Estuarine, Coastal and Shelf Science 57 (2003) 501–514
A common opportunistic foraminiferal species as an indicator
of rapidly changing conditions in a range of environments
Elisabeth Alve
Department of Geology, University of Oslo, P.O. Box 1047, Blindern, N-0316 Oslo, Norway
Received 21 June 2002; received in revised form 3 October 2002; accepted 10 October 2002
Abstract
Long-term biological and environmental time-series (several decades to centuries) are essential for distinguishing between
anthropogenically and naturally induced environmental change as well as for monitoring environmental change over time,
irrespective of the causes. Since such long time-series are virtually non-existent for most areas, other methods have to be explored
which can provide the best possible analogues. Numerous investigations have shown that benthic foraminifera (meiofaunal protists),
which leave a fossil record in most marine sediments, are well suited for this purpose. A prerequisite for performing sound
interpretations is an optimal understanding of their biology and ecology.
Stainforthia fusiformis (Williamson) is one of the most common benthic foraminiferal species in NW European waters and living
(stained) populations have been recorded in all clastic, soft bottom intertidal to outer shelf and slope areas with sediments consisting
of at least some fines (>4% <63 lm) as long as the salinity is >28. Its predominance in ephemerally dysoxic/anoxic areas has caused
it to be used as a proxy for severe oxygen depletion. A strong dominance (even >90%) of this species is, however, also reported from
well-oxygenated coastal and shelf settings and, consequently, high abundance of this species occurs in habitats with very different
environmental characteristics. A closer examination of these areas suggests that they can be roughly grouped into three categories:
(1) beneath hydrographic frontal areas, (2) physically disturbed areas of sediment, and (3) ephemerally dysoxic/anoxic basins. The
main characteristic feature that these highly different environments have in common is that they experience rapidly changing
conditions. It is concluded that the opportunistic life-strategy of S. fusiformis makes it highly adapted to cope with environmental
stress and that this, rather than tolerance to a particular environmental parameter, causes it to predominate in areas subject to
rapidly changing environmental conditions.
Ó 2003 Elsevier Science B.V. All rights reserved.
Keywords: hydrographic fronts; physical disturbance; ephemeral dysoxia/anoxia; trawling; Stainforthia fusiformis (Williamson); environmental change
1. Introduction
The number of studies focusing on biological and
environmental change in NW European waters has increased substantially over the past few decades. There is
now a voluminous amount of literature indicating that
human impact plays a central role in modifying these
marine ecosystems on local and sometimes regional
scales (e.g. Austen, Buchanan, Hunt, & Kendall, 1991;
Josefson, 1990; Kröncke & Knust, 1995; Lindeboom,
1995; Riegman, 1995). Most studies focus on human
E-mail address: ealve@geologi.uio.no
induced eutrophication but increases in riverine nutrient delivery is only well-documented for the last 30 or
40 years and biological time-series documenting benthic faunal variability before the 1970s are rare for most
areas. There is some evidence that, in some places such as
the Southern Bight of the North Sea, algal proliferation
as intense as observed at present was already occurring
at the end of the 19th century (Billen, Garnier, Deligne,
& Billen, 1999). On the other hand, some authors have
concluded that factors other than nutrient enrichment,
e.g. long-term climatic variations, are primarily responsible for the observed trends in environmental change
(e.g. Nordberg, Filipsson, Gustafsson, Harland, & Roos,
2001; Nordberg, Gustafsson, & Krantz, 2000; Owens,
0272-7714/03/$ - see front matter Ó 2003 Elsevier Science B.V. All rights reserved.
doi:10.1016/S0272-7714(02)00383-9
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E. Alve / Estuarine, Coastal and Shelf Science 57 (2003) 501–514
Cook, Calebrook, & Hunt, 1989; Tunberg & Nelson,
1998). Either way, since for most areas long-term
biological time-series back to (presumed) pre-impacted
times hardly exist, the only way to obtain information
about long-term environmental and biological changes
is through palaeoecological interpretations of the fossil
record. The fossilizable remains of benthic foraminifera
(meiofaunal protists) have been shown to provide successfully such information in, for example, Scandinavian waters (e.g. Alve, 1991, 1996, 2000; Christiansen,
Kunzendorf, Laima, & Pedersen, 1996; Moodley,
Troelstra, & Van Weering, 1993; Nordberg et al., 2000;
Seidenkrantz, 1993). The usefulness of this method,
however, requires: (1) that the area under study has a
reasonably high sediment accumulation rate (preferably
more than about 1–2 mm yr1 to provide high resolution
data sets); (2) that the sediments are not too physically
disturbed (e.g. by bioturbation) as this will blur the
stratigraphy; (3) that transport of tests in and out of the
area is low; and (4) that the assemblages are well preserved. Additionally, a thorough understanding of the
biology and ecology of the organisms is essential.
One of the most common benthic foraminiferal
species in NW European marine waters is Stainforthia
fusiformis (Williamson). It was first described by Williamson
(1858) from samples collected around the British Isles,
has since been recorded in a range of environments
from intertidal to bathyal depths (Gooday & Alve, 2001)
and is widely distributed on the continental selves and
upper slopes around the North Atlantic Ocean. It is, however, much more abundant on the European than on
the American side (e.g. it is only a minor constituent of
the assemblages in eastern Canadian estuaries, Scott,
Schafer, & Medioli, 1980). S. fusiformis changes aperture
characteristics during growth (Fig. 1) and both kinds of
apertures occur in European as well as in eastern North
American waters (documented specimens with terminal
aperture off NE America are reported in e.g. Schnitker,
1971; Williamson, Keen, & Mudie, 1984). On the other
hand, in Pacific Canadian fjords, populations remarkably similar to the Atlantic ones, show no individuals with
terminal aperture—they only possess apertures similar
to those of the younger Atlantic growth stages
(Patterson, Guilbault, & Thomson, 2000). Because of
this, the name Stainforthia feylingi (Knudsen & Seidenkrantz, 1994) is used in Pacific Canada. Both forms
dominate the same kinds of dysoxic/anoxic fjordic
environments (e.g. Alve, 1995, 1999b; Blais-Stevens &
Patterson, 1998; Gustafsson & Nordberg, 2000, 2001;
Patterson et al., 2000) and hence, there is a growing
tendency to use them as proxies for dysoxic–anoxic
environments. Oxygen depletion cannot, however, be the
only factor controlling its abundance because several
studies have also shown high abundance of this species
(in both relative and absolute terms) in well-oxygenated
and highly different environmental settings. Because
Fig. 1. A specimen of Stainforthia fusiformis from Oslofjord, Norway,
broken open to show the changing apertural features during growth.
