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Ecological Indicators 29 (2013) 219–233
Contents lists available at SciVerse ScienceDirect
Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind
Defining past ecological status and in situ reference conditions using benthic
foraminifera: A case study from the Oslofjord, Norway
Jane K. Dolven a , Elisabeth Alve a,∗ , Brage Rygg b , Jan Magnusson b
a
b
Department of Geosciences, University of Oslo, P.O. Box 1047, Blindern, 0316 Oslo, Norway
Norwegian Institute for Water Research (NIVA), Gaustadallèen 21, 0349 Oslo, Norway
a r t i c l e
i n f o
Article history:
Received 2 August 2012
Received in revised form
21 December 2012
Accepted 29 December 2012
Keywords:
Environmental monitoring
In situ reference conditions
Biological quality element
Conservation Paleobiology
European Water Framework Directive
Ecological Quality Status (EcoQS)
a b s t r a c t
Characterizing marine water bodies and defining ecological status, both present and past (pre-impacted),
has become an important task for EU’s Member States and their associates during the last decade due to
the implementation of the Water Framework Directive (WFD). However, none of the methods used to
define Ecological Quality Status (EcoQS) are able to accurately define the status for both the present-day
and reference conditions at a given site (i.e., in situ). Recent studies have revealed a significant correlation between the diversity of living (stained) fossilizable benthic foraminifera (protists) and associated
environmental parameters (e.g., dissolved oxygen concentration). The present study takes this relationship a step further by applying methods used to define present-day EcoQS on fossil benthic foraminiferal
assemblages and, thereby, defining past EcoQS (PaleoEcoQS). This is particularly useful for defining reference condition in areas where biological- and instrumental time-series are limited or lacking. Our
case study from the Oslofjord, Norway, shows that (1) the “Foraminiferal method” can define temporal
developments in in situ EcoQS from reference to present-day conditions, (2) results of the “Foraminiferal
method” reflect available historical biological records and hydrographic time series, (3) data (1993 and
2009) on macrofauna (traditional bio-monitoring tool) and benthic foraminifera from the same sites
define the same EcoQS, and (4) the changes in foraminiferal diversity through time are due to human
activity (pollution), rather than climate change. Using in situ data to define ecological reference conditions is preferable compared to modeling or comparisons with present-day supposedly similar reference
conditions.
© 2013 Elsevier Ltd. All rights reserved.
1. Introduction
During the last two centuries, Europe has experienced an industrial (and agricultural) revolution, a large population growth with
an increased anthropogenic pressure and consequently increasing
pollution problems severely threatening the water quality in many
areas. To better manage, preserve and protect European water
environments the need for a common European water policy and
legislation arose and, in 2000, the EU’s Member States, Norway
and the European Commission agreed on the Water Framework
Directive. This directive established a framework for long-term
protection of all water resources including lakes, rivers, transitional water, coastal water and groundwater, preventing these
water resources from further deterioration, enhancing their status
if needed and promoting sustainable water use (WFD, 2000/60/EC).
This was later complemented by the Marine Strategy Framework
Directive (2008). Much effort has been put into defining and
∗ Corresponding author. Tel.: +47 22 85 73 33; fax: +47 22 85 42 15.
E-mail address: ealve@geo.uio.no (E. Alve).
1470-160X/$ – see front matter © 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.ecolind.2012.12.031
identifying different types of water bodies based on geographical
and hydrological determinants. This identification has been necessary to accurately describe the water body’s status and compare
it to the Directive’s environmental objectives. Each water body is
classified into five status categories (High, Good, Moderate, Poor
and Bad) based on biological, chemical and physical quality elements (Table 1). Minimum requirements set by the Directive are
that all water environments must reach at least “Good” ecological
quality status (EcoQS) or the “reference condition” by 2015.
The main purpose of environmental monitoring is to investigate
the ecological quality status or “health” of the area in focus and
whether or not this has changed over time due to human impact.
The only way to determine if the status has changed is to compare
the present-day situation with the pre-impacted “reference conditions” (Alve, 1991). To define this, the following approaches are
recommended within the WFD: (1) Compare the biological characteristics of the area in question with those of assumed similar
areas that have not or barely been influenced by human activity
(“pristine” sites), (2) use models to reconstruct former “reference
conditions”, (3) use historical data, (4) use expert opinions (for
discussion, see Borja et al., 2012). Even though these methods for
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J.K. Dolven et al. / Ecological Indicators 29 (2013) 219–233
Table 1
Classification tools and class intervals used for defining status. The diversity indices for benthic foraminifera and geochem
and ES100 (class intervals for macro-invertebrates from Veileder 01: 2009), exp(Hbc
) (Bouchet
ical parameters include Hlog
2
et al., 2012), heavy metals (Cd, Cu, Zn; Bakke et al., 2010), and total organic carbon (TOC; Molvær et al., 1997).
Status
High
Good
Moderate
Poor
Bad
H’
>3.8
3.0-3.8
1.9-3.0
0.9-1.9
<0.9
ES100
>25
17-25
10-17
5-10
<5
Exp H’bc
>20
15-20
10-15
5-10
<5
mg Cd/kg
<0.25
0.25-2.6
2.6-15
15-140
>140
mg Cu/kg
<35
35-51
51-55
55-220
>220
mg Zn/kg
<150
150-360
360-590
590-4500
>4500
TOC
<2.0
2.0-2.7
2.7-3.4
3.4-4.1
>4.1
defining “reference conditions” have been the best available so far,
they suffer from lack of long biological and instrumental time-series
providing information back to pre-impacted times, and the comparative approach (1) is problematic, particularly in estuarine areas
(Alve, 1995a). Consequently, other approaches should be explored.
Paleoecological analyses of dated sediment cores can provide information about several aspects of ecological status in former times
and thereby reference conditions by means of e.g., diatoms to
reconstruct paleo-TN concentrations in the water masses (e.g.,
Clarke et al., 2003; Andersen et al., 2004), pigments to investigate
paleo-phytoplankton community structure (e.g., Reuss et al., 2005),
dinoflagellate cysts to detect possible eutrophication events (e.g.,
Dale, 2009), and benthic foraminifera to document anthropogenic
impacts on marine soft-bottom ecosystems (e.g., Alve, 1991; Scott
et al., 2001; Hayward et al., 2004; Tsujimoto et al., 2008). The
methodology and philosophy is closely linked to the field of conservation paleobiology (for examples and discussion, see Dietl and
Flessa, 2011).
The close links between benthic foraminiferal (protist) assemblages and environmental characteristics are well documented
(examples in Murray, 2006) and their use in human-impact studies
has recently been reviewed by Martínez-Colón et al. (2009). In an
effort to “adapt” the paleoecology-approach to the criteria and terminology used in conventional monitoring, a pilot study using the
Norwegian governmental classification system for characterization
of present-day ecological status was successfully applied on benthic foraminifera and geochemical data from sediment cores in the
inner Oslofjord, Norway (Alve et al., 2009a). Recently, significant
correlations between the diversity of benthic foraminifera in fjord
basins and environmental parameters (primarily bottom water
dissolved oxygen) have been established and a new foraminiferabased diversity index, i.e., the exponential, bias corrected Shannon
)), is proposed for assessing ecological status in Norindex (exp(Hbc
wegian coastal waters (Bouchet et al., 2012). This classification
system is based on the same five status classes as the classification
system of the WFD.
Our present study aims to investigate the potential of
applying conventional ecological classification systems on fossil
foraminiferal data for defining EcoQS back in time (i.e., PaleoEcoQS).
