Exposure to carbamate fungicide iodocarb does not affect reproductive behavior or milt volumes in precocious male brown trout (Salmo trutta L.) parr.

K Håkan Olsén, Hanna L Olsén
Author Information
  1. K Håkan Olsén: School of Natural Science, Technology and Environmental Studies, Södertörn University, SE-141 89, Huddinge, Sweden. hakan.olsen@sh.se.
  2. Hanna L Olsén: School of Natural Science, Technology and Environmental Studies, Södertörn University, SE-141 89, Huddinge, Sweden.

Abstract

Previous studies with olfactory-disturbing pesticides resulted after exposure in disturbed behavior and physiology in fish. In the present experiment, reproductive behavior and milt volumes of precocious brown trout (Salmo trutta L.) male parr were studied in a large stream aquarium after exposure to the olfactory-disturbing fungicide 15 μg l IPBC (iodocarb; 3-iodo-2-propynyl butyl carbamate) for 96 h. The statistical analyses did not reveal any significant differences for time attending females between controls and IPBC-exposed males. Furthermore, there were no significant differences in milt volumes. However, when taking all fish into consideration, there were significant differences in milt volumes between parr that had been attending females and those had not been attending females. Controls that had attended females had significantly higher milt volumes than controls or IPBC-exposed males that had not attended females. Taking all control and IPBC parr into consideration, there was a statistically significant positive correlation between time attended females and volume of milt and gonadosomatic index (GSI), respectively. In summary, 15 μg l IPBC did not have any significant effects on mature male parr reproductive behavior and milt volumes.

