MARINE ECOLOGY PROGRESS SERIES Published November 23 Mar Ecol Prog Ser
Sources of primary production, benthic-pelagic coupling, and trophic relationships within the Northeast Water Polynya: insights from 613cand 515~ analysis
Keith A. Hobson1**,William G.Ambrose ~r~,Paul E. ~enaud~
'Prairie and Northern Wildlife Research Center, Canadian Wildlife Service, Saskatoon. Saskatchewan. Canada S7N OX4 'Department of Biology, Bates College. Lewiston, Maine 04240,USA
ABSTRACT: We used stable carbon (l3C/I2C) and nitrogen (fS~/'") isotope analysis to investigate linkages between sources of primary production and the pelagic and benthic components of the North- east Water (NEW) Polynya off northeastern Greenland. Ice algae was enriched in 13C (mean 6I3C = -18.6 vs -27.9%) and I5N [mean 615~= 8.3 vs 4.9%0)over particulate organic matter [POM) suggesting that the relative importance of these sources might be traced isotopically. Most grazing crustaceans and filter-feeding bivalves had 6I3C and 615~values in the range of -21 to -23% and 7 to 9x0, respectively, indicating a direct pathway from POM. Close benthic-pelagic coupling was also confirmed for other benthic organisms examined with the exception of the predatory or deposit feeding echinoderms Ophioctin, Ophiacantha and Pontaster. Compared with other Arctic and temperate marine food webs, stable-carbon isotope values for the NEW Polynya were depleted in I3C. A S1'N trophic model that incorporated taxon-specific isotopic fractionation factors indicated that the NEW Polynya consisted of 4.5 to 5 trophic levels. Stable-isotope analysis Inay be well suited to establ~shingthe importance of polynyas as sites of high primary productivity and tight benthic-pelagic coupling relative to regions of more permanent ice cover.
KEYWORDS: Polynya . Stable isotopes - Carbon-13 . Nitrogen-15 Ice algae . Primary production
INTRODUCTION Barry 1991) where it has been suggested that a greater portion of biogenic material may reach the bottom than Marine benthic communities are generally depen- at lower latitudes (Petersen & Curtis 1980). In the few dent on primary production in the overlying water col- studies of biogenic sedimentation in boreal and Arctic umn for their energy. Consequently, the distribution systems, a large portion (30 to 96 %) of the carbon fixed and abundance of benthic organisms are often depen- annually fell ungrazed to the benthos (Atkinson & dent on water column processes which affect the trans- Wacasey 1987, Wassman 1991); this percentage is con- fer of organic material between benthic and pelagic siderably higher than that reaching the benthos at systems (Davis & Payne 1984, Fowler & Knauer 1986, lower latitudes (Smetacek 1980, Suess 1980, Forsskall Townsend & Cammen 1988). In general, pelagic-ben- et al. 1982, Davis & Payne 1984). For similar depth and thic coupling appears to be particularly tight in the substrate types, benthic biomass in the Arctic appears Arctic (reviewed by Carey 1991 and Grebmeier & to be greater than at lower latitudes (Petersen & Curtis 1980, Rowe 1983), suggesting that a greater proportion of the primary productivity may be cycled through the 'Address for correspondence: Canadian Wildlife Service, 115 Perimeter Road, Saskatoon, Saskatchewan, Canada S7N 0x4. benthos in the Arctic than in temperate or tropical E-mail. [email protected] regions.
0 Inter-Research 1995 Resale of full article not permitted 1Mar Ecol Prog Ser 128: 1-10, 1995
Oceanographic discontinuities can have a large degree of coupling between pelagic primary produc- effect on phytoplankton productivity, and therefore tion and the benthos. We hypothesized that significant may affect benthic dynamics. As recurring mesoscale inputs of carbon from bacterial or meiofaunal sources, areas of open water within areas of pack ice, polynyas or from ice algae, would result in greater 13C enrich- are one of the most conspicuous oceanographic fea- ment of benthic organisms than that expected from tures in polar regions and are important components of direct phytoplankton input. We also used stable-nitro- the Arctic ecosystem (Stirling 1980, Dunbar 1987, Mas- gen isotope analysis to delineate trophic relationships som 1988). These areas are also characterized by high within the NEW Polynya in order to confirm individual levels of primary productivity (Baumann 1989). Ben- species feeding patterns. thic communities under polynyas may, therefore, be very different from communities under nearby ice cov- ered areas (Ambrose & Renaud 1995). STUDY AREA AND METHODS Tracing sources of primary productivity supporting food webs is a difficult task, particularly in polar marine The NEW Polynya is largely a summer polynya cen- ecosystems where long-term sampling of food web tered off Nordostrundingen, northeast Greenland components may often be impossible. Even where or- (Parkinson et al. 1987; Fig. 1A). The