Journal of Foraminiferal Research, v. 31, no. 1, p. 12–24, January 2001
TEMPORAL VARIABILITY IN VERTICAL DISTRIBUTIONS OF LIVE (STAINED)
INTERTIDAL FORAMINIFERA, SOUTHERN ENGLAND
ELISABETH ALVE1
AND
JOHN W. MURRAY2
ics studies are needed to understand the development of
preserved benthic assemblages and to monitor short-term
environmental variability.
Although several investigations have studied temporal
variations based on frequent sampling (weeks) over a period
of more than a year (see Table 1 in Murray and Alve, 2000)
very few of these have considered temporal down-core distributions of such duration (Kitazato and Ohga, 1995; Ohga
and Kitazato, 1997; Gustafsson and Nordberg, 1999). The
only previous seasonal study of down-core foraminiferal
distributions in a non-marsh intertidal area is that of Castignetti (1996) on the Plym Estuary, England, carried out over
a period of 11 months.
The study area is the intertidal zone of the Hamble Estuary at Warsash, Hampshire, England (Alve and Murray,
1994, Fig. 1, W5-W8; see also Murray and Alve, 2000 and
references therein). The extreme tidal range is around 4.9 m
but mean spring tides are 4 m and neap tides 2 m. The river
Hamble is very small so its discharge has very little effect
on the salinity at Warsash which is commonly ⬎30 psu. The
climate is temperate with an annual water temperature range
of around 6 to 18 ⬚C although a wider range was measured
during the survey. During the late spring to autumn there is
a cover of macroalgae (especially Ulva and Enteromorpha)
resting on the sediment surface in the mid- to upper intertidal zone when the tide is out. There are no published data
on the annual contribution of organic carbon to the sediment. The area is moderately well sheltered from severe
wave activity, the sediment is muddy sand, and there is no
evidence of contemporary erosion in the area sampled.
The present study (the first part of which is presented in
Murray and Alve, 2000) was designed to investigate the
three-dimensional distributions of taxa (area, depth, patchiness) through time. The foraminifera of the study area were
initially investigated in 1992 (Alve and Murray, 1994), and
two stations from that study (W5 and W8) were selected for
more detailed investigation because they had shown contrasting ecological features due to relative elevation in the
intertidal zone.
The first part of the study discussed major faunal attributes, such as temporal variability of standing crop, dominant species, species diversity of the bulk assemblages in
the top 1 cm of sediment, the size distribution and biomass
of the three dominant species, and seasonal cyclicity. That
paper focused on the top 1 cm of sediment studied over a
27 month period.
The second part of the study (present paper) examines in
detail the hard-shelled foraminiferal depth distribution patterns in the surface 1 cm over 27 months (monthly sampling) and down to 4 cm for the first 14 months. Analyses
of deeper sediment sections ceased because, over a one-year
period the majority of the living fauna was found in the 0–
1 cm interval at the two investigated stations. The aims
include a detailed analysis of 1) seasonal microhabitat par-
ABSTRACT
The temporal variability (over 27 months) in abundance, depth of life in the sediment, and species diversity
of hard-shelled, live (stained) foraminifera in an intertidal area has been determined. Throughout the investigation period, the same three species (Haynesina germanica, Ammonia beccarii (tepida), Elphidium excavatum) were dominant at the two investigated stations, the
maximum abundance of all species (dominant and subsidiary) was in the surface 0.25 cm, and there was a
general lack of seasonal change in the vertical distribution of the foraminifera. Seasonality does not seem to be
a controlling factor for the vertical distribution of individuals in this area and none of the foraminifera showed
high subsurface abundances. Because of the difference
in depth position of the redox boundary within the sediment (often 1 cm) and the maximum abundance of individuals (surface 0.25 cm) the former cannot be the
main factor limiting their vertical distribution of abundance. The generally high dominance of individuals in
the surface few millimeters is probably related to the
presence there of microalgal food and limited burrowing
activity of the sparse macrofauna. Subsidiary species colonized the area ephemerally, thus the number of species
recorded varied from one season to another. The minimum and maximum number of species found at any single sampling event were 5 and 22, whereas the cumulative number of stained species found throughout the investigation period was 35 (plus at least three soft-shelled
forms). Species diversity is one of the principal univariate methods used to assess both natural variability and
possible human impacts. The large natural seasonal variability demonstrated here suggests that caution should
be taken in assessing the significance of diversity changes
when based on occasional sampling only.
INTRODUCTION
Traditionally most ecological studies of benthic foraminifera have been based on a single sampling of the surface
sediments (0–1 cm). In recent years there has developed a
greater awareness that some taxa live infaunally to a considerable depth in the sediment. Some authors have recognized distinctive morphotypes related to depth and others
have invoked a variety of controls (e.g., oxygen availability,
food supply) acting with varying intensity. Experimental
work has shown that infaunal depth habitats are not fixed
but vary according to changing environmental conditions.
All these aspects contribute to a fuller understanding of the
benthic ecosystem. Also, time series and population dynam1
Department of Geology, University of Oslo, P.O. Box 1047 Blindern,
N-0316 Oslo, Norway.
