)eep-Sea Research, Vol. 34, Nos 5/6, pp. 829-841. 1987. 'rimed in Great Britain.

(1198-t1149/87 $3.0t~ + !1.(10 1987 Pergamon Journals Ltd.

~SN and

13C abundances in the Antarctic Ocean with emphasis on the

biogeochemical structure of the food web

~ITARO WADA,* MAKOTO TERAZAKI,'~ YUKO KABAYA* a n d TAKAttlSA NEMOTOt

(Received 15 August 1985: in revised form 1 February 1986; accepted 15 May 1986)
Abstract--Distributions of ~ISNand ~5~3Cfor biogenic substances in the Antarctic Ocean were investigated to construct a biogeochemical framework for assessing the Antarctic ecosystem. Phytoplankton exhibited particularly low ~515N ((I.5%) and ~;C (-26.9%o) values in pelagic plankton samples. High nitrate concentrations, and high PCO, in the surface waters on the southern side of the polar front and the resulting slow growth rate of phytoplankton under low light intensity are suggested as possible factors in causing the low isotopic compositions. Mean fractionation factors of 1.029 and 1.006 were estimated for photosynthetic carbon fixation and for the assimilation of inorganic nitrogenous compounds (ammonium plus nitrate) during algal growth, respectively. Enrichment of LSN with increasing trophic level was confirmed for Antarctic ecosystems: 615N,nim,l%o = 3.3 (trophic level- 1) + 6LSN,Ig~, whereas 13C content did not increase in the same manner. Differences in lipid content among animals may be the main factor in causing this 6~C anomaly. I~N and 13C abundance of sedimentary organic nitrogen differed from phytoplankton and settling particles. An exact mechanism for explaining the high g~SN (around 5%) is not known. The very high ~3C value of-20.5%o at Sta. 3B may originate in ice algae that had grown under CO,-limited conditions. Particles collected by sediment traps gave characteristically low 6L~N values (-3.0 to 0.9%,,), strongly suggesting a phytoplankton origin. The 15~5Nand 6L~Cvalues of settling material showed similar vertical profiles with depth which might arise from temporal variation of algal growth.

INTRODUCTION CONSIDERABLE a t t e n t i o n has b e e n f o c u s e d on cycles of b i o p h i l i c e l e m e n t s in n a t u r a l systems. A t a given t i m e , living o r g a n i s m s a c c o u n t for a negligibly small p o o l size w h e n c o m p a r e d to g l o b a l i n v e n t o r i e s . H o w e v e r , n a t u r a l e c o s y s t e m s are active sites w h e r e i m p o r t a n t t r a n s f e r s of o r g a n i c m a t t e r o c c u r r a p i d l y a n d in a c o m p l e x m a n n e r . In this c o n t e x t , new w a y s to classify c o m p o n e n t s o f the a n i m a l k i n g d o m are highly d e s i r a b l e to c o n s t r u c t a b i o g e o c h e m i c a l f r a m e w o r k for assessing fluxes of b i o g e n i c s u b s t a n c e s . R e c e n t p r o g r e s s in i s o t o p e b i o g e o c h e m i s t r y m a y h e l p to m e e t this r e q u i r e m e n t , A n e n r i c h m e n t of tSN a l o n g t h e f o o d c h a i n was first f o u n d by M1YAKE a n d WADA (1967) a n d l a t e r c o n f i r m e d in c u l t u r e e x p e r i m e n t s (DENIRO a n d E P S T E I N , 1981) a n d in m a r i n e a n d t e r r e s t r i a l e c o s y s t e m s (ScHCIENINGERet al., 1983; SCHOENINGER a n d DENIRo, 1984). T h e e n r i c h m e n t of ~5N is w i d e s p r e a d a m o n g m o s t a n i m a l s , involving i n v e r t e b r a t e s a n d v e r t e b r a t e s i r r e s p e c t i v e o f t r o p h i c levels, h a b i t a t , f o r m o f n i t r o g e n e x c r e t e d a n d g r o w t h * Mitsubishi-Kasei Institute of Life Sciences, 11 Minamiooya, Machida, Tokyo 194, Japan. t Ocean Research Institute, University of Tokyo, 1-15-1 Minamidai. Nakano. Tokyo 164, Japan. 829