Scale bar ¼ 100 lm.
S. fusiformis (and the closely related S. feylingi) is so
common in many shelf and marginal marine environments and it represents one of the key species on which
several retrospective environmental studies are (and
probably will be) based (including Quaternary deposits,
e.g. Lagoe, Davies, Austin, & Olson, 1997; Scott, Mudie,
Vilks, & Younger, 1984), the primary aim of this paper is
to shed some light on the environmental conditions
which control its distribution. This knowledge is a
prerequisite for performing sound palaeoecological
interpretations where this species is or has been common.
2. The biology and ecology of S. fusiformis
S. fusiformis (referred to as Fursenkoina fusiformis by
some authors) is a small (length generally <250 lm),
elongate, thin-shelled, rotaliid, benthic foraminifera (for
details, see Gooday & Alve, 2001; Höglund, 1947).
Although its life cycle is still not known, there are lines
of evidence suggesting that reproduction in S. fusiformis
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E. Alve / Estuarine, Coastal and Shelf Science 57 (2003) 501–514
may be entirely asexual or that its life cycle is metagenic
(i.e. with sexual and asexual generations) but without
any significant test dimorphism (Gooday & Alve, 2001).
It probably reproduces throughout the year (Murray,
1992) and its life-history strategy seems to be highly
opportunistic (Alve, 1994). S. fusiformis is recorded from
intertidal habitats (Alve & Murray, 2001) to the bathyal
zone (at least 2200 m, Austin & Evans, 2000) in the
Arctic and North Atlantic Oceans (Gooday & Alve, 2001).
It is common in shelf areas off NW Europe (Table 1), in
parts of the Mediterranean Sea (e.g. Barmawidjaja,
Jorissen, Puskaric, & Van der Zwaan, 1992), along
the Atlantic seaboard of North America, and off NW
Africa (Murray, 1991). It seems to be ubiquitous in NW
European marine waters where it may dominate the
living (stained) foraminiferal assemblages in most types
of subtidal clastic sediments, from sands with only 4%
fines <63 lm (Murray, 1985) to muddy sediments with
>98% fines <63 lm (Alve, 1991, 1995) where the bottom
temperature ranges between 5 C (off Northumberland,
UK, Collison, 1980) and 16 C (Lyme Bay, UK, Murray,
1986) and with salinities >28 for most of the year
(Havstensfjord, W Sweden, Gustafsson & Nordberg,
2000). It is not reported from the Baltic, probably due to
reduced salinities. S. fusiformis is essentially an infaunal
species (i.e. it lives within the sediment). However,
whereas its maximum occurrence is commonly recorded
in the surface 0–1 cm (e.g. southern North Sea, Moodley,
1990; northern Adriatic, Barmawidjaja et al., 1992;
Havstensfjord, Sweden, Gustafsson & Nordberg, 2000)
or in the surface 0–2 cm (e.g. Skagerrak fjords, eastern
North Sea, Alve & Bernhard, 1995; Gustafsson &
Nordberg, 2001), Collison (1980) consistently recorded
maximum absolute abundances below the surface 0–1 cm
(in one instance at 10–11 cm), and Moodley (1990) reported it to live down to 25 cm in the southern North Sea,
probably governed by the burrowing activity of macrofauna. On the other hand, it may also become epifaunal,
emerging above the sediment–water interface (e.g. onto
polychaete tubes), when exposed to dissolved
oxygen concentrations <0.2 ml l1 (Alve & Bernhard,
1995). This reflects its highly dynamic microhabitat
Table 1
Maximum relative abundance of live (stained) S. fusiformis and maximum absolute abundance of living benthic foraminiferal assemblages recorded in
NW European waters (surface 0–1 or 0–2 cm of sediment, unless otherwise stated)
Geographic area
(1–11) ¼ areas
in Fig. 3
North Sea
Forties (1)
Ekofisk (2)
Off NE England
Off NE England (3)
Southern North Sea
Areas off SW England
Bristol Channel
Northern Celtic Sea (4)
Northern Celtic Sea (5)
S Cornish Coast
Off Plymouth
Lyme Bay
Reference
Murray (1985)
Murray (1985)
Collison (1980)
Murray (1992)
Moodley (1990)
Murray (1992)
Murray (1970)
Murray (1979)
Scott, Scourse,
and Austin (in press)
Murray (1970)
Murray (1970)
Murray (1986)
The Skagerrak and Kattegat open waters
Skagerrak, northern slope
Alve and Murray (1995, 1997)
Skagerrak, southern slope (6)
Alve and Murray (1995, 1997)
Silled fjords
Oslofjord, Norway
Oslofjord, Norway
Drammensfjord, Norwaya (7)
Frierfjord, Norwaya (8)
Outer Lyngdalsfj, Norway (9)
Gullmarfjord, Sweden (10)
Havstensfjord, Sweden (11)
Alve and Bernhard (1995)
Alve and Olsgard (1999)
Alve (1995)
Alve (1994, 2000)
Alve (1999b)
Gustafsson and Nordberg (2001)
Gustafsson and Nordberg (2000)
Max. abundance
of S. fusiformis
(10–70%)
Max. abundance
of S. fusiformis
(>70%)
Environmental
category
96
95
2
2
90
2
92
90
1
1
57 (0–11 cm)
21 (0–5 cm)
66
63
42
21
67
Max.
