Hydrostatic Pressure and Temperature Effects on the Membranes of a Seasonally Migrating Marine Copepod

Marine planktonic copepods of the order Calanoida are central to the ecology and productivity of high latitude ecosystems, representing the interface between primary producers and fish. These animals typically undertake a seasonal vertical migration into the deep sea, where they remain dormant for periods of between three and nine months. Descending copepods are subject to low temperatures and increased hydrostatic pressures. Nothing is known about how these organisms adapt their membranes to these environmental stressors. We collected copepods (Calanoides acutus) from the Southern Ocean at depth horizons ranging from surface waters down to 1000 m. Temperature and/or pressure both had significant, additive effects on the overall composition of the membrane phospholipid fatty acids (PLFAs) in C. acutus. The most prominent constituent of the PLFAs, the polyunsaturated fatty acid docosahexanoic acid [DHA – 22:6(n-3)], was affected by a significant interaction between temperature and pressure. This moiety increased with pressure, with the rate of increase being greater at colder temperatures. We suggest that DHA is key to the physiological adaptations of vertically migrating zooplankton, most likely because the biophysical properties of this compound are suited to maintaining membrane order in the cold, high pressure conditions that persist in the deep sea. As copepods cannot synthesise DHA and do not feed during dormancy, sufficient DHA must be accumulated through ingestion before migration is initiated. Climate-driven changes in the timing and abundance of the flagellated microplankton that supply DHA to copepods have major implications for the capacity of these animals to undertake their seasonal life cycle successfully

The role of microbes in the nutrition of detritivorous invertebrates: a stoichiometric analysis

Detritus represents an important pool in the global carbon cycle, providing a food source for detritivorous invertebrates that are conspicuous components of almost all ecosystems. Our knowledge of how these organisms meet their nutritional demands on a diet that is typically comprised of refractory, carbon-rich compounds nevertheless remains incomplete. ‘Trophic upgrading’ of detritus by the attached microbial community (enhancement of zooplankton diet by the inclusion of heterotrophic protozoans) represents a potential source of nutrition for detritivores as both bacteria and their flagellated protistan predators are capable of biosynthesizing essential micronutrients such as polyunsaturated fatty acids (PUFAs). There is however a trade-off because although microbes enhance the substrate in terms of its micronutrient content, the quantity of organic carbon is diminished though metabolic losses as energy passes through the microbial food web. Here, we develop a simple stoichiometric model to examine this trade-off in the nutrition of detritivorous copepods inhabiting the mesopelagic zone of the ocean, focusing on their requirements for carbon and an essential PUFA, docosahexaenoic acid (DHA). Results indicate that feeding on microbes may be a highly favourable strategy for these invertebrates, although the potential for carbon to become limiting when consuming a microbial diet exists because of the inefficiencies of trophic transfer within the microbial food web. Our study highlights the need for improved knowledge at the detritus-microbe-metazoan interface, including interactions between the physiology and ecology of the associated organisms

Loss of buoyancy control in the copepod Calanus finmarchicus

A mechanism is demonstrated that could explain large-scale aggregations of lipid-rich copepods in the surface waters of marine environments. Laboratory experiments establish that changes in salinity and temperature induce lipid-mediated buoyancy instability that entrains copepods in surface waters. Reduced hydrostatic pressure associated with forced ascent of copepods at fjordic sills, shelf breaks and seamounts would also reduce the density of the lipid reserves, forcing copepods and particularly those in diapause to the surface. We propose that salinity, temperature and hydrodynamics of the physical environment, in conjunction with the biophysical properties of lipids, explain periodic high abundances of lipid-rich copepods in surface waters

Protozoans as a food source for Antarctic krill, Euphausia superba: complementary insights from stomach content, fatty acids, and stable isotopes

We studied the diet of Antarctic krill, Euphausia superba, at five stations across the southwest Atlantic sector in summer 2003 by analyzing stomach content, fatty acids, and stable isotopes on the same individuals. Our aim was to examine what each method could contribute to our understanding of krill nutrition and whether differences seen in growth rates were linked to their food. All three methods indicated clear regional differences in diet, but small ontogenetic and sex-related differences. Overall, diatoms were the most abundant item in the stomach, but at three of the stations, tintinnids, large dinoflagellates, and other armored flagellates dominated the identifiable biomass. Copepod remains were rare. Fatty acids profiles gave additional information about feeding on weakly silicified diatoms and athecate heterotrophic dinoflagellates, with the latter being the main food source at one of the stations. Two independent indices of carnivory, d15N and the fatty acid ratio 18:1(n-9)/18:1(n-7), were correlated among krill from the same swarm, suggesting consistent differences in diet between individuals. An internal index of trophic position, (i.e., d15Nglutamic acid-d15Nphenylalanine) underlined the importance of heterotrophic food for the nutrition of krill, even in summer. Highest growth rates of krill were found during a diatom bloom and coincided with a mixed diet, large digestive gland, and fast stomach passage. However, even in a nonbloom, flagellate-dominated system, krill were able to sustain medium growth rates when feeding on heterotrophic dinoflagellates. Each method supplied specific information on krill nutrition, and the true picture is only revealed when the various methods are used together

