect of zinc on reproduction. Funct Ecol 4(3):393–397. doi:10.2307/2389601

    Article  Google Scholar 

  • Maltby L, Naylor C, Calow P (1990) Effect of stress on a freshwater benthic detritivore: scope for growth in Gammarus-pulex. Ecotoxicol Environ Saf 19(3):285–291. doi:10.1016/0147-6513(90)90030-9

    Article  CAS  Google Scholar 

  • Manassa RP, Dixson DL, McCormick MI, Chivers DP (2013) Coral reef fish incorporate multiple sources of visual and chemical information to mediate predation risk. Animal Behav 86(4):717–722

    Article  Google Scholar 

  • March JG, Benstead JP, Pringle CM, Ruebel MW (2001) Linking shrimp assemblages with rates of detrital processing along an elevational gradient in a tropical stream. Can J Fish Aquat Sci 58(3):470–478. doi:10.1139/cjfas-58-3-470

    Article  Google Scholar 

  • March JG, Pringle CM, Townsend MJ, Wilson AI (2002) Effects of freshwater shrimp assemblages on benthic communities along an altitudinal gradient of a tropical island stream. Freshw Biol 47(3):377–390. doi:10.1046/j.1365-2427.2002.00808.x

    Article  Google Scholar 

  • Marking LL, Dawson VK (1973) Toxicity of quinaldine sulfate to fish. Investigative Fish Control., vol 48. U.S. Fish and Wildlife Service, Department of the Interior, Washington, D.C., p 8

    Google Scholar 

  • McBride K, Slotnick B, Margolis FL (2003) Does intranasal application of zinc sulfate produce anosmia in the mouse? an olfactometric and anatomical study. Chem Senses 28(8):659–670

    Article  CAS  Google Scholar 

  • McCarthy SG, Incardona JP, Scholz NL (2008) Coastal storms, toxic runoff, and the sustainable conservation of fish and fisheries. In: McLaughlin KD (ed) Mitigating impacts of natural hazards on fishery ecosystems, vol 64. American Fisheries Society Symposium, Washington DC, pp 7–27

    Google Scholar 

  • Melbourne Water Corporation (2010) Constructed Wetland Guidelines, Melbourne, VIC

  • Ottoni EB (2000) EthoLog 2.2: a tool for the transcription and timing of behavior observation sessions. Behav Res Methods Instrum Comput 32(3):446–449. doi:10.3758/bf03200814

    Article  CAS  Google Scholar 

  • Passos C, Reyes F, Tassino B, Rosenthal GG, Gonzalez A (2013) Female annual killifish austrolebias reicherti (Cyprinodontiformes, Rivulidae) attend to male chemical cues. Ethology 119(10):891–897. doi:10.1111/eth.12129

    Article  Google Scholar 

  • Pestana JLT, Re A, Nogueira AJA, Soares A (2007) Effects of Cadmium and Zinc on the feeding behaviour of two freshwater crustaceans: Atyaephyra desmarestii (Decapoda) and Echinogammarus meridionalis (Amphipoda). Chemosphere 68(8):1556–1562. doi:10.1016/j.chemosphere.2007.02.053

    Article  CAS  Google Scholar 

  • Petranka JW, Kats LB, Sih A (1987) Predator prey interactions among fish and larval amphibians-use of chemical cues to detect predatory fish. Animal Behav 35:420–425. doi:10.1016/s0003-3472(87)80266-x

    Article  Google Scholar 

  • Powers JB, Winans SS (1973) Sexual behavior in peripherally anosmic male hamsters. Physiol Behav 10:361–368

    Article  CAS  Google Scholar 

  • Pringle CM (1996) Atyid shrimps (Decapoda: Atyidae) influence the spatial heterogeneity of algal communities over different scales in tropical montane streams,Puerto Rico. Freshw Biol 35(1):125–140. doi:10.1046/j.1365-2427.1996.00487.x

    Article  Google Scholar 

  • Richardson AJ, Growns JE, Cook RA (2004) Distribution and life history of caridean shrimps in regulated lowland rivers in southern Australia. Mar Freshw Res 55(3):295–308. doi:10.1071/mf03126

    Article  Google Scholar 

  • Schmidt KA, Dall SRX, van Gils JA (2010) The ecology of information: an overview on the ecological significance of making informed decisions. Oikos 119(2):304–316. doi:10.1111/j.1600-0706.2009.17573.x

    Article  Google Scholar 

  • Schmitt BC, Ache BW (1979) Olfaction: responses of a decapod crustacean are enhanced by flicking. Science 205(4402):204–206

