Wilhelm Hagen

Fatty acid trophic markers in the pelagic marine environment

Fatty acids have been used as qualitative markers to trace or confirm predator-prey relationships in the marine environment for more than thirty years. More recently, they have also been used to identify key processes impacting the dynamics of some of the worlds major ecosystems. The fatty acid trophic marker (FATM) concept is based on the observation that marine primary producers lay down certain fatty acid patterns that may be transferred conservatively to, and hence can be recognized in, primary consumers. To identify these fatty acid patterns the literature was surveyed and a partial least squares (PLS) regression analysis of the data was performed, validating the specificity of particular microalgal FATM. Microalgal group specific FATM have been traced in various primary consumers, particularly in herbivorous calanoid copepods, which accumulate large lipid reserves, and which dominate the zooplankton biomass in high latitude ecosystems. At higher trophic levels these markers of herbivory are obscured as the degree of carnivory increases, and as the fatty acids originate from a variety of dietary sources. Such differences are highlighted in a PLS regression analysis of fatty acid and fatty alcohol compositional data (the components of wax esters accumulated by many marine organisms) of key Arctic and Antarctic herbivorous, omnivorous and carnivorous copepod species. The analysis emphasizes how calanoid copepods separate from other copepods not only by their content of microalgal group specific FATM, but also by their large content of long-chain monounsaturated fatty acids and alcohols. These monounsaturates have been used to trace and resolve food web relationships in, for example, hyperiid amphipods, euphausiids and fish, which may consume large numbers of calanoid copepods. Results like these are extremely valuable for enabling the discrimination of specific prey species utilized by higher trophic level omnivores and carnivores without the employment of invasive techniques, and thereby for identifying the sources of energetic reserves. A conceptual model of the spatial and temporal dominance of group-specific primary producers, and hence the basic fatty acid patterns available to higher trophic levels is presented. The model is based on stratification, which acts on phytoplankton group dominance through the availability of light and nutrients. It predicts the seasonal and ecosystem specific contribution of diatom and flagellate/microbial loop FATM to food webs as a function of water column stability. Future prospects for the application of FATM in resolving dynamic ecosystem processes are assessed.

Diet-induced changes in the fatty acid composition of Arctic herbivorous copepods: Experimental evidence of trophic markers

To verify the potential of fatty acids as trophic markers, feeding experiments were carried out with the dominant herbivorous copepods Calanus finmarchicus, C. hyperboreus and C. glacialis from the Greenland Sea during two Arctic expeditions in June/July 1991. Depending on the fatty acid composition of these copepods, the diatom Thalassiosira antarctica or the dinoflagellate Amphidinium carterae were offered as food to induce deviating fatty acid compositions. Since the copepodite Stages CV of C. finmarchicus had very low amounts of the 16:1(n−7) fatty acid but high amounts of 18:4(n−3), the specimens were fed on T. antarctica rich in 16:1(n−7) over a period of up to 42 days. At the end of the feeding experiment the portion of the 16:l(n-7) fatty acid had strongly increased by 11%, while the 18:4(n−3) fatty acid was almost depleted. In contrast, high amounts of the 16:1(n−7) fatty acid in C. hyperboreus (CV) suggested feeding on diatoms, therefore its diet was changed to A. carterae dominated by high amounts of the 18:4(n−3) fatty acid. After 47 days the portion of 18:4(n−3) increased by 8%, whereas 16:1(n−7) decreased by 3 %. In female C. glacialis the changes in the fatty acid composition after feeding with A. carterae were less pronounced as compared to the other species, due to a severe lipid loss during the experiment. The feeding experiments document the incorporation and turnover of dietary fatty acids under controlled laboratory conditions and provide clear evidence for the potential of specific fatty acids as trophic marker lipids.