830

E. WAUAel aL

rate. ~SN enrichment averages +3.4 + 1.1%ofor a single feeding process (MINAO,\WAalld WADA, 1984). On the other hand, 8~5N of phytoplankton is variable, depending upon the nitrogen source used for growth and on physiological conditions (WA~)A, 19801. The latter factors also affect the 8~3(-"values of phytoplankton. Indeed, a close relationship between i5~3C values of phytoplankton and ambient seawater temperature (SAcKE'Vret al., 1973), strongly suggests the significance of growth rates on the variation of 8~3C. Rau et al. (1982) proposed that the latitudinal discrepancies in the ~'~Ccontent of plankton depend upon geographic differences in the kinetic isotope effect associated with plankton biosynthesis. The 813C values of animal tissue arc very close to those in their diet, and a small increase in ~-~Ccontent sometimes occur,, with increasing trophic level (DEN~RO and Et'S~HN, 1978, FRy et al., 1978: R,\tJ c~1a/ 1983; FRY and SHIRR, 1984). The lines of evidence described above suggest that ti~c isotopic composition of nitrogen and carbon in marine biota can provide basic infoimation on their growth condition, food source, and trophic level. The Antarctic Ocean provides a particularly good environment for examining ti~c physiochemical and biological structures of an ecosystem. The cold climate lowers watci temperatures in the euphotic zone and promotes vertical mixing which supplies nutrient salts and high Pco, to the euphotic zone. Primary production is moderate (ttOLM-tt-xNSt et al., 1977) under low temperature and low light intensity. Furthermore, nitrate concentration in the euphotic zone exceeds 2(1 ~M throughout the year, and the fraction of primary production that can be regarded as new production that can be transfered to :~ higher trophic level should be high (Du(;DALE and GOERING, 1967; OLSON, 1981). Seasonal variation of chlorophyll a in the euphotic zone as well as under fast ic~ generally exhibits a single maximum during the austral summer season (HART, 1942: FUKUCm et al., 1984). According to HASl.E (1969), diatoms are the most dominant group among phytoplankton. Krill, a herbivore, act as a central dietary source h)r carnivorou~ zooplankton, seals and whales (MACKINTOStt, 1960). In light of these facts, the stable isotope ratios of nitrogen and carbon for biogenic substances were investigated t~ describe the isotopic structure of the Antarctic ecosystem and to examine the applicabi. lity of isotopic methods for food web analysis.
MA't t.'RIALS AND M f ; I'II()I_)S

Samples were collected in the southern Ocean Australian Sector during the KH-83-4 cruise of the R.V. H a k u h o - M a r u as a part of the BIOMASS SIBEX-I project (22 November, 1983-24 February, 19841. The hydrographic data have been presented by NEMOTOand TERAZAKI(19851. Additional sampling of macrofauna was carried out by the Japanese pilot fishery for Antarctic krill and whale in the areas between 43W and 44.5W during 1982-1983. Water samples from a depth of 5 m (100 1) were collected with a water pump, and particulate organic matter (POM) was collected on Whatman type F glass-fiber filters pretreated at 400C for several hours. Plankton samples were collected by horizontal tows of MTD nets, 56 cm in diameter and with meshes of 0.10 mm (XX13) and 0.33 mm (GG54), and by vertical tows (0-200 m) with NORPAC nets (XX13). Other macrofauna such as Euphausiacea, Copepoda, Amphipoda and pisces, were collected from the indicated depth by ORI-69 nets or by IKMT nets with a diameter of 10 feet. Surface sediments were obtained by using a box core. Settling particles collected in sediment

15N and E~C abundances in the Antarctic Ocean

831

traps were supplied by Drs S. Tsunogai and K. Harada of Hokkaido University. Details of the trap system and mooring array are reported elsewhere (TsuNoGAI et al., 1982). Sample materials were frozen (-80C) and later vacuum-dried in the laboratory. Macrofauna were crushed, and passed through a 1 mm opening stainless-steel sieve. All biological samples (2-5 mg N) were converted to ammonium by Kjeldahl digestion. The ammonium produced was steam-distilled, collected in a 0.25 N H2SO4 trap and then converted in vacuo to nitrogen gas with alkaline hypobromite. Aliquots of the distillate were taken for nitrogen determination by calorimetry. The nitrogen gas was purified before mass spectrometric analysis. Details of the method are reported elsewhere (WADA and HAq'zORI, 1976). Before 613C measurement, all samples were treated with 1 N HCI, freeze-dried, and then converted to CO2 in an IR Gold Image Furnace combustion system (MLZUTA~Iand WADA, 1985). The CO2 evolved was measured by volumetry using a mercury manometer and then used for carbon isotopic measurements (NAKAMt~R.,\et al., 1984), Isotope ratios were measured by a Hitachi RMU-6R mass spectrometer fitted with a double collector for ratiometry and expressed in per rail deviations from a standard as defined by the following equation: ~515N or6'3C(%o) = ( R ..... pl~
\Rslandard

