The response of benthic foraminifers to carbon flux and primary production in the Arctic Ocean

Marine Micropaleontology 40 (2000) 189±231

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The response of benthic foraminifers to carbon ¯ux and primary production in the Arctic Ocean J.E. Wollenburg*, W. Kuhnt Department of Geosciences, Christian-Albrechts-University, Kiel, Germany Received 17 November 1998; accepted 20 December 1999

Abstract We examine the quantitative composition of benthic foraminiferal assemblages of Rose Bengal-stained surface samples from 37 stations in the Laptev Sea, and combine this data set with an existing data set along a transect from Spitsbergen to the central Arctic Ocean. Foraminiferal test accumulation rates, diversity, faunal composition and statistically de®ned foraminiferal associations are analysed for living (Rose Bengal-stained) and dead foraminifers. We compare the results of several benthic foraminiferal diversity indices and statistically de®ned foraminiferal associations, including Fisher's alpha and Shannon± Wiener diversity indices, Q-mode principal component analysis and correspondence analysis. Diversity and faunal density (standing stock) of living benthic foraminifers are positively correlated to trophic resources. In contrast, the accumulation rate of dead foraminifers (BFAR) shows ¯uctuating values depending on test disintegration processes. Foraminiferal associations de®ned by Q-mode principal component analysis and correspondence analysis are comparable. The factor values of the correspondence analysis allow a quantitative correlation between the foraminiferal fauna and the local carbon ¯ux, which may be used as a tool to estimate changes in primary productivity. q 2000 Elsevier Science B.V. All rights reserved. Keywords: benthic foraminifera; primary production; Arctic Ocean; biogeography

1. Introduction Today, the permanent ice-covered Arctic Ocean is one of the least productive areas in the world and provides a fascinating test case for productivity/paleoproductivity proxies at the oligotrophic end of the trophic resource continuum. A ®rst attempt to relate standing stock, diversity and the distribution of foraminiferal principal component (PC) associations to the availability of food was undertaken by * Corresponding address. A. Wegener Institute for Polar & Marine Research, Columbusstr., P.O. Box 120161, 27515 Bremerhaven, Germany. Tel.: 149-471-4831-1772; fax: 149-471-48311724. E-mail address: [email protected] (J.E. Wollenburg).

Wollenburg and Mackensen (1998a) in an initial analysis of living (Rose Bengal-stained) foraminifers from the Arctic Ocean. However, this study did not quantify the relation of foraminiferal parameters to the local carbon ¯ux. One of the main problems is the dif®culty to distinguish the small marine organic carbon component from the high terrigenous organic carbon component in the total organic carbon (TOC) (Stein et al., 1994; Schubert and Stein, 1996). For this reason we regard TOC values as fairly unreliable proxy indicators of organic carbon ¯ux resulting from primary production in the Arctic Ocean. Similarly, tracers for marine organic matter, alcenones, hydrogen index values and C/N ratios do not provide reliable estimates of Corg-¯ux in the Arctic Ocean (Stein et al., 1994; Schubert and Stein, 1996).

0377-8398/00/$ - see front matter q 2000 Elsevier Science B.V. All rights reserved. PII: S 0377-839 8(00)00039-6

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Table 1 References for primary production values of the study area and calculations on annual primary production and Corg-¯uxes for the sample locations

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Fig. 1. Map of study area with sample locations.

In this study we calculate carbon ¯ux values based on published primary production data of the study area using the equation of Suess (1980) (Table 1). To relate these carbon ¯ux values to foraminiferal assemblages we compare different quantitative methods, discuss similarities and differences between results and the main advantages and disadvantages of each method. We add the faunal results from 37 cores in the Laptev Sea to the data set of Wollenburg and Mackensen (1998a) (Fig. 1). The additional cores ®ll bathymetric gaps in the shelf to slope environment data set and allow direct comparison between foraminiferal counts and plant pigment concentration values measured at the same stations. Counts of dead foraminifers are added to the original data set of Wollenburg and Mackensen (1998a). Correspondence analysis is applied to the revised data set allowing to quantify

the relationship between foraminiferal associations and carbon ¯ux estimated from primary productivity data. 1.1. Environmental conditions Hydrographic conditions were described in Wollenburg and Mackensen (1998a), and a good general overview is given by Rudels (1996). Sea-ice borders and primary production ¯uctuate widely in response to seasonal (and regional) changes in wind patterns, insolation and surface water temperatures. Primary production is largely restricted to a period of 3 months at most in the seasonally ice-free coastal areas west and north of Spitsbergen ( < 54±60 gC/ m 2/y), where the Westspitsbergen Current transports heat to the Arctic Ocean (Wassman and Slagstad,

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Fig. 2. Plant pigment concentrations in surface sediments, after Boetius et al. (1996).

1991; Hulth et al., 1994; Anderson et al., 1994; Boetius et al., 1996 (Fig. 2, Table 1). In the Laptev Sea primary production amounts to 25±42 gC/m 2/y (Rachor, 1997; Boetius and Damm, 1998). For the permanently ice-covered interior of the Arctic Ocean spectacularly high primary production estimates of .10 gC/m 2/y were published by Aagaard et al. (1996), MacDonald (1996) and Wheeler et al.

