Combined effects of high temperature and pesticide mixture exposure on free-swimming behaviors and hepatic cytochrome P450 1A expression in goldfish, Carassius auratus

ABSTRACT

The synergy between multiple compounds and other stressors, including heat, creates volatility and greater unpredictability than standard single-chemical toxicity testing, especially in the case of pesticides and metabolites which might contain several noxious ingredients resulting in adverse ecological effects. To address this, the aim of this study was to examine the dose- and time-dependent effects of low- and high-dose pesticide mixture (metalachlor, linuron, isoproturon, tebucanazole, aclonifen, atrazine, pendimethalin, azinphos-methyl) and heat stress co-exposure (22°C control/32°C treatment for 4-week) on free-swimming behaviors and cumulative actionless time (CAT) of goldfish. Behavioral analysis showed a dose- and time-dependent decrease in distance swam, as well as a subsequent increase in CAT. Vertical and horizontal spatial behavioral use were affected under heat and pesticides co-exposure conditions. In 3- and 4-week(s) exposure groups, horizontal spatial behavioral use demonstrated elevated time spent in the lower third of the aquarium. Similarly, during 3- and 4-week(s) exposure (32°C control and 32°C high doses) vertical spatial behavioral use was found to increase time spent in the outermost edges of the aquarium. In all treatment groups, the final condition factor (KM) showed significant attenuation when compared to the initial KM. However, there was an unclear relationship between heat/pesticide co-exposure and growth most notably in 32°C high-dose groups. In addition, the expression of hepatic cytochrome P450 1A mRNA was significantly higher in pesticide-exposed groups. Taken together, data demonstrated that co-exposure with low- or high-dose pesticide mixture and heat stress significantly impacted natural swimming patterns, which over time might result in the broader population and ecological effects.

KEYWORDS:

• Environmental pollutants
• global warming
• fish behavior
• cytochrome P450 1A

Acknowledgments

The authors are grateful to Johana Castro, Luis Uribe, Jordan Wolfkill, Abigail Pozulp, and Brandon Escareno for their advice and commentary on the behavioral and statistical methods, and revision of the manuscript. Biological illustrations were created by author Michelle Rivera.

We would like to thank and appreciate Dr. Sam Kacew, Editor-in-Chief, Journal of Toxicology and Environmental Health, and four anonymous reviewers for providing valuable suggestions, constructive comments, and revisions on our manuscript.

Disclosure statement

No potential conflict of interest was reported by the authors.

Authors contributions and consent of participations

Md Saydur Rahman supervised the research. Brittney Lacy conducted laboratory studies. Brittney Lacy, Michelle Rivera, and Leinady Flores collected data. Brittney Lacy and Md Saydur Rahman analyzed data. Brittney Lacy, Michelle Rivera, Leinady Flores, and Md Saydur Rahman designed the figures. Brittney Lacy drafted the manuscript. Brittney Lacy, Michelle Rivera, Leinady Flores, and Md Saydur Rahman edited and reviewed the manuscript.

Availability of data

All relevant data are within the paper and available from the corresponding author upon request.

Consent to publish

All the authors have read and approved the publication of the final version of the manuscript.

Ethics statement

All animal husbandry practices, laboratory experimental procedures, and euthanasia protocols were developed in consultation with UTRGV’s veterinarian and approved by the UTRGV Institutional Animal Care and Use Committee.

Additional information

Funding

This study was funded in part by the start-up fund and University of Texas Rio Grandy Valley (UTRGV) College of Science SEED grant (grant no. 210000371) to Md Saydur Rahman, and the UTRGV Presidential Graduate Research Assistantship (PGRA) to Brittney Lacy.