may be abundant (Davis,. 1976 ... and J. R. Sargent, in prep.). Capelin are .... eastern Bering Sea (Laevastu and Larkins, 1981). The .... John Wiley, Chichester.
Rapp. P.-v. Réun. Cons. int. Explor. M er, 188: 146-153. 1989
Organization of a fjord community at 70° North: The pelagic food web in Balsfjord, northern Norway C. C. E. Hopkins, P. E. Grotnes, and J.-E. Eliassen
Hopkins, C. C. E ., Grotnes, P. E ., and Eliassen, J.-E. 1989. Organization of a fjord community at 70° North: The pelagic food web in Balsfjord, northern Norway. Rapp. P.-v. Réun. Cons. int. Explor. Mer, 188: 146-153. Key features regulating the productivity and structure of the pelagic food web in Balsfjord (70°N), northern Norway, are described and quantified. Seasonal aspects of anabolic and catabolic energy flux are analysed, and the characteristic features of the system leading to the production of stocks of capelin (M allotus villosus), herring (Clupea harengus), cod ( Gadus m orhua), and prawn ( Pandalus borealis) are high lighted. C. C. E. H opkins: Department o f A quatic Biology, Norwegian College o f Fishery Science, University o f Tromsø, P. O. B ox 3085, Guleng, N-9001 Tromsø, Norway. P. E. Grotnes and J.-E. Eliassen: Department o f Resource Biology, Norwegian Col lege o f Fishery Science, University o f Tromsø, P. O. B ox 3085, Guleng, N-9001 Tromsø, Norway.
Introduction The “Balsfjord Project” of the University of Tromsø is a multidisciplinary research project aimed at describing and quantifying the production processes in a fjord eco system at high latitudes. Research has been conducted on hydrography (e.g., Eilertsen et al., 1981a), phyto plankton (e.g., Eilertsen and Taasen, 1984), zooplank ton (e.g., Hopkins et al., 1984), sediments (e.g., Sar gent et al., 1983b), shellfish (e.g., Vahl, 1981 ; Hopkins, 1987a), and finfish (e.g., Eliassen and Vahl, 1982; Klemetsen, 1982; Hopkins et al., 1986). Trophic relationships play an essential part in shaping the pattern of species interactions. Delineating their existence, in the form of food chains and webs, provides important knowledge of ecosystems and how they func tion (Pimm, 1982). Their tabulation provides a guide to various key features that need to be incorporated into multispecies ecosystems models; the validity of such models depends to a large extent on their accuracy in depicting trophic behaviour (see Pope, 1976; Beddington, 1986). Despite this, detailed analyses of marine pelagic food webs are scarce, and most tend to resemble inverted species pyramids as the functional details of the lower trophic levels are frequently lacking (see Briand, 1983). The present paper, drawing on details of the ecology of individual species or components, traces the orga nization and trophic structure of the pelagic ecosystem 146
in Balsfjord leading from phytoplankton to fish apex predators. The biomasses at the various trophic levels are used to provide estimates of ecological efficiency in the fjord.
Materials and methods In describing the key plant and animal species present in Balsfjord (69°21'N 19°06'E), as well as relevant aspects of their seasonal cycles, reference has been made to specific, published studies (to date ca. 100 papers) from the “ Balsfjord Project” (see Hopkins, 1987b). Relevant refereed publications pertaining to Balsfjord are cited. To avoid a protracted literature list we have, where possible, referred the reader to publications where a review is provided. Trophic relationships can be delineated using several techniques. G ut contents are the most popular, and in the case of larger animals (e.g., fish) recognizable prey are frequently used to classify the trophic position of the predator. Nevertheless, differential digestion rates of resistant or malleable prey may cause problems (Jobling, 1987). Food chains can also be studied by follow ing the fate of marker compounds, such as lipids and hydrocarbons (Paradis and Ackman, 1977; Sargent and Whittle, 1981). Here the structure of the pelagic food web in Balsfjord has been traced on the basis of accu mulated results utilizing both of these techniques.