standing crop
(ind cm3)
200
222
31
66
107
57
16
55
20
ND
ND
70
38
86
1
200
332
3
3
3
3
3
23
27
9
5
35
159
26
23 (0–4 cm)
53
100
99
100
88
76
High abundance areas (max >70%) are categorized from 1 to 3, where 1 ¼ beneath hydrographic frontal areas, 2 ¼ physically disturbed sea floor,
3 ¼ oxygen-depleted basins.
a
Data represent the >125 lm fraction, all others represent the >63 lm fraction, except Murray (1970) who studied the >76 lm fraction. ND ¼ no
data.
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E. Alve / Estuarine, Coastal and Shelf Science 57 (2003) 501–514
adaption, which is probably dictated by nutrient availability and, if dissolved oxygen becomes exhausted at
depth, by the extent of bioturbation and the accompanying variations in pore water chemistry. Several benthic
foraminiferal species (including S. fusiformis) are able to
survive anoxia and even sulphidic conditions for periods
up to a few weeks (Bernhard & Alve, 1996; Bernhard &
Sen Gupta, 1999) and some can survive anoxic bottomwater conditions for more than 2 months (Moodley, van
der Zwaan, Herman, Kempers, & van Breugel, 1997).
Being a facultative anaerobe opportunist, S. fusiformis is,
without exception, the most abundant foraminiferal
species in those dysoxic and periodically anoxic silled
fjord basins along the Skagerrak coast where the salinity
exceeds 28 (references below). For an extensive discussion of possible physiological adaptions used by benthic
foraminifera (including S. fusiformis) inhabiting oxygendepleted environments, see Bernhard (1996). In southern
Norwegian fjords, S. fusiformis is by far the most
successful foraminiferal colonizer of formerly anoxic
environments (Alve, 1995) as well as of new, recently
established habitats (Alve, 1999a).
Benthic foraminifera utilize a broad range of feeding mechanisms and their nutritional resources include
among others algae, bacteria, yeasts, fungi, and in some
cases, smaller animals and dissolved organic carbon (see
Goldstein, 1999, and references therein). Living algal
cells are of particular importance for many species living
within the photic zone, whereas those inhabiting greater
depths can utilize plankton phytodetritus arriving at the
sea floor (e.g. Gooday, 1986). Even below the photic
zone, S. fusiformis is commonly observed with green
cytoplasm indicating that it sequesters chloroplasts (e.g.
Alve & Bernhard, 1995; Cedhagen, 1991; Scott et al.,
2003). This can be attributed to either an algal food
source or to the selective retention of their plastids (see
Bernhard & Bowser, 1999). The fact that it increased its
population by a factor of 7 within a month, probably as
a response to the spring phytoplankton bloom in the
Gullmarfjord, Sweden, and that its abundance showed a
positive correlation with the surface water chlorophyll a
content (Gustafsson & Nordberg, 2001) strongly suggests that it exploits micro-algae as food. By the end of a
behavioural response experiment, the protoplasmic
colour was pale and the individuals were recorded in
sediments devoid of fresh algae material, indicating that
it also utilizes other nutrient sources (Alve & Bernhard,
1995). On the other hand, it has also been shown that
foraminifera lose their cytoplasmic colouration during
the early stages of gametogenesis (e.g. Goldstein &
Moodley, 1993). Bacteria seem to be an indispensable
part of the diet for many foraminiferal species (Lee,
1980) and degraded organic material, and especially the
microbiotas associated with it, provide important food
resources for shallow (Heeger, 1990) to deeper infaunal
taxa (Goldstein & Corliss, 1994). Hence, bacteria asso-
ciated with rotting animals, with the redox boundary
(e.g. sulphide oxidizers, iron oxidizers, nitrate reducers)
(Alve & Bernhard, 1995), and with rotting terrestrial
vegetation in coastal, land-locked waters (Alve, 1991)
probably represent additional food resources for S. fusiformis. S. fusiformis changes the shape of its aperture
considerably during growth (Fig. 1) from being interiomarginal, horseshoe-shaped and deeply excavated with
a comb-like lip in juveniles, to become terminal and narrowly ovate comprising a ÔcollarÕ opposed by a doublefolded tongue, whose free shank is comb-like at the
adult stage (Höglund, 1947). Bernhard and Bowser
(1999) speculated that this comb-like structure and the
double-folded tongue are used to hold diatoms, to prize
apart their frustules, and extract chloroplasts which in
turn may enable this species to inhabit anoxic pore
waters.
3. Environments strongly dominated by S. fusiformis
3.1. Introductory comments
Modern benthic foraminiferal assemblages strongly
dominated (>70%) by S. fusiformis are almost solely
reported from NW European waters with only a few
scattered high abundance, modern occurrences reported
from off NE America (e.g. Murray, 1969; Poag, Knebel,
& Todd, 1980) and NW Africa (Lutze, 1980). The
following discussion focuses on the European examples.
All study areas cited here have salinity, temperature,
and substrate conditions well within the ranges where
frequent abundances of S. fusiformis have been recorded
(see above) which means that these factors should not be
limiting for its abundance.