Lipid biomarkers indicate different ecological niches and trophic relationships of the Arctic hyperiid amphipods Themisto abyssorum and T.libellula

Abstract. The hyperiid amphipods Themisto libellula and T. abyssorum are important components of Arctic pelagic ecosystems. Both species are carnivorous and prey on mesozooplankton. They represent a substantial food source for marine vertebrates and are a key link between zooplankton secondary production and higher trophic levels. We present data on the total lipid content, lipid class and fatty acid composition of T. libellula and T. abyssorum from northern Fram Strait and the central Arctic Ocean. Both species had moderate to high lipid contents of 14–42% of body dry mass. In T. abyssorum, total lipid content was correlated to body mass, while T. libellula showed sex-related differences in lipid content. Despite their smaller body size, females of T. libellula had higher lipid contents than males. Wax esters represented the major lipid class in both species with 41–43% of total lipid, while triacylglycerols contributed 23–32%. The fatty acid composition was dominated by the long-chain polyunsaturated moieties 20:5(n-3) and 22:6(n-3), short-chain saturated compounds (16:0 and 14:0) and monounsaturated fatty acids of varying length, i.e. 16:1(n-7), 20:1(n-9), 18:1(n-9) and 22:1(n-11). Species-specific and geographic variations in the fatty acid and alcohol patterns were apparently linked to differences in diet and life-cycle. High amounts of the fatty acids and alcohols 20:1(n-9) and 22:1(n-11) in T. libellula indicate predation on herbivorous Calanus copepodids. In addition, elevated levels of 20:5(n-3) in T. libellula indicate a close connection with ice-algal production and the importance of cryo-pelagic coupling processes (i.e. exchange processes between the sea ice and the pelagic communities) for the nutrition of this high-Arctic epipelagic species. In contrast, T. abyssorum is characterised by lower amounts of 20:5(n-3) and its biomarker ratios indicate a higher trophic level. This observation is consistent with the subarctic-boreal origin of T. abyssorum and its occurrence in deeper layers of the Arctic Ocean, where it may feed on omnivorous and/or carnivorous prey.

Herbivorous or omnivorous? On the significance of lipid compositions as trophic markers in Antarctic copepods

Three dominant Antarctic copepods, Calanoides acutus, Rhincalanus gigas and Metridia gerlachei (copepodite stages V and females), were collected during summer (January/ February) in the southern Weddell Sea south of 70°S. Detailed analyses of their lipid and fatty acid/ alcohol compositions were carried out. The trophic positions of these copepods were elucidated by means of the lipid compositions (“marker lipids”). High amounts of wax esters were found in C. acutus (92% of total lipids) and in R. gigas (84–86%). The level of wax esters in M. gerlachei was relatively low (27–42%), while the accumulation of triacylglycerols tended to be higher (19–22%). Characteristic lipid components of C. acutus were the long-chain monounsaturated fatty acids and fatty alcohols 20:1 (n-9) and 22:1 (n-11). These components together with elevated amounts of the 18:4 (n-3) and, to a lesser degree, of the 16:! (n-7) fatty acids, typical of phytoplankton lipids, indicate herbivorous feeding for C. acutus. Other abundant fatty acids were 20:5 (n-3) and 22:6 (n-3). The fatty acid composition of M. gerlachei was characterized by very high amounts of these 22:6 and 20:5 acids. Other important fatty acids were 18:1 (n-9) and 16:0, but only small amounts of 16:1 (n-7) and 18:4 (n-3) occurred. In contrast to C. acutus the fatty alcohols of M. gerlachei consisted almost exclusively of the short-chain components 14:0 and 16:0 M. gerlachei is known as an omnivorous species, which was clearly reflected by its lipid and fatty acid/alcohol pattern. Few data are available on the feeding of R. gigas, but it is usuaally described as an herbivorous small-particle feeder. R. gigas showed fatty acid/alcohol characteristics typical of either C. acutus or M. gerlachei. Higher amounts of the 16:1 (n-7) and 18:4 (n-3) fatty acids suggest herbivorous feeding, whereas the dominance of short-chain alcohols (14:0 and 16:0) resembled the lipid pattern found in the omnivorous M. gerlachei. Hence, the lipid composition of R. gigas showed an intermediate pattern, which implies a tendency towards an opportunistic feeding mode, positioned somewhere between the other two species.