The reliability of the method is tested by comparing the results
of the paleoecological analyses with historical biological records
and hydrographical time series. If the method works it is a good
indication that it will enable determination of in situ reference conditions even in areas where no historical information is available, an
accomplishment which is particularly important for implementing
the WFD. An additional aim is to compare the diversity of benthic foraminifera with other environmental proxies, such as total
organic carbon and concentrations of heavy metals. The final aim is
to investigate whether temporal changes in ecological status below
the seasonal layer in inner Oslofjord during the last century is a
result of changes in pollution or of a changing climate (or both).
2. Characteristics of the investigation area
2.1. Geomorphologic setting and hydrography
The inner Oslofjord is located in SE Norway (Fig. 1). It is separated from the outer Oslofjord by a narrow sound (width about
1600 m) with a shallow sill at 19.5 m water depth just north of
the small town of Drøbak. About half the width of the sound is
blocked by a submarine jetty reaching up to about 1 m below the
sea-surface. Seen from the air, the inner fjord system looks like the
neck and head of a swan. Choosing the shortest path, the inner fjord
stretches about 40 km from Drøbak in the south (“the swan neck”)
to the innermost part (“the beak”). Along this path there are two
main basins, Vestfjord and Bunnefjord, and several smaller basins.
The Vestfjord and Bunnefjord have a maximum water depth of
about 160 m. The north-south oriented Nesoddtangen-Bygdøy sill
with a water depth of about 50 m separates the two main basins and
influences the water exchange within the inner Oslofjord system.
Due to the narrow sound and shallow sill at Drøbak, the inner
Oslofjord is partly enclosed and the transport of water between the
outer and the inner fjord is limited, especially below sill depth. The
stratification above sill level in the inner fjord is often imported
from the outer fjord by the semidiurnal tide (range about 28 cm),
wind and atmospheric pressure variations. The local freshwater
discharge is low (annual averages of about 27 m3 /s; Baalsrud and
Magnusson, 2002) compared to the discharge from rivers to the
outer Oslofjord (Glomma and Drammenselva, annual averages 720
and 330 m3 /s, respectively). This often results in a transport of low
saline surface water from the outer to the inner fjord system during
the spring and summer (reversed estuarine circulation).
The deep water is renewed by denser water from the
outer fjord/Skagerrak during the winter and early spring
(October/November–April). The main driving force is northerly
winds over the Oslofjord/inner Skagerrak area. The strength and
duration of the northerly winds determine the amount of renewed
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J.K. Dolven et al. / Ecological Indicators 29 (2013) 219–233
221
Bunnefjord has been more severely affected by low oxygen than
the Vestfjord but in the former, water depths shallower than 80 m
have not experienced anoxia since the year 2000 (Berge et al., 2010).
2.2. Pollution history
Fig. 1. Inner Oslofjord with sampling sites, hydrographic stations, and location
of main sills (white dashed lines) indicated (after Lepland et al., 2010). Southern
sill = Drøbak sill, northern sill = Nesoddtangen-Bygdøy sill.
water (Gade, 1968). Deep-water renewals occur annually in the
Vestfjord, but only once every 3–4 years below 50–60 m (sill
depth) in the Bunnefjord. The difference between the two basins is
explained by the 5 times higher vertical diffusion in the Vestfjord,
reducing the density (salinity) in the deep water in the stagnation period (May–October) and increasing the possibility for denser
water at sill depth outside the sill to renew the Vestfjord (Gade,
1968).
While the surface water temperature is mainly influenced by
(local) air temperature, the deep water temperature varies with
the general winter air temperature in the inner Skagerrak/Oslofjord
area at a time preceding the renewal. That is why the deep water
temperature range is 6–7 ◦ C (Fig. 2), except in years with early deep
water exchange or in periods with milder winter climate that has
been frequent in the area after 1989. At 60 m depth the temperature is similar in Bunnefjord and Vestfjord as it is close to the
depth of the sill separating them (50 m). At 90–100 m the similarity is slightly less pronounced due to periodic differences in the
deep water renewal (Fig. 2). However, from an ecological point of
view, the temperature differences between the basins are small.
The salinity in the deep water is 32–34 (Baalsrud and Magnusson,
2002).
The fjord experienced a significant decrease in dissolved [O2 ]
since regular measurements started in 1934 until the middle of the
1980s from which time improvements are recorded (Fig. 3). The
In the Oslo area industrial pollution became prominent in the
second half of the 19th century (Baalsrud and Magnusson, 2002).
Paper mills, textile-, nail- and chemical-factories as well as breweries and other industries were discharging their untreated waste
directly into the small rivers and later via the municipal sewage
system. In addition to industrial waste the largest pollution source
in the inner Oslofjord during the last century has been municipal sewage discharge from the continuously growing population
of the city of Oslo (Arnesen, 2001; Baalsrud and Magnusson, 2002).
In the early 1900s the pollution was limited to near-shore or harbor areas, but as the population grew the entire inner fjord was
affected. In 1933 the Bunnefjord was found to be anoxic at 150 m
water depth (Braarud and Ruud, 1937) and in November 1950 the
hydrogen sulfide layer reached from the bottom up to 75 m depth
(Beyer and Føyn, 1951) due to the combined effects of pollution
and lack of deep water renewal. Oslo’s first (mechanical) wastewater treatment plant was established in 1910 and others were
established in the following decades (Arnesen, 2001). Although the
sludge method removed much of the organic material and bacteria from the wastewater, little was done to remove nutrients (like
phosphorus and nitrogen). The latter were discharged untreated
into the fjord assuming that the fjord was capable of purifying
itself. Instead the nutrients were fertilizing the fjord causing large
algal blooms from the 1930s. Settling of organic material related
to the high primary production in the surface water was causing
oxygen depletion in the bottom water layers. This link between
discharges of nutrients to the fjord, plankton blooms, and oxygen
deficiency was first suggested by Braarud and Ruud (1937), and
further explored by Braarud (1945), Beyer and Føyn (1951) and
NIVA (1968, 1970) and resulted in the building of modern treatment plants. It was not until 1982, that the majority of households
in the inner Oslofjord were connected to wastewater plants. The
new plants removed much of the phosphorus from the discharge
water. In addition, the wastewater was released deeper in the water
column to limit algal production between the deep water renewals.
Nitrogen removal was introduced between 1996 and 2001. Sewage
treatment in inner Oslofjord combined with increased freshwater to intermediate depths has allowed the fjord to slowly recover
(Magnusson et al., 2006), but it will take many years until fully
oxygenated bottom waters are re-established, especially where the
deep water renewal is limited as in Bunnefjord.
3. Materials and methods
Ten cores were collected in inner Oslofjord in February and April
2009 (Fig. 1, Table 2) using the R/V Trygve Braarud. When selecting sites, the following were considered: (1) choose areas with the
highest possible sedimentation rate; (2) avoid heavily trawled (i.e.,
disturbed) areas; (3) choose sites where macrofauna was sampled
in 1993 (Olsgard, 1995) and in 2009 (Norwegian Institute for Water
Research, unpublished); (4) for comparative reasons, choose sites
with similar water depth in the two main basins. One site outside
the inner Oslofjord (core Im4x) was sampled as a reference station.
All ten cores (8 cm diameter, 24–61 cm in length) were sampled using a “Gemini twin barrel corer” (a modified Niemistö
corer, Niemistö, 1974). At each station at least four cores were
collected and the most undisturbed was selected for down-core
study. As soon as possible after collection, the upper 20 cm of the
cores were divided into 1 cm thick slices (i.e., 0–1 cm, 1–2 cm, etc.)