(1996), in contrast to former estimates of 1 gC/m 2/y (English, 1961). However, Wheeler et al. (1998) in their calculation assumed a productive period of 3 months even for the central Arctic Ocean. This contrasts with other studies assuming a production phase of less than 2 weeks at 858N (StroÈmberg, 1989), increasing to 3 months at most in the seasonally ice-free coastal areas. Using the per day primary production values of Wheeler et al. (1998) and taking into account the decreasing production period towards the North Pole (Andersen, 1989) gives values of approximately 2 gC/m 2/y for the central Arctic Ocean, which agrees with those of English (1961) and Zheng et al. (1998). The amount of marine organic matter that becomes buried in the sediment is indicated by the concentration of plant pigments (Chlorophyll a and phaeopigments) in the core tops of the study area (Boetius et al., 1996) (Wollenburg and Mackensen, 1998a; Figs. 2±4).

2. Material and methods We studied 37 Rose Bengal-stained sediment cores (17 multiple cores and 20 box cores) recovered from shelf to basin areas of the eastern Laptev and western

Fig. 3. Standing stock (number of Rose Bengal-stained specimens per 10 cm 2).

Fig. 4. Standing stock, BFAR and species number in relation to water depth and Corg-¯ux.

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East Siberian Sea (POLARSTERN cruise ARK XI/1, 7 July±20 September 1995, cores are recovered from 37±3827 m water depth) (Table 2). Foraminiferal counts from sediment cores from the shelf to slope areas north of Spitsbergen and the Barents Sea, as well as from the western Nansen Basin, Gakkel Ridge, Amundsen Basin, central Lomonosov Ridge and northernmost Makarov Basin (cores are recovered from 95±4411 m water depth; Wollenburg and Mackensen, 1998a), were included in the data set. Sample treatment, statistical analyses of the living fauna (.125 mm), the Shannon±Wiener index and the distribution of foraminiferal associations generated by Q-mode PC analysis for living (Rose Bengalstained) foraminifers were described in Wollenburg and Mackensen (1998a) (Fig. 1, Table 2). In this study counts are based on the benthic foraminiferal fauna .63 mm; foraminiferal thanatocoenosis were studied additionally. We used the equation of Suess (1980) to calculate the organic matter ¯ux from primary production (Wassman and Slagstad, 1991; Rachor, 1997; Gosselin et al., 1998; Boetius and Damm, 1998; Zheng et al., 1998), and used these data to test the correlation of foraminiferal faunal parameters to the calculated organic carbon ¯ux (Table 1). Faunal density (standing stock) values are given in Rose Bengal-stained specimens per 10 cm 2 surface and 1 cm depth, although living foraminifers are also found below the surface centimetre (e.g. Mackensen and Douglas, 1989; Corliss and Emerson, 1990; Rosoff and Corliss, 1992; Barmawidjaja et al., 1992; Jorissen et al., 1992; Hunt and Corliss, 1993; Loubere et al., 1993; Corliss and Van Weering, 1993; Kitazato, 1994). However, in contrast to shallow-water habitats of the Canadian Arctic where 40±90% of the living foraminiferal population is found below the surface centimetre (Hunt and Corliss, 1993), shallow-water habitats of the study area reveal 63% (38±92%) of the living foraminiferal population .125 mm to be con®ned to the surface centimetre (Wollenburg and Mackensen, 1998b; pers. unpubl. data). The mean habitat depth (described as the 95% interval on a cumulative frequency curve; Emerson and Corliss, 1990) for foraminifers .125 mm is the surface centimetre (Wollenburg and Mackensen, 1998b; pers. unpubl. data). Benthic foraminiferal accumulation rates (BFAR)

are calculated using the number of dead specimens in 10 cm 2 surface sediment, down to 1 cm depth, and published sedimentation rates for the same stations (indicated in bold letters in Table 3) as well as interpolated areal sedimentation rates (Table 3). Diversity was measured using the Fisher's alpha index (Murray, 1991; Hayek and Buzas, 1997) and the Shannon±Wiener H(S) index (for method see Wollenburg and Mackensen, 1998a). Fisher's alpha values were calculated from N (number of individuals) and S (number of species) using a program written by P. Weinholz and A. Altenbach revised for Mac-Systems in Fortran 77 by U. P¯aumann. The resulting alpha values compare well with values given in Appendix 4 of Hayek and Buzas (1997). We distinguished foraminiferal associations by Qmode PC analyses with subsequent Varimax rotation using the commercially distributed statistics package systat 5 (Tables 6 and 7). Only samples containing a minimum of 30 specimens in the living and dead data set, and only species, which in more than two samples exceeded 1% of the fauna, were included. The critical point in applying PC analysis is the use of relative species abundances (percentage values). The relative abundance of species is not solely determined by species reproduction triggered by food supply, but also by the abundance of accompanying species. Thus, the conversion of absolute abundances to percentages may generate spurious correlations among species (Krumbein and Watson, 1972; Butler, 1979). Relationships between the loadings derived from PC analyses, the percentage abundance of the most important species in PC associations and the available environmental parameters were analysed using multiple regression (Table 8). Multiple correlation coef®cients of .0.8 re¯ect a statistically signi®cant correlation between the distribution of a particular benthic foraminiferal PC association and environmental variables. Multiple correlation coef®cients of .0.6 indicate a weak relationship between environmental variables and PC associations. Correlation coef®cients of ,0.6 indicate that important environmental parameters limiting the distribution of benthic foraminiferal associations are either not included in the regression or correlations are non-linear (Mackensen et al., 1995). Simple correlation coef®cients are given for comparison (Table 8).