polynya varies in ganic material in stomachs can be identified, several size and position among years but lies between 77" and limitations of conventional dietary approaches can con- 81" N latitude and 5" and 15" W longitude. At its maxi- found such analyses (Hyslop 1980). The value of mea- mal extent, the polynya is bound by the coast on the suring naturally occurring stable isotopes of carbon west, the shoreward edge of the south-flowing East and nitrogen within marine food webs is based on the Greenland Current on the east and ice on the south. The observation that these isotopes often undergo pre- NEW Polynya is a consistent annual feature opening for dictable step-wise enrichments between trophic levels the summer in April or May and closing in September. (Rau 1982, Wada et al. 1987, Fry 1988). Compared to Throughout the winter, parts of the polynya may peri- conventional dietary analyses which only provide a odically open and close (Schneider & Budeus 1995). measure of ingested food, stable isotope analysis of The bathymetry and water circulation on this section food web structure has the advantage of providing of the Greenland shelf are complex (Fig. 1B). The time-integrated averages of assimilated foods and, polynya is often centered over 2 shallow banks. The thus, represents a complimentary method for delin- southern and larger of the two, Belgica Bank, is bound eating patterns of trophic structure and energy flow on the north, south, and west by troughs with average (Fry 1988, Owens 1988, Harrigan et al. 1989, Hobson water depths of 300 m and some depths exceeding & Welch 1992, Rau et al. 1992). Where 2 isotopically 500 m (Fig. 1B).Most of the samples for isotopic analy- distinct sources of primary productivity are available sis were collected from the northern bank or from the to marine food webs, stable isotope analysis may also northern trough, areas which experience open water provide information on the relative importance of each every summer and which are located well within the source (reviewed by Fry & Sherr 1988) and the power of polynya. Circulation of surface water (
the evacuation of gut contents prior to isotopic analy- mass spectrometer without cryogenic separation. Both sis. Benthic infauna and epifauna, epibenthic preda- CO2 and N, gases were analysed using a VG OPTIMA tors, and fishes were collected using box cores, epiben- isotope-ratio mass spectrometer at the National thic sledges and Agassiz trawls. Tissues from birds and Hydrology Research Institute in Saskatoon, Saskat- polar bears were collected opportunistically by other chewan, Canada. Stable-isotope ratios were expressed researchers studying these groups. in 6 notation as parts per thousand (%o) according to When possible, we used muscle tissue for isotopic the following relationship: analysis. However, for most small invertebrates, tissues were obtained by combining a suitable number of whole specimens. Muscle tissue was dissected from where X is I3C or ISN and R is the corresponding ratio bivalves, fish, and seabirds. Whole blood samples from l3C/l2C or l5N/I4N. Standards for 13C and 15N are PDB polar bears were analysed. All tissues were freeze- and atmospheric N2 (AIR), respectively. Replicates dried and powdered with mortar and pestle or analyti- using laboratory standards indicate analytical errors cal mill. Samples comprised of whole organisms were of +0.1 and 0.3% for carbon and nitrogen samples, then treated with 2 N HC1 to remove carbonates. respectively. Because organisms may vary in their concentrations of Based on the findings of Hobson & Welch (1992), we isotopically lighter lipids (Attwood & Peterson 1989, generally applied an 15N trophic-enrichment factor of Monteiro et al. 1991, Sholto-Douglas et al. 1991), lipids +3.8%0 to obtain trophic level estimates according to were removed from all samples using a Soxhlet appa- the relationship: ratus for 4 to 6 h with chloroform as a solvent. Samples for I3C/l2C analysis were loaded into Vycor tubes with CuO and silver foil, sealed under vacuum where D is the 6I5N value of the organism, 4.9 refers to and then cornbusted at 850°C for 6 h. A similar the mean value of POM, and TL is the organism's approach was used for I5N/l4N analysis but samples trophic level (see Table 1). We also used this relation- were also loaded with copper wire and CaO to absorb ship to determine trophic level for polar bears even carbon dioxide and facilitate direct transfer of N2 to the though we examined bear blood and not muscle. Since
Fig. 1 Location (A: shaded area) and bathymetry (B) of the Northeast Water Polynya Mar Ecol Prog Ser 128: 1-10, 1995
Table 1 Location, depth, stable-carbon and nitrogen isotope values (mean ? SD) and estimated trophic level for components of the NEW Polynya marine food web. TL: trophic level
Sample N Location Sample 6I3C 615N TL depth (m) (mean)