Calanus finmarchicus seasonal cycle and diapause in relation to gene expression, physiology, and endogenous clocks: Calanus finmarchicus seasonal rhythmicity

The copepod Calanus finmarchicus plays a crucial role in the north Atlantic food web. Its seasonal life cycle involves reproduction and development in surface waters before overwintering in diapause at depth. Although diapause has been studied for more than a century, the factors responsible for the initiation and termination of it are still unclear. Endogenous clocks have been identified as potent tools for photoperiod measurement and seasonal rhythmicity in many terrestrial species, but knowledge of these remains scarce in the marine realm. Focusing on the dominant CV copepodid stage, we sampled a population of C. finmarchicus from a Scottish sea loch to characterize population dynamics, several physiological parameters, and diel and seasonal expression rhythms of 35 genes representing different metabolic pathways, including the circadian clock machinery. This generated a detailed overview of the seasonal cycle of C. finmarchicus including the most extensive field dataset on circadian clock gene expression in a marine species to date. Gene expression patterns revealed distinct gene clusters upregulated at different phases of the copepod's seasonal cycle. While diel clock cycling was restricted to the active spring/summer phase, many clock genes exhibited the highest expression during diapause. Our results provide new insights into diapause on physiological and genetic levels. We suggest that photoperiod, in interaction with internal and external factors (lipid content, temperature, food availability) and the endogenous clock mechanism, plays an important role in the timing of diapause in C. finmarchicus

Circadian Clock Involvement in Zooplankton Diel Vertical Migration

Biological clocks are a ubiquitous ancient and adaptive mechanism enabling organisms to anticipate environmental cycles and to regulate behavioral and physiological processes accordingly [1]. Although terrestrial circadian clocks are well understood, knowledge of clocks in marine organisms is still very limited [2, 3, 4, 5]. This is particularly true for abundant species displaying large-scale rhythms like diel vertical migration (DVM) that contribute significantly to shaping their respective ecosystems [6]. Here we describe exogenous cycles and endogenous rhythms associated with DVM of the ecologically important and highly abundant planktic copepod Calanus finmarchicus. In the laboratory, C. finmarchicus shows circadian rhythms of DVM, metabolism, and most core circadian clock genes (clock, period1, period2, timeless, cryptochrome2, and clockwork orange). Most of these genes also cycle in animals assessed in the wild, though expression is less rhythmic at depth (50–140 m) relative to shallow-caught animals (0–50 m). Further, peak expressions of clock genes generally occurred at either sunset or sunrise, coinciding with peak migration times. Including one of the first field investigations of clock genes in a marine species [5, 7], this study couples clock gene measurements with laboratory and field data on DVM. While the mechanistic connection remains elusive, our results imply a high degree of causality between clock gene expression and one of the planet’s largest daily migrations of biomass. We thus suggest that circadian clocks increase zooplankton fitness by optimizing the temporal trade-off between feeding and predator avoidance, especially when environmental drivers are weak or absent [8]

Trophic modes of large Antarctic Foraminifera: roles of carnivory, omnivory, and detritivory

Astrammina rara, Crithionina delacai, and Notodendrodes hyalinosphaira are 3 of the largest and most abundant members of the foraminiferal assemblage at a shallow-water (28 to 32 m) site in Explorers Cove, Antarctica. This study summarizes observations from 2 decades of research, during which we employed laboratory-based feeding experiments and fatty acid biomarker analysis to characterize trophic dynamics and ecological roles of the 3 species, In feeding experiments, A. rara consumed a variety of co-occurring metazoans (several Crustacea, Mollusca, Echinodermata, and a Nephtys species). C. delacai, N. hyalinosphaira, and a number of other foraminiferal species from Explorers Cove successfully trapped Artemia sp. nauplius prey in a setup designed to examine the efficiency of prey capture. Fatty acid analyses on samples from early (November 7, 2001) and late (January 31, 2002) austral summer revealed that the 3 species contained substantial amounts (33 to 45.5%) of polyunsaturated fatty acids (PUFAs), which are produced by microalgae, indicating the downwards transfer of carbon from sea-ice associated primary production. In the case of A. rara, this may be due to the ingestion of herbivorous metazoa, rather than direct uptake of microalgal material. A. rara contained significantly (p < 0.05) higher amounts of the zooplankton biomarkers 20:1(n-9) and 22:1(n-11), and C. delacai contained more PUFAs early, compared to late, in the season. Two morphotypes of N. hyalinosphaira had different fatty acid Profiles, indicating distinct trophotypes. Our results illustrate specific adaptations to different trophic resources in these protists, and they demonstrate the potential impact that large carnivorous species of Foraminifera may have on the structure of benthic communities where they are abundant