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J.K. Dolven et al. / Ecological Indicators 29 (2013) 219–233
Temperature at 60 m depth in Vestfjorden and Bunnefjorden.
A
9
8
Temperature (°C)
7
6
5
4
3
2
1
Bunnefjorden 60 m depth
Vestfjorden 60 m depth
0
1930 1935 1940 1945 1950 1955 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010
Year
Temperature 90-100 m depth in Vestfjorden and Bunnefjorden.
B
9
8
Temperature (°C)
7
6
5
4
3
2
1
Bunnefjorden 100 m depth
Vestfjorden 90 m depth
0
1930 1935 1940 1945 1950 1955 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010
Year
Fig. 2. (a) Temperatures at 60 m water depth in Bunnefjord (sta. Ep 1) and Vestfjord (sta. Dk 2). Observations mainly from October (or September–December). (b) Temperatures
at 100 m water depth in the Bunnefjord and 90 m depth in the Vestfjord. Observations mainly from October (or September–December). Data from Braarud and Ruud (1937),
Dannevig (1945), Beyer and Føyn (1951), Institute of Marine Research Flødevigen Research Station (1952–1961, unpublished) and Norwegian Institute for Water Research
(1962–2009, unpublished).
and 2 cm thick slices below 20 cm (20–22 cm, 22–24 cm, etc.). All
samples were freeze-dried and the water content calculated.
Seven cores were sent to The Gamma Dating Center in Denmark
and analyzed for 210 Pb-, 226 Ra- and 137 Cs-activity via gamma
spectrometry carried out on a Canberra ultralow-background
Ge-detector. A modified version of CRS-modeling (Appleby,
2001) was applied to most profiles. In some cases the measured age model did not cover the whole profile. A linear
Table 2
Details of the nine sediment cores collected in the inner Oslofjord and the reference station (*) sampled just outside the inner Oslofjord. TOC = total organic carbon; HM = heavy
metals; samp. = number of samples analyzed.
Core name
Latitude
Longitude
Water depth (m)
Collected (dd-mm-yy)
Core length (cm)
Dated
TOC samp.
HM samp.
Ep1
Cp3-1
B18x
EA1
Bo2-1
Fl1-1
Dk2-1
Dm2-1
Cj3-1
Im4x*
59.789551
59.835415
59.858215
59.850536
59.890549
59.750900
59.817249
59.826351
59.844734
59.645035
10.718650
10.706800
10.696383
10.738063
10.665517
10.575084
10.563367
10.616199
10.510067
10.613633
152
101
85
58
55
160
99
85
58
157
23-04-09
23-04-09
20-02-09
23-04-09
23-04-09
19-02-09
23-04-09
20-02-09
23-04-09
18-02-09
61
39
38
33
25
30
37.5
46
24
34
Yes
Yes
Yes
No
Yes
Yes
No
No
Yes
Yes
18
19
19
18
16
18
0
19
16
19
16
19
19
0
16
0
0
0
0
22
Foram samp.
11
9
8
6
6
3
2
6
10
6
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J.K. Dolven et al. / Ecological Indicators 29 (2013) 219–233
223
Fig. 3. Oxygen concentration (ml/l) 1933–2009 (October month). (a) 90 m water depth in Vestfjord (sta. Dk 2), (b) 150 m water depth in Bunnefjord (sta. Ep 1). Data from
Braarud and Ruud (1937), Dannevig (1945), Beyer and Føyn (1951), Institute of Marine Research, Flødevigen Research Station (1951–1960, unpublished), Føyn and Andersen
(1970–71, unpublished) and the Norwegian Institute for Water Research (1962–2009, unpublished).
extrapolation, assuming constant sedimentation rates, was therefore performed to get an indication of ages below the oldest
datum point. As there is much uncertainty connected to such calculations, the extrapolated ages are written in parenthesis and
italics.
Analyses of total organic carbon (TOC) were carried out using a
LECO Carbon Analyzer. Metal analyses were performed using the
HNO3 -method described in Norsk Standard (NS4770, 1994) (for
comments on the use of bioavailable, extractable concentration of
metals rather than the total, see Martínez-Colón et al., 2009; Alve
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J.K. Dolven et al. / Ecological Indicators 29 (2013) 219–233
Table 3
Radiometric dates (*) and sediment accumulation rates for the five successfully dated sediment cores in Oslofjord (details in Dolven and Alve,
2010). Ages without asterisks are calculated by interpolations between datum points. Numbers in parenthesis and italics are calculated by
extrapolation assuming constant sedimentation rates and are hence uncertain.
Depth
(cm)
0
0.5
1.5
2.5
3.5
4.5
5.5
6.5
7.5
8.5
9.5
10.5
11.5
12.5
13.5
14.5
15.5
16.5
17.5
18.5
19.5
21.0
23.0
25.0
27.0
29.0
31.0
33.0
35.0
37.0
39.0
41.0
Ep1
Age
Acc rate
(years) (kg m-2 y-1)
2009
2008
2005
2003
2000*
0.45
1997
1994*
0.39
1992
1989*
0.47
1987
1984*
0.52
1982
1980*
0.44
1978
1976*
0.49
1974
1972*
0.65
1970
1968*
0.52
1965
1961*
0.36
1956*
0.41
1946
1936*
0.39
(1926)
(1916)
(1906)
(1896)
(1886)
(1876)
(1866)
(1856)
Cp3
Bunn 18x
Age
Acc rate
Age
Acc rate
(years) (kg m-2 y-1) (years) (kg m-2 y-1)
2009
2009
2008*
0.5
2008*
0.43
2007*
0.5
2004
2004*
0.4
2000*
0.37
1997*
0.3
1996*
0.32
1986*
0.2
1992*
0.32
1980*
0.4
1986*
0.27
1975*
0.5
1982*
0.43
1971*
0.7
1979
1966*
0.7
1975*
0.55
1959*
0.6
1972*
0.83
1953*
0.6
1969
1.32
1949*
0.8
1967
1944*
0.9
1964*
1.53
1939
1962
1935
1959*
1.42
1930*
0.9
1956
1920
1952*
1.26
1910
1948
1900*
0.5
1943*
1.06
(1890)
1938
(1875)
1935*
1.55
(1855)
1930
(1835)
1925*
2.07
1917
(1815)
(1795)
1908*
1.18
(1775)
1897*
0.92
(1755)
1884
1870*
0.79
(1735)
(1715)
(1857)
(1700)
et al., 2009a). Freeze-dried samples for foraminiferal analyses were
gently homogenized and <2 g of sediment was weighed, washed
through a 63 ␮m sieve, and the largest fraction dried and examined under a binocular microscope. Only hard-shelled, fossilizable
species (sensu Bouchet et al., 2012) were included in this study. If
possible, more than 250 specimens (tests) were picked, mounted
on faunal slides and identified to species. Reworked, shallow-water
species (<10 tests per sample) were subtracted from the dataset
and not included in the calculations. Benthic foraminiferal accumulation rate, BFAR (number of tests/cm2 /year) (Herguera, 1992),
was calculated for all successfully dated cores. All sediment weights
were corrected for salt content due to varying marine pore water
content in the samples. Diversity indexes, i.e., the Shannon–Wiener
index (Hlog
) and the Hurlbert’s index (ES100 ), and cluster anal2
yses were calculated using PRIMER version 6.1.6 (Clarke and
Gorley, 2006). For cluster-analyses the data were transformed using
square root and resemblances calculated using the Bray Curtis
method (Bray and Curtis, 1957). The exponential bias corrected
), was calculated using the statisShannon–Wiener index, exp(Hbc
tical language R version 2.13.2 (http://www.r-project.org/) and the
Entropy package v. 1.1.6 (Hausser and Strimmer, 2011).
