Signaling in a Polluted World: Oxidative Stress as an Overlooked Mechanism Linking Contaminants to Animal Communication

Abstract

The capacity to communicate effectively with other individuals plays a critical role in the daily life of an individual and can have important fitness consequences. Animals rely on a number of visual and non-visual signals, whose production brings costs to the individual. The theory of honest signaling states that these costs are higher for low than for high-quality individuals, which prevents cheating and makes signals, such as skin and plumage coloration, indicators of individual's quality or condition. The condition-dependent nature of signals makes them ideally suited as indicators of environmental quality, implying that signal production might be affected by contaminants. In this mini-review article, we have made the point that oxidative stress (OS) is one overlooked mechanism linking exposure to contaminants to signaling because (i) many contaminants can influence the individual's oxidative balance, and (ii) generation of both visual and non-visual signals is sensitive to OS. To this end, we have provided the first comprehensive review on the way both non-organic (heavy metals, especially mercury) and organic [persistent organic pollutants (POPs)] contaminants may influence either OS or sexual signaling. We have also paid special attention to emerging classes of pollutants like brominated flame-retardants (BFRs) and perfluoroalkoxy alkanes (PFAs) in order to stimulate research in this area. We have finally provided suggestions and warnings for future work on the links among OS, sexual signaling, and contaminant exposure.

The potential utility of carotenoid‐based coloration as a biomonitor of environmental change

“…Pollution is known to impair habitat quality and is a common threat to wildlife biodiversity. Its impact on the expression of carotenoid displays in many species of bird and fish has been thoroughly reviewed, and the potential for carotenoid‐based coloration to be used for visual condition assessments evoked (Lifshitz & St Clair 2016, Marasco & Costantini 2016, Pacyna et al . 2018).…”

“…One of the main mechanisms by which pollution interferes with signalling is oxidative stress (Marasco & Costantini 2016;Fig. 1).…”

“…Both non‐organic and organic pollutants have the ability to increase oxidative stress in contaminated individuals by inducing the generation of new free radicals or via depletion of antioxidants (e.g. via oxidation of non‐protein and protein thiols) (Marasco & Costantini 2016). For example, experimental exposure to PCBs in American Kestrels Falco sparverius affected coloration in exposed parents and their offspring (Bortolotti et al .…”

Melanin-based coloration and host–parasite interactions under global change

“…In addition, melanin-based coloration and resistance to oxidative stress are tightly linked [51,52,81]. More generally, recent studies outline the increasing role of pollutants and oxidative stress in the signalling role of animal coloration [82]. Alternatively, darker morphs could be at a disadvantage compared with paler ones when food is scarce, because the former have a higher metabolic rate and higher energetic requirements [8].…”

Dietary intake of Deepwater Horizon oil-injected live food fish by double-crested cormorants resulted in oxidative stress

“…The concentration of antioxidants and antioxidant enzymes in the body are indicators of the amount of oxidative stress in the body (Koivula and Eeva, 2010). In a polluted environment, antioxidant systems can be induced as an adaptive response to allow organisms to combat oxidative stress (Marasco and Constantini, 2016). In contrast, the antioxidant system may also be inhibited, allowing for reduced protection and a greater susceptibility of cell damage.…”