Shift from Carbon Flow through the Microbial Loop to the Viral Shunt in Coastal Antarctic Waters during Austral Summer

The relative flow of carbon through the viral shunt and the microbial loop is a pivotal factor controlling the contribution of secondary production to the food web and to rates of nutrient remineralization and respiration. The current study examines the significance of these processes in the coastal waters of the Antarctic during the productive austral summer months. Throughout the study a general trend towards lower bacterioplankton and heterotrophic nanoflagellate (HNF) abundances was observed, whereas virioplankton concentration increased. A corresponding decline of HNF grazing rates and shift towards viral production, indicative of viral infection, was measured. Carbon flow mediated by HNF grazing decreased by more than half from 5.7 µg C L−1 day−1 on average in December and January to 2.4 µg C L−1 day−1 in February. Conversely, carbon flow through the viral shunt increased substantially over the study from on average 0.9 µg C L−1 day−1 in December to 7.6 µg C L−1 day−1 in February. This study shows that functioning of the coastal Antarctic microbial community varied considerably over the productive summer months. In early summer, the system favors transfer of matter and energy to higher trophic levels via the microbial loop, however towards the end of summer carbon flow is redirected towards the viral shunt, causing a switch towards more recycling and therefore increased respiration and regeneration

Plasticity in dormancy behaviour of Calanoides acutus in Antarctic coastal waters

Copepods that enter dormancy, such as Calanoides acutus, are key primary consumers in Southern Ocean food webs where they convert a portion of the seasonal phytoplankton biomass into a longer-term energetic and physiological resource as wax ester (WE) reserves. We studied the seasonal abundance and lipid profiles of pre-adult and adult C. acutus in relation to phytoplankton dynamics on the Western Antarctic Peninsula. Initiation of dormancy occurred when WE unsaturation was relatively high, and chlorophyll a (Chl a) concentrations, predominantly attributable to diatoms, were reducing. Declines in WE unsaturation during the winter may act as a dormancy timing mechanism with increased Chl a concentrations likely to promote sedimentation that results in a teleconnection between the surface and deep water inducing ascent. A late summer diatom bloom was linked to early dormancy termination of females and a second spawning event. The frequency and duration of high biomass phytoplankton blooms may have consequences for the lifespan of the iteroparous C. acutus females (either 1 or 2 years) if limited by a total of two main spawning events. Late summer recruits, generated by a second spawning event, likely benefitted from lower predation and high phytoplankton food availability. The flexibility of copepods to modulate their life-cycle strategy in response to bottom-up and top-down conditions enables individuals to optimize their probability of reproductive success in the very variable environment prevalent in the Southern Ocean

Diapause induces remodelling of the fatty acid composition of membrane and storage lipids in overwintering larvae of Ostrinia nubilalis, Hubn. (Lepidoptera: Crambidae)

Seasonal changes in the FA composition of triacylglycerols and phospholipids prepared from the whole body of non-diapausing and diapausing fifth instar larvae of Ostrinia nubilalis, Hubn. (Lepidoptera: Crambidae) were determined to evaluate the role of these lipids in diapause. Substantial changes in the FA composition of triacylglycerols and phospholipids were triggered by diapause development. This led to a significant increase in the overall FA unsaturation (UFAs/SFAs ratio), attributable to an increase in the relative proportion of MUFAs and the concomitant decrease in PUFAs and SFAs. In triacylglycerols, the significant changes in FAs composition is the result of an increase in the relative proportions of MUFAs, palmitoleic acid (16:1n-7) and oleic acid (18:1n-9), and a concomitant reduction in composition of SFAs and PUFAs, mainly palmitic acid (16:0) and linoleic acid (18:2n-6), respectively. Changes in the composition of phospholipids were more subtle with FAs contributing to the overall increase of FA unsaturation. Differential scanning calorimetry (DSC) analysis revealed that the melt transition temperatures of total lipids prepared from whole larvae, primarily attributable to the triacylglycerol component, were significantly lower during the time course of diapause compared with non-diapause. These observations were correlated to the FA composition of triacylglycerols, most likely enabling them to remain functional during colder winter conditions. We conclude that O. nubilalis undergoes remodelling of FA profiles of both energy storage triacylglycerols and membrane phospholipids as an element of its overwintering physiology which may improve the ability to cold harden during diapause