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Assessing predator-prey interactions in a chemically altered aquatic environment: the effects of DDT on Xenopus laevis and Culex sp. larvae interactions and behaviour

  • Josie SouthEmail author
  • Tarryn L. Botha
  • Nico J. Wolmarans
  • Victor Wepener
  • Olaf L. F. Weyl
Article

Abstract

Behavioural assays are used as a tool to understand ecotoxicological effects on organisms, but are often not applied in an ecologically relevant context. Assessment of the effect of chemical contaminants on behaviours relating to fitness and trophic interactions for example, requires incorporating predator-prey interactions to create impact assessments. Dichlorodiphenyltrichloroethane (DDT) is a controlled substance but is still regularly used as a form of mosquito control. There is little explicit information on the effect of DDT on animal behaviour and the consequent effects upon trophic interactions. This study uses a 3 × 2 factorial design to assess the feeding behaviour of Xenopus laevis toward Culex sp. larvae when supplied with different prey cues. We also assess the behavioural responses of mosquito larvae when supplied with no threat cue and predator threat cues when exposed to 0 µg/L, 2 µg/L and 20 µg/L DDT. There was a significant “DDT exposure” x “prey cue” interaction whereby DDT significantly decreased the foraging behaviour of X. laevis towards live prey cues, however there was no effect of DDT on X. laevis response to olfactory prey cues. Dichlorodiphenyltrichloroethane exposure caused mosquito larvae to appear hyperactive regardless of DDT concentration. Mosquito larvae anti-predator response was significantly dampened when exposed to 2 µg/L DDT, however when exposed to 20 µg/L the anti-predator responses were not impaired. Our results indicate a complex interplay in trophic interactions under DDT exposure, wherein effects are mediated depending on species and concentration. There are possible implications regarding reduced anti-predator behaviour in the prey species but also reduced foraging capacity in the predator, which could drive changes in ecosystem energy pathways. We demonstrate that in order to quantify effects of pesticides upon trophic interactions it is necessary to consider ecologically relevant behaviours of both predator and prey species.

Keywords

Dichlorodiphenyltrichloroethane Xenopus laevis Foraging Trophic interactions Contaminants Pesticides 

Notes

Acknowledgements

This study was partially funded by the National Research Foundation (NRF)—South African Research Chairs Initiative of the Department of Science and Technology (Inland Fisheries and Freshwater Ecology, Grant no. 110507) and the NRF (Grant no. SFH150624120779). The research was carried out in the Water Research Group NABF, which was funded through the NRF National Nanotechnology Equipment Program (Grant no. 99024). JS and OLFW acknowledge use of infrastructure and equipment provided by the SAIAB Research Platform and the funding channelled through the NRF-SAIAB Institutional Support system. Partial funding of this study was also provided by the Flemish Interuniversity Council (VLIR) to ECN (VLIR-OUS project—ZEIN21013PR396). Opinions expressed and conclusions arrived at, are those of the authors and are not necessarily to be attributed to NRF or VLIR.

