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Predation cues influence metabolic rate and sensitivity to other chemical stressors in fathead minnows (Pimephales promelas) and Daphnia pulex

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Abstract

The response of aquatic species to contaminants is often context dependent as illustrated by the influence that predation cues can have on the toxicity of some chemicals. We sought to gain additional insight into this interaction by examining how predation cues (alarm cue and fish kairomone) influence metabolic rate and the acute toxicity of sodium chloride and cadmium to fathead minnow larvae (Pimephales promelas) and sodium chloride to Daphnia pulex neonates. Consistent with a “flight or fight” response, the metabolic rate of fish larvae was elevated in the presence of alarm cue and growth of the minnows was also significantly reduced when exposed to alarm cue. The average 48-h LC50 for fathead minnows exposed to sodium chloride was significantly lower in the presence of alarm cue and kairomone combined as compared to tests with the salt alone. Analysis of the dose and survival response indicated alarm cue increased sensitivity of the fish to mid-range salt concentrations in particular. These results suggest an energetic cost of exposure to predation cues that resulted in enhanced toxicity of NaCl. Exposure to kairomone alone had no significant effect on salt toxicity to the minnows, which could be related to a lack of previous exposure to that cue. The acute toxicity of cadmium to the fish larvae was also not affected by the presence of predation cues which could be due to a metal-induced sensory system dysfunction or reduced bioavailability of the metal due to organic exudates from the predation cues. In contrast to the fathead minnow results, the metabolic rate of D. pulex and toxicity of NaCl to the daphnids were reduced in the presence of certain predator kairomones. This suggests an anti-predator response that enhanced tolerance to the salt. This study illustrates that the effect of predation cues on toxicity of aquatic contaminants can vary significantly based on the prey species, type of cue, and chemical stressor.

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References

  • Adelman IR, Smith Jr LL, Siesennop GD (1976) Acute toxicity of sodium chloride, pentachlorophenol, Guthion®, and hexavalent chromium to Fathead Minnows (Pimephales promelas) and Goldfish (Carassius auratus). J Fisheries Res Board Can 33:203–208

    Article  CAS  Google Scholar 

  • APHA-AWWA-WEF, American Public Health Association, American Water Works Association, Water Environment Association (1998) Standard Methods for the Examination of Water and Wastewater, 20th edn. United Book Press Inc., Baltimore, MD

    Google Scholar 

  • Atherton JA, McCormick MI (2015) Active in the sac: damselfish embryos use innate recognition of odours to learn predation risk before hatching. Anim Behav 103:1–6

    Article  Google Scholar 

  • Barreto RE, Barbosa A, Giassi ACC, Hoffmann A (2010) The ‘club’ cell and behavioural and physiological responses to chemical alarm cues in the Nile tilapia. Mar Freshw Behav Physiol 43:75–81

    Article  Google Scholar 

  • Barreto RE, Barbosa A, Hoffmann A (2012) Ventilatory responses to skin extract in catfish. Aquat Biol 15:205–214

    Article  Google Scholar 

  • Barreto RE, Luchiari AC, Marcondes AL (2003) Ventilatory frequency indicates visual recognition of an allopatric predator in naive Nile tilapia. Behav Process 60:235–239

    Article  Google Scholar 

  • Barry MJ, Syal S (2013) Metabolic responses of tadpoles to chemical predation cues. Hydrobiologia 700:267–276

    Article  Google Scholar 

  • Beggel S, Geist J (2015) Acute effects of salinity exposure on glochidia viability and host infection of the freshwater mussel Anodonta anatina (Linnaeus, 1758). Sci Total Environ 502:659–665

    Article  CAS  Google Scholar 

  • Belden JB, Gilliom RJ, Lydy MJ (2007) How well can we predict the toxicity of pesticide mixtures to aquatic life? Integr Environ Assess Manag 3:364–372

    Article  CAS  Google Scholar 

  • Beyers DW, Rice JA, Clements WH, Henry CJ (1999) Estimating physiological cost of chemical exposure: integrating energetics and stress to quantify toxic effects in fish. Can J Fisheries Aquat Sci 56:814–822

    Article  CAS  Google Scholar 

  • Birge WJ, Black JA, Westerman AG, Short TM, Taylor SB, Briser DM, Wallingford ED (1985) Recommendations on numerical values for regulating iron and chloride concentrations for the purpose of protecting warmwater species of aquatic life in the Commonwealth of Kentucky. Kentucky Natural Resources and Environmental Protection Cabinet, Lexington, KY, Memorandum of Agreement No. 5429