Key system components Physical environm ent and phytoplankton Balsfjord is a single-basin fjord, situated north of the Arctic Circle with a maximum depth of ca. 195 m (Fig. 1). Water exchange with the surrounding, warmer coas tal waters is limited by sills of 1 0 -3 0 m in depth. These features, coupled with a large catchment area for snow and ice, result in low bottom temperatures ( < 3°C most of the year). The 4°C isotherm only reaches 50-m depth during the latter part of the year (Eilertsen et a i, 1981a). The fjord is one of the coldest in Norway. Annual primary production measured by the 14C tech nique is ca. 115 g C itT2 (Eilertsen and Taasen, 1984). The spring bloom usually starts at the end of March and culminates by early May. The bloom is dominated by colonial diatoms (e.g., Chaetoceros socialis Laud, Nitzschia grunowii Hasle) and the haptophacean Phaeocystis pouchetii (Eilertsen et al., 1981b). The reduced standing crop in the summer is probably due to the combined effects of zooplankton grazing, vernal freshet (maximum phytoplankton densities are at ca. 10 m, under the pycnocline), and decreasing levels of incident
radiation (Fig. 2). A short bloom may occur in early autumn, but growth is restrained. Although the annual magnitude of total incident radiation can vary greatly, the months of March and O ctober, delineating the pri mary production season, are characterized by incident radiation of ca. 250 J cm -2 d ay-1.
Sedim entation and sedim ents A significant proportion of the annual phytoplankton production occurs before the macrozooplankton grazing population becomes established (Fig. 2) (Hopkins, 1981; Hopkins et al., 1984). The mean annual flux of phytoplankton carbon to 170 m is estimated as ca. 0.8 g C m -, or ca. 0.7 % of the annual carbon uptake rate. In early May, the flux of phytogenous carbon to the same depth is ca. 10 times greater (Lutter, 1984). Although copepods are active grazers of the primary production (see Hopkins et al., 1984), nearly all pellets in deeper water are from krill. Krill pellets account for the vast majority of recognizable organic matter reaching the fjord bottom (Lutter, 1984; Lutter et a l., in press).
Sandnes s u n d v . : '■;] ROMSO Tro m søs u n d
69
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Figure 1. Balsfjord, northern Norway. Location and fjord topography.
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Figure 2. Balsfjord, northern Norway. A ) Seasonal cycle of phytoplankton production, solar radiation, freshwater run-off, and B) A bundance of total zooplankton. Based on Eilertsen el al., 1981a; Hopkins, 1981; Hopkins et al., 1984.
Surface sediments from 195 m have shown negligible seasonal variation in total organic matter, organic C and N, amino acids, and lipids (Sargent etal., 1983b). Mask ing of the input from autochthonous detritus by extrane ous PIM and POM discharged by the freshet can be expected (Burrell, 1988). A significant proportion of the total fatty acids in the sediment are a mixture of odd-numbered straight-chain and branched-chain moie ties characteristic of microorganisms. The fatty acid composition of the sediment lipids reflects much more the presence of microorganisms than of planktonic ma terial. This is consistent with the rapid conversion of sedimenting material into a pool of sediment microor ganisms. The macrobenthos in the deep basin is dom inated by specialized deposit-eaters, such as the echinoderm Ctenodiscus crispatus, which accumulates fatty acids indicative of an extensive microbial input (FalkPetersen and Sargent, 1982; Sargent et al., 1983a).