The compositions of wax esters, triacylglycerols and phospholipids in Arctic and Antarctic copepods: evidence of energetic adaptations

Copyright (c) 1996 Elsevier Science B.V. All rights reserved. The fatty acid and fatty alcohol compositions of wax esters, triacylglycerols and phospholipids were determined in the Antarctic copepods Calanoides acutus, Calanus propinquus, Metridia gerlachei, Euchaeta antarctica and Euchirella rostromagna and in the Arctic copepods Calanus hyperboreus, C. glacialis, C. finmarchicus and M. longa to reveal similarities and differences between the nine species. The wax esters of the herbivorous species were clearly characterised by the long-chain monounsaturated fatty acids and alcohols 20:1 (n-9r and 22:1 (n-11r, whereas the omnivorous and carnivorous species usually had high relative amounts of the 18:1 (n-9r fatty acid and of the short-chain saturated alcohols 14:0 and 16:0. The wax ester-storing copepods contained only small amounts of triacylglycerol, but the latter was the dominant depot lipid in the Antarctic C. propinquus and E. rostromagna. The triacylglycerol fatty acid composition of C. propinquus deviated strongly from those of all other species due to large amounts of the two isomers 22:1 (n-11r and 22:1 (n-9r. The wax ester molecules of the herbivorous species had the highest energetic content, although the triacylglycerols of C. propinquus reached very similar energy levels. The wax ester-storing herbivorous species have developed similar lipid biochemical adaptations in both polar oceans. In contrast, predominantly triacylglycerol-storing species occur only in Antarctic waters. The phospholipids contained very high levels of polyunsaturated fatty acids, especially 22:6 (n-3r, which was about twice as abundant as 20:5 (n-3r and 16:0, the other characteristic fatty acids. In both, Arctic and Antarctic species, the fatty acid compositions of the phospholipids showed a pronounced uniformity. The extremely high degree of unsaturation is extraordinary as compared to other marine taxa.

Seasonal adaptations and the role of lipids in oceanic zooplankton.

Oceanic zooplankton species exhibit quite diverse life history traits. A major driving force determining their life strategies is the seasonal variability in food supply, which is most pronounced in polar oceans where fluctuations in primary production are extreme. Seasonal adaptations are closely related to the trophic level of zooplankters, with strongest pressures occurring on herbivorous organisms. The dominant grazers, calanoid copepods and krill (Euphausiacea), have developed fascinating solutions for successful overwintering at higher latitudes. They usually exhibit a very efficient storage and utilization of energy reserves to reduce the effect of a highly seasonal primary production. The predominant larger Calanus species from the Arctic and Calanoides acutus from the Antarctic biosynthesize large amounts of high-energy wax esters with long-chain monounsaturated fatty acids and alcohols (20:1 and 22:1 isomers) as major components. They survive the dark season at depth in a stage of dormancy called diapause. In contrast, the Antarctic Calanus propinquus, a winter-active species, synthesizes primarily triacylglycerols, which are dominated by long-chain monounsaturated fatty acids with 22 carbon atoms (2 isomers) and yield even higher calorific contents. The omnivorous and carnivorous species, which are less subjected to seasonal food shortage, usually do not exhibit such an elaborate lipid biosynthesis. Herbivores usually do not utilize much of their enormous lipid reserves for overwintering, but channel this energy towards reproductive processes in late winter/early spring. Timing of reproduction is critical especially at high latitudes due to the short production period, and lipid reserves ensure early spawning independent of external resources. These energetic adaptations (dormancy, lipid storage) are supplemented by other life strategies such as extensive vertical migrations, change in the mode of life, and trophic flexibility.