    Google Scholar 

  • Blechinger SR, Kusch RC, Haugo K, Matz C, Chivers DP, Krone PH (2007) Brief embryonic cadmium exposure induces a stress response and cell death in the developing olfactory system followed by long-term olfactory deficits in juvenile zebrafish. Toxicol Appl Pharmacol 224:72–80

    Article  CAS  Google Scholar 

  • Boersma M, Spaak P, De Meester L (1998) Predator-mediated plasticity in morphology, life history, and behavior of Daphnia: The uncoupling of responses. Am Naturalist 152:237–248

    CAS  Google Scholar 

  • Bourdeau PE, Johansson F (2012) Predator-induced morphological defences as by-products of prey behaviour: a review and prospectus. Oikos 121:1175–1190

    Article  Google Scholar 

  • Brown AH, Yan ND (2015) Food quantity affects the sensitivity of Daphnia to road salt. Environ Sci Technol 49:4673–4680

    Article  CAS  Google Scholar 

  • Brown C, Gardner C, Braithwaite VA (2005) Differential stress responses in fish from areas of high- and low-predation pressure. J Comp Physiol B-Biochem Syst Environ Physiol 175:305–312

    Article  Google Scholar 

  • Brown GE, Adrian JC, Patton T, Chivers DP (2001) Fathead minnows learn to recognize predator odour when exposed to concentrations of artificial alarm pheromone below their behavioural-response threshold. Can J Zool 79:2239–2245

    Article  Google Scholar 

  • Campero M, Slos S, Ollevier F, Stoks R (2007) Sublethal pesticide concentrations and predation jointly shape life history: behavioral and physiological mechanisms. Ecol Appl 17:2111–2122

    Article  Google Scholar 

  • Carreau-Green ND, Mirza RS, Martinez ML, Pyle GG (2008) The ontogeny of chemically mediated antipredator responses of fathead minnows, Pimephales promelas. J Fish Biol 73:2390–2401

    Article  Google Scholar 

  • Clinchy M, Sheriff MJ, Zanette LY (2013) Predator-induced stress and the ecology of fear. Funct Ecol 27:56–65

    Article  Google Scholar 

  • Congdon JD, Dunham AE, Hopkins WA, Rowe CL, Hinton TG (2001) Resource allocation-based life histories: a conceptual basis for studies of ecological toxicology. Environ Toxicol Chem 20:1698–1703

    Article  CAS  Google Scholar 

  • Corsi SR, Graczyk DJ, Geis SW, Booth NL, Richards KD (2010) A fresh look at road salt: aquatic toxicity and water-quality impacts on local, regional, and national scales. Environ Sci Technol 44:7376–7382

    Article  CAS  Google Scholar 

  • Dodson SI (1989) The ecological role of chemical stimuli for the zooplankton: predator-induced morphology in Daphnia. Oecologia 78:361–367

    Article  Google Scholar 

  • Etnier DA, Starnes WC (1993) The fishes of Tennessee. University of Tennessee Press, Knoxville, TN

  • Ferrari MCO, Wisenden BD, Chivers DP (2010) Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88:698–724

    Article  Google Scholar 

  • Gauthier C, Couture P, Pyle GG (2006) Metal effects on fathead minnows (Pimephales promelas) under field and laboratory conditions. Ecotoxicol Environ Saf 63:353–364

    Article  CAS  Google Scholar 

  • Giacomin M, Gillis PL, Bianchini A, Wood CM (2013) Interactive effects of copper and dissolved organic matter on sodium uptake, copper bioaccumulation, and oxidative stress in juvenile freshwater mussels (Lampsilis siliquoidea). Aquat Toxicol 144:105–115

    Article  Google Scholar 

  • Giri A, Yadav SS, Giri S, Sharma GD (2012) Effect of predator stress and malathion on tadpoles of Indian skittering frog. Aquat Toxicol 106:157–163

    Article  Google Scholar 

  • Gray JS (1989) Do bioassays adequately predict ecological effects of pollutants? Environmental Bioassay Techniques and their Application. In: Munawar M, Dixon G, Mayfield CI, Reynoldson T, Sadar MH (eds) Proceedings of the 1st International Conference held in Lancaster, England, 11–14 July 1988. Springer Netherlands, Dordrecht, pp 397–402