Status boundaries for Hlog
and ES100 are the same as
2
those used in the Norwegian classification system based on
), the stamacro-invertebrates (Veileder 01: 2009). For exp(Hbc
tus boundaries defined for complete living (stained) >63 ␮m
foraminiferal assemblages is used because of its highly significant
Cj3
Age
(years)
2009
2008*
2005*
2002*
1999
1995*
1991*
1986*
1981*
1977*
1973
1969*
1965
1961*
1956
1950*
1944
1938*
1932
1926*
1919
1909*
1898*
Acc rate
(kg m-2 y-1)
1.30
1.11
1.01
1.10
1.04
0.87
0.86
1.03
1.20
1.11
0.87
0.84
0.93
0.82
1.09
Im4x
Age
(years)
2009
2008
2007
2006*
2005
2004*
2002
2000*
1999
1997*
1995
1993*
1991
1988*
1985
1982*
1979
1975*
1972
1969*
1965
1962*
1954*
1947*
1940
1933*
1924*
1915*
Acc rate
(kg m-2 y-1)
2.3
2.5
2.6
2.2
2.1
2.0
1.8
1.6
1.4
1.7
1.8
1.3
1.4
1.7
1.4
1.5
correlation with diversity based on fossilizable living assemblages
(Bouchet et al., 2012). Ecological status with class boundaries for all
the abovementioned classification tools are shown in Table 1. In the
present study, following Alve et al. (2009a), sediments deposited
before the mid 1800s are used for characterizing the pre-industrial
background, or “reference conditions” (see also Willis and Birks,
2006).
4. Results
4.1. Chronology and sediment accumulation rates
Five of the seven dated cores (Ep1, Cp3, Bunn18x, Cj3, and Im4x)
showed a reliable chronology (Table 3; for details see Dolven and
Alve, 2010). The sediment record of all five cores date back to
the early 1900s, and two possibly back to the 18th century. The
sediment accumulation rate in the oldest dated parts of the three
Bunnefjord-cores ranges between 0.4 and 0.8 kg/m2 /year with the
higher values at the northern, shallower sites (Cp3 and Bunn18x)
closer to the city of Oslo. All three cores show a maximum accumulation rate during the late 1960s/early 1970s. The sediment
accumulation rate is quite uniform in the Vestfjord core (Cj3),
whereas at the reference site (Im4x), just outside the Drøbak sill,
the highest values occur during the last couple of decades and are
generally 4–5 times higher than in the deep Bunnefjord. Fl1 had a
calculated flux of unsupported 210 Pb about ten times larger than the
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J.K. Dolven et al. / Ecological Indicators 29 (2013) 219–233
Ref. Station
Vestfjord
Bunnefjord
Table 4
Diversity indices for benthic foraminifera in ten sediment cores from Oslofjord, Norway, and for
macrofauna samples collected at some of the same sites in 1993 and 2009. For explanation of
color codes, see Table 1; for further explanation, see text.
Sample
Ep1-1
Ep1-2,5
Ep1-13
Ep1-21
Ep1-25
Ep1-29
Ep1-33
Ep1-35
Ep1-43
Ep1-51
Ep1-60,5
Cp3-0,5
Cp3-2,5
Cp3-5,5
Cp3-8,5
Cp3-12,5
Cp3-15,5
Cp3-19,5
Cp3-31
Cp3-35
EA1-1,5
EA1-3,5
EA1-6,5
EA1-9,5
EA1-17,5
EA1-32,5
B18x-0,5
B18x-1,5
B18x-6.5
B18x-11,5
B18x13,5
B18x-17,5
B18x-23
B18x-37
Bo2-1,5
Bo2-4,5
Bo2-7,5
Bo2-12,5
Bo2-15,5
Bo2-24,5
Cj3-0,5
Cj3-1,5
Cj3-3,5
Cj3-5,5
Cj3-7,5
Cj3-9,5
Cj3-11,5
Cj3-14,5
Cj3-17,5
Cj3-23
Dm2-3,5
Dm2-9,5
Dm2-12,5
Dm2-16,5
Dm2-27
Dm2-45
Dk2-6,5
Dk2-31
Fl1-1,5
Fl1-17,5
Fl1-29
Im4-0,5
Im4-5,5
Im4-13,5
Im4-19,5
Im4-23
Im4-29
Foraminifera
Macrofauna
S
N ES(100)
H'(log2)
Exp H' bc Collected ES(100)
H'(log2)
6 100
6.00
0.84
2.00 2009
0.00
0.00
3
5
0.00
0.00
0.00 1993
0.00
0.00
2
10
0.00
0.00
0.00
5
7
0.00
0.00
0.00
14 216
9.91
2.22
5.12
16 288
12.72
2.66
6.56
20 253
13.18
2.72
7.35
14.58
2.82
7.84
23 295
21.41
3.67
14.06
30 270
33 200
22.77
3.58
14.60
36 227
24.86
4.00
18.84
8.07
1.72
3.58
12 247
11.95
2.08
4.78
18 236
6.90
1.50
3.02
12 338
11.34
2.34
5.52
19 333
21.03
3.60
14.29
35 275
32 273
21.00
3.76
15.27
36 334
21.91
3.86
16.29
26.90
4.17
20.74
43 293
23.39
3.79
16.22
42 324
11.37
2.22
5.01 2009
8.00
1.12
19 352
8.86
2.06
4.34
14 378
14.75
2.69
7.23
23 270
42 372
23.90
3.83
16.13
32 274
20.40
3.53
13.23
22.77
3.98
17.89
31 221
3
16
0.00
0.00
0.00
5
25
0.00
0.00
0.00
8.46
1.12
2.47
15 273
15.11
2.56
7.21
23 264
15.07
2.62
6.66
24 238
15.98
2.75
7.35
25 327
19.16
3.06
9.59
33 322
29 280
19.42
3.20
10.28
24 409
13.08
2.50
6.15 2009
10.58
1.69
12.14
2.28
5.46 1993
18.00
3.43
19 252
16 252
10.09
2.13
4.87
21.07
3.34
11.49
32 274
20.70
3.35
11.27
29 262
18.36
3.24
10.68
27 246
32 287
20.62
3.43
12.15 2009
27.42
4.12
33 315
20.38
3.16
10.10
16.86
2.81
8.05 1993
22.00
4.03
27 278
14.96
2.59
6.83
26 317
12.79
2.49
6.15
20 301
17.97
2.95
8.74
31 339
19.67
3.48
12.45
31 307
19.02
3.46
12.64
36 357
36 279
23.42
4.01
18.20
27.19
4.11
20.50
43 259
7 223
5.81
0.98
2.03 2009
?