Zoop lan kton The Balsfjord zooplankton is a species-poor, high bio mass (ca. 37 g wet weight m~2) community (Hopkins, 1981). Dense zooplankton sound-scattering layers (SSLs), dominated by krill, are present in the deep basin (Hopkins et a i, 1978; Evans and Hopkins, 1981). Only the common macroplanktonic copepods Cala148
nus finmarchicus and Metridia longa, the chaetognath Sagitta elegans, and the krill Thysanoessa raschi, T. inermis, and Meganyctiphanes norvegica form easily identifiable, trophic links in the transfer of materials to higher trophic levels. They all spawn during the phy toplankton production season, and growth is limited to this time ( A p ril-O c to b e r). Overwintering results in marked decreases in organic reserves, predominantly lipid in both copepods and krill, accounting for 40—7 0 % of that present at the end of the primary production season. C. finmarchicus, M. longa, and the two Thysanoessa species are primarily herbivorous, despite the length of the winter. Overwintering is successfully achieved by depositing large reserves of neutral lipids through feed ing to excess on phytoplankton. Fatty acid analyses of phytoplanktonic lipid from Balsfjord have confirmed the supposition that the abundance of (n-3) polyunsat urated fatty acids found in the neutral lipids in herbivo rous zooplankton from high latitudes is a direct conse quence of the abundance of (n-3) polyunsaturates in the phytoplankton biom embrane lipid (Sargent et al., 1985). Phaeocystis pouchetii figures significantly in the diet of herbivores (Sargent et al., 1985; Sargent and Falk-Petersen, in press; Tande and Båmstedt, 1987). It has been shown that the fatty alcohols of calanoids derive preferentially from de novo lipid biosynthetic activity, whereas the fatty acids derive preferentially from dietary lipid (Sargent et al., 1976; Sargent and Henderson, 1986). The m ajor fatty alcohols in the wax esters of C. finmarchicus are 20:1 and 22:1, while those in the wax ester of M. longa are 14:0 and 16:0 (Hopkins etal., 1985; Falk-Petersen etal., 1987). C. finmarchicus, with its abundance of 20:1 and 22:1 fatty alcohols, con tains a much greater proportion of its mass of wax esters as fatty alcohols, i.e., as de novo lipid. This is consistent with C. finmarchicus being strictly herbivorous (Sargent and Falk-Petersen, in press). On the basis of this, and seasonal changes in weight and chemical composition (Hopkins et al., 1986), Falk-Petersen et al. (1987) have classified M. longa as an omnivore, with possibly a mainly diatom input during the primary production p e riod; in the winter the lipid composition suggests a more carnivorous diet. The microzooplankton would be the most likely source. Nevertheless, the daily ration of M. longa in the winter does not balance metabolic require ments (Båmstedt et al., 1985). The krill T. raschi, T. inermis, and M. norvegica have different overwintering strategies (Falk-Petersen et al., 1981), and occupy different ecological niches (Hopkins et al., 1984). In midwinter, lipid-rich T. inermis contain ca. 55% of their dry weight as lipid, comprising 40% wax esters and 2 8 % triacylglycerol. A t this time the fatty alcohols of the wax esters are mainly 16:0 and 14:0, and small amounts of phytol (10 % of the total) are also present. The fatty acids of the wax esters are mainly 18:1 (76 % ); polyunsaturated fatty acids, primarily 20:5 (n-3) and 18:4 (n-3), are minor components ( < 6 % ).
Lipid-rich T. raschi in midwinter have 40 % lipids, com prising 4 4 % triacylglycerols and 10% wax esters. The fatty alcohol in the wax esters is then mainly phytol (93% of the total), whereas the fatty acids are more heterogeneous with 16:0 and 18:1 dominating. On the basis of this, the two Thysanoessa have been primarily classified as herbivores, yet T. raschi seems to switch to a detrital scavenging habit in the winter as indicated by the input of phytol when primary production is absent (Sargent and Falk-Petersen, 1981). M. norvegica is rich in triacylglycerols but does not contain wax esters. This, coupled with the presence of 20:1 and 22:1 fatty acids in the ratio 2:1, is consistent with a large dietary input of these fatty alcohols from wax esters of calanoid cope pods. M. norvegica is thus primarily a carnivore in Balsfjord (Sargent and Falk-Petersen. 1981). Small copepods (Pseudocalanus elongatus, Acartia longiremis, and Oithona spp.) may be abundant (Davis, 1976; Hopkins, 1981). They may provide food for larval cod, herring, and capelin (C. C. E. Hopkins, unpubl.), but are not a major pathway in the diet of post-larval and adult fish (Wiborg, 1949; Pearcy et a i, 1979; Klemetsen, 1982; Eliassen and G rotnes, 1985). They are eaten, though, by S. elegans and M. norvegica (C. C. E. Hopkins, unpubl.). S. elegans is the most abundant planktonic carnivore (Hopkins, 1981). It contains modest amounts of tria cylglycerols and only traces of wax esters; the former are probably derived from the wax esters of calanoid copepods as they contain appreciable amounts of 20:1 and 22:1 fatty acids, while the latter are rich in 20:1 and 22:1 fatty alcohols typical of calanoid wax esters (FalkPetersen et al., 1987). Although S. elegans feeds pre dominantly on the younger stages of C. finmarchicus and M. longa (Hopkins, 1981; Tande, 1983), successful recruitment also depends on nauplii from later repro ducing copepods or other microzooplankton (Tande, 1983). Despite its abundance S. elegans has only been registered very sporadically in the stomachs of cod (Klemetsen, 1983); it is essentially a trophic “dead-end” .