Algae POM 3 80" 27' N, 13" 40' W 6 -27.7 * 0.6 4.8 0.2 1 .O POM 2 80" 27' N, 13' 40' W 16 -28.4 5.0 Ice algae 2 7f0 10' N, 10" 28' W Surface -18.7 8.2 Ice algae 1 79" 57' N, 15' 05' W Surface -18.4 8.4 Ph ycodrys sp l 81" 00' N, 12" 54' W 48 -37.1 4.6 Crustaceans Calanus hyperboreus 4" 77" 10' N, 10' 29' W 0-200 -22.7 * 0.1 7.6 r 0.7 1.7 Calanus gracilis Id 79" 57' N, 15' 47' W 0-70 -22.3 8.2 1.9 Themisto sp. l 80" 08' N, 15" 47' W 0-70 -24.2 10.4 2.5 Gammarus wilkitskii l 80" 06' N, 10" 10' W 0-70 -23.0 9.3 2.2 Anonyx sp. l 80" 59' N, 10" 59' W 59 -26.3 8.3 1.9 Arcturus sp. 3d 81" 00' N, 12" 54' W 48 -24.0 +0.4 8.2 * 0.2 1.9 Spironlocaris sp. l 81" 00' N, 12" 54 W 48 -21.1 10.3 2.4 Sclerocrangon ferox Id 80" 01' N, 6" 43' W 310 -23.3 16.3 4.0 Bivalves Arctlnula groenlandica 8 81' 13' N. 11'31' W 4 5 -22.0 * 0.4 9.7 * 0.1 2.3 Astarte crenata 5 80" 06' N, 10" 42' W 194 -21.3 *O2 11.9 * 0.1 2.8 Gastropod Clione sp. 5 79" 57' N. 15' 47' W 0-70 -20.2 * 0 6 9.8 * 0.5 L 3 Echinoderms Ophiopleura borealis 8 80" 01' N, 6" 43' W 310 -21.1 ? 0.6 11.8 * 0.6 2.8 Ophioctin sericeum 33 80" 01' N, 6" 43' W 310 -18.5 i 1.1 l 1.7 * 0.2 2.8 Ophiacantha bidentata 3 80" 59' N, 10" 59' W 59 -18.0 * 0.5 12.9 2 0.1 3.1 Ophioscolex glacialis 6 80' 01' N, 6" 43' W 310 -22.3 * 0.5 11.7 * 0.5 2.8 Ophiura sarsia 2" 79" 53' N, 10' 56' W 169 -22.0 11.9 2.8 Pon taster tenuispinus 5 79" 55' N, 15" 00' W 165 -19.4 * 2.2 13.2 t 0.5 3.2 HeBometra glacialis 7 79" 55' N, 15" 00' W 165 -22.3 * 0.6 12.3 * 0.5 3.0 Polychaetes Nephtys sp. 5 80" 29' N, 13" 30' W 3.1 Maldanidae 4 77" 10' N, 10'29' W 3.0 Pisces Artedicellus europeus 3 80" 29' N, 13" 30' W 3.5 2 80" 01' N, 6" 43' W 3.8 Boreogadus saida 1 80" 40' N, 13" 13' W 3.3 1 80" 59' N, 11" 34 W 3.3 1 80" 35' N, 9" 21' W 3.1 Icelus bicornis 5 80" 59' N, 11" 34' W 3.3 Liparis koefoedi 7 80" 59' N, 10" 59' W 3.1 Lycodes rossi 3 80" 01' N, 6" 43' W 3.7 Micrnrne~istuspoutassou 3 80" 29' N, 13' 30' W 3.2 3 80" 01' N, 6" 43' W 3.1 Sebastes marinus 1 80" 01' N, 6" 43' W 3.5 Triglops nybelini 5 ND 3.3 Birds Larus hyperboreus 80" 38' N, 13" 43' W 4.0 Soma teria mollisima 80" 38' N,13" 43' W 3.3 Soma teria specta bilis 80" 38' N, 13" 43' W 3 5 Mammals Ursus maritimus 5 h -19.4 * 0.7 4.6
"Combined sample of several individuals (see 'Methods') 'Locations of polar bear captures ranged from 79" 07' to 80" 44' N and 10" 57' to 19" 20' W Hobson et al.: Insights from 6I3C and 6"~analysis
captive-rearing studies on birds suggest a diet-tissue Ursusmarlomus POLARBEAR isotopic fractionation factor of +2.4 'Xm is appropriate for - Larushyperboreus these taxa (Hobson & Clark 1992), we used this value somar~rlamolllsslma SEABIRDS -c and the relationships TLbird= 7Zprey+ 1 and D,,,, = Dblrd ~omarer~aspectab~lis - 2.4 in order to modify the above equation to: Arredielluseuropeus - Lycodesrossl Lipawkoeloedi I TLbird= (Dbird- 7.3)/3.8 + 2 Tnglopsnybehni & Icelusbicornis .+ FISH Sebasresmarinus Micromesisruspourassou .. Boreogadussaida -C
RESULTS Ophiacanrhabldenrala Ophiocansericium Ponrasrerrenuispinus Our isotopic analyses revealed a considerable range Ophiopleuraboreab Oph~urasarsr in both I3C and 15N values for food web components of Hel~omerrasp. the NEW Polynya (Table 1). Average stable carbon iso- Ophioscoiexglacialis I Nephryssp. POLYCHAETES tope ratios ranged from -37.1 %C,for the macroalga Phy- Maldanidae -C codrys through -18.0% for the echinoderm Ophiacan- BIVALVESB GASTROPODS tha. - Ice algae was enriched considerably in 13C over -c , POM indicating that stable carbon isotope analysis Arcr~nulagroenlandica Sp~ronrowrissp. may be used to discern the relative contributions of Calanusgracilis these sources of primary production. Considerable Calanus hyperboreus Gammaruswilkifskii CRUSTACEANS overlap in I3C values throughout the food web was Sclerocrangonlerox Themisfosp apparent with no clear pattern of trophic enrichment Arclurussp after the second trophic level (Fig. 2). Some organisms, Anonyxsp. particularly the bivalve Astarte crenata,and the echin- Ice algae ALGAE POM 4 POM - oderms Ophioctin, Ophiacantha and Pontaster were I I l I I I I notably enriched in I3C compared to conphyletics. The mean POM 613C value of -27.9% was consider- ably lower than values recorded for other regions of the Arctic. In order to determine if this low 613C value for Fig. 2. Distribution of stable-carbon isotope ratios (mean * SD) primary productivity in the NEW Polynya was trans- among food web components of the Northeast Water Polynya ferred characteristically throughout the food web, we contrasted our data with patterns of 613c distribution in other published studies of high latitude (western Benng Sea: McConnaughey & McRoy 1979, Chukchi Sea: Pelagic Benth~c Dunton et al. 1989, Lancaster Sound: Hobson & Welch 1992) or cold-temperate (Scotia Sea: Mills et al. 1984, Georges Bank: Fry 1988) marine systems (Fig. 3). We classified organisms primarily into