0.92
15 291
8.18
1.37
2.90
17 280
9.64
1.33
2.87
12.79
2.31
5.34
20 347
31 276
19.07
2.70
7.65
22.30
3.81
15.83
35 294
38 232
25.59
3.94
18.44 2009
22.16
3.07
22.16
3.96
17.81 1993
21.00
3.52
34 254
23.84
3.87
16.49 2009
13.97
2.28
35 281
26.28
4.26
21.39 1993
21.00
3.52
38 274
30.49
4.43
24.76
47 279
31.23
4.55
26.52 2009
32.39
4.48
45 263
33.37
4.74
30.01
48 280
31.93
4.77
30.87 1993
25.00
4.10
51 325
49 308
31.73
4.67
29.13
41 301
25.36
4.11
19.77
28.52
4.39
23.62
42 280
225
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Zn og Cu
Water content (%)
0
20
40
60
80
0
400
200
600
(ppm)
Forams
Water content (%)
MF
0
800 1000 1200
0
2000
Bunn18x
5
Forams
40
60
80
2
3
4
EA1
1992
5
1982
1972
10
1967
1962
Depth (cm)
20
0
15
1956
20
1938
10
15
1948
1930
20
25
1917
25
30
1897
30
1870
35
40
35
0
1
2
3
4
5
6
1
0
Zn og Cu
Water content (%)
MF
0
20
40
0
3
2
4
60
0
80
200
400
TOC (%)
Forams
(ppm)
600
800
10
0
20
40
0
60
0
200
4
0
1
400
(ppm)
600
Forams
800
0
1997
1980
1971
1978
Depth (cm)
80
2007
Cp3
5
1959
10
1970
20
Zn og Cu
Water content (%)
1000
2008
2000
1994
1989
1984
Ep1
1
0
Cd (ppm)
TOC (%)
1949
1956
1946
1936
15
1930
1910
30
(1900)
40
(1890)
20
25
(1850)
(1800)
30
50
(1800)
35
60
(1700)
0
2
1
3
0
4
1
2
Water content (%)
0
20
60
40
4
5
0
2
1
Zn og Cu
80
0
Forams
(ppm)
100
3
200
Water content (%)
MF
0
300
0
20
40
0
Im4x
10
1995
1977
10
1982
1969
1975
1961
1969
20
Forams
80
1986
1993
15
4
2002
5
1988
Depth (cm)
60
2002
1999
3
2008
Cj3-1
2006
5
2
Cd (ppm)
TOC (%)
Cd (ppm)
TOC (%)
MF
3
1962
1950
15
1938
1947
25
1926
20
1933
30
1909
1898
1915
35
25
0
1
2
TOC (%)
0
0.2
0.4
0.6
Cd (ppm)
0.8
1
0
1
2
3
4
TOC (%)
Fig. 4. Composite diagrams showing down-core distribution of total organic carbon (TOC), metal concentrations (Zn, Cu, Cd (ppm)) and Paleo-Ecological Quality Status
(PaleoEcoQS) based on fossil assemblages of benthic foraminifera (right hand arrows) in the five successfully dated and one undated sediment cores from Oslofjord. Additional
information includes EcoQS based on macrofauna (MF) collected in 1993 and 2009 (left hand arrows) (for explanation of color codes, see Table 1). (For interpretation of the
references to color in this figure, the reader is referred to the web version of the article.)
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J.K. Dolven et al. / Ecological Indicators 29 (2013) 219–233
227
“Poor” status. Core Bunn18x reveals the same transition, but later,
reaching “Poor” conditions in the early 1980s. Cores Cp3 and EA1
show similar patterns but both reveal an improvement in the upper
parts. In core Cj3 from the Vestfjord, the conditions change from
“High” to “Good” in the early 1900s, to “Moderate” in the 1960s and
back to “Good” conditions the last decade. The temporal development in the 85-m water depth core from Vestfjord (Dm2) changes
from “Good” to “Poor” status whereas the core located close to the
Nesodden-Bygdøy sill (Bo2) changes from “Good” to “Moderate”.
Neither of them show improvements in the uppermost recent part.
The reference core (Im4x) just outside the inner Oslofjord yields
) shows the same temporal pat“High” status throughout. Exp(Hbc
tern but the status is commonly one class lower compared to the
other two indices.
4.3. Similarity between foraminiferal assemblages
Fig. 5. Map of inner Oslofjord with sampling sites. Small circles = present-day ecological status; Large circles = “reference” conditions. For color codes, see Table 1.
Ecological status is based on ES100 and H . Dashed lines indicate the positions of the
main sills. Data from Bærum basin based on Alve et al. (2009b). (For interpretation
of the references to color in this figure, the reader is referred to the web version of
the article.)
estimated local atmospheric supply indicating intense sediment
focusing, whereas the profiles of unsupported 210 Pb and 137 Cs in
Bo2 indicate sediment mixing (Dolven and Alve, 2010). Hence, the
dating of the two latter cores is regarded as indicative only.
4.2. Foraminiferal diversity and EcoQS
As the main purpose of the present study is to test the application of conventional ecological classification systems on fossil
foraminiferal data to define PaleoEcoQS, rather than reconstructing the detailed development at each site, analyzing more cores
is prioritized at the expense of the number of samples per core.
Complete foraminiferal analyses, identifying >180 taxa, was performed on 67 samples from ten cores (census data available in
Dolven and Alve, 2010). The ES100 - and Hlog
-data give very similar
2
ecological status (Table 4). In cases where the indices do not give
the same status, the average is chosen after normalization of the
index values (Figs. 4–6) following Norwegian guidelines (Veileder
01:2009). All studied cores show “Good” or “High” EcoQS in the
deepest sample, corresponding to early 1900s or earlier. The four
Bunnefjord cores reveal a gradual change toward lower diversity
corresponding to “Moderate” or “Poor” ecological status when passing the mid-1900s. In Ep1, the core from the deepest and innermost
Bunnefjord station, “Poor” status is reached in the mid 1930s, it
developed into “Bad” by the mid 1950s and remains “Bad” until
present. The uppermost sample shows signs of improvement with
a diversity value lying close to the boundary between “Bad” and
Five samples were excluded from the cluster analysis due to
very low abundance (<30 specimens per sample). Except for an
outlier represented by the surface sample in core Ep1, which was
strongly dominated (85%) by Stainforthia fusiformis, the cluster
analysis defined three groups of assemblages (Fig. 7). The three
groups represent (1) the most recent–subrecent assemblages in
the Bunnefjord and north of Dk2 in Vestfjord, all with >40% (max
84%) S. fusiformis, abundant (>10%) Bulimina marginata, and in some
cases Bolivinellina pseudopunctata and Elphidium albiumbilicatum,
(2) the oldest parts of these cores plus Dk2 with abundant Adercotryma glomeratum/wrighti, Nonionella iridea, Cassidulina laevigata,
and Nonionellina labradorica, and (3) all assemblages in the reference core outside the sill (Im4x) plus the youngest and oldest
assemblage in the 160-m Vestfjord core (Fl1) with common (>5%)
Brizalina skagerrakensis, C. laevigata, S. fusiformis, N. iridea, A. glomeratum/wrighti, Pullenia osloensis, and Hyalinea balthica.
4.4. Benthic foraminiferal accumulation rate
Accumulation rates of foraminiferal tests have been calculated
for cores with the most reliable chronologies (Fig. 8). The general
trend is an increase from <30 to about 150 tests/cm2 /year during the late 1800s until the 1970s. From this time it continues to
increase to about 200 and 300 in the Vestfjord and at the reference
station, respectively, whereas a decrease to <50 is recorded in Bunnefjord. At the deep 152 m-site in Bunnefjord (Ep1) the maximum
accumulation rate occurs at the end of the 1800s. It approaches zero
around 1950 and stays low until a slight increase occurs at the time
of sampling (2009).
4.5. Total organic carbon and heavy metal concentrations
Total organic carbon (TOC) was analyzed in nine of the ten cores.
The lowermost samples in all cores show TOC < 1.9% (Fig. 4, Dolven
and Alve, 2010). Values <2% correspond to “High” EcoQS (Table 1).
An increase in TOC-values is seen around 1930 in the dated cores.