13 x 1000, /

where R = 15N:14N or 13C:12C. Atmospheric nitrogen (for ~15N) and Peedee belemnite (PDB) (for 613C) were used as the standards. Ammonium sulfate solutions (-3.4 and 1.3%) and sodium carbonate solutions (-19.4 and -11.0%) were used as running standards for 8L~N and 613C measurements, respectively. All data for 61:~C were corrected for oxygen errors according to the method of CRAIG (1957). The analytical precisions for isotopic analysis are within 0.2%0 for both isotopes,
RESULTS

Microscopic studies revealed that almost all particulate organic matter (POM on Whatman GF/F) consisted of diatoms. The 815N (0.4-0.5%o) and ~13C (-27,4 to -26.4%) for the POM were particularly low in marine pelagic phytoplankton. Indeed the 815N value of 0.4%o was the lowest among the present samples (Tables 1 and 2) and as low as those for N 2 fixing blue-green algae, Trichodesmium. Netted plankton mostly consisted of phytoplankton (XX13) and zooplankton (GG54) with a negligible detrital component. These mixed samples together with Euphausia, and Copepoda gave variable 615N (0.69.8%0) and 613C (-32.3 to -26.6%0) values. Among the zooplankton, the carnivorous Copepoda showed high 515N values, whereas the 813C values (average -29.1%o) were significantly lower than average POM, The herbivorous animals (Euphausiacea and Salpa) exhibited ~15N values (1.8-3,1%o) intermediate between POM and polychaeta. Macrofauna, such as pisces and squid, commonly showed rather high ~SN and 13C contents. The highest values ~15N (10.4%o) and ~13C(-23.4%0) in this study were found in Trematomus bernacchir (Table 2). 615N values of the marine biota collected on 13 January 1984 at Sta. 3' (6132'S, 15026'E) increased in the following order: POM (0.5%0) < Euphausia superba, young (1.0%o) < Salpa thompsoni (1.8%o) < E. superba, adult (3.1%o) < polychaeta sp. (4.8%0) < Sagitta maxima (5.6%0) < Notolepis coasti

Table 1, 615N and OI3C values for various biogenic materials in the Antarctic Ocean. Samples were collected during the R. V. H a k u h o M a r u cruise of the BIOMASS SIBEX-I operation, When more than one individual of a species was collected on a given date, analyses were carried out on a composite sample

Samples 25 Dec., 1983 21 Jan.. 1984 6126. l'S,15005.0'E 6000.6'S,11602,2'E 5 5 0.53 0.37

Station

Date

Location

Sampling depth (m) Nitrogen (%) Carbon (%) 615N;,i, (%0)

61~CpT~t~ (%0) -27.4 -26.4

Remarks Pump Pump

Particulate organic matter 3B 6

Netted plankton XXI3 GG54 XX13 GG54 Y 3' o 6 (!.46 3.75 13 Jan., 13 Jan., 21 Jan., 21 Jan,, 1984 1984 1984 1984 6132.0'S,15026.0'E 6t32.0'S,15(126.0'E 6000.6'S,11602.2'E 6(1(10.6'S.11602.2'E Surface Surface 0-200 (!--213(/

-14.5 22.7

2.2 5,4 0,58 2.1

-32.3 ~28,3 -26.8 27.4

MTD MTD NORPAC NORPAC

Euphausiid Euphausia triacantha 3' 13 Jan., t984 6!'32.3'S, t5026.YE 0- 535 5 19 Jan., 1984 (~5~3.115'S,118~03.9'E 0-890