Except for the early papers by authors such as Gabel
(1971), Höglund (1947), Jarke (1961), and Risdal (1964)
who studied total (i.e. live + dead) assemblages, most
later studies in the North Sea region have reported live
(stained) and dead (unstained) assemblages separately
(for discussion of why continued use of total assemblages is unacceptable, see Murray, 2000). There are
several lines of evidence suggesting that different taphonomic processes (e.g. loss or gain of tests through
transport; loss of calcareous tests through dissolution;
loss of organo-agglutinated tests through decomposition
of the organic cement) operate at different scales within
the NW European region (e.g. Alve & Murray, 1997;
Murray, 1986, 1992; Scott et al., in press). In order to
reduce the bias caused by these differences when
comparing assemblages from areas of different hydrodynamic and geochemical properties, the present paper
primarily focuses on the ÔliveÕ records. These are,
influenced by seasonal fluctuations and distributional
patchiness but they still indicate the potential abundance
within an area.
E. Alve / Estuarine, Coastal and Shelf Science 57 (2003) 501–514
Another problem, when comparing data from different studies, is the choice of size fraction analyzed. Some
Scandinavian workers have had a tradition of investigating the >100 or >125 lm rather than the >63 lm
fraction which is commonly used in biological studies
of benthic foraminifera. This is of particular importance
in the present context because S. fusiformis is a small and
elongate species, which is easily washed through the
125 lm sieve implying that its abundance is highly
dependant on the size fraction studied. For example,
while most common species at a site in the Oslofjord,
Norway, showed a 1.1–2.8-fold higher relative abundance in the >125 lm fraction as compared to the
>63 lm fraction, S. fusiformis showed the opposite pattern with a 14 times higher relative abundance in the
>63 lm fraction (Fig. 2). In terms of absolute abundance it had standing crops of 14.3 and 0.4 individuals
cm3 in the >63 lm and >125 lm fractions, respectively. The overall standing crop (i.e. all species) in the
63–125 lm fraction was nearly twice as high as that in
the >125 lm fraction. The studies discussed in this paper
are those reporting live assemblages in the >63 lm fraction unless otherwise stated. Species diversity patterns
have not been considered in this paper because with
increasing dominance of one species (here S. fusiformis),
the diversity is bound to decrease.
High abundances of S. fusiformis are reported from
areas with widely different environmental characteristics
(Fig. 3 and Table 1). A closer inspection of these areas,
suggest that they can be grouped into three categories:
(1) beneath hydrographic frontal areas; (2) physically
disturbed areas of the seafloor; and (3) ephemerally
dysoxic/anoxic basins.
3.1.1. Hydrographic frontal areas
The Celtic Sea tidal-mixing front, which is prominent
during the summer, extends between Britain and Ireland
Fig. 2. Relative abundance of common live (stained) benthic
foraminifera in the >63 and >125 fractions in the same surface (0–
1 cm) sample from Area C (Oslofjord, Norway) in Alve (1999a),
unpublished data.
505
and curves southwards, at around 51 N, along the
British coast (Scott et al., in press). The sediments beneath and slightly to the south of the front are strongly
dominated (up to 92%) by S. fusiformis (Murray, 1970,
1979; Scott et al., in press) (Fig. 3 and Table 1). The area
is subject to bottom disturbance through waves and
currents and the sediments range from coarse sand
and gravel to biogenic and quartz fine sand with silt and
much mud. Although the area in general is a region
of mud accumulation, Murray (1979) pointed out that
S. fusiformis showed no clear correlation with water depth
or sediment type. Phytoplankton blooms have been
shown to be associated with hydrographic fronts in
the northern Celtic and Irish Seas (Savidge, 1976). An
April phytoplankton bloom was reported in connection
with the northern Celtic Sea front by Pingree, Holligan,
Mardell, and Head (1976), and maximum chlorophyll a
values of about 1.0 and 1.6 mg m3 were recorded in
the frontal zone during two traverses in August 1973
(Savidge, 1976). It is well established that biological processes are enhanced on continental shelves influenced by
such fronts and support large stocks of pelagic and benthic organisms (e.g. Iverson et al., 1979; Munk, Larsson,
Danielsen, & Moksness, 1995, Munk et al., 1999). This is
because the same hydrographical mixing conditions that
produce the frontal systems largely determine the availability of light and nutrients necessary for phytoplankton growth (Pingree & Griffiths, 1978). Consequently,
the high dominance of S. fusiformis is probably directly
linked to the biological processes associated with the
front (Scott et al., in press). Furthermore, the fact that
the high dominance records of S. fusiformis have spanned
a time period of almost 30 years, i.e. from April–May
1968 (Murray, 1970) to June–July 1995/1996 (Scott et al.,
in press), indicates that its abundance is a characteristic,
long-term feature of the benthic foraminiferal assemblages associated with this frontal zone. All samples to the
south of the high dominance area showed significantly
lower abundances.
A hydrographic frontal area (shelf break-front) is
located on the Danish slope of the Skagerrak basin (Fig.
3) at about 120 m isobath, and an enhanced primary
production and abundance of both phyto- and zooplankton was recorded within the zone of the front
where chlorophyll a concentrations were >250 mg m2 as
compared to values <100 mg m2 outside (Munk et al.,
1995). A similar front was not detected off the Norwegian coast and, whereas the primary production off
Denmark was enhanced throughout most of the water
column, this was not the case on the Norwegian slope.
