Context-specific behavioural changes induced by exposure to an androgenic endocrine disruptor

Michael G. Bertram, Jake M. Martin, Minna Saaristo, Tiarne E. Ecker, Marcus Michelangeli, Nicholas D.S. Deal, Shu Ly Lim, Moira K. O'Bryan, Bob B.M. Wong

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Pharmaceutical contaminants are being detected with increased frequency in organisms and ecosystems worldwide. This represents a major environmental concern given that various pharmaceuticals act on drug targets that are evolutionarily conserved across diverse taxa, are often persistent in the environment, and can bioconcentrate in organisms and bioaccumulate in food chains. Despite this, relatively little is known about the potential for pharmaceutical contaminants to affect animal behaviour, especially across multiple fitness-related contexts. Here, we investigated impacts of 21-day exposure of wild-caught male eastern mosquitofish (Gambusia holbrooki) to a field-realistic level of the veterinary pharmaceutical 17β-trenbolone—a growth-promoting steroid used extensively in beef production worldwide and a potent androgenic endocrine disruptor repeatedly detected in surface waters affected by livestock effluent run-off. First, we examined male boldness, activity, and exploratory behaviour in a novel environment (maze arena) and found no significant effect of 17β-trenbolone exposure. Second, the same males were tested in a reproductive assay for their tendency to associate with a stimulus (unexposed) female behind a partition. Exposed males exhibited reduced association behaviour, taking longer to first associate with, and spending less time within close proximity to, a female. Third, all males were assayed for sperm function (computer-assisted sperm analysis, sperm viability) or quantity (total sperm count) and, although no significant main effects of 17β-trenbolone were seen on sperm traits, exposure altered the relationship between male morphology and sperm function. Lastly, morphological traits were assessed and exposed males were found to have, on average, increased mass relative to length. In combination, these results demonstrate that exposure to a field-realistic level of 17β-trenbolone can produce subtle but important trait alterations in male fish—including context-specific behavioural changes, disruption of key sperm function trade-offs, and altered morphology—with potential impacts on exposed wildlife.

Original languageEnglish
Pages (from-to)177-187
Number of pages11
JournalScience of the Total Environment
Volume664
DOIs
Publication statusPublished - 10 May 2019

Keywords

  • Androgen
  • Endocrine disrupting chemical
  • Hormonal growth promotant
  • Pharmaceutical pollution
  • Sperm
  • Trenbolone

Cite this

Bertram, Michael G. ; Martin, Jake M. ; Saaristo, Minna ; Ecker, Tiarne E. ; Michelangeli, Marcus ; Deal, Nicholas D.S. ; Lim, Shu Ly ; O'Bryan, Moira K. ; Wong, Bob B.M. / Context-specific behavioural changes induced by exposure to an androgenic endocrine disruptor. In: Science of the Total Environment. 2019 ; Vol. 664. pp. 177-187.
@article{c355ba8dc5eb47f1b650958a1b5d2838,
title = "Context-specific behavioural changes induced by exposure to an androgenic endocrine disruptor",
abstract = "Pharmaceutical contaminants are being detected with increased frequency in organisms and ecosystems worldwide. This represents a major environmental concern given that various pharmaceuticals act on drug targets that are evolutionarily conserved across diverse taxa, are often persistent in the environment, and can bioconcentrate in organisms and bioaccumulate in food chains. Despite this, relatively little is known about the potential for pharmaceutical contaminants to affect animal behaviour, especially across multiple fitness-related contexts. Here, we investigated impacts of 21-day exposure of wild-caught male eastern mosquitofish (Gambusia holbrooki) to a field-realistic level of the veterinary pharmaceutical 17β-trenbolone—a growth-promoting steroid used extensively in beef production worldwide and a potent androgenic endocrine disruptor repeatedly detected in surface waters affected by livestock effluent run-off. First, we examined male boldness, activity, and exploratory behaviour in a novel environment (maze arena) and found no significant effect of 17β-trenbolone exposure. Second, the same males were tested in a reproductive assay for their tendency to associate with a stimulus (unexposed) female behind a partition. Exposed males exhibited reduced association behaviour, taking longer to first associate with, and spending less time within close proximity to, a female. Third, all males were assayed for sperm function (computer-assisted sperm analysis, sperm viability) or quantity (total sperm count) and, although no significant main effects of 17β-trenbolone were seen on sperm traits, exposure altered the relationship between male morphology and sperm function. Lastly, morphological traits were assessed and exposed males were found to have, on average, increased mass relative to length. In combination, these results demonstrate that exposure to a field-realistic level of 17β-trenbolone can produce subtle but important trait alterations in male fish—including context-specific behavioural changes, disruption of key sperm function trade-offs, and altered morphology—with potential impacts on exposed wildlife.",
keywords = "Androgen, Endocrine disrupting chemical, Hormonal growth promotant, Pharmaceutical pollution, Sperm, Trenbolone",
author = "Bertram, {Michael G.} and Martin, {Jake M.} and Minna Saaristo and Ecker, {Tiarne E.} and Marcus Michelangeli and Deal, {Nicholas D.S.} and Lim, {Shu Ly} and O'Bryan, {Moira K.} and Wong, {Bob B.M.}",
year = "2019",
month = "5",
day = "10",
doi = "10.1016/j.scitotenv.2019.01.382",
language = "English",
volume = "664",
pages = "177--187",
journal = "Science of the Total Environment",
issn = "0048-9697",
publisher = "Elsevier",

}

Context-specific behavioural changes induced by exposure to an androgenic endocrine disruptor. / Bertram, Michael G.; Martin, Jake M.; Saaristo, Minna; Ecker, Tiarne E.; Michelangeli, Marcus; Deal, Nicholas D.S.; Lim, Shu Ly; O'Bryan, Moira K.; Wong, Bob B.M.