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Table 2 Sample number, water mass and sediment characteristics, after Anderson et al. (1994), Rudels and Schauer (unpublished), Stein et al. (1994, 1996), Boetius et al. (1996) and Boetius and Damm (1998)

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Table 3 Foraminiferal counts, standing stock, species number, Shannon±Wiener index, Equitability and Fisher's alpha index of living and dead foraminifers

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Table 3 (continued)

Correspondence factor analysis (AFC) (Benzecri, 1970) was used to examine the relation of Corg-¯ux to the distribution data of 249 benthic foraminiferal species at 91 stations (Tables 9±11). Species restricted to one sample location were omitted. The

foraminiferal counts were transformed into a 0±9 scale according to specimen abundance clusters (Table 12). Correspondence analysis usually reveals only one to three meaningful factors (Malmgren and Haq, 1982; Hermelin and Shimmield, 1995). This

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Table 4 Percentages of species of living foraminifers . 63 mm in samples from the Laptev and East Siberian Sea.

might be problematic in areas where faunas are in¯uenced by a larger number of environmental parameters. The main advantages of AFC compared to principal components analysis are: (1) simultaneous representation of constants and variables because their matrices have the same characteristic values; and (2) samples and species can be treated as active and passive elements, respectively. This allows the creation of an active data matrix and the possibility to run additional samples (for example from fossil material) as passive elements. Passive elements have no in¯uence on the position of the factor axis but are attributed to a certain factor value. This means that the observed correlation function between the recent foraminiferal fauna and the modern Corg-¯ux can

be used as transfer function for the geological past (Kuhnt et al., 1999). For all analyses we used the correspondence factor analysis software package ECOLOGIX written in 1982 by M. Roux (Montpellier University) in Fortran 4 for VAX-VMS systems. For the regression plots we used the commercial software package Cricket Graph III.

3. Results 3.1. Faunal density (standing stock) The abundance of living benthic foraminifers (standing stock) is positively correlated to the

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199

Table 4 (continued)

estimated carbon ¯ux (exponential correlation coef®cient of r ˆ 0:68† (Figs. 3 and 4, Table 2). Interestingly, the maximum standing stock value was observed in samples recovered during a local phytoplankton bloom (indicated by an arrow in Fig. 3). Generally, standing stock exhibits a negative correlation to water depth (exponential correlation coef®cient r ˆ 0:7† and sea-ice cover (see also Grebmeier et al., 1995). Highest standing stock values correspond to seasonally ice-free areas and the adjacent continental slope and basin re¯ecting down-slope organic matter transport. The number of living foraminifers under the permanent ice-cover is one order of magnitude lower than in seasonally ice-free areas of the same water depth. However, even in areas under

permanent ice-cover standing stock values differ signi®cantly in relation to minor differences in carbon ¯ux (Wollenburg and Mackensen, 1998a). 3.2. BFAR: reproduction and taphonomic controls In contrast to high standing stocks, empty benthic foraminiferal tests are less abundant in the thanatocoenosis of seasonally ice-free areas in comparison to areas under permanent ice-cover (Fig. 4). Surprisingly, BFAR are at least 10 times higher under the permanent ice-cover than within productive shelf and slope environments. Therefore, BFAR in the Arctic Ocean appear to be negatively correlated to carbon ¯ux or show no correlation to food availability.

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Table 5 Percentages of species of dead foraminifers

J.E. Wollenburg, W. Kuhnt / Marine Micropaleontology 40 (2000) 189±231 Table 5 (continued)

201

202 Table 5 (continued)

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J.E. Wollenburg, W. Kuhnt / Marine Micropaleontology 40 (2000) 189±231 Table 5 (continued)

203

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Table 6 Varimax principal component loadings of living and dead PC-association .63 mm

Foraminiferal assemblages of most stations with this unusual negative correlation exhibit intense carbonate dissolution, commonly observed in ®ne grained sediments within seasonally ice-free areas. The intensity of carbonate dissolution increases with decreasing water depth and with the duration of ice retreat (see also Hald and Steinsund, 1996). Carbonate dissolution is especially enhanced in the Laptev Sea, where even Rose Bengal-stained ªlivingº species are affected by carbonate dissolution (Fig. 4, Tables 4 and 5). Cores of the Laptev Sea shelf to upper slope environment are usually barren of empty calcareous tests from 3±4 cm

sediment depth. In contrast, empty foraminiferal tests show no signs of carbonate dissolution under the permanent ice-cover. Agglutined foraminifers have only low fossilisation potential in the modern Arctic Ocean. They are only a rare faunal component under the permanent ice-cover but are abundant in high productive shelf to upper slope environments. Consequently, the high proportion of agglutinated foraminifers in living faunas of seasonally ice-free areas further accentuates the low accumulation rate of fossil foraminifera in these areas.