The Skagerrak has a large area of stratified water during
the summer but there are also areas of different hydrographic regimes and mixing (Kiørboe et al., 1990),
which probably allow for increased flux of organic
material to the benthos. The density of the filter feeding
ophiuroid Amphiura filiformis has, for instance, increased
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E. Alve / Estuarine, Coastal and Shelf Science 57 (2003) 501–514
Fig. 3. Map showing the distribution and relative abundance of live (stained) S. fusiformis in NW European waters, where it makes up 70% of the
benthic foraminiferal assemblages. (1–11) ¼ location of areas, for details, see Table 1. xxxxx ¼ the position of hydrographic fronts in the northern
Celtic Sea (Scott et al., in press) and the Skagerrak (Munk, Larsson, Danielsen, & Moksness, 1999).
significantly in the eastern Skagerrak and in the Kattegat
from the 1970s onwards, and the reason is probably
increased food availability in an otherwise food limited
area (e.g. Josefson, 1990; Josefson & Jensen, 1992).
The most comprehensive records of living benthic
foraminiferal assemblages in the Skagerrak open waters
are those of Alve and Murray (1995, 1997). They
reported a strong dominance (60–86%) of S. fusiformis
between 117 and 519 m water depth on the Danish slope
beneath the same general area as the front. Bergsten,
Nordberg, and Malmgren (1996), described it as the
most characteristic species in their total assemblages
there but with a much reduced abundance due to their
use of the >125 lm fraction only. This area has probably been a Ôhot spotÕ for S. fusiformis for decades, as
Höglund (1947), noted that it was ‘‘extremely abundant
on the Danish side of the Skagerrak’’ in his samples
collected in 1937. On the other hand, the Norwegian
slope, where there is no evidence of a front (Munk et al.,
1995), is dominated by other species (Alve & Murray,
1995, 1997).
Maximum chlorophyll a values of about 1.0 and
1.6 mg m3 (most 0.4–0.6 mg m3) recorded in the surface water during two traverses of the Celtic Sea thermal
front in 1973 (Savidge, 1976) were lower than those
recorded on the Danish slope of the Skagerrak where
maxima of >5.8, >2.0, and >2.0 mg m3 were reported
for the years 1992, 1993, and 1994, respectively (Munk
et al., 1999). This is consistent with the lower standing
crops in the Celtic Sea as compared to those in the
Skagerrak (Table 1) and suggests that there is a strong
link between the primary production and the benthic
foraminiferal standing crop although the latter showed
large variations in the Skagerrak, probably indicating a
patchy supply of food to the seafloor (Fig. 4). It also
indicates that S. fusiformis, being an opportunistic
species, rapidly responds to increased organic carbon
flux and that its predominance is due to such sudden
enhanced inputs. This is in accordance with findings in
the deep sea where the sudden arrival of phytodetritus
on the deep sea floor is known to lead to a rapid increase
in opportunistic taxa such as Epistominella exigua and
Alabaminella weddellensis, whereas its effect on the
remainder of the fauna is less dramatic (Gooday, 1996).
Consequently, the moderate and high absolute abundance of S. fusiformis in the northern Celtic Sea and on
the Danish slope, respectively, and its high dominance
in both areas, seems to be connected to the presence of
overlying hydrographic frontal zones and their impacts
on the trophic conditions on the seabed beneath them.
Such a relationship between phytoplankton blooms and
the relative and absolute abundance of S. fusiformis
is in accordance with the findings of Gustafsson and
Nordberg (2001) and the fact that it often has a green
E. Alve / Estuarine, Coastal and Shelf Science 57 (2003) 501–514
Fig. 4. Relative abundance of live (stained) S. fusiformis plotted
against the overall standing crop of benthic foraminifera in Skagerrak
open waters (data from Alve & Murray, 1995, 1997).
colour, which suggests that it exploits algae as a nutrient
source (see above). On the other hand, many live,
unfixed, specimens from the Oslofjord lack green colour
but rather show dark spots of unidentified material
in their cytoplasm, indicating that it also exploits
other nutrient sources (Alve, unpublished data). Consequently, the information about its food requirements
is too limited to assess fully what influence different
kinds of food have on the abundance of S. fusiformis. At
the moment, it can only be stated in general terms, that
increased relative abundance of S. fusiformis seems to
be linked to seasonally increased organic flux. Total
organic carbon (TOC) is not, however, a good measure
for this as the organisms probably respond more to
fluxes of labile organic material, which is not necessarily
reflected in the sediment TOC. For example, the TOCvalues are nearly the same at the southern and northern
slopes of the Skagerrak basin (Alve & Murray, 1997).
There is a pronounced difference in chlorophyll a concentration over the two areas, which seem to be directly
reflected in both the relative and absolute abundance of
S. fusiformis. This strongly supports the view that
sediment organic carbon content is a weak proxy for
food availability (e.g. Levin & Gage, 1998).
3.1.2. Physically disturbed areas
The other areas in open, NW European waters
strongly dominated by S. fusiformis (Fig. 3 and Table 1)
are not influenced by hydrographic fronts, although the
Flamborough tidal front (Lindley & Williams, 1994;
Pingree & Griffiths, 1978) might have had an impact on
the areas off NE England investigated by Collison (1980)
and Murray (1992). Sand banks and sand waves characterize water depths <50 m in the Elphidium excavatum
507
dominated southernmost part of the southern North Sea
where the overlying waters are vertically mixed throughout the year (Murray, 1992). In addition to some
coastal areas around the UK (e.g. Lyme Bay), common
occurrences of S. fusiformis are essentially recorded in the
more central and northern parts of the North Sea, north
of about 53 309N, where thermal stratification develops
during the summer and current velocities are reduced,
allowing more fines to settle. Benthic foraminiferal
investigations of open coastal and shelf waters north of
about 58 N and at least up to 65 N are based on fractions
>125 lm (e.g. Klitgaard-Kristensen & Buhl-Mortensen,
1999; Klitgaard-Kristensen & Sejrup, 1996; Mackensen,
Sejrup, & Jansen, 1985; Sejrup et al., 1981). Consequently, reliable comparisons cannot be made between
these (where S. fusiformis is either not present in the data
sets, or it makes up a few percent of the assemblages only)
and studies based on the >63 lm fraction.