  • Hanazato T, Dodson SI (1992) Complex effects of a kairomone of Chaoborus and an insecticide on Daphnia pulex. J Plankton Res 14:1743–1755

    Article  CAS  Google Scholar 

  • Hanazato T, Dodson SI (1995) Synergistic effects of low oxygen concentration, predator kairomone, and a pesticide on the cladoceran Daphnia pulex. Limnol Oceanogr 40:700–709

    Article  CAS  Google Scholar 

  • Handelsman CA, Broder ED, Dalton CM, Ruell EW, Myrick CA, Reznick DN, Ghalambor CK (2013) Predator-induced phenotypic plasticity in metabolism and rate of growth: rapid adaptation to a novel environment. Integr Comp Biol 53:975–988

    Article  Google Scholar 

  • Hawkins LA, Armstrong JD, Magurran AE (2004) Predator-induced hyperventilation in wild and hatchery Atlantic salmon fry. J Fish Biol 65:88–100

    Article  Google Scholar 

  • Hawlena D, Schmitz OJ (2010a) Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics. Proc Natl Acad of Sci USA 107:15503–15507

    Article  CAS  Google Scholar 

  • Hawlena D, Schmitz OJ (2010b) Physiological stress as a fundamental mechanism linking predation to ecosystem functioning. Am Naturalist 176:537–556

    Article  Google Scholar 

  • Hintz WD, Relyea RA (2017a) Impacts of road deicing salts on the early-life growth and development of a stream salmonid: salt type matters. Environ Pollut 223:409–415

    Article  CAS  Google Scholar 

  • Hintz WD, Relyea RA (2017b) A salty landscape of fear: responses of fish and zooplankton to freshwater salinization and predatory stress. Oecologia. https://doi.org/10.1007/s00442-017-3925-1

  • Holopainen IJ, Aho J, Vornanen M, Huuskonen H (1997) Phenotypic plasticity and predator effects on morphology and physiology of crucian carp in nature and in the laboratory. J Fish Biol 50:781–798

    Article  Google Scholar 

  • Kerby JL, Hart AJ, Storfer A (2011) Combined effects of virus, pesticide, and predator cue on the larval Tiger Salamander (Ambystoma tigrinum). Ecohealth 8:46–54

    Article  Google Scholar 

  • Matsuo AYO, Playle RC, Val AL, Wood CM (2004) Physiological action of dissolved organic matter in rainbow trout in the presence and absence of copper: sodium uptake kinetics and unidirectional flux rates in hard and softwater. Aqua Toxicol 70:63–81

    Article  CAS  Google Scholar 

  • Maul JD, Farris JL, Lydy MJ (2006) Interaction of chemical cues from fish tissues and organophosphorous pesticides on Ceriodaphnia dubia survival. Environ Pollut 141:90–97

    Article  CAS  Google Scholar 

  • Merciai R, Guasch H, Kumar A, Sabater S, Garcia-Berthou E (2014) Trace metal concentration and fish size: variation among fish species in a Mediterranean river. Ecotoxicol Environ Saf 107:154–161

    Article  CAS  Google Scholar 

  • Mitchell MD, McCormick MI (2013) Ontogenetic differences in chemical alarm cue production determine antipredator responses and learned predator recognition. Behav Ecol Sociobiol 67:1123–1129

    Article  Google Scholar 

  • Mount DR, Gulley DD, Hockett JR, Garrison TD, Evans JM (1997) Statistical models to predict the toxicity of major ions to Ceriodaphnia dubia, Daphnia magna and Pimephales promelas (fathead minnows). Environ Toxicol Chem 16:2009–2019

    Article  CAS  Google Scholar 

  • Oris JT, Bailer AJ (1997) Equivalence of concentration–response relationships in aquatic toxicology studies: testing and implications for potency estimation. Environ Toxicol Chem 16:2204–2209

    CAS  Google Scholar 

  • Pestana JLT, Baird DJ, Soares A (2013) Predator threat assessment in Daphnia magna: the role of kairomones versus conspecific alarm cues. Mar Freshw Res 64:679–686

    Article  Google Scholar 

  • Pestana JLT, Loureiro S, Baird DJ, Soares A (2009) Fear and loathing in the benthos: responses of aquatic insect larvae to the pesticide imidacloprid in the presence of chemical signals of predation risk. Aqua Toxicol 93:138–149