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Table 6 (continued)

3.3. Diversity The diversity of living foraminifers (Fisher's alpha and Shannon±Wiener) correlates well with standing stock values (Figs. 4 and 5). Highest diversities are observed in samples from seasonally ice-free areas (Spitsbergen±Barents and Laptev Sea). Within these areas diversity increases with decreasing water depth (correlation coef®cient r ˆ 0:7 and r ˆ 0:75 for Shannon±Wiener index and Fisher's alpha index, respectively) and with increasing Corg-¯ux (correlation coef®cient r ˆ 0:7 for both Shannon±Wiener and

Fisher's alpha indices). The positive correlation between diversity and Corg-¯ux is only observed in areas of low to moderate food supply (Corg-¯ux ,7 gC/m 2/y). Shelf areas (,600 m water depth) exposed to high carbon ¯uxes reveal a negative correlation of diversity to water depth (r ˆ 0:6 and r ˆ 0:61 for Shannon±Wiener index and Fisher's alpha index), and to the availability of food (r ˆ 0:69 and r ˆ 0:71 for Shannon±Wiener index and Fisher's alpha index, Fig. 5, respectively). The diversity of foraminiferal thanatocoenosis follows the trend of the living faunas, revealing negative correlation to

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Table 7 Varimax principal component scores of living and dead PC-associations

J.E. Wollenburg, W. Kuhnt / Marine Micropaleontology 40 (2000) 189±231 Table 7 (continued)

207

208 Table 7 (continued)

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Table 8 Multiple regression coef®cients of living and dead PC-associations. Simple linear correlation coef®cients between single environmental variables and dominant species (absolute abundances per 10 cm 2) and single PC associations (PC loadings), respectively. Those of the simple correlation coef®cients that re¯ect a signi®cant in¯uence of the environmental parameters on the faunal composition as indicated by stepwise multiple regression analysis (cut-off at 95% probability level of single regression coef®cients) are given in bold numbers. Lower part of table gives multiple correlation coef®cients (R) of regression analyses of combined signi®cant environmental variables and single species and between signi®cant environmental variables and faunal associations (PC's), respectively. Note that only correlation coef®cients .0.6 are regarded as fair, i.e. indicate some in¯uence of the environmental parameters on the faunal composition

water depth and positive correlation to Corg-¯ux with correlation coef®cients to water depth of r ˆ 0:5 and 0.55 and to Corg-¯ux of r ˆ 0:5 and 0.4 for Shannon± Wiener index and Fisher's alpha index, respectively. However, whereas the Shannon±Wiener index shows similar values for living and dead faunas at Corg-¯ux levels ,7 gC/m 2/y, the Fisher's alpha shows approximately double values in the thanatocoenosis. A possible explanation of the unusually high Fisher's

alpha values of the thanatocoenosis at deeper stations may be the transport of foraminiferal tests of very shallow marine origin to areas under permanent icecover by drifting sea-ice. In areas of increased marine organic matter accumulation (.7 gC/m 2/y), the Fisher's alpha index shows approximately the same values for living and dead assemblages, although the Shannon±Wiener index is signi®cantly lower in the thanatocoenosis.

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Table 8 (continued)

These differences in the Shannon±Wiener index values mainly re¯ect the preferential preservation of robust tests, which are less susceptible to dissolution. 3.4. Distribution of foraminiferal associations discriminated by Q-mode PC analysis Most of the total variance of our data set can be explained by eight and six factors for living and dead foraminifers, respectively. The species composition in the living associations differs from the results of a previous PC analysis of stations predominantly from permanently ice-covered areas of the Arctic Ocean (Wollenburg and Mackensen, 1998a). These differences result from the inclusion of a large number of stations from seasonally ice-free

areas with high carbon ¯ux in our data set. Consequently, minor ¯uctuations in food availability under the permanent ice-cover are not discriminated by our PC analysis. This eight-factor model for living foraminifers reveals the prevalence of at least one foraminiferal association with factor loadings .0.4 for 85 of the 89 cores included in the statistical model (Tables 6 and 7). A six-factor model is used for the discrimination of dead foraminiferal PC associations, explaining 90 of the 91 cores included in the statistical model. Most dead associations correspond to almost identical living associations (Figs. 6 and 7, Table 13). The organic species Placopsilinella aurantiaca and the agglutinated species Adercotryma glomerata have only low fossilisation potential. Tests of unstained

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Table 9 Correspondence analysis of living foraminifers species factor values

A. glomerata, in particular, are only rare faunal components of the thanatocoenosis under permanent ice-cover. The distribution of foraminiferal PC associations is given in Table 13. Although it was already shown that multiple regression is an unreliable method for comparing PC associations to environmental parameters in the Arctic

Ocean (Wollenburg and Mackensen, 1998a), this method was applied for comparison with other studies revealing linear relationships between foraminiferal associations and prevailing environmental conditions (e.g. Mackensen et al., 1995; Schmiedl et al., 1997; Schmiedl and Mackensen, 1997; Table 8). None of the generated PC associations reveal a relation to

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Table 9 (continued)

the sediment composition (sand and carbonate content). Since water masses in the Arctic Ocean are vertically strati®ed, water depth and water mass characteristics such as salinity and temperature are always correlated. Reliable multiple regression coef®cients (multiple R . 0:6† are only observed for foraminiferal PC associations of the deepest (Stetsonia

horvathi-) and shallowest habitats (Portatrochammina karica- and Textularia torquata-association), indicating a correlation to increasing water depth. 3.5. Correspondence analysis (AFC) In this study only factor 1 values reveal an