8.98

34.1

3. l

-29, I

IKMq

E. superba (adult)
PI-3-2 17 Jan,, 1t184 6438,7'S.12713,8'E

111.4

29.(I

2.7

-29.3

IKMT

E. ~uperba (young)

Surface

1!).0

1.0

28.1

ORI

Copepoda Euavgaptilus laliceps PI-2 16 Jan., 1984 PI-2 16 Jan., 1984

(~4'~21.4'8,135~56,7'E

0875

--

9.6

--28.7

OR1

Euchaeta antarclk~
PI ~ It~J;m . !~)~4

64:'21.4'S.135'~56.7'E

~I-875

8.3

-29,5

ORI

P.~eudoclm'ella

(~421 I.b.!35'56 7'[:

i~-~75

u~

-292

()RI

Amphipoda

Parathemisto gaudichaudi
21 Jan., 1984 6(100.6'S,11602.2'E 0-200 7.411 29.7 1.8 6 3' 21 Jan., 1984 13 Jan., 1984 6000.6'S,11602.2'E 6132.3'S,15026.3'E 9.62 30.8 0-200 0-535 5,3 4,8

-27.1

NORPAC

Polychaeta

-27.1 -26.7

NORPAC IKMT

Thaliacea

Salpa thompsoni
13 Jan., 1984 6t32.3'S,15026.3'E 0-535 2.35

3'

1.8

28.1

[KMT

Chaetognatha

Sagitta maxima
13 Jan., 1984 6132.3'S,15026.3'E 0-535 6 21 Jan., 1984 61/1)3.3'S, 116114.(1'E 1~798

3'

5.6

-26.1

IKMT

Coelenterata

3.88

27.9

6.6

-24.6

ORI

Pisces (Micronekton)

Electrona antarctica
13 Jan., 1984 6132.3'S,15026.3'E

3' 3'
13 Jan., 1984 3B 5 P12 25 Dec., 1983 19 Jan., 1984 17 Jan., 1984

0-535

7.88

45.2

7.5

-27.1

IKMT

Notolepis coasti

61 32.3'S, 15026.3'E

0-535

34.9

7.1

-25.8

IKMT

Sediment

61026. I 'S, 15005.0'E 65114.1'S,11753.0'E 6411.6'S, 13541.3'E

3870 2540 3160

0.0378 0.0359 0.0155

11.112 11.167 11.1t55

4.9 5.2 5.5

-21/.5 "-25.3 -25.4

Box-core OKEAN OKEAN

-, Not determined.

834
7"able 2.
Samples Euphausiid Squid

E. WADA et al. 8~3Cand 615N of marine animals collected frorn the Antarctic Ocean during the Japanese pilot fisherv Sampling date 15 Jan., 1 9 8 3 15 Jan., 1 9 8 3 12 Jan., 1 9 8 3 14Jan., 1 9 8 3 16 Jan, 1 9 8 3 26 Jan., 1 9 8 3 25 Jan., 1982 Location 5925'S,4309'W 5925'S,4309'W 5940'S,4313'W 5934'S,4316'\V 5949'8,4347'W 5'457'S,4430'W South of Elephant Island, west coast of Antarctic Peninsula N (%) 6.75 10.9 13.7 14.2 15.1 15.4 13.2 (' (%) 45.3 30.6 22,9 ' ,4..'~ 21.6 21.0 33.2 615N (%,0 ..... 4.2 6.0 7.0 7.2 6.5 10.4 e;~( ' (%,,1 293 25.7 2~ !) -2(~. 1 --2-1.5 2"~ 5 2~,4

Kondakoria Iongirnama
Pisces

Trematom us bernacchir

(7.1%o) < Electrona antarctica (7.5%o). These samples, except for POM, were collected simultaneously by an oblique tow (0--535 m) of an IKMT net. On the other hand, the 8t3C values of these materials did not increase in the same manner and the lowest value was found for Euphausia superba (-29.1%o), while the highest value was for Notoch,psis coasti (-25.8%0). Sedimentary organic matter collected at the three stations differed in LSN and ~ ( abundance from surface POM (Table 11. The 6~5N values ranged from 4.9 to 5.5%o (the average was 5.2%0). Furthermore, a very high t3C value of-20.5%0 was found for the sediment sample from Sta. 3B, while -25.4%o was obtained for other sediments.