    Article  CAS  Google Scholar 

  • Pestana JLT, Loureiro S, Baird DJ, Soares AMVM (2010) Pesticide exposure and inducible antipredator responses in the zooplankton grazer, Daphnia magna Straus. Chemosphere 78:241–248

    Article  CAS  Google Scholar 

  • Pijanowska J, Kowalczewski A (1997) Predators can induce swarming behaviour and locomotory responses in Daphnia. Freshw Biol 37:649–656

    Article  Google Scholar 

  • Pollock MS, Chivers DP, Mirza RS, Wisenden BD (2003) Fathead minnows, Pimephales promelas, learn to recognize chemical alarm cues of introduced brook stickleback, Culaea inconstans. Environ Biol Fishes 66:313–319

    Article  Google Scholar 

  • Qin G, Presley SM, Anderson TA, Gao W, Maul JD (2011) Effects of predator cues on pesticide toxicity: toward an understanding of the mechanism of the interaction. Environ Toxicol Chem 30:1926–1934

    Article  CAS  Google Scholar 

  • Qin GQ, Xiong YX, Tang S, Zhao P, Doering JA, Beitel SC, Hecker M, Wang M, Liu HL, Lu HL, Du HM (2015) Impact of predator cues on responses to silver nanoparticles in Daphnia carinata. Arch Environ Contam Toxicol 69:494–505

    Article  CAS  Google Scholar 

  • Relyea RA (2003) How prey respond to combined predators: a review and an empirical test. Ecology 84:1827–1839

    Article  Google Scholar 

  • Relyea RA (2005) The lethal impacts of roundup and predatory stress on six species of North American tadpoles. Arch Environ Contam Toxicol 48:351–357

    Article  CAS  Google Scholar 

  • Relyea RA (2012) New effects of roundup on amphibians: predators reduce herbicide mortality; herbicides induce antipredator morphology. Ecol Appl 22:634–647

    Article  Google Scholar 

  • Relyea RA, Mills N (2001) Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor). Proc Natl Acad USA 98:2491–2496

    Article  CAS  Google Scholar 

  • Rose RM, Warne MSJ, Lim RP (2001) The presence of chemicals exuded by fish affects the life-history response of Ceriodaphnia dubia to chemicals with different mechanisms of action. Environ Toxicol Chem 20:2892–2898

    Article  CAS  Google Scholar 

  • Scheiner SM, Berrigan D (1998) The genetics of phenotypic plasticity. VIII. The cost of plasticity in Daphnia pulex. Evolution 52:368–378

    Article  Google Scholar 

  • Schoeppner NM, Relyea RA (2005) Damage, digestion, and defence: the roles of alarm cues and kairomones for inducing prey defences. Ecol Lett 8:505–512

    Article  Google Scholar 

  • Schulz R, Dabrowski JM (2001) Combined effects of predatory fish and sublethal pesticide contamination on the behavior and mortality of mayfly nymphs. Environ Toxicol Chem 20:2537–2543

    Article  CAS  Google Scholar 

  • Scott GR, Sloman KA, Rouleau C, Wood CM (2003) Cadmium disrupts behavioural and physiological responses to alarm substance in juvenile rainbow trout (Oncorhynchus mykiss). J Exp Biol 206:1779–1790

    Article  CAS  Google Scholar 

  • Selye H (1950) Stress and the general adaptation syndrome. Br Med J 1:1383–1392

    Article  CAS  Google Scholar 

  • Sih A, Bell AM, Kerby JL (2004) Two stressors are far deadlier than one. Trends Ecol Evol 19:274–276

    Article  Google Scholar 

  • Slos S, Stoks R (2008) Predation risk induces stress proteins and reduces antioxidant defense. Funct Ecol 22:637–642

    Article  Google Scholar 

  • Soucek DJ (2007) Bioenergetic effects of sodium sulfate on the freshwater crustacean,Ceriodaphnia dubia. Ecotoxicology 16:317–325

    Article  CAS  Google Scholar 

  • Steiner UK, Van Buskirk J (2009) Predator-induced changes in metabolism cannot explain the growth/predation risk tradeoff. PLoS ONE 4:e6160

    Article  Google Scholar 

  • Stibor H, Machacek J (1998) The influence of fish-exuded chemical signals on the carbon budget of Daphnia. Limnol Oceanogr 43:997–1000