pelagic versus ben- thic categories, and secondarily into the general feed- ing categories of POM grazers, planktivorous fish, ben- thic filter feeders and benthic omnivores. Throughout these components of the food web, organisms from the NEW Polynya were consistently less enriched in 13C compared to the other areas (Fig. 3).Within the pelagic LancoslerSound' zone, all studies showed a strong positive shift in 6I3c between POM and POM grazers generally followed by Georges Bonk4 a smaller enrichment to planktivorous fish. Within the Chukcna Seas benthos, omnivores were generally enriched over filter NE Greenlondb feeders. In the 5 cases where POM qrazers could be compared to benthic filter feeders within the same sys- POM POM Plankt~vorous Benthrc Benthbc Grazers Fish Filter Feeders Omnrvores tem, the NEW Polvnva. . and Lancaster Sound studies showed little difference in mean 613~ whereas Fig. 3. Average 6I3C values for selected food web components reported in this study and other Arctic and temperate isotopic the Georges Bank' and western Sea investigations. References for data: 'Hobson & Welch (19921, studies showed higher I3C enrichment between these ~M~c~~~~~~~~~& McRoy (1979), et al. (1984), 4~~~ feeding groups (Fig. 3). (i988),'~unton-et al. (1989). 'this study Mar Ecol Prog Ser 128: 1-10, 1995
Within species, I5N values were generally less vari- metra sp.); (Table 1, Fig. 3). Similar results have been able than 13C and a step-wise increase with trophic found in isotopic investigations of marine food webs in level ranged from an average of 4.9%0for POM through Lancaster Sound (Hobson & Welch 1992), the west 18.6x0 for polar bear blood (Table 1, Fig. 4) suggesting Bering Sea (McConnaughey & McRoy 1979), and the a food web consisting of approximately 5 trophic levels. eastern Chukchi Sea (Grebmeier et al. 1988, Dunton et Stable-nitrogen isotope values for POM were similar to al. 1989; Fig. 3). Benthic organisms in systems exhibit- those found at other arctic locations (reviewed by Hob- ing weaker benthic-pelagic coupling would be ex- son & Welch 1992) and were considerably less enriched pected to be substantially enriched in 13C relative to than ice algae. This indicates that 615N measurements both POM and POM grazers. Stable-carbon isotope might also be used to delineate relative inputs of ice values of the bottom nepholoid layer of the sediments algae and POM to the benthos. sampled in midsummer were primarily in the range of -24 to -23% (H.Notholt pers. comm.) and this again reflects the presence of ungrazed POM reaching the DISCUSSION benthos. We observed greater enrichment in 13C between Benthic-pelagic coupling POM and POM grazers than between higher trophic levels, a pattern common to other high latitude marine Our isotopic investigations of the NEW Polynya sup- food webs (Fig. 3). It is not clear why this pattern exists. port the hypothesis that a major component of the ben- One possibility may be the presence of a strong micro- thic community was supported primarily by ungrazed bial loop in which fixed carbon is first cycled through POM reaching the benthos. Carbon evidence for this is flagellates and microzooplankton before being con- the similarity in 613C values between pelagic POM- sumed by zooplankton. based feeders (e.g. Calanus spp., Themisto sp.) and In our study, POM and ice algae were the only possi- benthic filter feeders (Arctinula groenlandica, Helio- ble sources of significant primary production in the NEW Polynya. The red alga Phycodrys, while having a distinct and highly negative 613C value (Table l),likely POLAR BEAR - contributed little carbon to the food web because it is Larus hyperboreus restricted to shallow (<50 m) water and many of the Somareriaspecrabilis Somareriamollissima animals in this study were collected considerable dis-
Lycodes rossi tances from shallow banktops. The difference in 6I3C Anedielluseuropeus and 615N values between POM and ice algae (Table 1) Trrglops nybelini lcelus bicornis permitted further insight into the relative input of Boreogadussaida Micrornesrsruspoutassou these sources to the food web. While it is possible that Liparis koefoedi ice algae contributed to the 5%0enrichment in 13C we Nephryssp. - POLYCHAETES observed between POM and POM grazers, the contri- Maldanidae -c. bution was minimal since most grazing crustaceans ~eliomefiasp. -C and filter-feeding bivalves had 615N values in the Oph~acanrhabrdentara ECHINODERMS Ophiura sarsi . range of 7 to 9Yw (Table 1).This is consistent with Ophropleuraborealis -C Ophroctinsenceum )I direct feeding on POM and not the isotopically heavier Ophioscolexglacralis -C ice algae. Stable-carbon isotope values for these Astarre crenata i organisms were typically in the range of -21 to -23%0, Clionesp. * BIVALVES& GASTROPODS Arcrrnulagroenlandica which is consistent with a general depletion of 13C in