Keywords

References

  1. Bailey HC, Elphick JR, Potter A, Chao E, Zak B (1999) Acute toxicity of the antisapstain chemicals DDAC and IPBC, alone and in combination to rainbow trout (Oncorhynchus mykiss). Water Res 1:4210–2414
  2. Bjerselius R, Winberg S, Winberg Y, Zeipel K (1993) Ca protects olfactory receptor function against acute Cu (II) toxicity in Atlantic salmon. Aquat Toxicol 25:125–138
  3. Brown SB, Evans RE, Thompson BE, Hara TJ (1982) Chemoreception and aquatic pollutants. In: Hara TJ (ed) Chemoreception in fishes. Development in Aquaculture and Fisheries Science, vol. 8. Amsterdam, Oxford, New York, Elsevier, pp 363–394
  4. Canadian Council of Ministries of the Environment (1999) Canadian water quaility guidelines for the protection of aquatic life. IPBC. In: Canadian environmental guidelines, 1999, Canadian Council of Ministers of the Environment Winnipeg, pp 1–3
  5. Carbajo JB, Perdigon-Melon JA, Petre AL, Rosal R, Leton P, Garcia-Calvo E (2015) Personal care product preservatives: risk assessment and mixture toxicities with an industrial wastewater. Water Res 72:174–185 [PMID: 25585550]
  6. Dew WA, Azizishirazi A, Pyle GG (2014) Contaminant-specific targeting of olfactory sensory neuron classes: connecting neuron class impairment with behavioural deficits. Chemosphere 112:519–525 [PMID: 24630454]
  7. Farrell AP, Stockner E, Kennedy CJ (1998) A study of the lethal and sublethal toxicity of polyphase P-100, an antisapstain fungicide containing 3-iodo-2-propynyl butyl carbamate (IPBC), on fish and aquatic invertebrates. Arch Environ Contam Toxicol 35:472–478 [PMID: 9732479]
  8. Fulton MH, Key PB, DeLorenzo ME (2014) Insecticide toxicity in fish. In: Tierney KH, Farrell AP, Brauner CJ (eds) Organic chemical toxicology of fishes. Academic Press, London, UK, Waltham, MA, USA, San Diego, CA, USA, pp 309–368
  9. Gupta RC (1994) Carbofuran toxicity. Review article. J Toxicol Environ Health 43:483–418
  10. Hamdani EH, Døving KB (2006) Specific projection of the sensory crypt cells in the olfactory system in crucian carp, Carassius carassius. Chem Senses 31:63–67
  11. Hansen A, Rolen SH, Anderson K, Morita Y, Caprio J, Finger TE (2003) Correlation between olfactory receptor cell type and function in the channel catfish. J Neurosci 23:9328–9339 [PMID: 14561860]
  12. Hara TJ, Zhang C (1996) Spatial projections to the olfactory bulb of functionally distinct and randomly distributed primary neurons in salmonid fishes. Neurosci Res 26:65–74
  13. Hara TJ, Zhang C (1998) Topographic bulbar projections and dual neural pathways of the primary olfactory neurons in salmonid fishes. Neuroscience 82:301–313 [PMID: 9483522]
  14. Hellström G, Prestegaard T, Dannewitz J, Olsén KH (2012) Sperm from pheromone primed brown trout (Salmo trutta L.) produce more larvae. Fish Physiol Biochem 39:471–478 [PMID: 22976196]
  15. Hessel K, Kreuger J, Ulén B (1997) Kartläggning av bekämpningsmedelrester i yt-, grund- och regnvatten i Sverige 1985–1995. Resultat från monotoring och riktad provtagning. Division of Water Quality Management, Swedish University of Agricultural Sciences. Res Rep Ekohydrol 42:1–72 (In Swedish)
  16. Jaensson A, Olsén KH (2010) Effects of copper on olfactory mediated endocrine responses and reproductive behavior in mature male brown trout (Salmo trutta Linneaus) parr to conspecific females. J Fish Biol 76:800–817
  17. Jaensson A, Scott AP, Moore A, Kylin H, Olsén KH (2007) Effects of pyrethroid pesticide on endocrine responses to female odours and reproductive behaviour in male parr brown trout (Salmo trutta L.). Aquat Toxicol 81:1–9 [PMID: 17174415]
  18. Jarrard HE, Delaney KR, Kennedy CJ (2004) Impacts of carbamate pesticides on olfactory neurophysiology and cholinesterase activity in coho salmon (Oncorhynchus kisutch). Aquat Toxicol 69:133–148 [PMID: 15261450]
  19. Juergensen L, Busnarda J, Caux P-Y, Kent R (2000) Fate, behavior, and aquatic toxicity of the fungicide IPBC in the Canadian environment. Environ Toxicol 15:201–213
  20. Laberge F, Hara TJ (2003) Behavioural and electrophysiological responses to F-prostaglandins, putative spawning pheromones, in three salmonid fishes. J Fish Biol 62:206–221
  21. Laberge F, Hara TJ (2004) Electrophysiological demonstration of independent olfactory receptor types and associated neuronal responses in the trout olfactory bulb. Comp Biochem Physiol A 137:397–408
  22. Lari E, Razmara P, Bogart SJ, Azizishirazi A, Pyle GG (2019) An epithelium is not just an epithelium: effects of Na, Cl, and pH on olfaction and/or copper-induced olfactory deficits. Chemosphere 216:117–123 [PMID: 30366265]
  23. Lastein S, Hamdani EH, Døving KB (2006) Gender distinction in neural discrimination of sex pheromones in the olfactory bulb of crucian carp, Carassius carassius. Chem Senses 31:69–77 [PMID: 16322086]
  24. Liley NR, Olsén KH, Foote CJ, Van Der Kraak GJ (1993) Endocrine changes associated with spawning behavior in male kokanee salmon (Oncorhynchus nerka) and the effects of anosmia. Horm Behav 27:470–487 [PMID: 8294117]
  25. Miura T, Yamauchi K, Takahashi H, Nagahama Y (1992) The rule of hormones in the acquisition of sperm motility in salmonid fish. J Exp Zool 107:95–103