Author contributions

JS, TLB, NJW designed and completed experiments. JS analysed the data. JS, TLB, NJW, VW, OLFW drafted and edited the manuscript. VW and OLFW provided funding.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Akkermans LMA, van den Bercken J, Versluijs-Helder M (1975) Comparative effects of DDT, allethrin, dieldrin and aldrin-transdiol on sense organs of Xenopus laevis. Pestic Biochem and Physiol 5:451–457.  https://doi.org/10.1016/0048-3575(75)90018-8 Google Scholar
  2. Amiard-Triquet C (2009) Behavioral disturbances: the missing link between sub-organismal and supra-organismal responses to stress? Prospects based on aquatic research. Hum Ecol Risk Assess 15:87–110.  https://doi.org/10.1080/10807030802615543 Google Scholar
  3. Anderson JM, Petersont MR (1969) DDT: sublethal effects on brook trout nervous system. Science 164:440–441.  https://doi.org/10.1126/science.164.3878.440 Google Scholar
  4. Anderson JM (1968) Effect of sublethal DDT on the lateral line of brook trout, Salvelinus fontinalis. J Fish Res Bd Can 25:2677–2682Google Scholar
  5. Århem BP, Fraxkexhaeuser B (1974) DDT and related substances: effects on permeability properties of myelinated Xenopus nerve fibre. Potential clamp analysis. Acta Physiol Scand 91:502–511.  https://doi.org/10.1111/j.1748-1716.1974.tb05706.x Google Scholar
  6. Beard J (2006) DDT and human health. Sci Total Environ 355:78–89.  https://doi.org/10.1016/j.scitotenv.2005.02.022 Google Scholar
  7. Boone MD, Semlitsch RD (2003) Interactions of bullfrog tadpole predators and an insecticide: predation release and facilitation. Oecologia 137:610–616.  https://doi.org/10.1007/s00442-003-1394-1 Google Scholar
  8. Bouwman H, Coetzee A, Schutte CHJ (1990) Environmental and health implications of DDT-contaminated fish from the Pongolo Flood Plain. Afr J Zool 1990(104):275–286Google Scholar
  9. Bridges CM (1999) Effects of a pesticide on tadpole activity and predator avoidance behavior. J Herpetol 33:303–306.  https://doi.org/10.2307/1565728 Google Scholar
  10. Brodin T, Fick J, Jonsson M, Klaminder J (2013) Dilute concentrations of a psychiatric drug alter behavior of fish from natural populations. Science 339:814–815.  https://doi.org/10.1126/science.1226850 Google Scholar
  11. Brodin T, Johansson F (2004) Conflicting selection pressures on the growth/predation-risk trade-off in a damselfly. Ecology 85:2927–2932.  https://doi.org/10.1890/03-3120 Google Scholar
  12. Brodin T, Piovano S, Fick J, Klaminder J, Heynen M, Jonsson M (2014) Ecological effects of pharmaceuticals in aquatic systems—impacts through behavioural alterations. Philos Trans R Soc B 369:20130580.  https://doi.org/10.1098/rstb.2013.0580 Google Scholar
  13. Cagan RH, Zeiger WN (1978) Biochemical studies of olfaction: binding specificity of radioactively labeled stimuli to an isolated olfactory preparation from rainbow trout (Salmo gairdneri). Proc Natl Acad Sci USA 75:4679–4683Google Scholar
  14. Carey C, Bryant CJ (1995) Possible interrelations among environmental toxicants, amphibian development, and decline of amphibian populations. Environ Health Perspect 103:13–17Google Scholar
  15. Carreño CA, Nishikawa KC (2010) Aquatic feeding in pipid frogs: the use of suction for prey capture. J Exp Biol 213:2001–2008.  https://doi.org/10.1242/jeb.043380 Google Scholar
  16. Cooke AS (1971) Selective predation by newts on frog tadpoles treated with DDT. Nature 229:275–276.  https://doi.org/10.1038/229275a0 Google Scholar
  17. Cooke AS (1972) The effects of DDT, dieldrin and 2,4-D on amphibian spawn and tadpoles. Environ Pollut 3:51–68Google Scholar
  18. Cooke AS (1973) Response of Rana temporaria tadpoles to chronic doses of pp′-DDT. Copeia 1973:647–652.  https://doi.org/10.2307/1443062 Google Scholar
  19. Davidson G (1982) Developments in malaria vector control. Br Med Bul 38:201–206Google Scholar
  20. du Preez L, Carruthers V (2009) A complete guide to the frogs of Southern Africa. Random House, Cape TownGoogle Scholar
