The Seasonal Metabolic Activity Cycle of Antarctic Krill (Euphausia superba): Evidence for a Role of Photoperiod in the Regulation of Endogenous Rhythmicity

Antarctic krill (Euphausia superba), a key species in the Southern Ocean, reduce their metabolism as an energy saving mechanism in response to the harsh environmental conditions during the Antarctic winter. Although the adaptive significance of this seasonal metabolic shift seems obvious, the driving factors are still unclear. In particular, it is debated whether the seasonal metabolic cycle is driven by changes in food availability, or if an endogenous timing system entrained by photoperiod might be involved. In this study, we used different long-term photoperiodic simulations to examine the influence of light regime and endogenous rhythmicity on the regulation of krill seasonal metabolic cycle. Krill showed a seasonal cycle of growth characterized by null-to-negative growth rates during autumn-winter and positive growth rates during spring-summer, which was manifested also in constant darkness, indicating strong endogenous regulation. Similar endogenous cycles were observed for the activity of the key-metabolic enzyme malate dehydrogenase (MDH) and for the expression levels of a selection of metabolic-related genes, with higher values in spring-summer and lower values in autumn-winter. On the other side, a seasonal cycle of oxygen consumption was observed only when krill were exposed to simulated seasonal changes in photoperiod, indicating that light-related cues might play a major role in the regulation of krill oxygen consumption. The influence of light-regime on oxygen consumption was minimal during winter, when light-phase duration was below 8 h, and it was maximal during summer, when light-phase duration was above 16 h. Significant upregulation of the krill clock genes clk, cry2, and tim1, as well as of the circadian-related opsins rh1a and rrh, was observed after light-phase duration had started to decrease in early autumn, suggesting the presence of a signaling cascade linking specific seasonal changes in the Antarctic light regime with clock gene activity and the regulation of krill metabolic dormancy over the winter

Light regime affects the seasonal cycle of Antarctic krill (Euphausia superba): impacts on growth, feeding, lipid metabolism, and maturity

Light regime is an important zeitgeber for Antarctic krill (Euphausia superba Dana, 1850), which seems to entrain an endogenous timing system that synchronizes its life cycle to the extreme light conditions in the Southern Ocean. To understand the flexibility of Antarctic krill’s seasonal cycle, we investigated its physiological and behavioural responses to different light regimes and if an endogenous timing system was involved in the regulation of these seasonal processes. We analysed growth, feeding, lipid content, and maturity in a 2-year laboratory experiment simulating the latitudinal light regimes at 52°S and 66°S and constant darkness under constant food level. Our results showed that light regime affected seasonal cycles of growth, feeding, lipid metabolism, and maturity in Antarctic krill. Seasonal patterns of growth, feeding, and maturity persisted under constant darkness, indicating the presence of an endogenous timing system. The maturity cycle showed differences in critical photoperiods according to the simulated latitudinal light regime. This suggests a flexible endogenous timing mechanism in Antarctic krill, which may determine its response to future environmental changes

Seasonal and Form-Specific Gene Expression Signatures Uncover Different Generational Strategies of the Pelagic Tunicate Salpa thompsoni During the Southern Ocean Winter

The pelagic tunicate Salpa thompsoni is recognized as a major metazoan grazer in the Southern Ocean. Long term observations show an increase in this species’ biomass and a southward shift in its distribution both of which are positively correlated with ocean warming and winter sea ice decline around the Antarctic Peninsula. However, our understanding on how salps adapt their life cycle to the extreme seasonality of the Southern Ocean and the putative differences between its two reproductive forms (aggregates, solitaries) is rudimentary. In particular, our current knowledge of whether and how S. thompsoni overwinter is limited, largely due to winter sampling constraints. In this study, we investigated the form-specific gene expression profiles of Salpa thompsoni during the austral autumn and winter. Between the seasons, genes related to translation showed the biggest difference in gene expression. We found more genes were upregulated in solitaries compared to aggregates, indicating a potentially form-specific overwintering strategy. Our data provide first insights into the seasonal and form-specific physiology of salps by considering their complex life cycle, thereby contributing to a more comprehensive understanding of the response of salps to seasonal changes in their environment and to anthropogenic induced global climate change

The Seasonal Metabolic Activity Cycle of Antarctic Krill (Euphausia superba): Evidence for a Role of Photoperiod in the Regulation of Endogenous Rhythmicity