    Article  CAS  Google Scholar 

  • Sherba M, Dunham DW, Harvey HH (2000) Sublethal copper toxicity and food response in the freshwater crayfish Cambarus bartonii (Cambaridae, Decapoda, Crustacea). Ecotoxicol Environ Saf 46(3):329–333. doi:10.1006/eesa.1999.1910

    Article  CAS  Google Scholar 

  • Thomas CR, Hose GC, Warne MS, Lim RP (2008) Effects of river water and salinity on the toxicity of deltamethrin to freshwater shrimp, cladoceran, and fish. Arch Environ Contam Toxicol 55(4):610–618. doi:10.1007/s00244-008-9147-0

    Article  CAS  Google Scholar 

  • Tiefenthaler LL, Stein ED, Schiff KC (2008) Watershed and land use-based sources of trace metals in urban storm water. Environ Toxicol Chem 27(2):277–287. doi:10.1897/07-126r.1

    Article  CAS  Google Scholar 

  • Turner AO, Chislock MF (2010) Blinded by the stink: nutrient enrichment impairs the perception of predation risk by freshwater snails. Eco Appl 20(8):2089–2095

    Article  Google Scholar 

  • Von Der Emde G, Bleckmann H (1998) Finding food: senses involved in foraging for insect larvae in the electric fish Gnathonemus petersii. J Exp Bol 201:969–980

    Google Scholar 

  • Walsh CJ (2000) Urban impacts on the ecology of receiving waters: a framework for assessment, conservation and restoration. Hydrobiologia 431(2–3):107–114. doi:10.1023/a:1004029715627

    Article  Google Scholar 

  • Walsh CJ, Mitchell BD (1995) The freshwater shrimp Paratya australiensis (Kemp, 1917) (Decapoda: Atyidae) in estuaries of south-western Victoria, Australia. Mar Freshw Res 46(6):959–965. doi:10.1071/mf9950959

    Article  Google Scholar 

  • Walsh CJ, Leonard AW, Ladson AR, Fletcher TD (2004) Urban stormwater and the ecology of streams. Cooperative Research Centre for Freshwater Ecology and Cooperative Research Centred for Catchment Hydrology, Canberra

  • Wenger SJ, Roy AH, Jackson CR, Bernhardt ES, Carter TL, Filoso S, Gibson CA, Hession WC, Kaushal SS, Marti E, Meyer JL, Palmer MA, Paul MJ, Purcell AH, Ramirez A, Rosemond AD, Schofield KA, Sudduth EB, Walsh CJ (2009) Twenty-six key research questions in urban stream ecology: an assessment of the state of the science. J N Am Benthol Soc 28(4):1080–1098. doi:10.1899/08-186.1

    Article  Google Scholar 

  • Wong CK, Chu KH, Tang KW, Tam TW, Wong LJ (1993) Effects of chromium, copper and nickel on survival and feeding-behavior of Metapenaeus-Ensis larvae and postlarvae (Decapoda, Penaeidae). Mar Environ Res 36(2):63–78. doi:10.1016/0141-1136(93)90082-b

    Article  CAS  Google Scholar 

  • Zimmerfaust RK (1989) The relationship between chemoreception and foraging behavior in crustaceans. Limnol Oceanogr 34(7):1367–1374

    Article  Google Scholar 

Download references

Acknowledgments

Richard Kightley and Elisa Bruning are thanked for their assistance in the laboratory. The authors would like to acknowledge the financial support of the NSW Environmental Trust (2009/RD/0035), Sydney Metropolitan Catchment Management Authority and Sydney Water. LJO also received PhD Scholarship support from Macquarie University.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Environmental Science, Department of Environment and Geography, Macquarie University, North Ryde, Sydney, NSW, 2109, Australia

    Lois Jane Oulton & Mark P. Taylor

  2. Department of Biological Sciences, Macquarie University, North Ryde, Sydney, NSW, 2109, Australia

    Grant C. Hose & Culum Brown

Authors
  1. Lois Jane Oulton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mark P. Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Grant C. Hose
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Culum Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lois Jane Oulton.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oulton, L.J., Taylor, M.P., Hose, G.C. et al. Sublethal toxicity of untreated and treated stormwater Zn concentrations on the foraging behaviour of Paratya australiensis (Decapoda: Atyidae). Ecotoxicology 23, 1022–1029 (2014). https://doi.org/10.1007/s10646-014-1246-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-014-1246-2

Keywords

Search

Navigation