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Table 10 Correspondence analysis of dead foraminifers species factor values

interpretable correlation to the prevailing environmental conditions, whereas values for factors 2 and 3 reveal no obvious pattern. We processed linear and exponential correlations between the correspondence factor value F1 and the environmental parameters available. F1 shows no relation to the sediment composition, latitude and longitude. Furthermore, there is no obvious correlation to temperature and salinity. There is a correlation between F1 and water depth, with exponential correlation coef®cient r of 0.89 for living and 0.91 for dead foraminifers (Fig. 8). There is a 0.91 and 0.86

exponential correlation coef®cient to the estimated Corg-¯ux (Fig. 9). The comparison of F1 to the sedimentary plant pigment concentrations of Laptev Sea samples reveals an exponential correlation coef®cient of r ˆ .0:7 (Figs. 10 and 11). Three samples (PS2453, 2463, 2480) deviate from the general trend. These samples are all located in very shallow areas (30±70 m). The foraminiferal fauna of very shallow environments in the Arctic Ocean may be in¯uenced by additional environmental parameters independent of the availability of food, such as salinity-, temperature- or oxygen gradients.

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Table 10 (continued)

4. Discussion 4.1. Distribution patterns of benthic foraminiferal associations Wollenburg and Mackensen (1998a) examined the distribution of PC-associations of living foraminifers .125 mm. Only two PC-associations of living foraminifers .63 mm were included in their discussion (Table 14). We concentrate our discussion on PCassociations derived from the analysis of the .63 mm fraction not described in this earlier study.

Species related to increased current activity (e.g. Lobatula lobatula) are only subsidiary faunal components of the living fauna in the calm environment of the Laptev Sea. Furthermore, many calcareous foraminifers (e.g. A. gallowayi, Pullenia spp., Eilohedra nipponica, Discorbinella berthelothi) abundant in samples off Spitsbergen, are absent or only rare faunal components in samples from the Laptev Sea. Therefore, in our model, no PC association dominated by calcareous foraminifers is representative of shallow marine environments, as described off Spitsbergen by Wollenburg and Mackensen (1998a). In contrast,

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Table 11 Correspondence analysis of living and dead foraminifers sample factor values

shelf to upper slope samples of the Laptev Sea are usually dominated by agglutinated foraminifers. In Q-mode principal analyses on the total data set ¯uctuating abundance of Textularia torquata and Portatrochammina karica, are expressed by two factors, in contrast to one factor in the earlier investigation (Wollenburg and Mackensen, 1998a). Additionally, shallow samples of the Lomonosov Ridge are referred to the Epistominella arctica PC association in this study, but were referred to the Cassidulina teretis PC association by Wollenburg and Mackensen (1998a). The permanently ice-covered environment is characterised by four PC associations, two of which (Stetsonia horvathi and Placopsilinella aurantiaca)

are exclusively con®ned to it. The foraminiferal fauna is predominantely small, calcareous thinwalled, with un-ornamented tests. The S. horvathi association dominates basin environments and occasionally oceanic ridges and plateaus under higher current activity. Stations where Adercotryma glomerata disintegrates after death are also included in the dead S. horvathi PC association. It is assumed that the low trophic requirement of S. horvathi (Figs. 12 and 13), and the ability to cope with higher current activity than Epistominella arctica and A. glomerata determine the distribution of S. horvathi. Epistominella arctica is an opportunistic species reproducing during short, pulsed local phytoplankton blooms (see arrow on Fig. 6), releasing large numbers

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Table 12 Correspondence analysis of living and dead foraminifers foraminiferal counts coding Specimen numbers of living/dead foraminifers were transformed in a 0±9 matrix according to their absolute abundances per 10 cm 2 sediment surface/sample Living foraminifers

Dead foraminifers

Code

Counts

Code

Counts

0 1 2 3 4 5 6 7 8 9

,1 ,5 , 15 , 25 , 35 , 45 , 55 , 75 , 125 . 250

0 1 2 3 4 5 6 7 8 9

, 30 , 100 , 250 , 500 , 750 , 1250 , 2500 , 5000 , 10 000 . 10 000

of offspring. Epistominella exigua and related species are regarded as ªphytodetritus speciesº (Gooday, 1994; Smart et al., 1994; Thomas et al., 1995; Smart and Gooday, 1997). Highest numbers of living E. arctica occur during phytoplankton blooms, suggesting a close relationship to E. exigua and other ªphytodetritus speciesº. However, E. arctica is predominantly observed in oligotrophic habitats, which is at odds with its determination as a ªphytodetritus speciesº normally indicating enhanced productivity. E. arctica is less abundant in times of extremely low food availability when the living foraminiferal fauna is dominated by the Adercotryma glomerata association. The distribution of E. arctica at larger water depths in seasonally ice-free areas, rather than in areas under the permanent ice-cover, points to a low but distinctly higher trophic requirement of E. arctica in comparison to Stetsonia horvathi (see also Figs. 12 and 13). Adercotryma glomerata occurs in all water depths. It exhibits a very distinct test size variation. Specimens under the permanent ice-cover are exclusively ,125 mm, whereas in high productive areas up to 100% of the specimens exceed .125 mm test size. The A. glomerata PC association is distributed along the continental slope and oceanic ridges in water depths of 900±3400 m (Figs. 6 and 7, Table 13). An additional occurrence in 197 m (PS2143-1) con®rms a