Antarctic krill (Euphausia superba), a key species in the Southern Ocean, reduce their metabolism as an energy saving mechanism in response to the harsh environmental conditions during the Antarctic winter. Although the adaptive significance of this seasonal metabolic shift seems obvious, the driving factors are still unclear. In particular, it is debated whether the seasonal metabolic cycle is driven by changes in food availability, or if an endogenous timing system entrained by photoperiod might be involved. In this study, we used different long-term photoperiodic simulations to examine the influence of light regime and endogenous rhythmicity on the regulation of krill seasonal metabolic cycle. Krill showed a seasonal cycle of growth characterized by null-to-negative growth rates during autumn-winter and positive growth rates during spring-summer, which was manifested also in constant darkness, indicating strong endogenous regulation. Similar endogenous cycles were observed for the activity of the key-metabolic enzyme malate dehydrogenase (MDH) and for the expression levels of a selection of metabolic-related genes, with higher values in spring-summer and lower values in autumn-winter. On the other side, a seasonal cycle of oxygen consumption was observed only when krill were exposed to simulated seasonal changes in photoperiod, indicating that light-related cues might play a major role in the regulation of krill oxygen consumption. The influence of light-regime on oxygen consumption was minimal during winter, when light-phase duration was below 8 h, and it was maximal during summer, when light-phase duration was above 16 h. Significant upregulation of the krill clock genes clk, cry2, and tim1, as well as of the circadian-related opsins rh1a and rrh, was observed after light-phase duration had started to decrease in early autumn, suggesting the presence of a signaling cascade linking specific seasonal changes in the Antarctic light regime with clock gene activity and the regulation of krill metabolic dormancy over the winter

Assessing the potential of autonomous submarine gliders for ecosystem monitoring across multiple trophic levels (plankton to cetaceans) and pollutants in shallow shelf seas

A combination of scientific, economic, technological and policy drivers is behind a recent upsurge in the use of marine autonomous systems (and accompanying miniaturized sensors) for environmental mapping and monitoring. Increased spatial–temporal resolution and coverage of data, at reduced cost, is particularly vital for effective spatial management of highly dynamic and heterogeneous shelf environments. This proof-of-concept study involves integration of a novel combination of sensors onto buoyancy-driven submarine gliders, in order to assess their suitability for ecosystem monitoring in shelf waters at a variety of trophic levels. Two shallow-water Slocum gliders were equipped with CTD and fluorometer to measure physical properties and chlorophyll, respectively. One glider was also equipped with a single-frequency echosounder to collect information on zooplankton and fish distribution. The other glider carried a Passive Acoustic Monitoring system to detect and record cetacean vocalizations, and a passive sampler to detect chemical contaminants in the water column. The two gliders were deployed together off southwest UK in autumn 2013, and targeted a known tidal-mixing front west of the Isles of Scilly. The gliders’ mission took about 40 days, with each glider travelling distances of >1000 km and undertaking >2500 dives to depths of up to 100 m. Controlling glider flight and alignment of the two glider trajectories proved to be particularly challenging due to strong tidal flows. However, the gliders continued to collect data in poor weather when an accompanying research vessel was unable to operate. In addition, all glider sensors generated useful data, with particularly interesting initial results relating to subsurface chlorophyll maxima and numerous fish/cetacean detections within the water column. The broader implications of this study for marine ecosystem monitoring with submarine gliders are discussed

Commercial fishing patterns influence odontocete whale-longline interactions in the Southern Ocean

The emergence of longline fishing around the world has been concomitant with an increase in depredation-interactions by odontocete whales (removal of fish caught on hooks), resulting in substantial socio-economic and ecological impacts. The extent, trends and underlying mechanisms driving these interactions remain poorly known. Using long-term (2003–2017) datasets from seven major Patagonian toothfish (Dissostichus eleginoides) longline fisheries, this study assessed the levels and inter-annual trends of sperm whale (Physeter macrocephalus) and/or killer whale (Orcinus orca) interactions as proportions of fishing time (days) and fishing area (spatial cells). The role of fishing patterns in explaining between-fisheries variations of probabilities of odontocete interactions was investigated. While interaction levels remained globally stable since the early 2000s, they varied greatly between fisheries from 0 to >50% of the fishing days and area. Interaction probabilities were influenced by the seasonal concentration of fishing effort, size of fishing areas, density of vessels, their mobility and the depth at which they operated. The results suggest that between-fisheries variations of interaction probabilities are largely explained by the extent to which vessels provide whales with opportunities for interactions. Determining the natural distribution of whales will, therefore, allow fishers to implement better strategies of spatio-temporal avoidance of depredation