Sclerocrangonferox food webs with latitude in the northern hemisphere Themistosp. (Fontugne & Duplessy 1981, Rau et al. 1982, 1989, Spironrowrissp Gammaruswrlkirskii CRUSTACEANS Dunton & Schell 1987). Low 613C values were gener- Arcrurus sp Anonyx sp. ally maintained through the food web, including fishes Calanusgracilis Calanushyperboreus and benthic invertebrates, again confirming the impor- tance of POM as a food source for the entire food web. * ALGAE I l I The only notable exception to this pattern was some enrichment of 13C observed in the benthic deposit- feeding echinoderms, Ophioctin, Ophiacantha, and Pontaster (Table 1). Stable carbon isotope analysis, therefore, provides a complimentary data set support- Fig. 4. Distribution of stable-nitrogen isotope ratios (mean * SD) among food web components of the Northeast Water ing the evidence of benthic-pelagic coupling emerging Polynya from studies of the NEW Polynya. Ambrose & Renaud Hobson et al.: Insights from 613C and SlsN analysis 7
(1995) suggested that benthic and pelagic processes in 615N trophic enrichment in marine food webs develops. the NEW Polynya are tightly linked based on strong In general, the trophic positions predicted by 615N correlations between sediment pigment concentra- are in good agreement with literature on fish and tions and both water column pigment concentrations invertebrate gut contents and feeding behaviour. and benthic biomass. Additionally, low water column Based on the assumption that POM was the first and sedimentary microbial activity (NEWATER 1993) trophic level, our sample of crustaceans included pri- and reduced zooplankton grazing (K. Daly pers. marily POM grazers (i.e. TL 2), with the notable excep- comm.) increases the likelihood that POM reaches tion of a single Sclerocrangon ferox that occupied TL 4 benthic food webs relatively intact. and likely consumed small crustaceans and bivalves. Mechanisms controlling 613C fractionation between The pectinid bivalve Arctinula was primarily a filter inorganic substrates and marine algae are not well un- feeder, whereas Astarte with its more enriched 615N derstood (Fry & Sherr 1988).However, isotope fraction- value was more likely a deposit feeder. Echinoderms ation associated with carbon fixation may differ be- and polychaetes generally occupied the third trophic tween POM and ice algae due to local differences in the level (Table 1) and this is consistent with benthic availability of CO2 for photosynthesis. The enriched deposit feeding (e.g. Ophioctin, Pontaster; Mortenson ice-algal 613C values relative to those of POM might 1927, Warner 1982, Pearson & Gage 1984) or preda- also be caused by a more general phenomenon: that tor/scavenger (e.g. Ophiacantha; Warner 1982, Pear- isotopic discrimination in aquatic plants is related to the son & Gage 1984) foraging niches. Fish ranged over a thickness of diffusive boundary layers that ultimately trophic level from primarily planktivorous species such determine the rate of CO, or HC03- diffusion (Smith & as Liparis, Boreogadus and Micromesistus (TL 3.1 to Walker 1980). Well-defined boundary layers such as 3.3; Briskina 1939, Green 1983) through Artedicellus those associated with littoral or epontic algae lead to an and Lycodes (TL 3.5 to 3.8), which are predatory on entrapment of otherwise normally expelled or discrimi- larger benthic invertebrates and fishes (Briskina 1939, nated 13C. The subsequent enrichment in 13C of carbon Klekowski & Weslawski 1990, von Dorrien 1993). available for photosynthesis would thus result in higher Trophic-level estimates for both common Somateria 613C values of ice algae carbon (Keeley & Sandquist mollissima and king S. spectabilis eiders were similar 1992, see also Simenstad et al. 1993). Algae occurring and were about a trophic level above their assumed in pelagic or turbulent water conditions such as those bivalve prey (Godfry 1986). Gut contents of the same associated with POM are expected to have reduced birds analyzed in this study were similar, consisting boundary layers and consequently decreased 613C val- primarily of bivalves (J. M. Weslawski pers. comm.). ues. In a recent review of the literature, France (1995) The trophic level estimate for Larus hyperboreus determined that in marine coastal areas, littoral algae (TL4.0, Table 1) is consistent with published studies of may be enriched by up to 10%0(mean 6%0)relative to their preference for fish, bird chicks, and carrion (Ain- pelagic algae. The boundary layer which develops over ley & Sanger 1979, Stempniewicz & Weslawski 1992). attached algae within the littoral zone may be a key Trophic level estimates for polar bears near the NEW factor determining the observed enrichment in I3C of Polynya were slightly lower than those obtained from benthic organisms that was previously associated with Lancaster Sound (Hobson & Welch 1992). This may be bacterial or