This is particularly evident in the three deepest and most undisturbed Bunnefjord cores (i.e., Ep1, Cp3 and Bunn18x) which show
maximum TOC-values of 4.6–6.0% between 1970 and 1980 corresponding to “Bad” EcoQS. Vestfjord TOC-maxima are slightly lower
(3.5–5.5%) corresponding to “Poor” to “Bad” EcoQS, whereas the
reference core Im4x shows a maximum TOC of 2.7%, i.e., “Moderate” to “Good”. All cores (except EA1 and Bo2) show a gradual
decrease in TOC-content after the maximum peak. This decrease
is best depicted in the Bunnefjord cores, where TOC decreases to
about 3% in the core top, corresponding to “Moderate” EcoQS.
The concentrations of acid soluble Cu, Cd and Zn were analyzed in five cores; Ep1, Cp3, Bunn18x from the Bunnefjord, Bo2
from the Vestfjord, and in the reference core Im4x (Fig. 4). As with
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ES100
0
5
10
15
H’log2
20
25
30
35
1
2
Exp H’bc
3
4
5 0
5
10
15
20
25
30
35
2010
1960
1910
1900
1860
1810
1760
1710
1800
Cj3 Vestfjord
Cp3
Ep1
Bunnefjord
Bunn18x
Im4x Ref. station
1700
Fig. 6. ES100 , Hlog
and exp(Hbc
) values plotted against age in the five successfully dated sediment cores from Oslofjord, Norway. For explanation of color codes along the
2
lower x-axes, see Table 1. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
the TOC, the lowest concentrations of heavy metals are found in
the lowermost part of the analyzed cores, i.e., 160–190 ppm Zn,
0.6–0.8 ppm Cd, and 23–28 ppm Cu. These correspond to “Good”
EcoQS for Zn and Cd and “High” for Cu (Table 1). The concentrations
in the Bunnefjord cores increase in sediments deposited during the
1950s and 1960s and show maxima for Zn (1135 ppm), Cd (4.4 ppm)
and Cu (300 ppm) in the 1970s/1980s, almost synchronously with
the TOC-peaks. Depending on element, the peak-values correspond
to “Moderate” to “Bad” EcoQS. Subsequently, all concentrations
decrease and, in most cases, the surface sediments (i.e., post 2005)
reach “Good” EcoQS. Core Bo2 also shows increased concentrations
up core but for Zn and Cd EcoQS remains “Good” throughout the
profile. For Cu, however, the concentration increases from 25 ppm
in the lowermost sample to a maximum of 157 ppm in the 1970s
corresponding to a change from “High” to “Poor” status. The lack
of a clear maximum in the metal concentrations reflects some disturbance in the chronology, as indicated by the unreliable dating
results. The heavy metal concentrations in the reference core Im4x
reflect “Good” to “High” EcoQS with maximum concentrations during the 1960s and 1970s.
5. Discussion
5.1. Chronological framework
The maximum metal concentrations around 1970/1980 agree
with Cu-results from cores collected closer to Oslo harbor (Lepland
et al., 2010). Minor discrepancies may be attributed to local disturbance of the sediments, different distance to the source (Oslo
city) and thickness of the analyzed sediment slices (time-average
effect). However, the overall picture illustrates the usefulness of
Cu and Cd as chronostratigraphic markers in the inner Oslofjord
as suggested by Lepland et al. (2010) and the present study shows
that the same applies for Zn and TOC (Fig. 4). This information can
be used to correlate, and thereby indirectly date, similar levels in
radiometrically undated cores from other parts of the basin. The
fact that comparable down-core metal distribution profiles occur
in cores with oxic and in cores with anoxic surface sediments makes
it unlikely that the subsurface metal-maxima are significantly
influenced by diagenetic remobilization (cf. Lepland et al., 2010).
The present results with lower sediment accumulation rates in Bunnefjord, both in time and space, with increasing distance from Oslo
harbor during the middle part of the last century and a clear reduction during the last 40–50 years, also support the conclusion that a
recent decrease in accumulation may be linked to improved waste
handling (Lepland et al., 2010).
5.2. Bunnefjord
According to the foraminiferal data, the deepest parts of Bunnefjord (Ep1) were characterized by “Good” EcoQS during the last
half of the 1700s and first half of the 1800s, and the status at 100 m
water depth (Cp3) was even better (Figs. 4 and 6). Unfortunately,
there is no historical information about the environmental conditions from these early times with which to test these results.
However, for the last half of the 1800s when the foraminiferal
record reflects deterioration from “Good” to “Moderate” EcoQS,
some comparative information is available. Sars (1879) concluded
that a bottom fauna of arctic origin recorded in Bunnefjord represented “surviving remnants of the fauna that once existed there”
and that low temperature probably was responsible for their survival. Similar observations were reported for 1897 and 1899 (Hjort,
1900) and prawns were caught during the 1890s. Furthermore,
brown clay (i.e., oxic conditions) and large quantities of rotting terrestrial vegetation were present in Hjort’s bottom trawl at 150 m
depth in 1897. These observations indicate acceptable oxygen conditions for benthic fauna. However, in connection with the first
hydrographical investigations performed in inner Oslofjord, critical bottom water [O2 ] of 0.79 ml/l was recorded at 160 m depth in
Bunnefjord in April 1899 (Hjort and Gran, 1900), hence supporting
the deteriorating trend shown by the foraminiferal data.
From the late 1800s to late 1900s, the population in Oslo grew
from about 100,000 to >500,000, and the introduction of WC had
increased the transport of waste-water to the fjord (Baalsrud and
Magnusson, 2002). Limited deep water renewals made Bunnefjord
vulnerable to increased organic load and caused the increase in
organic matter-supply (Fig. 8) to affect the benthos differently
in different parts of the basin. In the deeper parts (Ep1), the
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J.K. Dolven et al. / Ecological Indicators 29 (2013) 219–233
229
Fig. 7. (upper) Cluster analysis of benthic foraminifera in sediment cores from Oslofjord. For explanation of cluster groups 1–3, see text, (lower) diagram showing rough
temporal changes in benthic foraminiferal assemblages in sediment cores as defined by cluster analysis. The stations (cores), with water depth indicated, are arranged along a
transect from the outermost (seaward) part of the investigated area (left) to the innermost part (right), see map, Fig. 1. Pinkish colors reflect “low oxygen-tolerant” Stainforthia
fusiformis-dominated assemblages. *Cores with uncertain ages. (For interpretation of the references to color in this figure, the reader is referred to the web version of the
article.)
ecological quality status (EcoQS) had turned “Poor” by 1936 and
“Bad” by 1956 (Fig. 4) indicating a transition to dominantly anoxic
conditions. This fits well with the first comprehensive record of
H2 S in the deep water in 1950 (Beyer and Føyn, 1951) and with
a transition from gray to black sediments at 6 cm depth in an
undated core collected at 150 m in 1962 (Risdal, 1963). The culmination of nutrient- and organic matter-supply during the 1960s
and 1970s (Baalsrud and Magnusson, 2002) is reflected by TOCmaxima in the dated Bunnefjord cores (Fig. 4) and corresponds with
eutrophication signals from retrospective lipid studies (PinturierGeiss et al., 2002). At the shallower 85-m (Bunn18x) and 100-m
(Cp3) stations deterioration to “Moderate” status occurred later, in
the 1940s and around 1960, respectively. The accompanying faunal
response included a change from Cassidulina laevigata/Adercotryma
wrighti/Nonionella iridea-assemblages via assemblages with more
common B. marginata and E. albiumbilicatum to a more
anoxia-tolerant, opportunistic S. fusiformis assemblage and the
benthic foraminiferal production increased (Fig. 8). These faunal changes characterize environments undergoing eutrophication
and gradually developing oxygen deficiency on the sea floor (discussion in Alve et al., 2009a). The core from 58 m water depth (EA1)
was not dated but shows the same general pattern in faunal change
as the others, probably with a slight time delay as “Moderate” status
only occurs in the upper 6 cm of the core (Fig. 4). This time-delay
at the shallower site reflects the temporal change in [O2 ] (Fig. 3).