  21. Elepfandt A, Lebrecht S, Schroedter K, Brudermanns B, Hillig R, Schuberth C, Fliess A (2016) Lateral line scene analysis in the purely aquatic frog Xenopus laevis Daudin (Pipidae). BBE 87:117–127.  https://doi.org/10.1159/000445422 Google Scholar
  22. Elepfandt A, Wiedemer L (1987) Lateral-line responses to water surface waves in the clawed frog, Xenopus laevis. J Comp Physiol 160:667–682.  https://doi.org/10.1007/BF00611939 Google Scholar
  23. Faulk CK, Fuiman LA, Thomas P (1999) Parental exposure to ortho, para-dichlorodiphenyltrichloroethane impairs survival skills of atlantic croaker (Micropogonias undulatus) larvae. Environ Toxicol Chem 18:254–262.  https://doi.org/10.1002/etc.5620180223 Google Scholar
  24. Fleeger JW, Carman KR, Nisbet RM (2003) Indirect effects of contaminants in aquatic ecosystems. Sci Total Environ 317:207–233.  https://doi.org/10.1016/S0048-9697(03)00141-4 Google Scholar
  25. Gaworecki KM, Klaine SJ (2008) Behavioral and biochemical responses of hybrid striped bass during and after fluoxetine exposure. Aquat Toxicol 88:207–213.  https://doi.org/10.1016/j.aquatox.2008.04.011 Google Scholar
  26. Gerber R, Smit NJ, Van Vuren JHJ, Nakayama SMM, Yohannes YB, Ikenaka Y, Ishizuka M, Wepener V (2016) Bioaccumulation and human health risk assessment of DDT and other organochlorine pesticides in an apex aquatic predator from a premier conservation area. Sci Total Environ 550:522–533.  https://doi.org/10.1016/j.scitotenv.2016.01.129 Google Scholar
  27. Gliem S, Syed AS, Sansone A, Kludt E, Tantalaki E, Hassenklöver T, Korsching SI, Manzini I (2013) Bimodal processing of olfactory information in an amphibian nose: odor responses segregate into a medial and a lateral stream. Cell Mol Life Sci 70:1965–1984.  https://doi.org/10.1007/s00018-012-1226-8 Google Scholar
  28. Haynes KF (1988) Sublethal effects of neurotoxic insecticides on insect behavior. Ann Rev Entomol 33:149–168.  https://doi.org/10.1146/annurev.en.33.010188.001053 Google Scholar
  29. Hoffmann F, Kloas W (2016) p,p′-Dichlordiphenyldichloroethylene (p,p′-DDE) can elicit antiandrogenic and estrogenic modes of action in the amphibian Xenopus laevis. Physiolo Behav 167:172–178.  https://doi.org/10.1016/j.physbeh.2016.09.012 Google Scholar
  30. Holt RD (1997) Community modules. In: Gange AC, Brown VK (eds) Multitrophic interactions in terrestrial systems. Blackwell Science, Oxford, p. 333–350Google Scholar
  31. Ide FP (1967) Effects of forest spraying with DDT on aquatic insects of salmon streams in New Brunswick. J Fish Res Bd Can 24:769–805.  https://doi.org/10.1139/f67-067 Google Scholar
  32. Kasumyan AO (2001) Effects of chemical pollutants on foraging behavior and sensitivity of fish to food stimuli. J Ichthyol 41:76–87Google Scholar
  33. Kidd KA, Paterson MJ, Rennie MD, Podemski CL, Findlay DL, Blanchfield PJ, Liber K (2014) Direct and indirect responses of a freshwater food web to a potent synthetic oestrogen. Philos Trans R Soc B 369:20130578.  https://doi.org/10.1098/rstb.2013.0578 Google Scholar
  34. Little EE, Finger SE (1990) Swimming behavior as an indicator of sublethal toxicity in fish. Environ Toxicol Chem 9:13–19.  https://doi.org/10.1002/etc.5620090103 Google Scholar
  35. Lorenz R, Brüggemann R, Steinberg CEW, Spieser OH (1996) Humic material changes effects of terbutylazine on behavior of zebrafish (Brachydanio rerio). Chemosphere 33:2145–2158.  https://doi.org/10.1016/0045-6535(96)00305-0 Google Scholar
  36. Macphail RC, Tilson HA (1995) Chapter 10—Behavioral screening tests: past, present, and future. In: Chang LW, Slikker W (eds) Neurotoxicology. San Diego: Academic Press, p 231–238.  https://doi.org/10.1016/B978-012168055-8/50015-7
  37. McCallum ES, Krutzelmann E, Brodin T, Fick J, Sundelin A, Balshine S (2017) Exposure to wastewater effluent affects fish behaviour and tissue-specific uptake of pharmaceuticals. Sci Total Environ 605–606:578–588.  https://doi.org/10.1016/j.scitotenv.2017.06.073 Google Scholar