"2'8 -~;7 -:;e -:is -~/4 6~3c~*/**

-3
r

-2

-I

0
i

615NaW/oo

,=2
3

Fig. 1. Vertical profiles of 6~5N and /SL~C values for settling particles ~,t Sta. 3 (6033.0'S,15027.0'E) of the KH-83-4 cruise of the Hokuho-Maru. Collections were performed at depths of 0.69, 0.93, 1.33, 2.33, and 3.13 km tot 24 days from 10 December, 1983 to 13 January, 1984. The depth of this station is 3580 m. Open circles and triangles denote the 6~N and the ~3C values, respectively.

tSN and ~3C abundances in the Antarctic Ocean

835

The material collected by sediment traps consisted mainly of diatom frustules and fecal pellets packed with frustules. The ~ISN and 6t3C values of the trap samples gave similar vertical profiles with depth (Fig. 1). The ~SN of the 690 m sample was -0.5%0 and increased to 0.86%o at 1330 m (a maximum value) and then decreased to -3.0%0 at 3130 m. The lowest 8~3C value was obtained for the 690 m sample (-27.9%0), followed by a maximum (-25.6%o) at 1330 m, and then a decrease to -26.7%0 below 2330 m.
DISCUSSION

Samples for this study were collected south of the Polar Front where near-uniform nutrient, temperature and salinity distributions were observed in the euphotic zone. The surface temperature ranged from -0.5 to 2C and the Pco, of the surface waters was significantly higher than the atmospheric Pco: (INouEand SUGIMURA,1985). The rate of primary production was limited by water temperature (YAMAGUCHI et al,, 1985). The nitrate concentration was ubiquitously higher than 20 gM and the ammonium concentration was <0.5 gM. According to OLSON (1981), percent nitrate uptake [nitrate uptake rate/(ammonium + nitrate uptake rates) 100] ranges from 8.1 to 70.3% (average 43.1%) in the nitrate-rich waters of the Scotia Sea. Turnover time for ammonium uptake may be less than 2 weeks. Phytoplankton in these conditions, thus, use nitrate and ammonium, that is ultimately derived from ambient nitrate for their growth. The 15N and ~3C contents in POM and net plankton (XX13) were quite low (615N ca. 1%o; ~I3c - 28%0) in comparison to those of temperate regions (SACKE~ et al., 1973; SWEENEY et al., 1978; WADA et al., 1984). The nitrogen isotopic fractionation becomes larger in cases where ambient nitrate plus ammonium concentration does not limit the assimilation rates, and a high value of 1.005 was reported for nitrate assimilation in the boreal areas of the North Pacific Ocean where nitrate is not limiting (WADA, 1980). In the study area, the physico-chemical conditions of the euphotic zone were quite similar to those in the boreal North Pacific as the phytoplankton growth was limited by low temperatures and possibly by low light intensity. This condition enhanced the kinetic isotope effect and produced a depletion of ~SN in the algal body. The ~15N values of nitrate in this region may be 7%0, as high as those in the North Pacific Ocean (WADA, 1980); a fractionation factor of ca. 1.006 is obtained for the assimilation of inorganic nitrogenous compound during algal growth. O'LEARY (1981) demonstrated that the carbon isotope effect in the C3 pathway is partially rate-limited by diffusion of CO2, and this serves to make the in vivo fractionation smaller. The fractionation was found to be inversely correlated with Pco; and growth rate (CALDER and PARKER, 1973; MIZUTANI and WADA, 1982; WADA and PARKER, unpublished data). It was thus concluded that HCO~-CO2 isotope exchange equilibrium at temperatures below 2C, low light intensity, high Pco,, and low temperature caused very low 13C content in the phytoplankton. A mean fractionation factor of 1.029 was obtained for the photosynthetic carbon fixation between HCOq and the algal body. There are many reports of the feeding habits of animals living in the Antarctic Ocean. Parathemisto gaudichaudii (Amphipoda) is a typical voracious carnivorous zooplankter but its young is omnivorous. P. gaudichaudii is very important as the food of sei whales (NEMOTO and Yoo, 1970) and is also comsumed by many fishes (HURLEY, 1959). Polychaeta, Sagitta maxima (Chaetognatha) and Coelenterata are also carnivores, and copepods are their main food organisms (ALVARINO, 1965; FAUCHALDand JUMARS, 1979).