The north-western and northern central North Sea,
north of a line from the English coast at about 54 N, the
river Humber, to southern Norway/northern Denmark
(i.e. including the Ekofisk and Forties areas), is mainly
influenced by Atlantic inflow. It is not affected by riverinduced eutrophication, and the nutrient concentrations
have generally not changed significantly by anthropogenic activity since 1955 (Pätsch & Radach, 1997). The
North Sea is also generally well oxygenated although
some areas, such as the Oyster Ground, southern North
Sea, where overall annual primary production rates of
74–198 g C m2 were recorded in 1989 and 1990, may
experience oxygen saturations down to 50% during
periods of stable stratification (Peeters et al., 1995). Such
values are, however, not critical to benthic foraminifera
and should have no impact on the assemblage compositions.
Depth-integrated, annual primary production in the
North Sea was modelled by Moll (1998), who reported
large regional differences but with an overall increasing
trend from north (92 g C m2 yr1) to south (345 g C m2
yr1 in the German Bight), and from the central northern
towards the coastal areas. Values <200 g C m2 yr1
characterized the seasonally stratified waters with <100 g
C m2 yr1 and about 100 g C m2 yr1 in the Forties and
Ekofisk areas, respectively. The values for the latter two
areas fall within the definitions of oligotrophic and transition to mesotrophic ecosystems in the trophic classification for marine systems proposed by Nixon (1995). This,
together with the seasonal thermal stratification of the
water masses, which tends to reduce the benthic–pelagic
coupling (e.g. Heip et al., 1992), implies that the reason
for the high abundance of S. fusiformis in these areas is
probably not the same as that beneath the hydrographic
frontal areas.
Strong dominance of S. fusiformis (up to 96%) was
recorded in the Forties and Ekofisk areas (Murray,
1985) and off NE England (Murray, 1992), the latter
508
E. Alve / Estuarine, Coastal and Shelf Science 57 (2003) 501–514
within the same general area as Collison (1980) found it
to be dominant (57% of the living assemblage in five
subcores of 11 cm length). It was also very common
(21–66%) north of the Netherlands (Moodely, 1990;
Murray, 1992). The whole of the North Sea is commercially trawled. Jennings et al. (1999) estimated the total
international trawling effort in the entire North Sea to
be 2.25 million h yr1 in 1995. The three areas strongly
dominated by S. fusiformis are mainly subject to otter
trawling and, according to maps presented in Jennings
et al., the Ekofisk and Forties are moderately trawled
(e.g. about 5000 and 15,000 h yr1, respectively, in 1990),
whereas the areas off NE England are heavily trawled
(about 15–50,000 h yr1). Consequently, there are several
lines of evidence suggesting that the ÔnaturalÕ ecosystems
studied are already heavily human-influenced systems
(Lindeboom, 1995).
There is a growing realization that commercial fishing
using mobile gear causes changes in macro-benthic communities because they remove a large proportion of the
biomass of target as well as by-catch species and because
trawl gears have direct impacts on the substratum and
associated biota (Jennings et al., 1999). Infaunal population densities decrease immediately after the passage
of gear, individuals left at the sediment surface become
exposed to predators and invading scavengers, and disturbance of the sediment causes reduction in habitat
complexity and an increase in suspended solids in the
overlying water (see Frid, Clark, & Hall, 1999, and references therein). Pearson and Mannvik (1998) pointed
out that trawling tends to promote the dominance of
small opportunistic mobile or semi-mobile species, particularly polychaetes. This may also be the case for
benthic foraminifera. To the author’s knowledge, there
are no studies focusing on what possible effects trawling
may have on them but it is reasonable to assume that
their communities are affected as well and, due to its
opportunistic characteristics, S. fusiformis is a perfect
candidate to thrive in and rapidly bloom subsequent to
physical disturbance.
In addition to trawling, erosion and redeposition of
sandy sediments and very local sedimentation of finegrained deposits occur in the northern North Sea (de
Haas, Boer, & van Weering, 1997). Both the Ekofisk
and Forties areas are physically disturbed by vigorous
wave activity and the sediments in both areas are
muddy fine sand with only 3.6–6.5% and 10–39% fines
<63 lm, respectively (Murray, 1985). The Norway lobster (Nephrops norvegicus) and the deep-water shrimp
(Pandalus borealis) are commercially fished at Forties
and off NE England, exactly within the area of maximum S. fusiformis (see Frid et al., 1999; Lee & Ramster,
1981). The former digs burrows that often are extensive
and represent, together with the trawling and wave
activities, substantial physical disturbance of the surface
sediments.
The benthic foraminiferal standing crops in the Forties and Ekofisk areas are among the highest reported
from NW European waters (Table 1) and according
to Murray (1985), this indicates that they are very
fertile. He speculated that the strong dominance of
S. fusiformis might be a seasonal feature as most samples
were collected in June (as were also those of Collison,
1980) and this is in accordance with the spring bloom
of this species reported by Gustafsson and Nordberg
(2000, 2001). Indirect evidence of the effects of bottom
trawling on sediment resuspension were observed in the
seasonal collection of large (up to 14 cm length), infaunal
polychaete worms, along with substantial amounts of
resuspended bottom sediment, in a sediment trap deployed 25 m off the bottom in the Gulf of Main (Pilskaln,
Churchill, & Mayer, 1998). The authors noted that continental shelf environments in which trawling activity is
concentrated typically receive about half their nutrients
for primary production from the sediment and that
this has important implications for regional nutrient
budgets. Consequently, in addition to the nutrients supplied from spring phytoplankton blooms, the foraminifera in these physically disturbed areas may benefit
from recycled nutrients. On the other hand, too vigorous
a physical disturbance probably has a negative effect on
sediment-dwelling, mobile foraminifera. For example,
the two bioclastic, high-energy environments on the continental shelf of the Fair Isle Channel and to the west of
Scotland were completely dominated by attached forms,
both immobile and mobile on hard substrates (Murray,
1985). S. fusiformis was not recorded dead or alive in these
habitats and they were probably too disturbed (lack of
mud and associated organic material) to allow even
short-term blooms of this species. Hence, the reduced
standing crops off NE England (Table 1), as opposed to
the Forties and Ekofisk areas, may be due to the fact that
this area is up to 10 times as disturbed by trawling activity
(see above).