  38. Mennigen JA, Sassine J, Trudeau VL, Moon TW (2010) Waterborne fluoxetine disrupts feeding and energy metabolism in the goldfish Carassius auratus. Aquatic Toxicol 100:128–137.  https://doi.org/10.1016/j.aquatox.2010.07.022 Google Scholar
  39. Merritt RW, Dadd RH, Walker ED (1992) Feeding behavior, natural food, and nutritional relationships of larval mosquitoes. Annu Rev Entomol 37:349–374.  https://doi.org/10.1146/annurev.en.37.010192.002025 Google Scholar
  40. Michaels CJ, Das S, Chang Y-M, Tapley B (2018) Modulation of foraging strategy in response to distinct prey items and their scents in the aquatic frog Xenopus longipes (Anura: Pipidae). The Herpetol Bull 143:1–6. 2018Google Scholar
  41. Ogilvie DM, Anderson JM (1965) Effect of DDT on temperature selection by young Atlantic salmon, Salmo salar. J Fish Res Bd Can 22:503–512.  https://doi.org/10.1139/f65-046 Google Scholar
  42. Perez MH, Wallace WG (2004) Differences in prey capture in grass shrimp, Palaemonetes pugio, collected along an environmental impact gradient. Arch Environ Contam Toxicol 46:81–89.  https://doi.org/10.1007/s00244-002-0249-9 Google Scholar
  43. Relyea RA (2003) Predator cues and pesticides: a double dose of danger for amphibians. Ecol Appl 13:1515–1521.  https://doi.org/10.1890/02-5298 Google Scholar
  44. Roberts D (2014) Mosquito larvae change their feeding behavior in response to kairomones from some predators. J Med Entomol 51:368–374.  https://doi.org/10.1603/ME13129 Google Scholar
  45. Rodríguez-Prieto I, Fernández-Juricic E, Martín J (2006) Anti-predator behavioral responses of mosquito pupae to aerial predation risk. J Insect Behav 19:373–381.  https://doi.org/10.1007/s10905-006-9033-4 Google Scholar
  46. Roeder KD, Weiant EA (1946) The site of action of DDT in the cockroach. Science 103:304–306Google Scholar
  47. Roeder KD, Weiant EA (1948) The effect of DDT on sensory and motor structures in the cockroach leg. J Cell Comp Physiol 32:175–186.  https://doi.org/10.1002/jcp.1030320206 Google Scholar
  48. Roeder KD, Weiant EA (1951) The effect of concentration, temperature, and washing on the time of appearance of Ddt-induced trains in sensory fibers of the cockroach. Ann Entomol Soc Am 44:372–380.  https://doi.org/10.1093/aesa/44.3.372 Google Scholar
  49. Saaristo M, Brodin T, Balshine S, Bertram MG, Brooks BW, Ehlman SM, McCallum ES, Sih A, Sundin J, Wong BBM, Arnold KE (2018) Direct and indirect effects of chemical contaminants on the behaviour, ecology and evolution of wildlife. Proc R Soc B 285:20181297.  https://doi.org/10.1098/rspb.2018.1297 Google Scholar
  50. Saaristo M, McLennan A, Johnstone CP, Clarke BO, Wong BBM (2017) Impacts of the antidepressant fluoxetine on the anti-predator behaviours of wild guppies (Poecilia reticulata). Aquat Toxicol 183:38–45.  https://doi.org/10.1016/j.aquatox.2016.12.007 Google Scholar
  51. Sandhreinrich MB, Atchison GJ (1990) Sublethal toxicant effects on fish foraging behavior: Empirical vs. mechanistic approaches. Environ Toxicol Chem 9:107–119Google Scholar
  52. Scott GR, Sloman KA (2004) The effects of environmental pollutants on complex fish behaviour: integrating behavioural and physiological indicators of toxicity. Aquat Toxicol 68:369–392.  https://doi.org/10.1016/j.aquatox.2004.03.016 Google Scholar
  53. Sievers M, Hale R, Swearer SE, Parris KM (2018) Contaminant mixtures interact to impair predator-avoidance behaviours and survival in a larval amphibian. Ecotoxicol Environ Saf 161:482–488.  https://doi.org/10.1016/j.ecoenv.2018.06.028 Google Scholar
  54. Sih A (1986) Antipredator responses and the perception of danger by mosquito larvae. Ecology 67:434–441.  https://doi.org/10.2307/1938587 Google Scholar
  55. Sternburg J (1960) Effect of insecticides on neurophysiological activity in insects. J Agric Food Chem 8:257–261.  https://doi.org/10.1021/jf60110a002 Google Scholar
  56. Telfer AC, Laberge F (2013) Responses of Eastern red backed salamanders (Plethodon cinereus) to chemical cues of prey presented in soluble and volatile forms. Physiol Behav 114:6–13Google Scholar
