Thermal Tolerance and Cadmium Susceptibility of Amphipods Endemic to Lake Baikal

Lena.Jakob [ at ]


Lake Baikal, the world’s most ancient and by volume largest freshwater body on earth, is affected by global change and regional human activities; this concerns littoral regions of the lake in particular. The direct and indirect effects of rising temperatures and pollution on the unique endemic littoral amphipod fauna of Lake Baikal are as yet unresolved. Thus, the aim of this thesis is to provide insights into the physiological processes determining thermal tolerance and toxicant susceptibility in two of the most abundant littoral amphipod species (Eulimnogammarus verrucosus and Eulimnogammarus cyaneus) in comparison with the related gammarid Gammarus lacustris, which is ubiquitously spread in the Holarctic. The three species experience different temperature regimes. G. lacustris experiences the highest thermal fluctuations as it inhabits shallow water habitats, followed by E. cyaneus, which stays in the upper littoral of Lake Baikal throughout the year. By contrast, E. verrucosus migrates to sublittoral areas when temperatures in the upper littoral of Lake Baikal rise in summer. Further, the species differ in body size (body length from the rostrum to the uropods); E. verrucosus (3.5 - 4 cm) is about 3 - 4 times larger than E. cyaneus (ca. 1 cm). G. lacustris (ca. 1 - 1.5 cm) is only slightly larger than E. cyaneus. It inhabits some of Lake Baikal but is not part of the typical littoral amphipod community. Whether global change will promote a widespread invasion of the non-endemic G. lacustris from isolated shallow bays into Lake Baikal is yet unknown. In a comparative framework thermal plasticity of physiological performance parameters was studied on the whole animal, biochemical and molecular level in all three amphipod species under progressive temperature increase (0.8°C d-1; start: 6°C). Toxicant susceptibility was investigated by measuring cadmium (Cd2+) uptake, subcellular cadmium compartmentalization, concentration-mortality relationships and physiological responses to low biologically effective concentrations derived from concentration-mortality relationships. Ventilation rates were limited at lower temperatures in E. verrucosus (10.6°C) than in E. cyaneus (19.1°C) and G. lacustris (21.1°C). These so-called breakpoint temperatures (BPTs) were correlated with migration of E. verrucosus from the upper littoral to deeper and cooler areas. Moreover, there was strong indication that the BPTs of ventilation correspond to the maximal habitat temperature of E. cyaneus and G. lacustris. Thus, within the framework of oxygen- and capacity-limitation of thermal tolerance (OCLTT), it was suggested that the BPTs of ventilation reflect the first level of thermal limitation, i.e. the pejus (“getting worse”) temperatures of the species. Like ventilation, oxygen consumption was constrained at lower temperatures E. verrucosus (15.0°C) than in E. cyaneus (25.2°C) and G. lacustris (23.6°C). Surpassing the BPTs of oxygen consumption led to exponentially increasing mortality. Consequently, the BPTs of oxygen consumption were proposed to correspond to the critical temperatures of the studied species. Temperature-dependent changes in activities of key metabolic enzymes were correlated with those in oxygen consumption rates in all three amphipod species, however, the shapes of curves representing these changes differed between the species. In E. verrucosus, maximal activities of aerobic enzymes in response to changing temperatures followed hyperbolic or peak-shaped curves and, like oxygen consumption rates, decreased at a breakpoints of around 15°C. Only lactate dehydrogenase, which is involved in anaerobic processes increased significantly beyond 15°C. Simultaneously, transcriptional levels of genes coding for enzymes involved in aerobic metabolic processes were down-regulated and genes involved in the response to hypoxia simultaneously up-regulated in E. verrucosus. By contrast, no breakpoint was observed for aerobic enzyme activities of E. cyaneus and G. lacustris. Enzyme acitivities increased exponentially under elevated temperature. While E. cyaneus showed slight thermal compensation through progressively decreasing RNA transcript levels of many enzymes with rising temperature, no thermal compensation was observed for G. lacustris. Consequently, Q10-relationships of enzyme activities at high temperatures were lower in E. cyaneus than in G. lacustris. In contrast to E. verrucosus, smaller-sized E. cyaneus and G. lacustris had faster cadmium uptake rates and thus lower lethal concentrations, likely due to their higher ratio of permeable body surface area to body volume. Subsequent effect-scaled experiments (exposure to species-specific LC1 of CdCl2; G. lacustris had to be excluded due to high cannibalism) revealed that more cadmium was bound to heat stable proteins in E. cyaneus than in E. verrucosus, congruent to its higher cellular stress response capacity. In contrast, exposure to their species-specific LC1, led to similar concentrations of cadmium associated with the metal sensitive fraction (contains cadmium bound to subcellular fractions which includes heat denaturable proteins and cell organelles) in the two species, however, with species-specific physiological responses of the oxygen supply system. Sublethal cadmium concentrations resulted in metabolic depression and reduced ventilation in E. verrucosus but not in E. cyaneus. Furthermore, the combination of cadmium (sublethal concentration at 6°C) and increased temperature was shown to be more deleterious than each single factor alone reflected by elevated mortality in both species. In conclusion, thermal constraints on the oxygen supply system in E. verrucosus, E. cyaneus and G. lacustris may shape the upper temperature limits to the thermal habitats of the species, in line with the theory of an allometry of thermal tolerance and the hypothesis of a systemic to molecular hierarchy of thermal tolerance with the tightest constraints at the highest hierarchical level (whole animal). Concomitant changes at different organizational levels observed for E. verrucosus suggest a tightly regulated system in response to decreasing systemic oxygen availability caused by elevated temperatures. The results presented here underline that both physiological and behavioral responses to changing environmental conditions may determine a species’ success under global change. E. verrucosus has a high behavioral plasticity (mediated by its migration behavior) but low physiological plasticity to cope with rising temperatures. By contrast E. cyaneus has a higher capacity to tolerate current thermal fluctuations in the upper littoral. However, present summer temperatures may already touch the pejus range of E. cyaneus. Consequently, despite the higher thermal tolerance of E. cyaneus it might be more severely affected by future global change than E. verrucosus. Furthermore, despite the fact that lethal concentrations of cadmium were much lower for E. cyaneus, E. verrucosus showed a stronger physiological response (metabolic depression) to concentrations far below lethal ones. Consequently, the extremely sensitive reaction of E. verrucosus to low levels of a chemical stressor underlines that sublethal effects may not necessarily mirror sensitivity rankings based on mortality data. These findings underscore the necessity of water management strategies strictly avoiding chemical contamination of Lake Baikal waters. Rising temperatures likely enhance the deleterious effects of chemical stressors as shown here for cadmium. Whether global change will provide a competitive advantage for G. lacustris in comparison to Baikal endemics and, by extension, promote the widespread invasion of this non-endemic species, could not be elucidated. G. lacustris showed only slightly non-significantly higher heat tolerance than the Baikal endemic E. cyaneus and showed a similar cadmium susceptibility as E. cyaneus. Secondary effects of global change such as eutrophication, which has been found in the littoral of Lake Baikal, are important factors that need to be considered in future studies. Organisms which are sensitive to hypoxic conditions are likely the first to be affected by such changes.

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Jakob, L. (2016): Thermal Tolerance and Cadmium Susceptibility of Amphipods Endemic to Lake Baikal , PhD thesis,

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