Copepods' true colors: astaxanthin pigmentation as an indicator of fitness

Abstract

Pigmentation is often overlooked in zooplankton, since these organisms are mostly colorless to fit the translucid water medium. However, one of the dominant zooplankton taxa in aquatic ecosystems—copepods—often show a bright red‐orange or blue coloration owing to the accumulation of carotenoid pigments in some parts of their bodies. Even though there are many functional traits describing copepod's performance (e.g., size, feeding, and reproductive modes), it is surprising that the role of such a simple and visible trait as coloration has not been studied in a coherent manner yet. Here, by reviewing 95 studies, we demonstrate that carotenoid‐based pigmentation (mainly caused by astaxanthin molecules) is a widespread functional trait in freshwater and marine copepods. We propose a way to disentangle the complex and thus intriguing patterns of pigment expression along latitudinal and altitudinal gradients, addressing its relationship to diet quality and quantity, temperature, ultraviolet radiation stress, predation pressure, lipid metabolism, and reproduction. We show that large‐scale variations in pigmentation are difficult to tackle because of the fundamental plasticity of this trait at short time scales (i.e., hours, days), and the most recent information about carotenoid bioconversion are addressed (genes and enzyme identification, and influence of microbiota). From this literature review, we hypothesize that pigments play a “Swiss‐army knife” role for copepod's fitness, useful in various ecosystem conditions owing to the strong antioxidant power and the finely‐tuned metabolism of astaxanthin. With larger antioxidant capacities (survival), higher metabolisms (growth), and more offspring in better condition (reproduction), red morphs appear more successful than their uncolored siblings. Also, the potential camouflage strategies allowed by red and blue pigmentation are discussed. We finally formulate new directions and future research fields from molecular to ecosystem scales. Routine quantifications of copepod's pigmentation through trait‐based approaches could be useful (1) to obtain an accurate copepod fitness indicator and (2) to better estimate the transfer of antioxidant to higher trophic levels in ecosystems, including humans.

Variations in photoprotective compounds in surface-dwelling copepods in subtropical open waters

“…This study showed that surface-dwelling copepods in the subtropical North Pacific have detectable levels of photoprotective compounds, although their concentrations vary among taxonomic groups. The range of mean carotenoid content (0.0148-0.0965 µg mg dry wt −1 ) in this study was lower than the median content in marine copepods (0.137 µg mg dry wt −1 ) (Vilgrain et al 2023). As for MAAs, to the best of our knowledge, this is the first study in the Pacific to report the MAA content in subtropical marine copepods, using adequate sampling procedures after gut evacuation, following a similar study in the Atlantic (Fileman et al 2017).…”

“…and Acrocalanus spp., had relatively high carotenoid contents. Although the function of carotenoid accumulation in copepods is still debated (Vilgrain et al 2023), its photoprotective role against reactive oxygen species produced by short-light radiation is well known (Hairston 1976). One well-known example is the blue pigmentation produced by carotenoids in neustonic pontellid copepods, which protects them from strong sunlight (Herring 1965).…”

Morphological and taxonomic diversity of mesozooplankton is an important driver of carbon export fluxes in the ocean

“…Quantifying transparency might give information about the organism's ecology (reproduction with gonads or eggs, feeding with guts content, Orenstein et al., 2022). Transparency and colour can also be related to physiological functions (Vilgrain et al., 2022), for example, carotenoids effects against oxidative stress (Brüsin et al., 2016), or possibly the utilization of pigmentation and DVM in order to escape visual predators (Hays et al., 1994).…”

Establishing an astaxanthin-rich live feed strain of Pseudodiaptomus annandalei

“…The trade-off between predation stress and copepod body colors has been noted in several studies 51 . Typically, highly pigmented copepods are more susceptible to predator detection in shallow waters 52 .…”

“…The strain-specific variations in astaxanthin content might stem from differential capacity in astaxanthin bioconversion and accumulation. The biosynthesis pathway of astaxanthin could involve many steps of enzymatic activities that produce a diverse groups of precursor metabolites (β-carotene, echinenone, and canthaxanthin), yet it is scarcely studied in copepod species 51 , 58 . In the future, the comparison of biosynthesize enzymes or relative gene expression levels between the two P. annandalei strains should be investigated using molecular biotechnology techniques, such as transcriptomic or metabolomic analysis, to uncover the molecular mechanisms that cause the variation of their astaxanthin concentration.…”