Lyme Bay is the largest area of muddy sediment
accumulation in the whole English Channel and has
vertically mixed water at all seasons (Murray, 1986).
Two samples collected just outside the Exe Estuary in
October 1982, and February 1985, which had the highest
relative abundance of S. fusiformis (67 and 39%, respectively) also had by far the highest overall standing crop
(70 and 51 individuals cm3 in the top 1 cm, respectively). An unbalanced competitive situation (strong
dominance of detritivores among which many species
were competing for the same food resource) was recorded in the macrofauna of Lyme Bay where sewage
sludge from Exeter is dumped (Eagle & Hardiman,
1977). Despite this, the authors ascertained that the
fauna, which had very few trophic levels and was dominated by detritivores, showed no detectable effect of the
sludge dumping. They rather suggested that the unbalanced situation might be due to the magnitude and
E. Alve / Estuarine, Coastal and Shelf Science 57 (2003) 501–514
period of hydrographic fluctuations relative to the
response time of the community, such that climax
community had not been attained.
In addition to the physical disturbance, the coastal
waters around Britain used to receive large amounts of
sewage and the coastal sea floor was the dumping site of
sewage sludge and industrial waste for at least a century.
Data provided by Lee and Ramster (1981) for 1974–
1975 show that several hundred millions m3 of treated
and untreated sewage were discharged per year into each
of the study areas of Collison (1980) and Murray (1970,
1979, 1986, 1992). Lyme Bay and the Celtic Sea each
received <200,000 tons yr1 in 1978, Bristol Channel
and the western coast of England north of 53 N received 400–600,000 tons yr1 each. In fact, the abovementioned sludge dumping in the Celtic Sea is located in
the area where maximum abundance of S. fusiformis was
recorded by Murray (1979). Although sludge dumping
has ceased, it is not possible to judge whether or not it
had an effect on the benthic foraminifera.
3.1.3. Ephemerally dysoxic=anoxic basins
The northern and eastern parts of the Skagerrak
(Fig. 3) are rimmed by numerous fjords and inlets. Some
of them, particularly in Norwegian waters but also
along the Swedish coast, have bottom water which is
partly separated from the open coastal waters by one or
more sills. Together with low tidal activity, estuarine
circulation patterns, and local meteorological conditions, the sills hamper efficient deep-water renewals
within the fjords and in many cases, this leads to the
development of dysoxic to periodic or ephemeral anoxic bottom waters (Fig. 5); some for natural and some
for anthropogenic reasons. These basins represent the
third kind of environment with strong dominance of
S. fusiformis. It has also been recorded as a common
faunal component in oxygen-depleted ([O2] 1.5 ml l1)
Fig. 5. The relative abundance of S. fusiformis in three Norwegian
silled, ephemerally anoxic to dysoxic fjords and in samples collected
just outside the sills.
509
parts of western Norwegian fjords; 44 and 12% in total
assemblages (>125 lm fraction) in Barsnesfjord and
Ikjefjord, Sognefjord, respectively (G. Mikalsen, personal communication, 2000).
So far, all investigated ephemerally dysoxic/anoxic
Skagerrak fjords with salinities higher than about 28,
have been found to be strongly dominated by S. fusiformis. They all have well-oxygenated surface waters
with subsequently decreasing dissolved [O2] at depth.
The [O2] along depth profiles within each basin varies
with season and year depending on the frequency and
magnitude of deep-water renewals. Fjords with permanently to nearly permanently anoxic bottom waters do
not support any living foraminiferal assemblages where
the [O2] is less than about 0.1 ml l1 but S. fusiformis
strongly dominates the shallower, slightly more oxygenated areas (e.g. Drammensfjord, Alve, 1995). The
upper limits of its dominance vary between fjords
depending on local hydrographic conditions and, due
to the seasonal and annual variability of the hydrographic properties, it is not possible (with our present
state of knowledge) to link its upper limit of dominance
to a particular environmental parameter or combination
of parameters. Five of these fjords have been investigated for living (stained) benthic foraminiferal assemblages (Fig. 3 and Table 1). The three Norwegian ones
(Drammensfjord, Frierfjord, outer Lyngdalsfjord) have
up to 100% S. fusiformis in the deeper parts where
anoxic to nearly anoxic bottom-water conditions frequently occur (Fig. 5). Although the [O2] in the bottom
water sometimes is higher, the surface sediments are
generally completely black, occasionally with a thin
brownish veneer, and they often smell of H2S. This
shows that the dissolved [O2] in the sediment pore water,
where foraminifera have been recorded living (e.g. Alve,
1994), is extremely low if present at all, and that the
foraminifera sometimes are exposed to hydrogen sulphide. On the other hand, in the Swedish Gullmarfjord
and Havstensfjord, where the [O2] only occasionally gets
below 1 ml l1, it has not been reported to constitute
more than 88% of the living assemblages (e.g. Fig. 6). In
other words, as opposed to the Norwegian fjords, it does
not seem to constitute mono-specific foraminiferal
assemblages in these slightly more oxygenated environments. The fact that S. fusiformis has been shown to be
the first and most successful colonizer of new as well as
of previously anoxic sediments (Alve, 1999a), indicates
that the environments with mono- or nearly monospecific occurrence of S. fusiformis have suffered
prolonged anoxia (probably for several months; at least
more than 2 months, Moodley et al., 1997) killing off the
foraminiferal assemblages, and that they only recently
have been recolonized. This does not, however, explain
why S. fusiformis strongly dominates oxygen-depleted
fjordic environments which have not experienced
prolonged anoxia.