  26. Moore A, Waring CP (1996) Sublethal effects of the pesticide diazinon on olfactory function in mature male Atlantic salmon parr. J Fish Biol 48:758–775
  27. Moore A, Waring CP (1999) Reproductive priming in mature male Atlantic salmon parr exposed to the sound of redd cutting. J Fish Biol 55:884–887
  28. Moore A, Waring CP (2001) The effects of a synthetic pyrethroid pesticide on some aspects of reproduction in Atlantic salmon (Salmo salar L.). Aquat Toxicol 52:1–12 [PMID: 11163426]
  29. Moore A, Olsén KH, Lower N, Kindahl H (2002) The role of F-series prostaglandins as reproductive priming pheromones in the brown trout. J Fish Biol 60:613–624
  30. Moran DT, Rowley JC, Aiken GR, Jafek BW (1991) Ultrastructural neurobiology of the olfactory mucosa of the brown trout (Salmo trutta). Microsc Res Tech 23:28–48
  31. Newcombe CP, Hartman GF (1980) Visual signals in the spawning behaviour of rainbow trout. Can J Zool 58:1751–1757
  32. Olsén, K.H. 2011. Effects of pesticides and other pollutants on olfactory mediated behaviors in fish and crustaceans. In: Chemical communication in crustaceans pp. 507–529. Edited by Breithaupt T. and Thiel M. New York: Springer Verlag
  33. Olsén, K.H. 2015. Effects of pollutants on olfactory detection and responses to chemical cues including pheromones in fish. In: Fish pheromones and related cues pp. 217–236. Edited by Sorensen P. and Wisenden B. NJ, USA: John Wiley & Sons Inc.
  34. Olsén KH, Liley NR (1993) The significance of olfaction and social cues in milt availability, sexual hormone status and spawning behaviour of male rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 89:107–118 [PMID: 8428642]
  35. Olsén KH, Järvi T, Mayer I, Petterson E, Kroon F (1998) Spawning behaviour and sex hormone levels in adult and precocious brown trout (Salmo trutta L.) males and the effect of anosmia. Chemoecology 8:9–17
  36. Razmara P, Lari E, Mohaddes E, Zhang Y, Goss GG, Pyle GG (2019) The effect of copper nanoparticles on olfaction in rainbow trout (Oncorhynchus mykiss). Environ Sci: Nano. https://doi.org/10.1039/c9en00360f
  37. Saglio P, Trijasse S, Azam D (1996) Behavioral effects of waterborne carbofuran in goldfish. Arch Environ Contam Toxicol 31:232–238 [PMID: 8781074]
  38. Saglio P, Bretaud S, Rivot E, Olsén KH (2003) Chemobehavioral changes induced by short-term exposures to prochloraz, nicosulfuron and carbofuran in goldfish. Arch Environ Contam Toxicol 45:515–524 [PMID: 14708668]
  39. Sandahl JF, Baldwin DH, Jenkins JJ, Scholz NL (2004) Odor-evoked field potentials as indicators of sublethal neurotoxicity in juvenile coho salmon (Oncorhynchus kisutch) exposed to copper, chlorpyrifos, or esfenvalerate. Can J Fish Aquat Sci 61:404–413
  40. Satou M, Takeuchi H, Takei K, Hasegawa T, Okumoto N, Ueda K (1987) Involvement of vibrational and visual cues in eliciting spawning behaviour in male Hime salmon (landlocked red salmon, Oncorhynchus nerka). Anim Behav 35:1556–1558
  41. Scott AP, Sumpter JP, Stacey N (2010) The role of the maturation-inducing steroid, 17,20β-dihydroxypregn-4-en-3-one, in male fishes: a review. J Fish Biol 76:183–224 [PMID: 20738705]
  42. Solomon KR, Dalhoff K, Volz D, Van Der Kraak G (2014) Effects of herbicides in fish. In: Tierney KH, Farrell AP, Brauner CJ (eds) Organic chemical toxicology of fishes. academic press, London, UK, Waltham, MA, USA, San Diego, CA, USA, pp 369–409
  43. Tierney, K. B., Ross, P. S., Jarrard, H.E., Delaney, K. R. and Kennedy, C. J. 2006a a. Changes in juvenile coho salmon electro-olfactogram during and after short-term exposure to current-use pesticides. Environ Toxicol Chem 25: 2809–2817
  44. Tierney KB, Taylor AL, Ross PS, Kennedy CJ (2006b) The alarm reaction of coho salmon parr is impaired by the carbamate fungicide IPBC. Aquat Toxicol 79:149–157 [PMID: 16854476]
  45. Tierney KB, Singh CR, Ross PS, Kennedy CJ (2007) Relating olfactory neurotoxicity to altered olfactory-mediated behaviors in rainbow trout exposed to three currently-used pesticides. Aquat Toxicol 81:55–64 [PMID: 17145086]
  46. Thommesen G (1983) Morphology, distribution and specificity of olfactory receptor cells in salmonid fishes. Acta Physiologica Scandinavica 117:241–249
  47. Tjus SE (2014) 3-Jod-2-propynylbutylkarbamat (IPBC). In: Biociders spridning i miljön och deras hälso- och miljörisker. Screening 2000-2003. Swedish Environment Protection Agency Report 6634, pp 81–86
  48. Waring CP, Moore A (1997) Sublethal effects of a carbamate pesticide on pheromonal mediated endocrine function in mature Atlantic salmon (Salmo salar L.) parr. Fish Physiol Biochem 17:203–211
  49. Zhang C, Hara TJ (2009) Lake char (Salvelinus namayacush) olfactory neurons are highly sensitive and specific to bile acids. J Comp Physiol A 195:203–215
  50. Zheng W, Strobeck C, Stacey NE (1997) The steroid pheromone 17α,20β-dihydroxy-4-pregnen-3-one increases fertility and paternity in goldfish. J Exp Biol 200:2833–2840 [PMID: 9344969]

Grants

  1. 87/03/the Foundation for Baltic and Eastern European Studies (Östersjöstiftelsen).

MeSH Term

Analysis of Variance
Animals
Antifungal Agents
Carbamates
Female
Male
Random Allocation
Sexual Behavior, Animal
Statistics, Nonparametric
Trout

Chemicals

Antifungal Agents
Carbamates
3-iodo-2-propynylbutylcarbamate

Word Cloud

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