In: Science of the Total Environment, Vol. 664, 10.05.2019, p. 177-187.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Context-specific behavioural changes induced by exposure to an androgenic endocrine disruptor

AU - Bertram, Michael G.

AU - Martin, Jake M.

AU - Saaristo, Minna

AU - Ecker, Tiarne E.

AU - Michelangeli, Marcus

AU - Deal, Nicholas D.S.

AU - Lim, Shu Ly

AU - O'Bryan, Moira K.

AU - Wong, Bob B.M.

PY - 2019/5/10

Y1 - 2019/5/10

N2 - Pharmaceutical contaminants are being detected with increased frequency in organisms and ecosystems worldwide. This represents a major environmental concern given that various pharmaceuticals act on drug targets that are evolutionarily conserved across diverse taxa, are often persistent in the environment, and can bioconcentrate in organisms and bioaccumulate in food chains. Despite this, relatively little is known about the potential for pharmaceutical contaminants to affect animal behaviour, especially across multiple fitness-related contexts. Here, we investigated impacts of 21-day exposure of wild-caught male eastern mosquitofish (Gambusia holbrooki) to a field-realistic level of the veterinary pharmaceutical 17β-trenbolone—a growth-promoting steroid used extensively in beef production worldwide and a potent androgenic endocrine disruptor repeatedly detected in surface waters affected by livestock effluent run-off. First, we examined male boldness, activity, and exploratory behaviour in a novel environment (maze arena) and found no significant effect of 17β-trenbolone exposure. Second, the same males were tested in a reproductive assay for their tendency to associate with a stimulus (unexposed) female behind a partition. Exposed males exhibited reduced association behaviour, taking longer to first associate with, and spending less time within close proximity to, a female. Third, all males were assayed for sperm function (computer-assisted sperm analysis, sperm viability) or quantity (total sperm count) and, although no significant main effects of 17β-trenbolone were seen on sperm traits, exposure altered the relationship between male morphology and sperm function. Lastly, morphological traits were assessed and exposed males were found to have, on average, increased mass relative to length. In combination, these results demonstrate that exposure to a field-realistic level of 17β-trenbolone can produce subtle but important trait alterations in male fish—including context-specific behavioural changes, disruption of key sperm function trade-offs, and altered morphology—with potential impacts on exposed wildlife.

AB - Pharmaceutical contaminants are being detected with increased frequency in organisms and ecosystems worldwide. This represents a major environmental concern given that various pharmaceuticals act on drug targets that are evolutionarily conserved across diverse taxa, are often persistent in the environment, and can bioconcentrate in organisms and bioaccumulate in food chains. Despite this, relatively little is known about the potential for pharmaceutical contaminants to affect animal behaviour, especially across multiple fitness-related contexts. Here, we investigated impacts of 21-day exposure of wild-caught male eastern mosquitofish (Gambusia holbrooki) to a field-realistic level of the veterinary pharmaceutical 17β-trenbolone—a growth-promoting steroid used extensively in beef production worldwide and a potent androgenic endocrine disruptor repeatedly detected in surface waters affected by livestock effluent run-off. First, we examined male boldness, activity, and exploratory behaviour in a novel environment (maze arena) and found no significant effect of 17β-trenbolone exposure. Second, the same males were tested in a reproductive assay for their tendency to associate with a stimulus (unexposed) female behind a partition. Exposed males exhibited reduced association behaviour, taking longer to first associate with, and spending less time within close proximity to, a female. Third, all males were assayed for sperm function (computer-assisted sperm analysis, sperm viability) or quantity (total sperm count) and, although no significant main effects of 17β-trenbolone were seen on sperm traits, exposure altered the relationship between male morphology and sperm function. Lastly, morphological traits were assessed and exposed males were found to have, on average, increased mass relative to length. In combination, these results demonstrate that exposure to a field-realistic level of 17β-trenbolone can produce subtle but important trait alterations in male fish—including context-specific behavioural changes, disruption of key sperm function trade-offs, and altered morphology—with potential impacts on exposed wildlife.

KW - Androgen

KW - Endocrine disrupting chemical

KW - Hormonal growth promotant

KW - Pharmaceutical pollution

KW - Sperm

KW - Trenbolone

UR - http://www.scopus.com/inward/record.url?scp=85061320661&partnerID=8YFLogxK

U2 - 10.1016/j.scitotenv.2019.01.382

DO - 10.1016/j.scitotenv.2019.01.382

M3 - Article

VL - 664

SP - 177

EP - 187

JO - Science of the Total Environment

JF - Science of the Total Environment

SN - 0048-9697

ER -