836

E. WADA et al.

On the other hand, Euphausia triacamha, E. superba (Euphausiacea) and Salpa thompsoni (Thaliacea) are herbivores (MAt tCttI.INE and FISHER, 1969; AI.IA)REI)(;E and MARDIN, 1982). Pisces living in the Antarctic Ocean mainly consume Euphausia superha (PERMmN, 1970). Euphausiacea and Copepoda are the main food organisms of Minke Whale, Balaenoptera acutorostrata (NEMOTO. 1970). Additionally, ANDRIAS~I~V (1968) defined trophic levels (TL) for Antarctic organisms. Based on the above studies, the possible TL of organisms in the Antarctic ecosystem was determined (Table 3). On the basis of this classification, TL of representative samples were determined and compared with each corresponding 6~SN value. Clear increases in 615N a r e suggested from the food base of a community to the higher TL (Fig. 2). A linear regression analysis gave 6~SN (animal) %0 = 3.3 (TL-1)-0.2 with a correlation coefficient of 0.997 (Fig. 2). The average increase of 8tSN per TL was 3.3%,, from the slope of the best-fit line. This value is close to the 3.4 _+ 1.3%o value for the mean enrichment value for marine and land animals reported by MINAGAWAand WADA (1984). The 613C values, on the other hand, showed no significant trends. As will be discussed later, the 6~SN value of phytoplankton (4).2%0 in the equation) seems to be variable during the austral summer season. A~
Table 3. The trophic level of the representative organisms in the food web of the Antarctic ecosystem Organisms Diatoms: POM (1.2) Euphausiacea: E. triacantha ( I. 9--2.3). E. superba (1.9); Salpa thompsoni

Trophic level (I. Nutrient salts (NO~, HCOi) 1. Phytoplankton 2. Hcrbiw)res. zooplankton 3. Carnivores, zoophmkton
4.

( l.~)
Carnivores, nekton

Polychacta (2.6), Chaetognathu (2.8L Coelenterate (3.1) Pisces: Trematomus bernac(htr (4.2)

Numerical values in parentheses stand for the calculated values of trophic levels of organisms using the equation 8tSN %0 = 3.3 (TL-1)-0.2.

*/. /.,, -25 15

0

.0

6'~c / ,45 ,,~./

-30 10

-35

-40

0 Trophic level (TL.)

Fig. 2. Animal 615N versus trophic level for the biota from thc Antarctic Ocean. The Irophic levels were estimated from the previous knowledge of each animal's feeding babits. A solid line for 8~SN is derived from linear regression of the mean 8~SN and tile trophic level (TL). ~,]c POM: 0 , Euphausia spp.; A, Salf m thompsoni: U], Sagitta maxima; II, ('oelenterata; , Tremutomu,s hernacchir,

~SN and ~3C abundances in the Antarctic Ocean

837

present, however, we do not have enough data to evaluate the mean ~ISN value of phytoplankton in the Antarctic Ocean. The linear relation between the ~lSN value of animals and their TL seems to be applicable to organisms not included in the regression. For instance, a mean TL of 3.1 _ 0.1 (n -- 4) was calculated for squid that mainly consume Euphausiacea (NEMoTo et al., 1985). Young Euphausia superba and young Euthemisto gaudichaudii exhibited TL values of 1.4 and 1.6, respectively, and the latter is omnivorous. The TL value for micronekton was 3.3 which could be expected from differences in their feeding habits relative to the large pisces (TL = 4). The XX13 samples collected from the surface layers exhibited smaller TL values (1.2-1.7) than those (1.7-2.7) of the GG54 samples. Herbivorous zooplankton such as Calanoides acutus, Calanus propinquus, Rhincalanus gigas (copepoda) and Salps spp, were abundant in the GG54 sample, while the former samples mainly consisted of diatoms. Euaugaptilus, Euchaeta and Pseudochirella (mesopelagic copepods) feed on herbivorous and carnivorous zooplankton (HARDING, 1947). The high TL values of ca. 4.0 for these copepods may reflect their feeding in the deeper layers. Furthermore, our recent study found that Balaenoptera acutorostrata (Minke Whale) from Antarctica exhibited an average 815N value of 6.1 + 0.6 (1 S.D.) %0 (unpublished data) which corresponded to a TL value of 2.9. Minke Whale is a well known animal that feeds on E. superba. Copepods from the Southern California Bight were found to have higher 6~5N values than those from the North Pacific Central Gyre, reflecting differences in the source of inorganic nitrogenous compounds for the growth of associated phytoplankton (MVLLlY et al., 1984). Consequently, the equation for the relation between 8~5N values of animals and their trophic level is restricted to our study region. No correlation was observed between the ~fSN and 6~3C values in this study (Fig. 3). More than half of the animals had lower ~3C values than the particulate organic matter