Prawns and fish Deep-water prawns (Pandalus borealis) are abundant in Balsfjord (Hopkins, 1987a; Hopkins and Nilssen, in press). Their stomachs contain little benthic material. Remains of calanoid copepods appear frequently in 0and 1-group prawns, and a major input of Thysanoessa spp. appears in the 3- and 4-group prawns. In many cases the minute scales of capelin {Mallotus villosus) are present in stomachs in high numbers (C. C. E. Hopkins and J. R. Sargent, in prep.). Capelin are caught as bycatch by prawn trawlers in Balsfjord, and the dead capelin are discarded on the trawling grounds. As live capelin are unlikely to be caught by prawns, the likely explanation is that the discarded capelin are scavenged upon by prawns on the bottom: a fascinating example of
a man-made feedback loop providing a trophic advan tage, through by-catch, for the species fished. A signif icant dietary input of 20:1 and 22:1, and 14:0 and 16:0 fatty acids (Hopkins and Sargent, in prep.) supports the stomach contents analyses. There is a lack of branched, short-chain fatty acids, suggesting that sediment-feeding is negligible. There is an indigenous stock of capelin (Mallotus villosus) in Balsfjord, in which two-year-olds compose the bulk of the spawning stock (Nyholmen and H op kins, 1988). Offshore capelin from Norwegian waters have lipid rich in 20:1 and 22:1 fatty acids, reflecting a large dietary input of calanoid wax esters rich in 20:1 and 22:1 fatty alcohols (Falk-Petersen et al., 1986). These same fatty acids are relatively scarce in Balsfjord capelin (Henderson et al., 1984), suggesting that they predominantly consume Thysanoessa spp. that lack very long chain monoenes. This is confirmed from stomach contents, which show that krill dominate the diet of Balsfjord capelin, although the calanoid M. longa (whose m ajor wax ester alcohols are 14:0 and 16:0, as found in T. inermis) is also common; C. finmarchicus is practically absent from the capelin diet (Pearcy et al., 1979; K. Aase, C. C. E. Hopkins, and O. Nyholmen, unpubl.). This is noteworthy, as C. finmarchicus is abundant in the fjord (Tande, 1982). Herring (Clupea harengus) in Balsfjord comprise two distinct groups: the genetically unique Balsfjord herring characterized by low vertebrae number and a very high frequency of a rare allele, and a migratory population of Atlanto-Scandian herring spawned off the Norwegian coast (Jørstad and Pedersen, 1986). Copepods (mainly M. longa and some Pseudocalanus) and krill ( Thysa noessa spp.) dominate the diet of Balsfjord herring (Pearcy et al., 1979; K. Aase and C. C. E. Hopkins, unpubl.). The Balsfjord herring live mainly near the head of the fjord, and their diet is dominated by M. longa (up to 104 per stomach). Herring found in the deep basin eat proportionately more krill (see Pearcy et al., 1979). Krill SSLs are generally restricted to the deep basins of fjords and are heavily preyed upon by pelagic fish (Evans and Hopkins, 1981; Falk-Petersen and H op kins, 1981). Herring and capelin tend to be segregated during most of the year, but occur together in the spring when mature capelin congregate at the head of the fjord for spawning (Nyholmen and Hopkins, in press). At this time capelin hardly feed (Hopkins et al., 1988), so that little trophic competition exists. A total of 72 taxa have been recorded in the diet of Balsfjord cod (Klemetsen, 1982). There are ca. 20 spe cies of fish present in Balsfjord; ca. 15 have been rec orded in the diet of cod, but only capelin and herring are major forage species (Pearcy et al., 1979; Klem et sen, 1982). P. borealis and Thysanoessa are the only other significant prey of Balsfjord cod (Wiborg, 1949; Pearcy e ta l., 1979; Klemetsen, 1982; Eliassen and Grotnes, 1985). Pearcy etal. (1979) suggested that in Balsfjord some cod were primarily benthic and did not 149
PH YT O PLANKTON
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Figure 3. Pelagic food web, Balsfjord. Fundamental trophic relationships determ ined from lipid m arkers and stomach contents. Symbols of O dum (1971).
migrate far off the bottom to feed, while others were predominantly pelagic and preyed on vertically migrat ing capelin and krill associated with dense krill SSLs (see Evans and Hopkins, 1981; Falk-Petersen and H o p kins, 1981).
