The Adaptive Significance of Cuticular Pigmentation in Daphnia

Cuticular pigmentation has been reported in a number of cladoceran crustaceans, but its adaptive significance remains unclear. This study involved an analysis of the distribution and adaptive significance of pigmentation in the Daphnia pulex Leydig group. A survey of more than 1000 ponds in temperate and arctic North America established that pigmented forms predominate in the high arctic, co-occur with unpigmented clones in the low arctic and are absent from the temperate zone except in coastal sand-dune habitats. In the low arctic, pigmented clones dominate clear-water ponds, while unpigmented clones dominate ponds with high concentrations of dissolved humics. Where they co-occur, pigmented clones tend to remain higher in the water column during daytime. Biochemical studies showed that the pigment is melanin, and although it comprised only 0 03% of body weight, it prevented transmission of more than 90% of incident ultraviolet radiation. Melanic clones of both D. pulex and D. middendorffiana Fischer survived exposure to 20W m-2 of near ultraviolet for twice as long as unpigmented clones. Reciprocal transplant experiments confirmed that unpigmented clones were only able to survive in ponds with high concentrations of dissolved organics, while melanic clones survived in both clear and humic water ponds. It is clear that unpigmented clones in the D. pulex group -are restricted to habitats where they are sheltered from ultraviolet exposure by shading or dissolved humics, while melanic clones are restricted to clear-water ponds where u.v. exposure is high. The failure of melanics to colonize other habitats is apparently largely a consequence of the cost of melanin production. Key-words: Arctic, Cladocera, Daphnia, melanin, ultraviolet *Present address: P.D. N. Hebert, Department of Zoology, University of Guelph, Guelph, Ontario N1G 2W1, Canada. Introduction The dark pigmentation of both zooplankton and benthos from arctic and alpine freshwater habitats has been noted for more than 50 years (Brehm, 1938). Studies concerning the adaptive significance of pigmentation have focused on calanoid copepods, which appear to employ carotenoids and carotenoproteins for protection from short wavelength radiation (300-500 nm). Hairston (1976) showed that pale individuals of Diaptomus nevadensis suffered higher mortality than heavily pigmented individuals when exposed to short wavelength light. Comparable mortality differences have been observed between pigmented and unpigmented forms of several other calanoid species (Hairston 1978, 1979ab; Luecke & O'Brien, 1983). Siebeck (1978ab) reported similar differences among cladoceran species which varied in their carotenoid levels. Despite the concordance of these results, there remains some controversy concerning their interpretation (Byron, 1982). Ringelberg (1980, 1981) has argued that the pigments may serve either as a direct energy source or may be correlated with the nutritional status of the organism. If correct, the increased survivorship of pigmented individuals under high light intensity might reflect nothing more than the greater resistance of well-fed individuals to environmental stress. The present study examines the adaptive significance of pigmentation in another group of microcrustaceans the cladocerans. While many cladocerans sequester carotenoids, certain species deposit a tan-brown to black pigment in their cuticle. As the pigmented cuticle is shed at each moult, the need for pigment synthesis is recurrent. This suggests a clear cost to the maintenance of pigmentation, and hence avoids one of the interpretative difficulties associated with studies on carotenoids. Cuticular pigmentation has been reported in several genera of cladocerans, although more detailed investigations have so far been limited to the genus Daphnia. Luecke & O'Brien (1983) have shown that a pigmented form of D. middendorffiana Fischer was less susceptible to light exposure than an unpigmented form. However, Dodson This content downloaded from 157.55. 39.178 on Fri, 05 Aug 2016 05:39:47 UTC All use subject to http://about.jstor. org/terms 704 (1984) has suggested that pigmented forms may be P. D. N. more resistent to invertebrate predation as a result Hebert & of their tougher cuticles. The present study has C. J. Einery focused on members of the Daphnia pulex Leydig group, which dominate pond habitats throughout North America. The taxonomy of the group is in flux, but pigmented forms have been recognized in only two species. D. middendorffiana is apparently restricted to low arctic habitats, where it is normally the sole daphniid in ponds occupied by the predatory copepod Heterocope septentrionalis Juday & Muttkowski (Hebert & Loaring, 1980). D. pulex has a broader distribution, being found from the temperate zone to the high arctic. Genetic analysis has shown that populations of both D. pulex and D. rmiddendorffiana are clonally diverse and that individual clones show conspicuous variation in the extent of their pigmentation (Hebert & McWalter, 1983; Weider & Hebert, 1987ab; Weider, Beaton & Hebert, 1987). The present study had two aims. Firstly, to investigate the macroand microgeographical distribution patterns of pigmented clones among members of the D. pulex group. The rationale behind such study was to establish if the distribution of pigmented forms coincided with gradients in predation intensity or with light regimes and secondly, to determine the biochemical nature of the pigment, its role in light interception, and also its effectiveness in providing photoprotec-