10

halopoda

~s

Polychaeta

.~ XX13 ]

Zooplankton (GG54) Euphausiacea

0
-

'

'

30.0

-27.5 -25.0 613CPDB(o1~)

-22.5

Fig. 3. Relationship between ~15N and 813C values of Antarctic biogenic nitrogen. Vertical and horizontal bars indicate 1 S.D. Organisms were divided into several groups based on their feeding habit and species.

838

E. WADAet al.

at 5 m depth: This fact contrasts with previous reports of an enrichment of about 1%o o! 613C value for a single feeding step (DENtRO and EPSTEIN, 1978: HAJNS and MONTA(;t I, 1979; RAU and ANDERSON, 1981). The lipid fractions of organisms ubiquitously show lower 6~3C values relative to whole organisms and other protein-rich fractions (PaRKJm 1964; DEGENS et al., 1968; GORML and SACKETT, 1977; FRY et al., 1978). For cxampic, mesopelagic copepods with low 613C values (Fig. 3) are known to contain a high amount of lipid in their body (LEE and HmOTA, 1973). Differences in lipid content among these animals are strongly suggested, therefore, as a main cause of the 613C anomaly. The 6~( ' values of zooplankton were more variable than those of macrofauna such as squid and pisces, which suggests the variation of ~3C content in phytoplankton. The high 6Z3C value of-20.5%o for the sedimentary organic matter at Sta. 3B has never before been found in the Antarctic Ocean (SAcKEVr et al., 1973). The sediment at this station mostly consisted of siliceous ooze, an assembly of dead diatoms. A 6~-~C value near -20%o can only be understood if phytoplankton had grown under a limited supply of carbon dioxide. A high pH of 9 was sometimes observed in Antarctic fast ice when ice algae were blooming (HosftlAI, 1981). Ice algae are, thus, suggested to be one of the probable candidates for the organic matter source in this sediment. The 6L~N values ~l sedimentary organic matter (4.9-5.5%0) were significantly different from those of POM and settling particles (-3.0 to 0.5%0). The high 6L~N in the sediment may be a result of nitrogen isotope fractionation that takes place during epidiagenesis of particulate organic materials in deeper layers. The low 6LSN value of the settling particles clearly indicates that they originate trom diatoms, as no materials other than phytoplankton and fecal pellets can give such low 6~5N values. This is also supported by microscopic observations. However, an exact reason for the shape of the vertical profiles of 615N and 6J3C in these particles (Fig. 1) i~ not known. Perhaps the variations reflect an algal blooming cycle that occurs in the Antarctic Ocean during austral summer (HART, 1942; HASI E, 1969; FUKt~(IU et al., 1984), The maximum values observed at 1330 m could therefore arise from diatoms that grc~, rapidly during the algal bloom, since high values under these cor]ditions are expected from culture experiments (WAI),.,, and HATTORI, t978: WADA and PARKrR, in preparation). The isotopic-biogeochemical structure of the Antarctic ecosystem is schematically illustrated in Fig. 4. The fluctuation of the isotopic abundances in the food web mainly

r~I

I "''''-~.........t I

16'~=3~TL-3.S,~ I

''

'I

p-c
ml~ 5 -

~JZ
J -7.5*/,
J33o - 4o

NHz.( 0.5-2ugot.N/[ )

L ppm ca~l Verti Mixing

Fig. 4,

(Settling PQrticles~ ( Sediment ] PN:-~.O;tSz. / / 6"N: s.2:o.3v-/ L 6'~E::'26;1-+0'8%'J L6~C:-2'5~-25"41~

Schematic presentation of the isotopic structure of t h e A n t a r c t i c ecosystem,

