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Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2014

Open Access 01-12-2014 | Research

Ovulation but not milt production is inhibited in fathead minnows (Pimephales promelas) exposed to a reproductively inhibitory pulp mill effluent

Authors: Andrew Waye, Wudu E Lado, Pierre H Martel, John T Arnason, Vance L Trudeau

Published in: Reproductive Biology and Endocrinology | Issue 1/2014

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Abstract

Background

A 5-day fathead minnow (FHM) spawning assay is used by industry to monitor pulp mill effluent quality, with some mill effluents capable of completely inhibiting spawning. The purpose of this report is to characterize the effect of an inhibitory effluent on egg and milt production in FHM.

Methods

Eight tanks were treated with an inhibitory effluent while eight were kept with clean water. Each tank contained two males and four females as per the 5-day FHM spawning assay used by industry. Females were stripped of ovulated eggs and males of milt in four effluent-exposed and four control tanks. Eggs oviposited in every tank were also counted and checked for fertilization and data analyzed with 2-way ANOVA.

Results

We show that female, but not male, fathead minnow reproductive function is impaired in the 5-day fathead minnow spawning assay used by industry to evaluate pulp mill effluent quality in Canada. Milt production was not changed in the control or exposed males mid-way and at the end of the five day exposure (p > 0.05; n = 8). Total egg production (stripped + oviposited) was impaired (p < 0.05) in fathead minnows exposed to effluent (288 eggs/tank, n = 4 tanks) compared to those in control tanks (753 eggs/tank, n = 4 tanks).