Ontogenetic and seasonal changes in lipid and fatty acid/alcohol compositions of the dominant Antarctic copepods Calanus propinquus, Calanoides acutus and Rhincalanus gigas

Lipid compositions of the dominant Antarctic copepods Calanoides acutus, Rhincalanus gigas and Calanus propinquus from the Weddell Sea have been investigated in great detail. Copepods were collected during summer in 1985 and late spring/early winter in 1986. The analyses revealed specific adaptations in the lipid biochemistry of these species which result in very different lipid components. The various copepodite stages of C. acutus synthesize wax esters with long-chain monounsaturated moieties and especially the alcohols consisted mainly of 20:1(n-9) and 22:1(n-11). R. gigas also generates wax esters, but with moieties of shorter chain length. The fatty alcohols consisted mainly of 14:0 and 16:0 components, while the major fatty acids were 20:5, 18:4 and 22:6, of which 18:4 probably originated from dietary input. In contrast, C. propinquus accumulates triacylglycerols, a very unusual depot lipid in polar calanoid copepods. Major fatty acids in C. propinquus were the long-chain monounsaturates 22:1(n-9) and 22:1(n-11), which may comprise up to 50% of total fatty acids. In C. acutus and C. propinquus there was a clear increase of long-chain fatty acids with increasing developmental stage. In contrast, the fatty acid and alcohol composition of the R. gigas copepodite stages were characterized by the dominance of the polyunsaturated fatty acids as well as high amounts of the monounsaturates 18:1(n-9) and 16:1(n-7). There was a considerable decrease of the dietary fatty acid 18:4(n-3) towards the older stages during summer; in late winter/early spring 18:4 was only detected in very low amounts. This tendency was also found in the other two species, but was less pronounced. In all three species dry weight and lipid content increased exponentially from younger to older stages. The highest portion of wax esters, or of triacylglycerols in C. propinquus, was found in the adults. Dry weight and lipid content were generally higher during summer. In late winter/early spring the variability was more pronounced and lipid-rich specimens showed a selective retention of long-chain monounsaturated fatty acids, whereas in lipid-poor specimens these fatty acids were very much depleted.

Zooplankton biomass in the ice-covered Weddell Sea, Antarctica

Zooplankton was sampled by a Rectangular Midwater Trawl (RMT 1 + 8) in Weddell Sea surface waters (0 to 300 m) between 66 and 78°S during austral summer (February – March 1983). Sixty-nine taxa including different developmental stages were considered and divided into 16 size classes between <1 and >39.5 mm length. Biomass was determined by taxon and size class for three different meso- and macroplankton communities in the oceanic region, on the northeastern shelf and on the southern shelf of the Weddell Sea. The highest biomass of 11.2 mg DW m−3 (3.4 g DW m−2) was found in the northeastern shelf community (70 to 74°S), where juvenile and adultEuphausia crystallorophias accounted for 3.7 mg DW m−3 (1.1 g DW m−2). Although not quantitatively sampled, early copepodite stages (CI to CIII) ofCalanoides acutus andCalanus propinquus ranked second with 2.7 mg DW m−3 (0.8 g DW m−2). Biomass in the northeastern shelf community was concentrated in the size ranges 1 to 4 mm and 19.5 to 39.5 mm. The oceanic community of the central Weddell Sea was dominated by copepods smaller than 5 mm, which made up half of the total oceanic biomass. The tunicateSalpa thompsoni (7.0 to 8.5 mm) was the dominant single species with 1.6 mg DW m−3 (0.5 g DW m−2). Euphausiids, mainly juvenile and adult krillEuphausia superba, comprised 1.2 mg DW m−3 (0.4 g DW m−2). Total standing stock in the oceanic community was 9.4 mg DWm−3 (2.8 g DW m−2). Lowest biomass values were found in the southern shelf community (south of 75°S) with 4.0 mg DW m−3 (1.2 g DW m−2), concentrated in the 1 to 4 mm and 14.5 to 34.5 mm size classes. Abundant species were the pteropodLimacina helicina (1 to 2 mm; 0.7 mg DW m−3; 0.2 g DW m−2) andE. crystallorophias (24.5 to 39.5 mm; 0.9 mg DW m−3; 0.3 g DW m−2). The data reveal that it is essential to distinguish among subsystems in the Southern Ocean. This leads to a better understanding of the structure and function of those pelagic food webs which represent alternatives to the paradigmatic krill-centered system.