510
E. Alve / Estuarine, Coastal and Shelf Science 57 (2003) 501–514
Fig. 6. Occurrence of phytoplankton blooms and relative (upper) and absolute (lower) abundance of S. fusiformis in a seasonal study of
Gullmarfjord, Sweden (data from Gustafsson & Nordberg, 2001).
The strong dominance of S. fusiformis beneath hydrographic fronts and its positive response to phytoplankton blooms probably indicate that its dominance might
be due to pulsed food input from these blooms which
promote a quicker response in this opportunistic species
as compared to other species. If this was the sole reason
for its high abundance inside the sills of the oxygendepleted fjords, one would also expect it to dominate the
areas just outside the sills. However, this is not the case
(Fig. 5) despite the fact that the residence time of the
surface water in the fjords is very short (1–4 days) which
should imply that the nutrient supply to the benthic
fauna is lower there than in the areas outside the sills.
Might the fact that S. fusiformis strongly dominates the
assemblages in the severely oxygen-depleted fjords and
not outside the sills, indicate that it somehow benefits
from the environmental conditions caused by the oxygen
deficiency? Of the five dominant genera in an experiment where benthic foraminifera were exposed to anoxic
bottom-water conditions for 78 days, the densities of
Stainforthia (mainly S. fusiformis) and Nonionella were
significantly higher under anoxic conditions (Moodley
et al., 1997). On the other hand, a significant decrease in
densities of stained S. fusiformis under sulphidic treatments over a 66-day period, suggested that the species
did not reproduce but that its survival was enhanced by
conditions created by the sulphidic treatment (although
life-checks indicated they were dead) (Moodley, Schaub,
van der Zwaan, & Herman, 1998). Furthermore, 13 weeks
of exposure to hypoxic bottom-water conditions, of
which the last 5 had dissolved oxygen concentrations
<0.2 ml l1, did not cause a convincing increased abundance of S. fusiformis, in either relative or absolute terms
(Alve & Bernhard, unpublished data) (Fig. 7). However,
the dysoxia killed off the majority of the metazoans
potentially competing with the foraminifera for food.
This indicates that dysoxic conditions alone do not promote increasing abundance of S. fusiformis, while weeks
of exposure to anoxia may do so, probably due to reduced competition.
4. Discussion
In the foregoing sections, the areas strongly dominated by S. fusiformis have been grouped into three
basically different environmental categories—beneath
hydrographic frontal areas, physically disturbed areas,
and ephemerally dysoxic/anoxic basins. This does not
mean that some of the characteristic processes acting in
one do not also act in the others. For example, the
seabed underlying the hydrographic frontal area on the
Danish side of the Skagerrak is also commercially
trawled. The highest frequency of trawling is found
throughout the shelf down to depths of about 150–
200 m (Skov & Durinck, 1998). Most of the high
S. fusiformis abundance samples on the Danish side
were collected at 117–262 m water depth so it is
reasonable to assume that these stations were either
directly or indirectly (e.g. additional nutrients, Pilskaln
E. Alve / Estuarine, Coastal and Shelf Science 57 (2003) 501–514
511
sediment in highly stressed areas again and again and
rapidly colonize new areas (Gray, 1980). In the same way,
S. fusiformis seems to be able to flourish in the abovementioned environments due to its opportunistic lifehistory strategy. The fact that it seems to be among the
most successful foraminiferal colonizers is probably due
to a combination of this life-strategy and, as recently suggested by Alve and Goldstein (2002), that tiny propagules
of benthic foraminiferal species are widely dispersed and
readily available for growth and reproduction as soon
as the environmental conditions get suitable.
Although more concrete information about its life
cycle and ecological requirement is needed, it seems that
S. fusiformis can be used as an indicator of rapidly
changing environmental conditions, whether physical or
chemical. When, however, used in palaeoecological interpretations, it is still a matter of which, or what combination, of these factors the interpreter thinks is the most
likely to have occurred.
Acknowledgements
I thank John Murray, Kjell Nordberg, and James
Scourse for stimulating discussions and useful comments on the manuscript.
Fig. 7. Dissolved oxygen concentrations (ml l1) and relative (upper)
and absolute (lower) abundance of S. fusiformis in experimental and
control mesocosms at selected times over a 36 weeks period. a and b
denotes replicate samples from the respective weeks (unpublished data
from Alve & Bernhard, 1995).
et al., 1998) affected by the trawling in addition to
the biological processes connected to the hydrographic
front. In the same way, some oxygen-depleted basins
(e.g. Gullmarfjord, Gustafsson & Nordberg, 2001) are
subject to pronounced phytoplankton blooms in addition to the stress caused by the oxygen depletion of
the bottom waters. Also, increased organic flux to
the sediments subsequent to phytoplankton blooms,
whether they occur in frontal zones or fjords, are likely
to reduce the [O2] in the sediment pore water where S.
fusiformis actually lives. The main point is that although
these areas do not seem to have any particular physical
or chemical parameters in common which could explain
the dominance of S. fusiformis, they are all subject
to rapidly changing environmental conditions. Consequently, it is suggested that its opportunistic life-history
strategy is the key to explain this, rather than high tolerance to a particular environmental parameter.
The dominance of the polychaetes Capitella capitata
and Polydora ciliata along gradients of eutrophication in
heavily polluted areas is probably due to an adaption to
continuous disturbance by being able to recolonize the
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