Conclusions

Our results indicate that males are able to detect female signals and prepare appropriately for spawning while in females inhibition of ovulation is occurring somewhere along the hypothalamus-pituitary-gonad reproductive axis. These results suggest female-specific neuroendocrine disruption and provide mechanistic insight into an assay used by industry to assess pulp mill effluent quality.
Appendix
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Literature
1.
Hewitt LM, Parrott JL, McMaster ME: A decade of research on the environmental impacts of pulp and paper mill effluents in Canada: sources and characteristics of bioactive substances. J Toxicol Environ Health B Crit Rev. 2006, 9: 341-356. 10.1080/15287390500195976.CrossRefPubMed
2.
McMaster ME, Hewitt LM, Parrott JL: A decade of research on the environmental impacts of pulp and paper mill effluents in Canada: field studies and mechanistic research. J Toxicol Environ Health B Crit Rev. 2006, 9: 319-339. 10.1080/15287390500195869.CrossRefPubMed
3.
Parrott JL, McMaster ME, Hewitt LM: A decade of research on the environmental impacts of pulp and paper mill effluents in Canada: development and application of fish bioassays. J Toxicol Environ Health B Crit Rev. 2006, 9: 297-317. 10.1080/15287390500195752.CrossRefPubMed
4.
Hewitt LM, Kovacs TG, Dube MG, MacLatchy DL, Martel PH, McMaster ME, Paice MG, Parrott JL, van den Heuvel MR, van der Kraak GJ: Altered reproduction in fish exposed to pulp and paper mill effluents: roles of individual compounds and mill operating conditions. Environ Toxicol and Chem. 2008, 27: 682-697. 10.1897/07-195.1.CrossRef
5.
Kovacs TG, Martel PH, Ricci M: A shortened adult fathead minnow reproduction test developed for investigation of cause and investigation of solution work involving pulp and paper mill effluents. Water Qual Res J Can. 2007, 42: 91-100.
6.
Martel PH, Kovacs TG, O’connor BI, Semeniuk S, Hewitt LM, Maclatchy DL, McMaster ME, Parrott JL, van den Heuvel MR, Van Der Kraak GJ: Effluent monitoring at a bleached kraft mill: Directions for best management practices for eliminating effects on fish reproduction. J Environ Sci Heal A. 2011, 46: 833-843. 10.1080/10934529.2011.579850.CrossRef
7.
Ankley GT, Jensen KM, Kahl MD, Korte JJ, Makynen EA: Description and evaluation of a short-term reproduction test with the fathead minnow (Pimephales promelas). Environ Toxicol Chem. 2001, 20: 1276-1290. 10.1897/1551-5028(2001)020<1276:DAEOAS>2.0.CO;2.CrossRefPubMed
8.
Parrott JL: Overview of methodology and endpoints in fathead minnow lifecycle tests assessing pulp and paper mill effluents. Water Qual Res J C. 2005, 40: 334-346.
9.
Basu N, Ta CA, Waye A, Mao J, Hewitt M, Arnason JT, Trudeau VL: Pulp and paper mill effluents contain neuroactive substances that potentially disrupt neuroendocrine control of fish reproduction. Environ Sci Technol. 2009, 43: 1635-1641. 10.1021/es802552m.CrossRefPubMed
10.
Basu N, Waye A, Trudeau VL, Arnason JT: Extracts from hardwood trees used in commercial paper mills contain biologically active neurochemical disruptors. Sci Total Environ. 2012, 414: 205-209.CrossRefPubMed
11.
Waye A, Trudeau VL: Neuroendocrine disruption: more than hormones are upset. J Toxicol Environ Health B Crit Rev. 2011, 14: 270-291. 10.1080/10937404.2011.578273.PubMedCentralCrossRefPubMed
12.
Waye A, Annal M, Tang A, Picard G, Harnois F, Guerrero-Analco JA, Saleem A, Hewitt LM, Milestone CB, MacLatchy DL, Trudeau VL, Arnason JT: Canadian boreal pulp and paper feedstocks contain neuroactive substances that interact in vitro with GABA and dopaminergic systems in the brain. Sci Total Environ. 2014, 468–469: 315-325.CrossRefPubMed
13.
Milestone CB, Orrego R, Scott PD, Waye A, Kohli J, O'Connor BI, Smith B, Engelhardt H, Servos MR, Maclatchy DL, Smith DS, Trudeau VL, Arnason JT, Kovacs T, Heid Furley T, Slade AH, Holdway DA, Hewitt LM: Evaluating the potential of effluents and wood feedstocks from pulp and paper mills in Brazil, Canada, and New Zealand to affect fish reproduction: chemical profiling and in vitro assessments. Environ Sci Technol. 2012, 46: 1849-1858. 10.1021/es203382c.CrossRefPubMed
14.
Eaton AD, Franson MAH, Association APH, Association AWW, Federation WE: Standard Methods for the Examination of Water & Wastewater. 2005, Washington: American Public Health Association
15.
Voss RH, Rapsomatiotis A: An improved solvent-extraction based procedure for the gas chromatographic analysis of resin and fatty acids in pulp mill effluents. J Chromatogr A. 1985, 346: 205-214.CrossRef
16.
Kovacs TG, Martel PH, O'Connor BI, Hewitt LM, Parrott JL, McMaster ME, MacLatchy DL, Van Der Kraak GJ, Van Den Heuvel MR: A survey of Canadian mechanical pulp and paper mill effluents: Insights concerning the potential to affect fish reproduction. J Environ Sci Heal A. 2013, 48: 1178-1189. 10.1080/10934529.2013.776440.CrossRef
17.
Kovacs TG, Martel PH, O'Connor BI, Parrott JL, McMaster ME, Van Der Kraak GJ, MacLatchy DL, van den Heuvel MR, Hewitt LM: Kraft mill effluent survey: progress toward best management practices for reducing effects on fish reproduction. Environ Toxicol Chem. 2011, 30: 1421-1429. 10.1002/etc.526.CrossRefPubMed
18.