meiofaunal processes (McConnaughey & due to the fact that trophic level estimates for bears at McRoy 1979, Dunton et al. 1989). the NEW Polynya site were based on 615N analyses of blood instead of muscle, and it is not known to what extent isotope fractionation values differ for various Trophic structure of the polynya bear tissues. Bear tissue samples were also obtained in late spring at the NEW Polynya site versus in winter for Our 615N trophic model for the NEW Polynya is in the Lancaster Sound study. It is possible that seals general agreement with our expectation of a 4 to 5 taken by bears differed in their trophic level between trophic level system in the high Arctic and demon- these seasons and locations. Seals depend on inverte- strates again the utility of the isotope approach to brates as well as fish; and young seals, in particular, marine food web studies (Minagawa & Wada 1984, Fry may consume more invertebrates than older seals and 1988, Hobson & Welch 1992). Moreover, our model is so may occupy a lower trophic position (Bradstreet et among the first to apply more than one 6I5N trophic al. 1986, Hobson & Welch 1992). Our data suggest that enrichment factor to various taxa within the food web seals taken by bears off northeastern Greenland occu- based on evidence from captive-rearing studies (see pied an average trophic level of about 3.6. also Hobson & Welch 1992, Hobson 1993). Undoubt- For some organisms, direct comparisons could be edly, further refinements of this model will be appro- made between trophic level estimates for the NEW priate as our understanding of processes resulting in Polynya and Lancaster Sound food webs (Hobson & 8 Mar Ecol Prog Ser 128: 1-10, 1995
Welch 1992). Trophic relationships of species may vary LITERATURE CITED regionally but reasonable agreement in TL estimates was obtained for the invertebrates Calanus hyper- Ainley DG, Sanger GA (1979) Trophlc relations of seabirds in boreus (1.7 vs 2.0) and Gamarus wilkitskii (2.2 vs 2.6), the northeastern Pacific Ocean and Ber~ngSea. In: Barto- neck JC, Nettleship DN (eds) Conservation of marine for the fish Boreogadus saida (3.1 to 3.3 vs 3.6) and b~rdsof North America. US Department of Interior Fish Icelus bicornis (3.3 vs 3.4),and for the birds Somateria and Wlldlife Service Research Report, Washington, DC, mollisslma (3.6 vs 3.4, Hobson 1993) and Larus hyper- p 95-122 boreus (4.2 vs 4.4). Alexander V. Chapman T (1981) The role of epontic algal communities in Bering Sea ice. In: Hood DW, Calder JA (eds) Bering Sea shelf: oceanography and resources, Vol2. University of Washington Press, Seattle, p 773-780 Further applications of stable-isotope anlaysis Ambrose WG, Renaud PE (1995) Benthic response to water in polynya studies column productivity patterns: evidence for benthic- pelagic coupling in the Northeast Water Polynya. J geo- phys Res (in press) In this study, we have shown that stable isotope Atkinson EG, Wacasey JW (1987) Sedimentation in Arctic analyses can be used to assess the linkage between the Canada: particulate organic carbon flux to a shallow water column and benthic processes. There is a dis- manne benthic community in Froblsher Bay. Polar Biol tinct difference in patterns of isotope enrichment 8:3-7 Attwood CG, Peterson WT (1989) Reduction in fecundity and between tightly coupled systems and those where lipids of the copepod Calanus australis (Brodskii) by microbial or meiofaunal pathways or benthic algae are strongly pulsed upwelling. J exp mar Biol Ecol 129: more important, such as in Georges Bank (Fig. 3 and 121-131 references within). Complementary studies document- Baumann ME (1989) Primary productivity and phytoplank- ing additional evidence for tight coupling linkages in ton growth in the marginal ice zone of the Fram Strait and the interpretation of the field data with autecological the NEW Polynya (e.g. Ambrose & Renaud 1995) experiments. Rapp P-v Reun Cons int Explor Mer 188: strengthen our findings. It is likely, therefore, that sta- 81-89 ble isotope techniques can be used to address ques- Bradstreet MSW, Finley KJ, Sekerak AD, Griffiths WB, Evans tions of benthic-pelagic coupling in other systems and CR, Fabijan M, Stallard HE (1986) Aspects of the biology of Arctic cod (Boreogadus saida) and its importance in to make predictions on the relative importance of rem- Arctic marine food chains. Can Tech Rep Fish Aquat Sci ineralization and detrital pathways in carbon cycling. 