Some benthic foraminifera can survive a few weeks of anoxia
using nitrate respiration (Risgaard-Petersen et al., 2006) but they
cannot survive anoxia for extended periods of time (Alve, 1995b).
Consequently, the near lack of foraminiferal tests in sediments
deposited in the deepest basin after the 1940s, indicates predominantly anoxic conditions (Fig. 8). The fact that the assemblages
prior to the anoxic period do not seem to have developed as high
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2000
1975
1950
1925
1900
Year
1900
1875
1850
1825
Cj3 Vestfjord
Cp3
1800
Ep1
Bunn18x
1775
1750
1800
Bunnefjord
Im4x Ref. station
0
50
100
150
200
250
0
300
Foram accumulation rate (no./cm2/yr)
1
2
3
4
5
6
7
TOC (%)
Fig. 8. Benthic foraminiferal accumulation rates (BFAR) and total organic carbon (TOC) in the five successfully dated sediment cores from Oslofjord, Norway.
abundance populations as those developed at shallower sites at a
later stage (see also Risdal, 1963), indicates that the change to predominantly anoxic conditions happened when relatively moderate
amounts of organic material were added to the deep basin floor. In
other words, the deep basin was more vulnerable to organic input
(i.e., increased oxygen consumption and limited water renewal)
than the shallower areas. This is supported by the fact that, as
opposed to the development in the deep basin, maximum production of foraminiferal tests occurred at the two shallower 100 m and
85 m stations during the eutrophication period (1960–1970s), i.e.,
prior to their faunal collapse.
The few foraminiferal tests deposited in the deep basin during the predominantly anoxic period may either represent short
re-colonization events if the bottom water conditions became
re-oxygenated for some months or a year (Alve, 1995b) or they
may have been re-deposited, i.e., transported into the basin from
shallower areas in connection with e.g., deep-water renewals. Possible positive effects of deep-water renewals during the 1960s
were indicated by Skei (personal communication in Baalsrud and
Magnusson, 2002). The facts that the bottom sediments at the
85 m-station (Bunn18x) started deteriorating some 20 years earlier
than those at the deeper 100 m-station (Cp3) and that the former
developed a more extremely S. fusiformis-dominated, low diversity
assemblage than the latter, indicates local environmental differences. This illustrates the importance of obtaining in situ temporal
records.
5.3. Vestfjord
The oldest record of bottom-water oxygen concentrations in
Vestfjord, 5.8 ml/l from April 1899 (Hjort and Gran, 1900), is in
accordance with the foraminiferal data suggesting “reference” conditions of either “High” or “Good” status (Table 4). Gradually
deteriorating EcoQS is seen both in the foraminiferal and TOC
records of the 85 m (Dm2) and 58 m (Cj3) cores probably reflecting
accelerating eutrophication with the most impacted assemblages
occurring from the 1970s to 1990s during which time the dissolved
[O2 ] also was at its minimum (Fig. 3). This parallels the fact that
the catching of prawns, which has been recorded since the early
1950s, failed completely between 1970 and 1986 after which time
it has continuously improved (Baalsrud and Magnusson, 2002). As
in Bunnefjord, the deterioration was accompanied by increased
foraminiferal production (Fig. 8), particularly represented by S.
fusiformis and B. marginata. However, except at the 85-m station
(Dm2), where “Bad” EcoQS had developed in a semi-enclosed subbasin (Fig. 1, Table 4), the EcoQS in Vestfjord never declined as much
as in Bunnefjord. The fact that Vestfjord has been less affected than
Bunnefjord is probably because it is (1) closer to the outer Oslofjord
where the water is renewed more often and (2) situated SW of the
Nesoddtangen-Bygdøy sill further away from the main pollution
source, the city of Oslo. Exceptions include sub-basins such as the
85 m-station (Dm2), which is not representative for the Vestfjord,
and the Bærum basin (Fig. 5) where the deepest part (i.e., >25 m
water depth) has been naturally anoxic since the 1700s (Alve et al.,
2009b). Again, this demonstrates the importance of doing in situ
investigations to determine local EcoQS both past and present.
5.4. Temporal patterns in EcoQS
One of the main advantages of using foraminifera in environmental monitoring is that it allows reconstructions of EcoQS to
times before conventional monitoring started (Alve et al., 2009a).
In other words, depending on the time covered by the deposits
in the sedimentary basin in focus, the method makes it possible to define in situ PaleoEcoQS as far back in time as needed
and, thereby, show possible temporal changes in status. This is
particularly important in complex systems like estuaries “where
a multiplicity of changing environmental parameters causes
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J.K. Dolven et al. / Ecological Indicators 29 (2013) 219–233
natural changes in the faunal composition over small geographic
areas” (Alve, 1995a). Many silled fjords have an estuarine circulation pattern and the deep-water at the landward side of the
sill(s) may be oxygen depleted or even anoxic for natural reasons
(Syvitski et al., 1987). In such cases, oxygen depletion represents
the reference conditions. This fact represents a challenge for the
authorities when classifying water bodies – is the fjord in focus
oxygen depleted for natural reasons or is the depletion due to
anthropogenic forcing? If the latter is the case, has human impact
affected the whole water column or only parts of it, e.g., the deepest
parts, and to what extent?
In the present study, the EcoQS defined by the foraminifera
is similar to EcoQS defined by soft-bottom macrofauna collected
in 1993 and 2009 (data from Olsgard, 1995; NIVA, unpublished;
Krajczyk, 2011) at eight stations where data from both groups
are available (Fig. 4). This integrates the foraminifera-based retrospective bio-monitoring method with conventional bio-monitoring
and strengthens its applicability. The present study also illustrates
that even if different diversity values do not reflect exactly the
same EcoQS, the temporal pattern revealed by the indices is the
same (Fig. 6). Examples include the Vestfjord core (Cj3) which
shows a declining status from the reference conditions to the 1980s
followed by an improvement during recent decades, the deep Bunnefjord core (Ep1) with a dramatic decline from background to
“Bad” conditions from about the 1940s onwards, and the reference
core (Im4x) with “High” status throughout the time interval covered, i.e., since the early 1900s. For all cores, the same temporal
pattern emerges irrespective of diversity index used. This suggests
that for fossil benthic foraminifera, the temporal pattern and scale
of change in an index within a core (i.e., at the same site) is more
important than which index is being used. However, in order to
reach the most sound conclusion, it is still advisable to use and
compare the development in several independent indices.
The main challenges for the international scientific communities
dealing with ecological quality criteria include inter-calibration of
biotic indices and agreeing on stations that are most suited to serve
as references sites for impacted stations (e.g., Borja et al., 2007,
2010; Gamito, 2008). The method presented here is not limited by
these challenges. It shows directly if, when, and to what extent,
EcoQS has changed at the investigated sites irrespective of index
used and irrespective of former knowledge about the local environmental conditions (Fig. 5).
