Complementary UV protective compounds in zooplankton

Abstract

Zooplankton accumulate several groups of photoprotective compounds to shield against damaging ultraviolet radiation (UV). One of these groups, the carotenoids, makes the animals more conspicuous to visually hunting predators, whereas others, such as the mycosporine-like amino acids (MAAs) may not. The blend of photoprotective compounds is therefore important for the UV defense but also for the ability to escape predation through crypsis. Here we assess laboratory and field data from different latitudes to examine how UV, predation threat, and pigment availability (in food) affects the mixture of UV-protective compounds in copepods. Overall, the blend of MAAs and carotenoids was partly explained by the availability of MAAs in the food, the UV-threat, and the presence of predators. Copepods upregulated their MAA content when UV threat was increasing (i.e., if MAAs were abundant in food), and in field data this accumulation only occurred at high levels of predation threat. If MAAs were scarce, copepods instead compensated with higher carotenoid accumulation. However, when there was a high predation threat this carotenoid compensatory effect was disadvantageous, and low concentrations of both MAAs and carotenoids at high UV-threat resulted in lower reproduction. In all, these results showed that carotenoids and MAAs are complementary substances, i.e., one is high when the other is low, and copepods are, hence, able to adjust their blend of different UV-protective compounds to optimize their defenses to the threats of UV and predation. These defense systems may buffer against direct food-web interactions and help the zooplankton to survive in environments with high UV threat.

UV photoprotectants in arctic zooplankton

“…The MAA concentrations in copepods in the present study were in generally at the low end of this range, but showed high variation between 0.02 and 10 µg mg -1 , depending on species and site, perhaps because ponds are more heterogeneous habitats than the lakes that were studied by Hylander et al (2009b).…”

“…The distribution of this species was restricted to the DOC-poorest ponds that were <1 m in depth, and the species was, therefore, highly exposed to UV radiation. Recently, Hylander et al (2009b) reported a latitudinal pattern in copepod MAA concentration, with low concentrations in Subarctic and temperate copepods (1.0 and 1.4 µg mg -1 ) compared to dry-temperate copepods (up to 58 µg mg -1…”

“…The benthic fairy shrimp Branchinecta paludosa was the only species that did not have any MAAs, despite the presence of MAAs in the benthic mats that were potentially available to this species in its food. Worldwide, MAAs are the most commonly encountered UV-absorbing compounds in aquatic organisms and are found, for example, in UV-exposed phytoplankton and copepods (Sommaruga & Garcia-Pichel 1999, Tartarotti et al 2001, 2004, Moeller et al 2005, Hansson et al 2007, Hylander et al 2009b) and in arctic benthic and planktonic algae , Hylander et al 2009b. MAAs have their absorption maxima in the UV range, between 310 and 360 nm, and provide protective screening against radiation before it penetrates the cell.…”

Roles of phosphorus and ultraviolet radiation in the strength of phytoplankton‐zooplankton coupling in a Mediterranean high mountain lake

“…Our results further support that the mechanism behind the detrimental UVR was organism death. However, the large C content per individual under UVR suggests the storage of lipids associated with carotenoid pigmentation (Hylander et al 2009), which may be interpreted as a tolerance mechanism against UVR-induced stress.…”

Carotenoid accumulation in copepods is related to lipid metabolism and reproduction rather than to UV‐protection

“…The red coloration of copepods is due to carotenoids, a large family of lipid-soluble pigments that are synthesized only in primary producers but may be either accumulated by zooplankton or biologically converted to other carotenoids, notably astaxanthin, which is the primary carotenoid among crustaceans (Matsuno 2001;Andersson et al 2003;Rhodes 2006). Astaxanthin is a powerful antioxidant (McNulty et al 2007) occurring both in free form and esterified with fatty acids or associated with proteins (Cheesman et al 1967;Matsuno 2001).In zooplankton, carotenoid accumulation is a highly variable trait that has been linked to photoprotection against ultraviolet radiation (UVR) in field studies comparing lakes with differential UVR exposure and in experimental studies (Hairston 1976;Moeller et al 2005;Hylander et al 2009;Rautio and Tartarotti 2010;Sommaruga 2010). The underlying mechanism ascribing astaxanthin photoprotection properties involves the quenching of singlet oxygen ( 1 O 2 ) produced during UVR exposure rather than direct absorption or reflectance of the hazardous wavelengths (Krinsky 1979;Kobayashi and Sakamoto 1999).…”