2School of Ocean and Earth Science, Southampton Oceanography Centre, European Way, Southampton SO14 3ZH, England.
12
13
TEMPORAL VARIABILITY IN VERTICAL DISTRIBUTIONS
titioning with respect to depth in the sediment, 2) the
ephemeral colonization of the area by species not permanently living in the area, 3) temporal down-core variation
in species diversity, and 4) compilation of a complete list
of taxa found living in the area during the survey period.
METHODS
SAMPLING PROCEDURE
Samples were collected every month over a 27 month
period from one low intertidal station (sta. 1) and one intermediate intertidal station (sta. 2), the latter being affected
by a cover of macroalgae during the summer months. Full
details of the methodologies are given in Murray and Alve
(2000). In both January and February 1994 a single core
was collected from each of the two stations, but thereafter
two replicate cores were collected every month from each
station until March 1996. The area studied for each sample
at each station was 66.4 cm2 for the first three months and
subsequently 45.4 cm2. Except for the first two months,
when the surface sediment was sectioned in two 0.5 cm
slices, each core was sampled in slices as follows: four slices 0.25 cm thick from the 0–1 cm interval, then 3 slices 1
cm thick from 1 to 4 cm. This yielded seven samples per
core and therefore a total of 28 samples each month. Examination of samples deeper than 1 cm ceased after March
1995. Two 12 cm long cores (one from each station) were
taken in December 1994 and the interval from 4 to 12 cm
was divided into 2 cm slices.
SAMPLE PROCESSING
AND
PICKING
In the laboratory the foraminiferal samples were washed
on a 63 ␮m sieve, stained with rose Bengal for 1 hour,
washed again to remove the surplus stain, and dried in air.
Rose Bengal is considered to be the most practical method
to determine the occurrence of live specimens in this kind
of study (Murray and Bowser, 2000). The samples were then
gently brushed through a 1 mm sieve to break up organic
aggregates and a flotation was carried out using trichloroethylene. Altogether, a total of 562 samples have been picked and analyzed for live (stained) benthic foraminifera. Of
the 420 samples representing the upper 0–1 cm, 338 were
picked completely, and for 82, where the number of living
forms was very large (⬎500), only a portion (generally
⬎300 individuals) was picked and the standing crop numbers calculated for the whole. All abundance data have been
calculated to a standard unit of 10 cm3 to eliminate the effects of differing sample size between the sediment slices.
The H(S) and Fisher alpha diversity index values are low
in all surface (0–1 cm) samples (Murray and Alve, 2000),
and the number of specimens in individual slices below 0.5
cm was often too low for reliable determinations of diversity
indices. Therefore, for comparing the down-core sediment
slices, the number of species in each sample is given instead. An additional single sample from sta. 2 (March 1995)
was sieved on a 38 ␮m sieve and partly wet-picked to look
for juveniles and soft-shelled taxa.
RESULTS
Although down-core data were collected for January and
February 1994, these cores were divided into 0.5 cm slices
FIGURE 1.
tions.
Time/depth distributions of standing crop for both sta-
in the top 1 cm as opposed to 0.25 cm slices for all other
months. Therefore, the year over which the most detailed
down-core data have been gathered runs from March 1994
to February 1995.
DOWN-CORE DEPTH DISTRIBUTIONS (0–4
CM)
Standing crop
Without exception, the highest abundances of all species
were found in the top 0.25 cm of sediment not only in the
first year, when samples were analyzed down to 4 cm (Fig.
1), but also in the second year, when only the surface 1 cm
was analyzed. In the first year, both stations showed a similar overall pattern in standing crop per 10 cm3 with medium
values in the surface 0.25 cm interval in March to May,
lowest values in June and July followed by a rapid increase
in August. The values were low at depths greater than 0.25
cm from March to July. In August the standing crop increased at all depths and remained higher until November.
Overall the values were higher at sta. 2 than sta. 1.
Taking the cumulative relative abundance of the standing
crop in the surface 4 cm sampled interval as 100%, throughout the study period the range of the surface 0.25 cm value
was 46–79% (mean 60%) at sta. 1 and 40–82% (mean 59%)
at sta. 2. Furthermore, for the surface 1 cm (pale bars in
14
ALVE AND MURRAY
FIGURE 3. The standing crop of the surface 0.25 cm slice expressed as a percentage of that of 0–1 cm.
Subsidiary species
FIGURE 2. Cumulative relative abundance of standing crop
throughout the 0–4 cm interval for both stations. Light shading ⫽ 0.25
cm sediment slices; dark shading ⫽ 1 cm slices.
Fig. 2) the values were 58–95% (mean 77%) for sta. 1 and
62–92% (mean 79%) for sta. 2. The four sediment slice data
down to 1 cm are available for all 27 months. Here the
standing crop of the surface 0.25 cm interval made up 44–
93% (mean 78%) and 34–92% (mean 72%) of the 0–1 cm
for stations 1 and 2 respectively (Fig. 3). Although there is
a positive correlation between the percent values for years
one and two at sta. 2 (r ⫽ 0.78, p ⬍ 0.01), there is no such
correlation for sta. 1 (r ⫽ 0.27).