~SN and t3C abundances in the Antarctic Ocean

839

results from the variation of ~5N and 13C contents in phytoplankton grown under different conditions during austral summer. In fact, the standard variations of 81SN and 8~3C of phytoplankton appear to be up to 2%0, judging from the variations for netted plankton and settling particles. On the other hand, the coefficient of variation of macrofauna is expected to be small, since the time dependency of phytoplankton may be smoothed out by an averaging effect over several seasons. Significant correlations between 815N values of the macrofauna and their TL are still to be expected in the Antarctic Ocean. With respect to carbon isotopes, the measurement of the lipid-free fraction is required for further discussion. In conclusion, the Antarctic ecosystem seems to be an isotopically ordered chemical system in a first approximation, and the ~SN abundances in the ecosystem may be useful for classifying its components.
Acknowledgements--The authors appreciate the cooperation of all the crew members of the Hakuho Maru. They also extend their gratitude to Drs S. Tsunogai and K. Harada, Hokkaido University for kindly supplying the trap samples. The authors are indebted to Dr L. A. Codispoti for reviewing the manuscript. REFERENCES AI,LDREDGE A. L. and C. P. MARDIN (1982) Pelagic tunicatcs: Unique herbivores in the marine phmkton. BioScience, 32, 655-663. AEVAR1NO A. (1965) Chaetognatha. Oceanography and Marine Biology, Annual Review, 3, 115-194. ANDRIASHEV A. P. (1968) The problem of the life community associated with the Antarctic fast ice. Symposium on Antarctic oceanography, Santiago, Chile, 1966, R. I. CURRIF, cditor, Scott Polar Research Institute, Cambridge, pp. 147-155. CALDER J. A. and P. L. PARKER (1~73) Geochemical implications of induced changes in C ~3 fractionation by blue-green algae. Geochimica et Cos'mochimica Acta, 37, 133-140. CRAIO H. (1957) Isotopic standards for carbon and oxygen and correction factors for mass-spectrometric analysis of carbon dioxide. Geochimica et ('osmochimica Aeta, 12, 133-149. DEGENS E. T., M. BEHRENDT, B. GOTrlIARDT and E. REPPMANN (1968) Metabolic fractionation of carbon isotopes in marine plankton--II. Data on samples collected off the coast of Peru and Ecuador. Deep-Sea Research, 15, 11-20. DENIRO M. J. and S. EPSTEIN (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta, 42,495-506. DENmO M. J. and S. EPSTHN (1981) Influence of diet on the distribution of nitrogen in animals. Geochimica et Cosmochimica A cta, 45,341-351. DUGDALE R, C. and J. J. GOEmNG (1967) Uptake of new and regenerated l\)rms of nitrogcn is primary productivity. Limnology and Oceanography, 12, 196-206. FAU('ttAI.D K. and P. A. JUMARS(1979) The diet of worms: a study of polychaete feeding guilds. Oceanography and Marine Biology, Annual Review, 17, 193-284. FRY B. and E. B. SHERR (1984) ~SC measurements as indicators of carbon flow in marine and frcshwater ecosystems. (2mtributions in Marine Science, 27, 13-47. FRY B., W. L. JENG, R. S. SCALAN and P, L. PARKER (1978) 13C food web analysis of a Fexas sand dune community. Geochimica et Cosmochimica Acta, 42, 1299-131)2. FUKUCHI M., A. TANIMURAand H. OHTSUKA (1984) Seasonal change of chlorophyll a under fast ice in LiitzowHolm Bay, Antarctica. Memoirs o f the National Institute for Polar Research, Special Issue, 32, 51-59. GORMEY J. R. and W. M. SACKHq" (1977) Carbon isotope evidence for the maturation of marine lipids. Advances in Organic Geochemisoy, 1975, 321-341). HAINES E. B. and C. L. MONTAGUE (1979) Food sources of estuarine invertebrates analysed using ~C/~eC ratios. Ecology, 60, 48-56. HARDING G. C. H. (1974) The food of deep-sea copepods. Journal of the Marine Biological Association o]'the United Kingdom, 54, 141-155. HART T. J. (1942) Phytoplankton periodicity in Antarctic surface water. Discovery Report, 21,261-356. HASI_E G. R, (1969) An analysis of the phytoplankton of the Pacific Southern Ocean: Abundance, composition and distribution during the Brateggy Expedition, 1947-1948. Hvalradets Skrifter, 52, 1-168. HOLM-HANSEN O., S. D. EL-SAYED, G. A. FRANCES('II1NIand R. L. CUtlEL (1977) Primary production and the factors controlling phytoplankton growth in the Southern Ocean. In: Adaptations with Antarctic ecosystems, G. A. LEANO, editor, Gulf Publishing Co., Houston, TX, pp. 11-50.

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