Do microplastics impair male dominance interactions in fish? A test of the vector hypothesis

Abstract

Microplastics (MPs) are widespread in aquatic environments and have become a critical environmental issue in recent years due to their adverse impacts on the physiology, reproduction, and survival of aquatic animals. Exposure to MPs also has the potential to induce sub‐lethal behavioral changes that can affect individual fitness, but these effects are understudied. Many plastic additives introduced during the manufacture of MPs are known endocrine‐disrupting chemicals (EDCs) that mimic the action of natural hormones, alter sexual and competitive behavior, and impair reproductive success in fish. In addition, EDCs and other aquatic contaminants may adhere to MPs in the environment, the latter of which may serve as transport vectors for these compounds (i.e., the vector hypothesis). In this study, we staged territorial contests between control males, and males exposed to virgin MP particles or to MPs previously immersed in one of two environmentally relevant concentrations of 17‐alpha ethinyl estradiol (EE2; 5 ng/L and 25 ng/L) to evaluate the independent and synergistic effects of exposure to MPs and a common environmental estrogen on male–male aggression and competitive territory acquisition in a freshwater fish, Pimephales promelas. Short‐term (30 days) dietary exposure to MPs did not impair the ability of males to successfully compete for and obtain a breeding territory. Overall levels of aggression in control and exposed males were also similar across trial series. These results help to fill a critical knowledge gap regarding the direct and indirect (vector‐borne) effects of MPs on the reproductive behavior of aquatic vertebrates in freshwater systems.

Independent and synergistic effects of microplastics and endocrine‐disrupting chemicals on the reproductive social behavior of fathead minnows (Pimephales promelas)

“…Similar results were recently reported by Swank et al. ( 2022 ), who found that exposure to MPs did not influence male aggression in P. promelas , or the ability of exposed males to compete for and acquire a territory. However, other studies have reported changes in other behaviors associated with MP exposure, including the suppression of shoaling in zebrafish ( Danio rerio ) and medaka ( Oryzias latipes ; Santos et al., 2022 ; Takai et al., 2022 ), increases in boldness in gilt‐head bream ( Sparus aurata ; Rios‐Fuster et al., 2021 ) and decreases in gastropod antipredator responses (Seuront, 2018 ).…”

“…Methods for the preparation of exposure treatments and exposure protocol followed Swank et al. ( 2022 ). This project used clear polyethylene microspheres (300–350 μm, Cospheric).…”

“…The fish underwent twice‐daily exposures following an established dietary feeding protocol (Swank et al., 2022 ). Exposures were separated by at least 7 h to ensure motivation to forage.…”

“…Such changes in behavior following exposure to contaminants can translate into population and community declines (Kidd et al., 2007 , 2014 ; Rearick et al., 2018 ). In addition, little is known about the independent and synergistic impacts of MPs and other environmental stressors on individuals, populations, and communities (Swank et al., 2022 ). For example, growing evidence suggests that the hydrophobic nature and large surface area of MP particles allows for organic contaminants, heavy metals, endocrine‐disrupting chemicals (EDCs), and microbiota to sorb to the surface of the particles (Caruso, 2019 ; Wang, Ge, & Yu, 2019 ), which then act as an additional vector of exposure for these compounds (Wang, Ge, & Yu, 2019 ; Wu et al., 2016 ).…”

Behavioral Studies of Zebrafish Reveal a New Perspective on the Reproductive Toxicity of Micro- and Nanoplastics

“…Territorial acquisition by males is also crucial for mating. MNPs can mimic natural hormones, reducing circulating androgen levels in male fish and thereby diminishing aggression and competitive behavior, which are essential for successful spawning [ 70 ]. A decrease in courtship behavior or reduced pairing success can indicate an impaired reproductive capacity in zebrafish.…”