5.5. Climate change or anthropogenic forcing?
Shifts in the North Atlantic Oscillation (NAO) system have been
suggested as a cause for changes in the benthic foraminiferal
assemblages in the Gullmar Fjord, Sweden (Nordberg et al., 2000;
Filipsson and Nordberg, 2004). In the Skagerrak region positive
NAO-indices are generally accompanied by westerly winds, preventing the exchange of bottom-water in the fjords, increasing
oxygen depletion in the bottom waters, and thereby favoring lowoxygen-tolerant species like S. fusiformis (Nordberg et al., 2000). In
the Gullmar Fjord, such a faunal change took place in the 1970s
together with a switch to a positive NAO-mode (Nordberg et al.,
2000; Filipsson and Nordberg, 2004). Later investigations in the
same fjord (Polovodova et al., 2011), however, did not find similar
correlations (i.e., change to a “low-oxygen-tolerant fauna”) related
to the Medieval Warm Period (MWP; about 1000–1350 AD), even
though a positive NAO is believed to be the driving force of this
warm period as well (Trouet et al., 2009).
Erlandsson et al. (2006) found that physical factors (like NOAshifts) could explain a part (40%) of the decreased oxygen minimum
concentrations since 1950 in the Gullmar Fjord, related to the timing of renewal of basin water. The main factor (60%) was connected
to the increased oxygen consumption, suggesting an import from
231
Skagerrak and a long-term increase in organic production there.
Thus climatic “effects” in the Gullmar Fjord cannot be ignored
when analyzing variations in oxygen concentrations over longer
periods.
In the inner Oslofjord we see changes toward a similar “lowoxygen-tolerant” assemblage as in Gullmar Fjord, but here the
timing of the changes is diachronous. The cluster analysis shows
that a uniform benthic foraminiferal assemblage occupied all the
investigated sites inside the Drøbak sill during the last part of
the 1800s and beginning of the 1900s (Group 2, Fig. 7). This
“reference” assemblage was then successively replaced by a S.
fusiformis-dominated “low-oxygen-tolerant” assemblage (Group
1). The replacement started in the deepest part of Bunnefjord in
the late 1800s/early 1900s and expanded to shallower depths.
However, the expansion does not seem to have followed a simple pattern from deeper to shallower water depths but was rather
controlled by local bathymetry/water circulation (e.g., compare the
development at the Cj3-site and that in the semi-enclosed Dm2
sub-basin, Table 4). From the 1940s the diversity clearly differs
between the Bunnefjord, the Vestfjord and the reference station
Im4x (Fig. 6), and the trend at the two former is deteriorating during
the next three to four decades. Comparing e.g., the deepest station
in the Bunnefjord (Ep1) and the reference station outside the inner
fjord (Im4x), both collected at about the same water depth (i.e.,
152 and 157 m), their EcoQS differ by about 4 classes in the 1960s
(Fig. 6) even though their starting point was almost the same at the
beginning of their records.
In the inner Oslofjord physical and chemical parameters have
been monitored since the mid 1930s. While the foraminiferal
record shows the largest faunal changes between the 1930s and
1980s, the temperature was quite stable until the late 1980s and
the temperature values co-vary at the same depths in the two
basins (Fig. 2). On the other hand, the oxygen concentration differs
dramatically between the two basins (Fig. 3). The Bunnefjord experiences oxygen depletion from the 1940s, especially in the deepest
parts of the fjord, probably due to increased organic production
in the surface waters and limited deep-water water exchange. A
much less dramatic development is seen in the Vestfjord. Consequently, the present data indicate that the changes seen in the
foraminiferal assemblages between 1930 and 1980 are a result
of anthropogenic forcing and not of temperature changes. This
is supported by the hydrographic time series (Figs. 2 and 3) and
the increasing TOC-values, reaching maxima at the same time as
the diversity in the fjord reaches its minimum values in the late
1970s/early 1980s. Since the early 1980s the discharge of phosphorus and nitrogen to the inner Oslofjord has been substantially
reduced, causing decreasing algal blooms and thereby reduced flux
of organic material to the sea-floor. There is a weak trend indicating
higher diversities after the mid 1980s.
6. Conclusions
Paleoecological analyses of benthic foraminifera and geochemical parameters in dated sediment cores from Oslofjord, Norway,
have been performed in order to test the application of conventional ecological classification systems on fossil foraminiferal data.
The overall conclusions are as follows:
• Conventional ecological classification systems developed for
macrofauna can be applied on fossil assemblages of benthic
foraminifera to define in situ paleoecological quality status (PaleoEcoQS).
• Comparisons of the results with historical macrofauna data and
hydrographical time-series illustrate that the fossil assemblages
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J.K. Dolven et al. / Ecological Indicators 29 (2013) 219–233
reflect the temporal development in EcoQS from reference- to
present-day conditions.
• Although the use of several indices as metrics to characterize
EcoQS is advisable, for fossil benthic foraminifera, the temporal
pattern and scale of change in one index within a core (i.e., at the
same site) is more important for defining possible deviation from
reference conditions than which index is being used.
• In Oslofjord, EcoQS started declining in the deeper, inner parts
during the late 1800s. During the 1900s, the negative trend in
EcoQS developed diachronously to shallower depths and other
parts of the fjord, depending on local conditions, and the assemblage composition changed accordingly. The declining EcoQS
followed the development of bottom-water oxygen-deficiency
during decades of stable bottom-water temperatures.
The present study illustrates the efficiency of the foraminiferal
method and its ability to define temporal in situ changes in EcoQS
over centuries. The method should be applicable in other sediment accumulation basins and, as it can provide information about
reference conditions in areas where no historical information is
available, it should be of particular importance for the implementation of the WFD.
Acknowledgements
We would like to thank Jonas H. Enoksen, Aina Marie Nordskog,
and Mufak Naoroz for performing the metal- and TOC analyses. We
are grateful for the assistance from Silvia Hess, Vincent Bouchet and
the captain Sindre Holm and his crew during the R/V Trygve Braarud
cruises in 2009. We would also like to thank Thorbjørn J. Andersen,
University of Copenhagen, Denmark, for dating the cores, Aivo Lepland, the Geological Survey of Norway, whom so kindly provided
the Oslofjord map in Fig. 1, Hans Skjerpen for help with the Rprogram, and John Murray for useful comments on the manuscript.
The project was funded by “Fagrådet for vann og avløpsteknisk
samarbeid i indre Oslofjord”, “Fylkesmannen i Oslo og Akershus”,
the Climate and Pollution Agency, the University of Oslo, and by the
Norwegian Research Council project PES (No. 184870).
Appendix A. Faunal reference list
Generic classification follows Loeblich and Tappan (1987).
The original descriptions can be found in the Ellis and Messina
world catalog of foraminiferal species on www.micropress.org. The
species are listed alphabetically.
Adercotryma glomeratum (Brady) = Lituola glomerata Brady, 1878.
Adercotryma wrighti Brönnimann and Whittaker, 1987. In the
present study, due to high degree of morphological similarity, particularly in smaller individuals, this form has been grouped with
A. glomeratum.
Bolivinellina pseudopunctata (Höglund) = Bolivina pseudopunctata
Höglund, 1947.
Bulimina marginata d’Orbigny, 1826.
Cassidulina laevigata d’Orbigny, 1826.
Elphidium albiumbilicatum (Weiss) = Nonion pauciloculum Cushman, subsp. albiumbilicatum Weiss, 1854.
Hyalinea balthica (Schröter) = Nautilus balthicus Schröter, 1783.
Nonionella iridea Heron-Allen and Earland, 1932.
Pullenia osloensis Feyling-Hanssen, 1954.
Stainforthia fusiformis (Williamson) = Bulimina pupoides d’Orbigny
var. fusiformis Williamson, 1858.
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