1491 There is some disagreement in the literature regard- Briskina MM (1939) Feeding on non-commercial fishes of the ing the importance of ice algae as a food source for the Barents Sea. Trans Inst Mar Fish Oceanogr USSR 4: benthos (see Alexander & Chapman 1981, Carey 339-354 Budeus G, Schneider, W (1995) On the hydrography of the 1987). While we do not dispute that for some period Northeast Water Polynya. J. geophys Res 100:4287-4299 during the year it may constitute a large portion of the Carey AG Jr (1987) Particle flux beneath fast ice in the shal- available carbon at the sea floor, ice algae does not low southwestern Beaufort Sea, Arctic Ocean. Mar Ecol appear to make a substantial contribution to the inte- Prog Ser 40:247-257 Carey AG Jr (1991) Ecology of North American Arctic conh- grated diets of benthic organisms in the NEW Polynya. nental shelf benthos: a revlew Cont Shelf Res 11:865-883 Studies are needed, however, to compare carbon Davls JM, Payne P (1984).Supply of organic matter to the sed- sources for benthic organisms underlying permanent iment in the North Sea during a spring phytoplankton versus seasonal ice cover. Using stable isotope analysis bloom. Mar Biol 78:315-324 to discern between 2 potential carbon sources is not Dunbar MJ (1987) Arctic seas that never freeze. Nat Hist 4: 50-53 new in ecology (see papers in Lajtha & Michener Dunton KH, Saupe SM. Golikov AN, Schell DM, Schonberg 1994), but the possibility that it may help resolve the SV (1989) Trophic relationships and isotopic gradients fate and role of ice algae is a novel application of this among Arctic and subarctic marine fauna. Mar Ecol Prog technique. Ser 5639-97 Dunton KH, Schell DM (1987) Dependence of consumers on macroalgal (Laminana solidungula) carbon i.n an Arctic Acknowledgements. We thank the crew and scientific party of kelp community: 6I3Cevidence. Mar Biol 93:615-625 the FS 'Polarstern' ARK IX/2,3 Expedition for their assistance Fontugne MR, Duplessy JC (1981) Organic carbon isotopic in collecting these specimens. E. Born and J. Thomasson col- fractionation by marine plankton in the temperature range lected polar bear samples and R. M Kristensen provided blrd -1 to 31°C. Ocean01 Acta 4:85-90 tissue samples. We also thank Len Wassenaar for the use of his Forsskall MA, Lakkonen A, Leppanen JM (1982) Seasonal stable isotope facility at the National Hydrology Research cycle of production and sedimentation of organic matter at Institute and Randy George for assistance with the preparation the entrance to the Gulf of Finland. Neth J Sea Res 16: of samples for isotopic analysis. Other laboratory fachties were 290-299 provided by the Prairie and Northern Wildlife Research Center. Fowler SW, Knauer GA (1986) Role of large sinking particles The assistance of D. Dyck in the preparation of figures is greatly in the transport of elements and organic compounds appreciated. This work was funded by a supplement to a through the water. Prog Oceanogr 16:147-194 National Science Foundation grant to W.G.A. (DPP 91-13756). France RL (1995) Carbon-13 enrichment in benthic compared Hobson et al.: lnsights from 6'" and 6I5N analysis
to planktonic algae: foodweb implications. Mar Ecol Prog NEWATER Steering Committee and Principal Investigators Ser 124:30?-312 (1993) Northeast Water Polynya: polar sea cruise results. Fry B (1988) Food web structure on Georges Bank from stable EOS 74:184, 195-196 C, N and S isotopic compositions. Limnol Oceanogr Owens NJP (1988) Natural variations in "N in the marine 33:1182-1190 environment. Adv mar Biol 24:389-451 Fry B, Sherr EB (1988) 6I3C measurements as Indicators of Parkinson CL, Comiso JC, Zwally HJ, Cavalieri DJ, Gloersen carbon flow in marine and freshwater ecosystems. In: Run- P, Campbell WJ (1987) Arctic Sea Ice, 1973-1976: satellite del PW, Ehleringer JR, Nagy KA (eds) Stable lsotopes in passive microwave observation. NASA SP-489, Washing- ecological research. Springer Verlag, New York, p ton, DC 196-229 Pearson M, Gage JD (1984) Diets of some deep-sea br~ttle Godfry E (1986) The birds of Canada, revised edn. National stars in the Rockall Trench. Mar Biol 82:247-258 Museums of Canada, Ottawa Petersen GH, Curtis MA (1980) Differences in energy flow Grebmeier JM, Barry JP (1991) The influence of oceano- through major components of subarctic, temperate and graphic process on pelagic-benthic coupling in polar tropical marine shelf ecosystems. Dana 1:53-64 regions: a benthic perspective. J mar Syst 2:495-518 Kau CH (1982) The relationship between trophic level and Grebmeier JM, McRoy CP, Feder HM (1988) Pelagic-benthic stable isotopes of carbon and nitrogen. In: Bascom W (ed) coupling on the shelf of the northern Bering and Chukchi Coastal water research project biennial report for the Seas. I. Food supply source and benthic biomass. Mar Ecol years 1981-1982. South Calif coast Water Res Proj, Long Prog Ser 4857-67 Beach, p 143-148 Green JM (1983) Observations on the food of marine fishes Rau GH, Ainley DG, Bengston JL, Torres JJ, Hopkins TL from Resolute Bay, Cornwallis Island, Northwest Territo- (1992) I5N/l4N and I3C/l2C in Weddell Sea birds, seals, ries. Astarte 12:63-68 and fish: imphcations for diet and trophic structure Mar Harrigan P, Zieman JC, Macko SA (1989) The base of nutri- Ecol Prog Ser 84:l-8 tional support for the gray snapper (Lutjanus griseus): an Rau GH, Sweeney RE, Kaplan IR (1982) Plankton I3C:l2cratio evaluation based on a combined stomach content and sta- changes with latitude: differences between northern and ble isotope analysis. Bull mar Sci 44:65-77 southern oceans. Deep Sea Res 29:1035-1039 Hobson KA (1993) Trophic relationships among high Arctic Rau GH, Takahashi T. Des Marais DJ (1989) Latitudinal vari- seabirds: insights from tlssue dependent stable-isotope ations in plankton 6I3C: implications for CO2 and produc- models. Mar Ecol Prog Sei- 95-7-18 tivity in past oceans. Nature 341:516-518 Hobson KA. Clark RG (1992) Assessing avian diets using Rowe GT (1983) Biomass and productivity of the deep-sea stable-isotope analysis. 