Copepods in Turbid Shallow Soda Lakes Accumulate Unexpected High Levels of Carotenoids

Tobias Schneider,Alois Herzig,Karin A Koinig,Ruben Sommaruga,Terence Evens

doi:10.1371/journal.pone.0043063

Abstract

Carotenoids are protective pigments present in many aquatic organisms that reduce the photooxidative stress induced by short-wavelenght solar radiation, yet increase their susceptibility to predators. Arctodiaptomus spinosus, a calanoid copepod typically found in many fishless shallow soda lakes, shows large between-lake differences in pigmentation. Here, we attribute these differences to the environmental state of these ecosystems, namely, ‘dark water’ lakes with submersed vegetation and turbid ‘white’ lakes lacking macrophytes. Copepod carotenoid concentration in the turbid ‘white’ lakes was significantly (about 20-fold) higher than in the ‘dark water’ ones, although the latter systems were characterized by higher transparency. In addition, males had on a dry weight basis around three times higher carotenoid concentrations than females. Mycosporine-like amino acids (direct UV screening substances) were found in all cases, but in low concentration. The environmental conditions in these ecosystems were largely shaped by the presence/absence of submersed macrophytes Thus, in the turbid lakes, the strong wind-driven mixis allows for copepods to be brought to the surface and being exposed to solar radiation, whereas in ‘dark water’ ones, macrophytes reduce water turbulence and additionally provide shelter. Our results explain the counter-intuitive notion of strong red pigmentation in copepods from a turbid ecosystem and suggest that factors other than high UV transparency favor carotenoid accumulation in zooplankton.

Highlights

Shallow lakes can be defined by polymixis and by their ability to sustain submersed macrophytes [1]
Chlorophyll a concentration was correlated with Kd 380 (R = 0.740, N = 41, P,0.001), it did have relatively little impact on the underwater radiation climate, as its contribution to attenuation was never more than 4% in any of the lakes (Fig. 3B)
All Kd values were strongly correlated with the total suspended solids (TSS) content (R .0.99 for each wavelength Kd vs. TSS, N = 41, P,0.001) and they were excluded in the principal component analysis (PCA) to avoid bias

Summary

Introduction

Shallow lakes can be defined by polymixis and by their (theoretical) ability to sustain submersed macrophytes [1]. In habitats with deep UVR penetration relative to the maximum depth (i.e., with low depth refuge) or shallow lakes with important winddriven mixis, zooplankton might not be able to avoid hazardous radiation levels, and rely on the accumulation of photoprotective compounds (PPCs) [4]. These substances either directly screen UV radiation, or reduce UVR-induced damage by quenching ROS [3]. Some PPCs are only synthetized by primary producers, but may be passed on to the heterotrophic host (e.g., in corals) or to consumers (e.g., copepods) [10,11,12]

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