widespread species distribution. The A. glomerata PC association at larger water depths replaces the Epistominella arctica PC association at shallower water depths and the Portatrochammina karica PC association in areas of moderate current activity or lower Corg-¯uxes. The species is commonly reported from low energy environments and substrates with low organic carbon content (Kaminski and SchroÈder, 1987; SchroÈder-Adams et al., 1990; Hunt and Corliss, 1993). However, the mobile infaunal A. glomerata replaces E. arctica and P. karica in areas exposed to moderate current activities (Wollenburg and Mackensen, 1998b). Areas exposed to higher current activities under the permanent ice-cover are dominated by Stetsonia horvathi, and in seasonally ice-free areas by Reophax guttifer and Lobatula lobatula (Table 13). Six foraminiferal PC associations are revealed from samples of the seasonally ice-free areas, two of which (Epistominella arctica and Adercotryma glomerata) are also present under the permanent ice-cover. The mean test size of benthic foraminifers of seasonally ice-free areas is much larger than in permanently icecovered areas. Foraminiferal faunas of the outer shelf to slope environments, in particular, are often dominated by species with adult individuals exceeding .125 mm in test size. The Reophax guttifer PC association occurs in water depths of 900 to 2500 m (Figs. 6 and 7, Table 13). It is restricted to the continental slope of Spitsbergen and the Yermak Plateau in the living fauna. Due to the low fossil potential of Adercotryma glomerata, R. guttifer is also a dominant component of the Barents and Laptev Sea thanatocoenosis. An association of the total foraminiferal fauna (living 1 dead) characterised by R. guttifer has been described by Scott and Vilks (1991) from the Yermak Plateau. These authors proposed that corrosive bottom waters prevented the secretion of calcareous tests, favouring the distribution of agglutinated species. It is also assumed in this study that the distribution of corrosive bottom water in¯uences the ratio of agglutinated versus calcareous foraminifers. However, if the distribution of the living R. guttifer association were solely determined corrosive bottom waters, the association should not be absent in the Laptev Sea. In the correspondence analysis of living foraminifers R. guttifer shows lower factor values than A. glomerata (Figs. 12 and 13). Since correspondence analysis factor values

Fig. 5. Fisher's alpha and Shannon±Wiener index of living and dead foraminifers in relation to water depth and Corg-¯ux.

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Fig. 6. Distribution of living benthic foraminiferal associations, highest PC values.

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Fig. 7. Distribution of dead benthic foraminiferal associations, highest PC values.

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Table 13 Short description of living (a) and dead (b) benthic foraminiferal PC-associations 220 J.E. Wollenburg, W. Kuhnt / Marine Micropaleontology 40 (2000) 189±231

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Fig. 8. Correspondence analyses factor 1 sample values of living and dead foraminifers, respectively, in relation to water depth.

are inversely to the availability of food (Fig. 9), the distribution of R. guttifer may be related to higher Corg-¯uxes than that of A. glomerata. Lobatula lobatula dominates Arctic shelf areas under high current activities (Wollenburg and Mackensen, 1998a; Fig. 6, Table 13). However, this environment is usually characterised by the smallsized agglutinated foraminifers Portatrochammina karica and Textularia torquata (Figs. 6 and 7, Table 13). The P. karica PC association usually dominates the outer continental shelf, whereas the T. torquata PC association occupies the inner shelf environment. Both environments are characterised by seasonally ¯uctuating salinities due to river input and winter water formation (Table 8). T. torquata was related to the distribution of low saline waters (Mudie et al., 1984; Murray, 1991). However, as T. torquata and P. karica are assigned an infaunal microhabitat (Hunt and Corliss, 1993 (P. karica as P. bipolaris); Wollenburg and Mackensen, 1998b) food availability may rather determine the distribution of these species. Agglutinated foraminiferal assemblages dominate seasonally ice-free areas, where extensive carbonate dissolution controls the composition of foraminiferal thanatocoenosis (Hald and Steinsund, 1996; Wollenburg and Mackensen, 1998a). This is especially obvious in the Laptev Sea due to severe carbonate dissolution on the extended shelf and slope (Fig. 7).

However, at water depths ,500 m even the foraminiferal biocoenosis is exclusively dominated by agglutinated foraminifers (Fig. 6). The ªcalcareousº shelf to slope PC associations (Cassidulina teretis, Lobatula lobatula) of the Spitsbergen and Barents Sea area are absent in the Laptev Sea. In contrast, unilocular agglutinated foraminifers (Crithionina spp., Saccammina sphaerica, Saccammina socialis, Hippocrepinella spp.) ¯ourish in the Laptev Sea, essentially contributing to the living Portatrochammina karica PC association (Table 13). The construction of sediment ªcocoonsº around the foraminiferal test is a common feature in the Laptev Sea, where most calcareous and some agglutinated species are at least occasionally found ªprotectedº. The function of this sediment cocoon may be protection of the foraminiferal test against corrosive bottom and pore waters, indicating that periodically corrosive waters may effect the living foraminiferal fauna (see also Greiner, 1974; Scott and Vilks, 1991; Hunt and Corliss, 1993). However, this hypothesis needs to be veri®ed by culturing experiments. 4.2. Relation of benthic foraminiferal assemblages to Corg-¯ux Several attempts were made to quantify the relation between benthic foraminiferal abundance, diversity

Fig. 9. Correspondence analyses factor 1 sample values of living and dead foraminifers, respectively, in relation to Corg-¯ux.