11. Factors influencing diet-tissue macrobenthos. In: Rowe GT (ed) The sea: deep-sea biol- fractionation. Condor 94:189-197 ogy, Vol8. J Wiley, New York, p 97-121 Hobson KA, Piatt JF, Pitocchelli J (1994) Using stable isotopes Schneider W, Budeus G (1995) On the generation of to determine seabird trophic relationships. J Anim Ecol63: the Northeast Water Polynya. J geophys Res 100: 786-798 4269-4286 Hobson KA, Welch HE (1992) Determination of trophic rela- Sholto-Douglas AD, Field JG, James AG, van der Merwe NJ tionsh~pswithin a high Arctic marine food web using 6I3C (1991) I3C/l2C and I5N/l4Nisotope ratios in the Southern and 6I5N analysis. Mar Ecol Prog Ser 84:9-18 Benguela Ecosystem: indicators of food web relationships Hyslop EJ (1980) Stomach contents analysis - a review of in different size-classes of plankton and pelagic fish; dif- methods and their application. J. Fish Biol. 17:411-429 ferences between fish muscle and bone collagen tissues. Keeley JE, Sandquist DR (1992) Carbon: freshwater plants. Mar Ecol Prog Ser 78:23-32 Plant Cell and Environ 15:1021-1035 Simenstad CA, Duggins DO, Quay PD (1993) High turnover of Klekowslu RZ, Weslawski JM (1990) Atlas of the marine organic carbon in kelp habitats as a sources of 6I3C vari- fauna of southern Spitsbergen. Vol l Vertebrates. Polish ability in marine food webs. Mar Biol 116:147-160 Academy of Sciences Press, Warsaw Smetacek V (1980) Annual cycle of sedimentation in relation Lajtha K, Michener RH (1994) Stable isotopes in ecology and to plankton ecology in western Kiel Bight. Ophelia (Suppl) environmental science. Blackwell Scientific Publications, 1:65-76 London Smith FR, Walker NA (1980) Photosynthesis by aquatic plants: Massom RA (1988) The biological significance of open water effects of unstirred layers in relation to assimilation of CO2 within the sea ice cover of the polar regions. Endeavour and HCO- and to carbon isotopic discrimination. New 12:21-26 Phyt01 86:245-259 McConnaughey T, McRoy CP (1979) Food-web structure and Stempniewicz L, Weslawslu JM (1992) Outline of trophic rela- the fractionation of carbon isotopes in the Bering Sea. Mar tionships in Hornsund fiord, SW Spitsbergen (wiih special Biol 53:257-262 consideration of seabirds). In: Institute of Ecology (ed) Mills EL, Pittman K,Tan FC (1984) Food-web structure on the Landscape, life and man in the high Arctic world: Polish Scotian Shelf, eastern Canada: a study using I3C as a food- Academy of Sciences Press, Warsaw, p 271-298 chain tracer. Rapp Pv Reun Cons int Explor Mer 183:lll-118 Stirling 1 (1980) The biological importance of polynyas in the Minagawa M, Wada E (1984) Stepwise enrichment of 15N Canadian Arctic. Arctic 33:303-315 along food chains: further evidence and the relation Suess E (1980) Particulate organlc flux in the ocean- between 6I5N and animal age. Geochim cosmochim Acta surface productivity and oxygen utilization. Nature 288: 48:1135-1140 260-263 Monteiro PMS, James AG, Sholto-Douglas AD, Field JG Townsend DW. Cammen LM (1988) Potential importance of (1991)The 6I3C trophic position isotope spectrum as a tool the timing of spring phytoplankton blooms to benthic to define and quantify carbon pathways In marine food pelagic coupllng and recruitment of demersal fishes. Biol webs. Mar Ecol Prog Ser 78:33-40 Oceanogr 5 215-229 Mortenson T (1927) Handbook of the echinoderms of the von Dorrien CF (1993) Ecology and respiration of selected British Isles. Oxford University Press, Oxford Arctic benthic fish species. Ber Polarforsch 125-99 10 Mar Ecol Prog Ser 128: 1-10, 1995
Wada E, Terazaki M, Kabaya Y, Nemoto T (1987) I5N and I3c uroidae. In: Jangoux M, Lawrence JM (eds). Echinoderm abundances in the Antarctic Ocean with emphasis on the nutrition. AA Balkema, Rotterdam, p 161-181 biogeochemical structure of the food web. Deep Sea Res Wassman P (1991) Dynamics of primary production and sedi- 34:829-84 1 mentation in shallow fjords and polls of western Norway. Warner G (1982) Food and feeding mechanisms: Ophi- Oceanogr mar Biol A Rev 29:87-154
This article was submitted to the editor Manuscript first received: February 13, 1995 Revised version accepted: May 31, 1995