The combined effects of diet, environment and genetics on pigmentation in the Giant Tiger Prawn, Penaeus monodon
Introduction
Many crustacean tissues attribute their colouration to the presence of various carotenoids, particularly those that provide external colouration. In addition to providing a protective camouflage to the animal, colour plays a major role in consumer acceptability, perceived quality and price paid for commercial crustacean species (Chien and Jeng, 1992, Erickson et al., 2007, Parisenti et al., 2011a, Shahidi and Metusalach Brown, 1998). This colour may be embedded in the exoskeleton, or in pigment structures within the underlying hypodermal layer known as chromatophores (Rao, 1985). The most abundant carotenoid in crustacean tissues is astaxanthin (Axn) (Castillo et al., 1982, Lenel et al., 1978, Tanaka et al., 1976), where it is found in free, esterified and protein-bound forms. The amount and distribution of pigment are dependent upon a range of dietary, environmental and genetic factors that have been considered independent from one another, with each having been studied in isolation.
Several crustacean species have been shown to lose or not develop pigmentation if not supplied a diet with sufficient carotenoids (Dall, 1995, Daly et al., 2013, Tlusty and Hyland, 2005). Dietary astaxanthin supplementation is known to improve crustacean colour through the abundance of epithelial astaxanthin and astaxanthin esters (Barclay et al., 2006, Boonyaratpalin et al., 2001, Kumar et al., 2009, Supamattaya et al., 2005, Yamada et al., 1990). Crustaceans have the metabolic capacity to interconvert different carotenoids, such as canthaxanthin and ß-carotene, into astaxanthin (Negre-Sadargues, 1978, Schiedt et al., 1993). Dietary astaxanthin between 50 and 100 mg/kg fed for one month was sufficient to produce optimal pigmentation in a range of prawn species (Chien and Jeng, 1992, Petit et al., 1997, Yamada et al., 1990). Within the exoskeleton and hypodermal tissue of crustaceans, free astaxanthin is often also bound within a multimeric protein complex called crustacyanin (CRCN) (Wald et al., 1948). The interaction of CRCN and Axn modifies the naturally red carotenoid to blue or any other colour in the visible spectrum, producing the diverse array of colours seen in the exoskeleton of crustaceans (Cianci et al., 2002). During cooking, this interaction is disrupted, releasing the distinct red colouration of cooked seafood.
In response to various physiological cues, crustacean chromatophores expand and contract that is mediated by hormones secreted from the eyestalk (Bagnara and Hadley, 1973, Rao, 2001). This rapid and reversible response strongly contributes to the degree of individual colouration, particularly for species with thin opaque shells like prawns (Fingerman, 1965). The environmental cues can span aspects such as background colour, light source and photoperiod (Latscha, 1990, Rao, 1985). Short-term exposure to black substrates has been shown to improve prawn pigmentation through expansion of hypodermal chromatophores (Parisenti et al., 2011b, Tume et al., 2009). This expansion was linked with the accumulation of the colour protein CRCN in the hypodermal tissues (Wade et al., 2012). Improvements in prawn colour have been linked with improved product quality, increased consumer acceptance and higher market prices (Parisenti et al., 2011a, Tume et al., 2009).
The present study sought to determine whether the long-term beneficial effect of feeding high levels of dietary astaxanthin could be combined with the short-term beneficial effects of exposure to dark coloured substrates. In addition, this study sought to assess the ability of dietary carotenoid supplementation to overcome the negative effects of short-term exposure to white substrates. Whether the colour protein CRCN has a role in regulating colour change was also assessed. Raw or cooked prawn colour was monitored using digital images, expansion of chromatophores was assessed using microscopy, and CRCN protein abundance was quantified by western blotting. Lastly, the ability to transfer this knowledge to the industry was assessed during harvesting of farmed Penaeus monodon.
Section snippets
Animal handling
Juvenile prawns, P. monodon, were obtained from commercial farms and maintained at CSIRO Marine and Atmospheric Research (CMAR) laboratories at Bribie Island. For all trials, filtered seawater was heated then pumped through the tanks at 1.2 L min− 1 maintaining water temperatures at 28 °C and salinity at 35 g/L. Animals were held in a total of 36 red polyethylene tanks that held 80 L seawater in each. The experiment was conducted indoors under low artificial light conditions and a 12–12 light–dark
Prawn colour change in response to diet
The different carotenoid inclusion levels produced a strong change in average abdominal colour (Fig. 1), a clear visual difference in uncooked prawn colour (Supplementary Fig. 1), and quantifiable differences in the RGB values between the different treatments (Supplementary Table 1). Time had a significant effect on R (F = 31.04, p < 0.001), G (F = 13.14, p < 0.001) and B (F = 4.75, p = 0.006). Diet significantly affected G (F = 4.01, p < 0.013) and B (F = 6.56, p < 0.001). There were many significant differences
Combined effects of diet and background colour exposure on the colour of prawns
As observed in most crustaceans (Barclay et al., 2006, Boonyaratpalin et al., 2001, Kumar et al., 2009, Supamattaya et al., 2005, Yamada et al., 1990), this study showed that prawns not receiving dietary carotenoid became paler while those receiving the highest dietary carotenoid became darker in colour. Prawns also rapidly respond to the colour of their surroundings (Parisenti et al., 2011b, Tume et al., 2009), and in this study became paler when exposed to white substrates and darker when
Acknowledgments
This study received funding through the Australian Seafood CRC (Project 2011/731), DSM Nutritional Products, and the CSIRO Agricultural Productivity Flagship. Prawns for tank based work and farm trials were kindly supplied by Gold Coast Marine Aquaculture, coordinated by Nick Moore. The authors would also like to thank Stuart Arnold, Kinam Salee, Natalie Habilay, Nick Polymeris, Dylan Rylatt and Richard Thaggard for setup and maintenance of the tank trial.
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2022, Food Research InternationalCitation Excerpt :There was no significant difference in the content of astaxanthin (11.80–14.68%), zeaxanthin (0.43–0.58%) and canthaxanthin (11.92–12.04%) in the two groups (P < 0.05). Color values are important parameters to evaluate the seafood color, which are related to the composition and concentration of carotenoids in their tissues (Supamattaya, Kiriratnikom, Boonyaratpalin, & Borowitzka, 2005; Wade, Budd, Irvin, & Glencross, 2015). In a previous study, the color parameters of rainbow trout (Oncorhynchus mykiss) fillets showed the carotenoid-type effect (Choubert, Brisbarre, & Baccaunaud, 2011).