Kovacs T, Martel P, Ricci M, Michaud J, Voss R: Further insights into the potential of pulp and paper mill effluents to affect fish reproduction. J Toxicol Environ Health A. 2005, 68: 1621-1641. 10.1080/15287390590956533.CrossRefPubMed
19.
Peter RE: Neuroendocrine control of reproduction in teleosts. Can J Fish Aquat Sci. 1982, 39: 48-55. 10.1139/f82-007.CrossRef
20.
Popesku JT, Martyniuk CJ, Mennigen J, Xiong H, Zhang D, Xia X, Cossins AR, Trudeau VL: The goldfish (Carassius auratus) as a model for neuroendocrine signaling. Mol Cell Endocrinol. 2008, 293: 43-56. 10.1016/j.mce.2008.06.017.CrossRefPubMed
21.
Trudeau VL: Neuroendocrine regulation of gonadotrophin II release and gonadal growth in the goldfish, Carassius auratus. Rev Reprod. 1997, 2: 55-68. 10.1530/ror.0.0020055.CrossRefPubMed
22.
Dufour S, Sebert ME, Weltzien FA, Rousseau K, Pasqualini C: Neuroendocrine control by dopamine of teleost reproduction. J Fish Biol. 2010, 76: 129-160. 10.1111/j.1095-8649.2009.02499.x.CrossRefPubMed
23.
Peter RE, Chang JP, Nahorniak CS, Omeljaniuk RJ, Sokolowska M, Shih SH, Billard R: Interactions of catecholamines and GnRH in regulation of gonadotropin secretion in teleost fish. Recent Prog Horm Research. 1986, 42: 513-548.
24.
Van Der Kraak GJ, Munkittrick KR, McMaster ME, Portt CB, Chang JP: Exposure to bleached kraft pulp mill effluent disrupts the pituitary-gonadal axis of white sucker at multiple sites. Toxicol Appl Pharm. 1992, 115: 224-233. 10.1016/0041-008X(92)90327-O.CrossRef
25.
Gibbons WN, Munkittrick KR, McMaster ME, Taylor WD: Monitoring aquatic environments receiving industrial effluents using small fish species 2: comparison between responses of trout-perch (Percopsis omiscomaycus) and white sucker (Catostomus commersoni) downstream of a pulp mill. Environ Toxicol Chem. 1998, 17: 2238-2245.
26.
McMaster ME, Van Der Kraak GJ, Munkittrick KR: An epidemiological evaluation of the biochemical basis for steroid hormonal depressions in fish exposed to industrial wastes. J Great Lakes Res. 1996, 22: 153-171. 10.1016/S0380-1330(96)70947-4.CrossRef
27.
van den Heuvel MR, Martel PH, Kovacs TG, MacLatchy DL, Van Der Kraak GJ, Parrott JL, McMaster ME, O’Connor BI, Melvin SD, Hewitt LM: Evaluation of short-term fish reproductive bioassays for predicting effects of a Canadian bleached Kraft mill effluent. Water Qual Res J Can. 2010, 45: 175-186.
28.
Ankley GT, Kahl MD, Jensen KM, Hornung MW, Korte JJ, Makynen EA, Leino RL: Evaluation of the aromatase inhibitor fadrozole in a short-term reproduction assay with the fathead minnow (Pimephales promelas). Toxicol Sci. 2002, 67: 121-130. 10.1093/toxsci/67.1.121.CrossRefPubMed
29.
Villeneuve DL, Blake LS, Brodin JD, Cavallin JE, Durhan EJ, Jensen KM, Kahl MD, Makynen EA, Martinović D, Mueller ND, Ankley GT: Effects of a 3β-hydroxysteroid dehydrogenase inhibitor, trilostane, on the fathead minnow reproductive axis. Toxicol Sci. 2008, 104: 113-123. 10.1093/toxsci/kfn073.CrossRefPubMed
30.
Munkittrick KR, McMaster ME, McCarthy LH, Servos MR, Van Der Kraak GJ: An overview of recent studies on the potential of pulp-mill effluents to alter reproductive parameters in fish. J Toxicol Environ Health B Crit Rev. 1998, 1: 347-371. 10.1080/10937409809524558.CrossRefPubMed
31.
Wartman CA, Hogan NS, Hewitt LM, McMaster ME, Landman MJ, Taylor S, Kovacs TG, van den Heuvel MR: Androgenic effects of a Canadian bleached kraft pulp and paper effluent as assessed using threespine stickleback (Gasterosteus aculeatus). Aquat Toxicol. 2009, 92: 131-139. 10.1016/j.aquatox.2009.02.003.CrossRefPubMed
32.
Linton ED, Scuton DA, McKinley RS: Physiological effects of thermomechanical newsprint mill effluent on Atlantic salmon (Salmo salar L.). Ecotox Environ Safe. 2005, 62: 317-330. 10.1016/j.ecoenv.2004.09.002.CrossRef
33.
Stacey N, Sorensen P: Reproductive pheromones. Fish Physiology. Volume 24. Edited by: Katherine A, Sloman RWW, Sigal B. 2005, Academic Press, 359-412.
34.
Popesku JT, Tan EYZ, Martel PH, Kovacs TG, Rowan-Carroll A, Williams A, Yauk C, Trudeau VL: Gene expression profiling of the fathead minnow (Pimephales promelas) neuroendocrine brain in response to pulp and paper mill effluents. Aquat Toxicol. 2010, 99: 379-388. 10.1016/j.aquatox.2010.05.017.CrossRefPubMed
35.
Liu AC, Tran HG, Zhang EE, Priest AA, Welsh DK, Kay SA: Redundant function of REV-ERBα and β and non-essential role for Bmal1 cycling in transcriptional regulation of intracellular circadian rhythms. PLoS Genet. 2008, 4: e1000023-10.1371/journal.pgen.1000023.PubMedCentralCrossRefPubMed
36.
Clayton JB: Effects of Photoperiod on the Reproductive Success of Fathead Minnows (Pimephales promelas). 1997, Texas Tech University, MSc Thesis
37.
Werner J, Ouellet JD, Cheng CS, Ju Y-J, Law RD: Pulp and paper mill effluents induce distinct gene expression changes linked to androgenic and estrogenic responses in the fathead minnow (Pimephales promelas). Environ Toxicol Chem. 2010, 29: 430-439. 10.1002/etc.48.CrossRefPubMed
Metadata
Title
Ovulation but not milt production is inhibited in fathead minnows (Pimephales promelas) exposed to a reproductively inhibitory pulp mill effluent
Authors
Andrew Waye
Wudu E Lado
Pierre H Martel
John T Arnason
Vance L Trudeau
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2014
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-12-43

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