  57. Thorp CJ, Alexander ME, Vonesh JR, Measey J (2018) Size-dependent functional response of Xenopus laevis feeding on mosquito larvae. PeerJ 6:e5813.  https://doi.org/10.7717/peerj.5813 Google Scholar
  58. UNEP (2002) Stockholm convention on persistent organic pollutants (POPs) United Nations Environment Programme, Geneva; UNEP/Chemicals/2002/9Google Scholar
  59. van den Bercken J, Akkermans LMA, van der Zalm JM (1973) DDT-like action of allethrin in the sensory nervous system of Xenopus laevis. Eur J Pharmacol 21:95–106.  https://doi.org/10.1016/0014-2999(73)90212-4 Google Scholar
  60. van den Berg H (2009) Global status of DDT and its alternatives for use in vector control to prevent disease. Environ Health Perspect 117:1656–1663.  https://doi.org/10.1289/ehp.0900785 Google Scholar
  61. van der Bercken J (1972) The effect of DDT and dieldrin on myelinated nerve fibres. Eur J Pharmacol 20:205–214.  https://doi.org/10.1016/0014-2999(72)90150-1 Google Scholar
  62. van der Sluijs I, Gray SM, Amorim MCP, Barber I, Candolin U, Hendry AP, Krahe R, Maan ME, Utne-Palm AC, Wagner HJ, Wong BBM (2011) Communication in troubled waters: responses of fish communication systems to changing environments. Evol Ecol 25:623–640.  https://doi.org/10.1007/s10682-010-9450-x Google Scholar
  63. Van Dyk JC, Bouwman H, Barnhoorn IEJ, Bornman MS (2010) DDT contamination from indoor residual spraying for malaria control. Sci Total Environ 408:2745–2752Google Scholar
  64. Vieira EDR, Torres JPM, Malm O (2001) DDT environmental persistence from its use in a vector control program: a case study. Environ Res 86:174–182.  https://doi.org/10.1006/enrs.2001.4258 Google Scholar
  65. Viljoen IM, Bornman R, Bouwman H (2016) DDT exposure to frogs: a case study from Limpopo province, South Africa. Chemosphere 159:335–341Google Scholar
  66. Weis JS, Candelmo A (2012) Pollutants and fish predator/prey behavior: a review of laboratory and field approaches. Curr Zool 58:9–20.  https://doi.org/10.1093/czoolo/58.1.9 Google Scholar
  67. Weis JS, Smith G, Zhou T, Santiago-Bass C, Weis P (2001) Effects of contaminants on behavior: biochemical mechanisms and ecological consequences Killifish from a contaminated site are slow to capture prey and escape predators; altered neurotransmitters and thyroid may be responsible for this behavior, which may produce population changes in the fish and their major prey, the grass shrimp. BioScience 51:209–217.  https://doi.org/10.1641/0006-3568(2001)051[0209:EOCOBB]2.0.CO;2 Google Scholar
  68. Wells M, Leonard L (2006) DDT contamination in South Africa. The International POPs Elimination Project (IPEP). Report for preparation for the Stockholm Convention. GroundWork, PietermaritzburgGoogle Scholar
  69. Welsh JH, Gordon HT (1947) The mode of action of certain insecticides on the arthropod nerve axon. J Cell Comp Physiol 30:147–171Google Scholar
  70. Wolmarans NJ, Du Preez LH, Yohannes YB, Ikenaka Y, Ishizuka M, Smit NJ, Wepener V (2018) Linking organochlorine exposure to biomarker response patterns in Anurans: a case study of Müller’s clawed frog (Xenopus muelleri) from a tropical malaria vector control region. Ecotoxicology 27:1203–1216.  https://doi.org/10.1007/s10646-018-1972-y Google Scholar
  71. Zala SM, Penn DJ (2004) Abnormal behaviours induced by chemical pollution: a review of the evidence and new challenges. Anim Behav 68:649–664.  https://doi.org/10.1016/j.anbehav.2004.01.005 Google Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Josie South
    • 1
    Email author
  • Tarryn L. Botha
    • 2
  • Nico J. Wolmarans
    • 2
    • 3
  • Victor Wepener
    • 2
  • Olaf L. F. Weyl
    • 1
  1. 1.DST/NRF Research Chair in Inland Fisheries and Freshwater Ecology Laboratory, South African Institute for Aquatic Biodiversity (SAIAB)GrahamstownSouth Africa
  2. 2.Unit for Environmental Sciences and Management, Water Research GroupNorth-West UniversityPotchefstroomSouth Africa
  3. 3.Laboratory of Systemic, Physiological and Ecotoxicological Research, Department of BiologyUniversity of AntwerpAntwerpBelgium

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