222 J.E. Wollenburg, W. Kuhnt / Marine Micropaleontology 40 (2000) 189±231

Fig. 10. Correspondence analyses factor 1 sample values of living and dead foraminifers, respectively, in relation to the chlorophyll a content of surface sediments.

J.E. Wollenburg, W. Kuhnt / Marine Micropaleontology 40 (2000) 189±231 223

Fig. 11. Correspondence analyses factor 1 sample values of living and dead foraminifers, respectively, in relation to the chlorophyll a and phaeopigment content of surface sediments.

224 J.E. Wollenburg, W. Kuhnt / Marine Micropaleontology 40 (2000) 189±231

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Fig. 12. Correspondence analyses factor 1 species values and characterising species of PC associations of living foraminifers.

225

226

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Fig. 13. Correspondence analyses factor 1 species values and characterising species of PC associations of dead foraminifers.

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Table 14 PC-associations of Wollenburg and Mackensen (1998a) and this study Wollenburg and Mackensen (1998a) PC-association .125 mm (living)

This study PC-association .63 mm (living)

PC-association .63 mm (dead)

Placopsilinella aurantiaca ªPrimitiveº foraminifers Cassidulina teretis Loanella tumidula Reophax fusiformis± Hippocrepi-nella ¯exibilis Lobatula lobatula Oridorsalis tener± Triloculina frigida Fontbotia wuellerstor® ±

Placopsilinella aurantiaca ± Cassidulina teretis ± ±

± ± ± ± ±

± ±

Lobatula lobatula ±

± Adercotryma glomerata

± ± ± ±

Reophax guttifer Stetsonia horvathi a Epistorminella arctica a Portatrochammina karica

± Reophax guttifer±Adercotryma glomerata

±

Textularia torquata a

Stetsonia horvathi Epistorminella arctica Portatrochammina karica± Lagenammina dif¯. arenulata Textularia torquata

Denotes PC-association .63 mm described in Wollenburg and Mackensen (1998a).

and assemblage composition and Corg-¯ux. These works also took into account the carbon isotopic difference between benthic foraminifers of different microhabitats (McCorkle et al., 1985, 1990; Zahn et al., 1986; Loubere, 1987), the accumulation rate of benthic foraminiferal tests (Herguera and Berger, 1991; Loubere, 1997; Martinez et al., 1999) and the species composition of benthic foraminiferal associations (Loubere, 1994, 1997). Recent studies have shown, that benthic foraminifers are sensitive to seasonal ¯uctuations in primary production (Gooday and Lambshead, 1989; Gooday, 1993; Thomas et al., 1995; Thomas and Gooday, 1996; Loubere, 1997; Fariduddin and Loubere, 1997). These studies regard the abundances of ªphytodetritus speciesº (Epistominella exigua; Alabamina weddellensis ˆ Eilohedra nipponica in this study) and mobile, predominantly deep infaunal species (Melonis barleanum, Melonis zaandami, Uvigerina peregrina) as indicators of predominantly seasonally pulsed versus continuous primary production. However, both these species groups are absent or only rare faunal components in the seasonally icefree shelf to upper slope environments of the Arctic

Ocean and their abundance patterns cannot be used for phytodetritus ¯ux reconstructions within the shallow Arctic environments. Benthic foraminiferal diversity is positively correlated to organic carbon ¯ux in the Arctic Ocean, however, we observed differences for living and dead assemblages and different diversity indices. The input of allochthonous foraminifers by drifting sea-ice obviously increases the Fisher's alpha values in thanatocoenosis in samples from areas under permanent ice-cover. The Shannon±Wiener index is unaffected by these allochthonous tests since it is less sensitive to the presence of rare species. Using the Shannon±Wiener index, approximately equal values are calculated for living and dead assemblages from samples under the permanent ice-cover. In contrast, the taphonomic loss caused by intensive carbonate dissolution within seasonally ice-free areas has little in¯uence on the Fisher's alpha values of foraminiferal thanatocoenosis, but signi®cantly decreases the Shannon±Wiener index to approximately half of the values for the living fauna. Wollenburg and Mackensen (1998a) suggested, that the composition of living foraminiferal PC