Fundamentals o f the pelagic food web in Balsfjord The trophic relationships detailed here allow the funda mental characteristics of the pelagic food web in Bals fjord to be sketched in the form of a conceptual flow model (Fig. 3). The idea of discrete trophic levels with structured food chains has been criticized because of the difficulties in categorically assigning a trophic level to a specific species (Rigler, 1975). Attributable factors are the seasonal and ontogenetic cyclical nature of pelagic food webs; adults and juveniles eat prey, and eggs and young may themselves be prey for species which in turn are eaten by the adults (Hardy, 1924). As growth pro 150
ceeds the smaller prey species are released from preda tion by a particular predator as large ones become sub ject to it (Wyatt, 1976). Although conveniently summa rizing much information, the dynamic nature of food webs can never be adequately presented. Despite these qualifiers the conceptual model sketched here illustrates some important characteristics of the Balsfjord system. Cod are the apex predator of the pelagic system, with krill, capelin, and herring being the dominant prey; they are only weakly connected with the benthic community (c.f. the North Sea, D aan, 1973). The prawn is trophically dependent on the péla gial, a feature contrary to the general tendency to clas sify it in the literature as part of the benthic food chain (see Shumway et al., 1985). On average the number of trophic levels to cod is ca. 3.5, as it may either feed on krill at the second trophic level or on planktivorous fish and prawns at the third trophic level. In Balsfjord primary production provides short peri ods of plentiful food followed by long periods of food shortage. The primary production supports high cope-
pod and krill production, which is characterized by sum mer periods of lipid anabolism alternating with winter periods of catabolism (Hopkins et a i, 1984). Fatty fish (capelin and herring) crop the secondary production, which is easily accessible as concentrated sound-scatter ing layers. Although this is not significantly different from the Barents Sea, the preferential selection of krill by Balsfjord capelin is very different from that seen by the open-sea stocks. In Balsfjord the predominant paths of lipid transfer occur in 14:0 and 16:0 fatty acids (M . longa and Thysanoessa) and not 20:1 and 22:1 charac teristic of C. finm archicus-dom inated food chains (e.g., the North Sea and the Barents Sea). Annual primary production in Balsfjord is ca. 115 g C i t T 2 (Eilertsen and Taasen, 1984). The mean zooplank ton dry biomass is 4 g i t T 2, of which ca. 65 % is cope pods and 30% is krill (Hopkins, 1981). This is equiv alent to a “herbivore” standing stock of ca. 1.5 g C n r 2. Applying P/B of 6.5 for copepods and 5 for krill (C. C. E. Hopkins, unpubl.), this provides an estimate of an nual herbivore production of ca. 9 g C n r 2, or ca. 8 % of the annual phytoplankton production. In 1986 echointegrator and trawl surveys estimated the standing stock of 1+ age groups of capelin, herring, and cod in the fjord (240 km2) to be ca. 1500 tonnes (J.-E. Elias sen, unpubl.), or ca. 2 g C n T 2. With an expected “community” P/B of ca. 0 .5 - 1 .0 for these fish (gener ation times of 3 - 8 years), production will be rather less than unity. This indicates that high ecological efficien cies (ca. 2 0 % ) may be operative from the second trophic level onwards. In conclusion, much of the spring bloom does not sediment and appears not to be cropped by herbivores, and the pelagic production in the basins of northern Norwegian fjords provides high levels of commercially utilizable fish production. This fish production accounts for ca. 1 % of particulate primary production, and is generally comparable with the highly harvested, north ern continental shelf ecosystems, such as Georges Bank (ca. 1—2 % , Sissenwine, 1986), the North Sea (Steele, 1974; Andersen and Ursin, 1977; Daan, 1986), and the eastern Bering Sea (Laevastu and Larkins, 1981). The high transfer efficiencies suggest that the energetics of the Balsfjord ecosystem are relatively tightly bound in relation to pelagic fish production. However, the simi larity ceases when comparing the proportionate energy flow through the pelagic and benthic fish fractions; in Balsfjord the benthic production appears to drive a microbially dominated detritus food web which does not support a commercially harvestable production.
A cknow ledgem ents This paper is dedicated to all the scientists, technicians, students, and crew of research vessels who have taken part in the “Balsfjord Project” . We are grateful to the Norwegian Fisheries Research Council (NFFR), who have financially supported many aspects of this work.
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