Seasonal lipid dynamics in dominant Antarctic copepods: Energy for overwintering or reproduction?

Abstract Copepodite stages V and females of four dominant Antarctic species of calanoid copepods were collected during various expeditions to the eastern Weddell Sea in mid-winter, late winter to early spring, summer and autumn. Analyses of total lipid content and sexual maturity showed some general similarities between species concerning the seasonal cycle of energy reserves and gonad maturation, but also revealed important interspecific differences in the life histories of these copepods. Calanus propinquus and Metridia gerlachei exhibited a seasonal lipid pattern with maxima in autumn and lipid minima during spring. Lipid decrease in the females usually coincided with gonad maturation, which proceeded well before the onset of phytoplankton production. This basic pattern was not as clearly discernible in the females of Calanoides acutus and Rhincalanus gigas . In the Weddell Sea, C. propinquus and C. acutus reached much higher lipid levels and seemed to rely more on internal energy depots than did M. gerlachei and R. gigas . The specific timing of reproduction in the Weddell Sea also differed among the species. M. gerlachei had the longest reproductive period, probably extending from September to March, followed by C. propinquus (October–February) and C. acutus (November–March). In contrast, R. gigas seemed to reproduce only from late December to February in the eastern Weddell Sea. Our findings emphasize the importance of lipid reserves for fueling reproductive processes before the spring phytoplankton bloom becomes available. Only a smaller portion of the accumulated energy stores appears to be utilized for metabolic maintenance during the food-limited winter period.

Breaking the ice: large-scale distribution of mesozooplankton after a decade of Arctic and transpolar cruises

Abstract Mesozooplankton collected during five summer expeditions to the Arctic Ocean between 1987 and 1991 was analysed for regional patterns in biomass and species distribution, distinguishing between an epipelagic (0–100 m) and a deeper (0–500 m) layer. A total of 58 stations was sampled mainly in the Nansen, Amundsen and Makarov Basins of the central Arctic Ocean and in areas of the Greenland Sea, West Spitsbergen Current and Barents Sea. Results from the different expeditions were combined to create a transect extending from the Fram Strait across the Eurasian Basin into the Makarov Basin. Mesozooplankton dry mass in the upper 500 m decreased from 8.4 g m−2 in the West Spitsbergen Current to less than 2 g m−2 in the high-Arctic deep-sea basins. In the central Arctic Ocean, biomass was concentrated in the upper 100 m and was dominated by the large copepods Calanus hyperboreus and C. glacialis. In contrast, the mesozooplankton in the West Spitsbergen Current was more evenly distributed throughout the upper 500 m, with C. finmarchicus as the prevailing species. The distribution of abundant mesopelagic species reflected the hydrographic regime: the calanoid copepod Gaetanus tenuispinus and the hyperiid amphipod Themisto abyssorum were most abundant in the Atlantic inflow, while Scaphocalanus magnus was a typical component of the high-Arctic fauna. The relatively high mesozooplankton biomass and the occurrence of boreal-Atlantic species in the central Arctic Ocean are indicators for the import of organic material from allochthonous sources, especially from the northern North Atlantic. Hence, in spite of its enclosure by land masses, the Arctic Ocean is characterized by an exchange of water masses and organisms with the North Atlantic, and advection processes strongly influence the distribution of plankton species in this high-latitude ecosystem.