    Article  CAS  Google Scholar 

  • Stoler AB, Walker BM, Hintz WD, Jones DK, Lind L, Mattes BM, Schuler MS, Relyea RA (2017) Combined effects of road salt and an insecticide on wetland communities. Environ Toxicol Chem 36:771–779

    Article  CAS  Google Scholar 

  • Sunardi T, Asaeda, Manatunge J (2007) Physiological responses of topmouth gudgeon, Pseudorasbora parva, to predator cues and variation of current velocity. Aqua Ecol 41:111–118

    Article  Google Scholar 

  • Szulkin M, Dawidowicz P, Dodson SI (2006) Behavioural uniformity as a response to cues of predation risk. Anim Behav 71:1013–1019

    Article  Google Scholar 

  • Trekels H, Van F, de Meutter, Stoks R (2013) Predator cues magnify effects of the pesticide endosulfan in water bugs in a multi-species test in outdoor containers. Aqua Toxicol 138:116–122

    Article  Google Scholar 

  • USEPA (2002a) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms, 5th edn. U.S. Environmental Protection Agency, Office of Water, Washington, DC, EPA-821-R-02-012

    Google Scholar 

  • USEPA (2002b) Short-term methods for estimating the chronic toxicity of effluents and receiving waters to freshwater organisms, 4th edn. U.S. Environmental Protection Agency, Office of Water, Washington, DC, EPA-821-R-02-013

    Google Scholar 

  • USEPA (2016) Aquatic life, ambient water quality criteria, cadmium- 2016, EPA-820-R-16-002. U.S. Environmental Protection Agency, Office of Water, Washington, DC

    Google Scholar 

  • Von Elert E, Pohnert G (2000) Predator specificity of kairomones in diel vertical migration of Daphnia: a chemical approach. Oikos 88:119–128

    Article  Google Scholar 

  • Wang J, Zhang P, Yang L, Huang T (2016) Cadmium removal from urban stormwater runoff via bioretention technology and effluent risk assessment for discharge to surface water. J Contam Hydrol 185–186:42–50

    Article  Google Scholar 

  • Weber A (2003) More than one ‘fish kairomone’? Perch and stickleback kairomones affect Daphnia life history traits differently. Hydrobiologia 498:143–150

    Article  Google Scholar 

  • Wisenden BD (2008) Active space of chemical alarm cue in natural fish populations. Behaviour 145:391–407

    Article  Google Scholar 

  • Wood CM, Al-Reasi HA, Smith DS (2011) The two faces of DOC. Aqua Toxicol 105:3–8

    Article  CAS  Google Scholar 

  • Yadav SS, Giri S, Singha U, Boro F, Giri A (2013) Toxic and genotoxic effects of Roundup on tadpoles of the Indian skittering frog (Euflictis cyanophlyctis) in the presence and absence of predator stress. Aqua Toxicol 132:1–8

    Article  Google Scholar 

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Acknowledgements

The authors thank Naomi Cooper for assistance with culturing and maintenance of test organisms, Dr. Jason Belden who provided input on statistical analyses, and three anonymous reviewers whose comments substantially improved the manuscript.

Compliance with ethical standards

Funding for this study was provided by the Ecotoxicology and Water Quality Research Laboratory, Oklahoma State University. Support for A. Hankins was also provided in the form of a graduate teaching assistantship from the Department of Zoology, Oklahoma State University. All applicable international, national and institutional guidelines for the care of use of animals were followed.

Conflict of interest

The authors declare that they have no competing interests.

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Authors and Affiliations

  1. Robison Wildlife Solutions, LLC, 9401S. Harrah Rd, Newalla, OK, 74857, USA

    Amie L. Robison

  2. Department of Biological Sciences, East Tennessee State University, Box 70703, Johnson City, TN, 37614, USA

    Trevor Chapman & Joseph R. Bidwell

  3. Prior address: Department of Zoology, Oklahoma State University, 501 Life Sciences West, Stillwater, OK, 74078, USA

    Amie L. Robison & Joseph R. Bidwell

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  1. Amie L. Robison
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Robison, A.L., Chapman, T. & Bidwell, J.R. Predation cues influence metabolic rate and sensitivity to other chemical stressors in fathead minnows (Pimephales promelas) and Daphnia pulex . Ecotoxicology 27, 55–68 (2018). https://doi.org/10.1007/s10646-017-1870-8

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