Chemical communication in wood frog (Rana sylvatica) tadpoles is influenced by early-life exposure to naphthenic acid fraction compounds

Chris K Elvidge; Chloe E Robinson; Rowena A Caza; L Mark Hewitt; Richard A Frank; Diane M Orihel

doi:10.1016/j.aquatox.2023.106435

Chemical communication in wood frog (Rana sylvatica) tadpoles is influenced by early-life exposure to naphthenic acid fraction compounds

Aquat Toxicol. 2023 Apr:257:106435. doi: 10.1016/j.aquatox.2023.106435. Epub 2023 Feb 18.

Authors

Chris K Elvidge¹, Chloe E Robinson², Rowena A Caza², L Mark Hewitt³, Richard A Frank³, Diane M Orihel⁴

Affiliations

¹ Department of Biology, Queen's University, 116 Barrie Street, Kingston, ON K7L 3N6, Canada. Electronic address: chris.k.elvidge@gmail.com.
² Department of Biology, Queen's University, 116 Barrie Street, Kingston, ON K7L 3N6, Canada.
³ Water Science and Technology Directorate, Environment and Climate Change Canada, Burlington, ON L7S 1A1, Canada.
⁴ Department of Biology, Queen's University, 116 Barrie Street, Kingston, ON K7L 3N6, Canada; School of Environmental Studies, Queen's University, 116 Barrie Street, Kingston, ON K7L 3N6, Canada.

PMID: 36889125
DOI: 10.1016/j.aquatox.2023.106435

Abstract

Environmental pollutants can disrupt chemical communication between aquatic organisms by interfering with the production, transmission, and/or detection of, as well as responses to, chemical cues. Here, we test the hypothesis that early-life exposure to naphthenic acid fraction compounds (NAFCs) from oil sands tailings disrupts antipredator-associated chemical communication in larval amphibians. Wild adult wood frogs (Rana sylvatica) captured during their natural breeding period were combined (1 female:2 males) in six replicate mesocosms filled with either uncontaminated lakewater or with NAFCs isolated from an active tailings pond in Alberta, Canada, at nominal 5 mg/L concentrations. Egg clutches were incubated and tadpoles maintained in their respective mesocosms for ∼40 days post-hatch. Tadpoles (Gosner stage 25-31) were then transferred individually to trial arenas filled with uncontaminated water and exposed to one of six chemical alarm cue (AC) stimuli solutions following a 3 × 2 × 2 design (3 AC types × 2 stimulus carriers × 2 rearing exposure groups). Relative to control tadpoles, NAFC-exposed tadpoles demonstrated higher baseline activity levels (line crosses and direction changes) when introduced to uncontaminated water. Antipredator responses differed in graded fashion with AC type, with control ACs eliciting the greatest latency to resume activity, water the least, and NAFC-exposed ACs intermediate. Pre- to post-stimulus difference scores were non-significant in control tadpoles, while NAFC-exposed tadpoles demonstrated significantly greater variation. While this suggests that exposure to NAFCs from fertilization through hatching may have interfered with AC production, it is unclear whether the quality or quantity of cues was affected. There was also no clear evidence that NAFC carrier water interfered with ACs or the alarm response in unexposed control tadpoles. These results emphasize the importance of understanding how behavioral and physiological effects of early-life NAFC exposure on critical antipredator responses may persist across life history stages.

Keywords: Antipredator behavior; Damage-released chemical alarm cues; NAFCs; Oil sands process-affected water (OSPW); Semiochemicals; Tailings ponds.

MeSH terms

Alberta
Animals
Communication
Female
Larva
Oil and Gas Fields*
Ranidae
Water / chemistry
Water Pollutants, Chemical* / toxicity

Substances

naphthenic acid
Water Pollutants, Chemical
Water