Patterns of at-sea behaviour at a hybrid zone between two threatened seabirds

Patterns of behavioural variation and migratory connectivity are important characteristics of populations, particularly at the edges of species distributions, where processes involved in influencing evolutionary trajectories, such as divergence, mutual persistence, and natural hybridization, can occur. Here, we focused on two closely related seabird species that breed in the Mediterranean: Balearic shearwaters (Puffinus mauretanicus) and Yelkouan shearwaters (Puffinus yelkouan). Genetic and phenotypic evidence of hybridization between the two species on Menorca (the eastern and westernmost island in the breeding ranges of the two shearwaters, respectively) has provided important insights into relationships between these recently diverged species. Nevertheless, levels of behavioural and ecological differentiation amongst these populations remain largely unknown. Using geolocation and stable isotopes, we compared the at-sea movement behaviour of birds from the Menorcan ‘hybrid’ population with the nearest neighbouring populations of Balearic and Yelkouan shearwaters. The Menorcan population displayed a suite of behavioural features intermediate to those seen in the two species (including migration strategies, breeding season movements and limited data on phenology). Our findings provide new evidence to support suggestions that the Menorcan population is admixed, and indicate a role of non-breeding behaviours in the evolutionary trajectories of Puffinus shearwaters in the Mediterranean

Investigations of the variability of tidal mixing fronts and their importance for shelf-sea ecosystems across multiple trophic levels

Tidal mixing fronts establish during the summer months over shelf-seas, and separate tidally-mixed from stratified water masses. They play an important part in shelf-sea bio-physical processes, including volume transport and facilitation of primary productivity. Frontal hydrodynamics provide the physical necessities for prey aggregations to develop, holding the potential for biodiversity hotspots. However, there is limited knowledge on long-term variability of tidal mixing fronts and its effect on associated ecosystems, due to a lack of adequate datasets. Such information would greatly benefit spatial conservation efforts and improve our understanding of ecosystem dynamics on the continental shelf. Satellite-derived frontal maps and extensive biological datasets (from 1990-2010) are employed here to investigate spatio-temporal variability of tidal mixing fronts and their significance for shelf-sea biology from zooplankton tomegavertebrates in the Celtic Sea. In addition, this study assesses the suitability and limitations of satellite-derived frontal metrics for quantitative analyses and employs innovative technology (submarine gliders) to fill data gaps in species-environment interactions. This research provides guidance on the use of frontal metrics in quantitative analysis, such as the need to account for data variability over the years and the careful consideration of the employed frontal metric. This thesis furthermore, represents the first description of long-term temporal variability of tidal mixing fronts on the European shelf and highlights a potential sensitivity to climate change due to positive correlations with rising temperatures. Consequences could include extension of the frontal season and intensification of the frontal density gradient with knock-on effects on associated biota. The density gradient of tidal mixing fronts was shown to act as a direct distribution boundary for plankton between different shelf-sea domains. Climate-change-driven shifts in the seasonality of these fronts may have a direct impact on dispersal of passive floating organisms, habitat connectivity and adult populations of species with planktonic larvae, including commercially important fish and the benthos. Apart from a barrier function, fronts were also found to be important foraging areas for specialist megavertebrates, which were strongly associated with persistent frontal areas, whereas generalist feeders were not. Tidal mixing fronts represent suitable conservation areas for sensitive species in shelf-seas. The underlying mechanisms leading to bio-aggregations at these sites require more research. High-resolution data, simultaneously collected across multiple trophic levels can be obtained by autonomous robotic fleets in the near future. <br/

Facing Southern Ocean warming: Temperature effects on whole animal performance of Antarctic krill (Euphausia superba)

The ongoing environmental changes in the Southern Ocean may cause a dramatic decrease in habitat quality. Due to its central position in the food web, Antarctic krill (Euphausia superba) is a key species of the marine Antarctic ecosystem. It is therefore crucial to understand how increasing water temperatures affect important krill life-cycle processes. Here, a long-term (August – March) laboratory acclimation experiment at different temperature scenarios (0.5 ◦C, 1.5 ◦C, 2.5 ◦C, 3.5 ◦C, 5 ◦C, 7 ◦C) was performed and the effects of elevated temperatures on whole animal parameters (O2 consumption, body length, length of the digestive gland) were analyzed. The response of krill oxygen consumption to different experimental temperatures differed between acute/short-term and long-term acclimation. After 8 months, krill oxygen consumption remained unchanged up to temperatures of 3.5 ◦C and was significantly higher at temperatures > 3.5 ◦C. Krill acclimated to temperatures ≥ 3.5 ◦C were significantly smaller at the end of the experiment. Limited food intake and/or conversion may have contributed to this effect, especially pronounced after the onset of the reproductive period. In addition, the seasonal growth pattern in males differed from that of females. Together, our findings indicate that warming Southern Ocean waters are likely to increase metabolic rate in krill, possibly altering the amount of energy available for other important life-cycle processes, a finding directly related to future population dynamics and fisheries management