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associations in the Arctic Ocean is related to the availability of food. Yet, the study of Wollenburg and Mackensen (1998a) was lacking some crucial data, such as foraminiferal counts from seasonally icefree areas or photopigment concentration data, to quantify this relationship. We included the original data set of Wollenburg and Mackensen (1998a) in the new Q-mode analyses, which now include the area of the Laptev Sea. As a result the composition and distribution of the PC associations in the study area of these authors are slightly changed (Fig. 6 compared to Fig. 7b in Wollenburg and Mackensen, 1998a). Because of the dominance of the Cassidulina teretis PC association at shallower sites of the Lomonosov Ridge, Wollenburg and Mackensen (1998a) argued, that the Lomonosov Ridge might be an area of periodically increased Corg-¯ux. However in the extended PC analysis, samples of the Lomonosov Ridge, formerly ascribed to the C. teretis PC association, are now referred to the Epistominella arctica PC association. The faunal evidence for an increased Corg-¯uxes at the Lomonosov Ridge became obscured by increasing the data set. In contrast, adding the foraminiferal counts of the Laptev Sea obviously improved the faunal pattern revealed from the seasonally ice-free areas. With the large data set available now, the regional distribution of PC associations appears to correlate to productivity and C-¯ux patterns (Figs. 6 and 7, Table 13), although no statistically signi®cant quantitative correlation is obtained using Q-mode PC-analysis (Table 8). Correspondence analysis reveals only a small number of meaningful factors, but shows a very close correlation of the ®rst factor to the most in¯uential environmental parameter. This may be problematic in areas, where the benthic foraminiferal fauna is strongly in¯uenced by several environmental parameters such as salinity, temperature and organic carbon ¯ux. However, there are only minor ¯uctuations in bottom water salinity and temperature in the deep Arctic Ocean and these minor ¯uctuations have no in¯uence on the species composition of benthic foraminiferal assemblages. The critical environmental parameter in¯uencing Arctic benthic foraminifers is the episodic supply of food derived from the low and extreme seasonal primary production. We calculated this Corg-¯ux using available primary production data (Table 1). Correlating calculated Corg-¯ux values

with F1 values of the correspondence analysis, revealed correlation coef®cients of r ˆ 0:9 for living and dead foraminifers (Fig. 9). Similar results were obtained by comparing the F1 values with sedimentary plant pigment concentrations …r ˆ .0:7† (Figs. 10 and 11). Additional samples can be treated in the correspondence analysis as passive parameters that have no in¯uence on the position of the factor axis but will be assigned a factor value. Based on the nowexisting surface data set it will be possible to calculate Corg-¯uxes from new recent or fossil foraminiferal samples of other areas of the Arctic Ocean. Thus, the relationship of F1 to Corg-¯ux may provide a reliable transfer function for fossil samples (Wollenburg et al., 2000). 5. Conclusion The main purpose of this study was to examine the relation of foraminiferal bioconosis and thanatoceonosis to the carbon ¯ux- and productivity-dependent availability of food in the Arctic Ocean. Three approaches were tested: (1) abundance of living foraminifera (standing stock) and BFAR; (2) diversity using different diversity indices; and (3) composition and distribution of benthic foraminiferal associations using two different multivariate statistical techniques (Q-mode principal component analysis and correspondence analysis). Principal results of are: 1. Although the standing stock reveals an obvious correlation to Corg-¯ux …r ˆ 0:7†; the BFAR show no correlation to Corg-¯ux gradients. At any given water depth highest BFAR are revealed from areas under permanent ice-cover, lowest are found in seasonally ice-free areas. 2. Diversities reveal a positive correlation to the availability of food at Corg-¯ux levels ,7 gC/m 2/y, but change to a negative correlation at higher Corg¯uxes levels. Signi®cant differences in the postmortem diversity change were revealed when applying the Shannon±Wiener and Fisher's alpha indices. The Shannon±Wiener index of fossil samples most likely re¯ects the original diversity of biocoenosis within intermediate to deep-water environments, whereas the Fisher's alpha index is strongly in¯uenced by rare allocthonous species. In

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samples from seasonally ice-free areas, which are strongly affected by dissolution-related taphonomic loss, the Fisher's alpha index of foraminiferal thanatocoenoses agrees better with the diversity of the original biocoenosis. 3. The composition and distribution of foraminiferal associations are determined by the local Corg-¯ux. The correspondence analysis reveals high correlation coef®cients between the local Corg-¯ux, and the assemblage composition of living and dead foraminifers. We obtained a r ˆ 0:91 (live) and r ˆ 0:86 (dead) correlation coef®cient between the ®rst factor of the correspondence analysis and the calculated carbon ¯ux. The correlation equation can be used as a transfer function relating foraminiferal counts to Corg-¯ux and primary production. Acknowledgements First of all we thank our colleague Andreas Mackensen for making the POLARSTERN samples available to us, for many fruitful remarks, and for inspiring discussions. We are grateful to Ann Holbourn for critical reading the manuscript and correcting the English. Many thanks go to the reviewers (Otto Hermelin and Ellen Thomas) for their constructive comments, especially Ellen Thomas' extensive review helped us to signi®cantly improve the original manuscript. We extend our thanks to our colleagues RuÈdiger Stein, K. Fahl, E. Damm and A. Boetius who shared unpublished sediment data. This study was supported by DFG grant KU649/6. References Aagaard, K., Barrie, L.A., Carmack, E.C., Garrity, C., Jones, E.P., Lubin, D., MacDonald, R.W., Swift, J.H., Tucker, W.B., Wheeler, P.A., Whritner, R.H., U, S., 1996. Canadian researchers explore the Arctic Ocean. EOS 209, 213. Andersen, O.G.N., 1989. Primary production, chlorophyll, light, and nutrients beneath the Arctic sea ice. In: Herman, Y. (Ed.). The Arctic Seas, Climatology, Oceanography, Geology and Biology, Van Nostrand Reinhold, New York, pp. 147±191. Anderson, L.G., Olsson, K., Skoog, A., 1994. Distribution of dissolved inorganic and organic carbon in the Eurasian Basin of the Arctic Ocean In: Johannessen, O.M., Muench, R.D., Overland, J.E. (Eds.), The polar oceans and their role in shaping

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