Pollutant-induced changes in fish pigmentation and spatial patterns

TL;DR

Environmental pollutants can disrupt fish pigmentation by perturbing inter-cellular signaling among chromatophores. The authors develop nonlocal reaction–diffusion–advection PDEs with Morse-type kernels to model melanophore–xanthophore interactions and incorporate a pollution field $T(x,y)$ that modulates adhesion and repulsion, validated by methane exposure experiments showing pigment fragmentation and hypopigmentation. The results indicate that pollutant effects are strongest on homotypic interactions, can cause hypo- or hyperpigmentation, and depend on exposure duration and domain growth, with saturation at high pollutant levels. Overall, the work provides a mechanistic link between environmental contamination and shifts in pigment patterning, offering quantitative predictions and guiding future toxicology studies.

Abstract

Pigmentation abnormalities, ranging from hypo- to hyperpigmentation, can serve as biomarkers of developmental disruption in fish exposed to environmental contaminants. However, the mechanistic pathways underlying these alterations remain poorly understood. Studies have shown that pattern formation in fish development requires specific pigment cell interactions. Motivated by experimental observations of pigmentation alterations following contaminant exposure, we investigate how pollutants influence pigment cell self-organization using a continuum reaction-diffusion-advection framework. The model incorporates nonlocal Morse-type kernels to describe short- and long-range interactions among melanophores and xanthophores. Our results show that perturbations to the strengths of adhesion or repulsion can drive transitions between stripes, spots, and mixed patterns, reproducing phenotypes characteristic of fish pigmentation mutants. In particular, homotypic interactions are sensitive to contamination, leading to pronounced changes in melanophore density and resulting pigmentation patterns. Time-dependent simulations indicate that pigment changes from early short-term contaminant exposure may be recoverable, whereas prolonged exposure can lead to sustained pigment loss. In a growing fish, contaminant-induced changes in cell-cell interactions directly influence stripe formation rate, stripe number, and pigmentation levels. Overall, our study provides insight into the mechanistic link between experimentally observed pigmentation alterations and the changes in spatial patterns of adult fish.

Figures (13)

• Figure 1: Examples of marine and freshwater species displaying a wide variety of pigment patterning outcomes. These patterns are determined by the number, spatial arrangement, and interactions of melanophores, xanthophores, iridophores, and other chromatophore classes. (a) Blue-ring angelfish Pomacanthus annularis; (b) emperor bream (genus Lethrinus); (c) Desjardini sailfin tang Zebrasoma desjardinii; (d) bumblebee cichlid Pseudotropheus crabro; (e) rabbitfish (genus Siganus); (f) pale African cichlid; (g) banded leporinus Leporinus fasciatus; (h) electric blue hap Sciaenochromis fryeri; (i) red-bellied piranha Pygocentrus nattereri.
• Figure 2: Illustrations of homotypic and heterotypic interactions. (a) In the homotypic case, only short-range attraction and long-range repulsion occur among cells of the same type, with no interactions between different cell types. (b) In the heterotypic case, an additional one-directional long-range attraction and a short-range repulsive interaction between the two cell types are present, producing a chase–and–run–type behavior in which xanthophores chase melanophores while melanophores avoid xanthophores.
• Figure 3: Inhibition of melanin pigmentation in zebrafish larvae at 4 dpf exposed to methane at different concentrations (6-24 fish samples considered for each concentration) (a) Melanin percentage in the head-dorsal region at different exposure levels for; (b) Histogram of average grayscale (AGS) and melanin percentage for control and methane-exposed larvae; (c) Dorsal view of the head region of a zebrafish sample used in the experiment.
• Figure 4: Localized inhibition of pigmentation near the tail region in zebrafish larvae exposed to 25 $\%\, \mathrm{CH}_4$ at 4 dpf compared to control.
• Figure 5: Image-based fragmentation analysis of pigmentation patterns at 4 dpf. The left panel shows continuous stripe development in a control larva, along with the thresholded image and the identified connected pigment regions. The right panel shows a fragmented pigmentation pattern in a larva exposed to $25\%\,\mathrm{CH}_4$, with thresholded images revealing a larger number of spatially disconnected pigment regions.