Because all species were generally more abundant in the
surface 0.25 cm, comments are first made on their occurrence throughout the whole investigation period (i.e., 27
months). Additional comments are then made on the downcore data (0–4 cm) for the first year.
The pattern of abundance of subsidiary species in the surface 0.25 cm layer for the full study period did not show
repetition from one year to another (Fig. 6). Two subsidiary
species, Elphidium williamsoni and Aubignyna hamblensis,
were common at both stations and the former occurred every month together with the three dominant species (Table
1). Additionally, Hopkinsina pacifica and Stainforthia sp.
were abundant at sta. 1, whereas Quinqueloculina dimidia-
Dominant species
These were Ammonia beccarii (tepida), Elphidium excavatum and Haynesina germanica. For each species, the
data are presented as standing crop and percent (each slice
as a percent of the total 0–4 cm) (Fig. 4, sta. 1; Fig. 5, sta.
2). Haynesina germanica at sta. 1 showed minimum standing crop in summer (June–July) whereas the relative abundance showed an overall decline throughout the study period
(March 1994–February 1995). Ammonia beccarii and Elphidium excavatum at sta. 1 showed a similar pattern with
highest standing crop at the surface during autumn and winter but there was no obvious similar trend in the relative
abundance. Haynesina germanica at sta. 2 showed maximum standing crop values in the surface 0.25 cm in late
winter to spring whereas A. beccarii and E. excavatum had
maximum values in autumn and winter (Fig. 5). Ammonia
beccarii also showed higher subsurface values from August
to November 1994. A general feature for all species is that
the relative abundances at depth were inevitably greater
when the standing crop values at the surface were at a minimum.
FIGURE 4. Time/depth distributions of standing crop and cumulative relative abundance for Haynesina germanica, Ammonia beccarii
and Elphidium just excavatum for sta. 1 where the cumulative relative
abundance from 0 to 4 cm sums to 100% for each species.
15
TEMPORAL VARIABILITY IN VERTICAL DISTRIBUTIONS
ta, Fissurina lucida, and Elphidium oceanensis were abundant at sta. 2. There the latter three species and agglutinated
taxa were hardly present from January to June, 1994, after
which time their numbers increased dramatically. The abundance of only one of the subsidiary species, A. hamblensis,
showed a significant positive correlation (r ⫽ 0.648, p ⬍
0.01) over time between the two stations. The bolivinids
(Bolivina pseudoplicata, Bolivinellina pseudopunctata,
Brizalina variabilis, Brizalina sp.) were common (max. 29
individuals/10 cm3 in 0–0.25 cm, Oct., 1994, sta. 2) only in
the autumn/early winter of both years.
The agglutinated forms, mainly comprising Ammoscalaria runiana, Eggerelloides scaber (small individuals only),
Paratrochammina (L.) haynesi, and Textularia tenuissima,
were either rare or absent at both stations but had a maximum of 51 individuals/10 cm3 in the surface 0.25 cm at sta.
2 in September, 1994. A general trend for all the subsidiary
species is that although they occasionally were present down
to 4 cm, their abundance below 1 cm was extremely low
(Fig. 7).
Number of species
FIGURE 5. Time/depth distributions of standing crop and cumulative relative abundance for Haynesina germanica, Ammonia beccarii
and Elphidium just excavatum for sta. 2 where the cumulative relative
abundance from 0 to 4 cm sums to 100% for each species.
TABLE 1.
Number of months
27
27
27
27
26
26
26
25
24
24
24
23
23
22
14
12
10
10
10
9
9
8
5
5
4
3
3
2
The total number of live (stained) species throughout the
study period (27 months) was 35 of which 26 were identified to species level (see faunal reference list). The single
wet-picked sample revealed at least three additional species
of soft-shelled taxa (one saccamminid and two allogomiids)
which collapsed when dried and are therefore not found in
the studied assemblages. The cumulative number of recorded hard-shelled species at sta. 1 reached 28 in November
1994 and increased to 35 from August 1995 to March 1996
(Fig. 8). At sta. 2, the numbers reached a maximum value
Rank order of species by frequency of occurrence in the surface 1 cm.
Station 1
Ammonia beccarii
Elphidium excavatum
Haynesina germanica
Elphidium williamsoni
Hopkinsina pacifica
Nonion depressulus
Stainforthia sp.
Aubignyna hamblensis
Elphidium oceanensis
Fissurina lucida
Quinqueloculina dimidiata
Bolivinellina pseudopunctata
Buliminella elegantissima
Brizalina sp.
Textularia tenuissima
Elphidium margaritaceum
Paratrochammina (L.) haynesi
Elphdium sp.
Stainforthia fusiformis
Bolivina variabilis
Nonion sp.
Bulimina gibba/elongata
Eggerelloides scaber
Ammobaculites balkwilli
Nonionella sp.
Bolivina pseudoplicata
Rolsalina sp.
Bolivinia
Number of months
Station 2
27
27
27
27
26
25
24
23
23
22
22
20
18
18
17
6
6
5
5
4
4
4
4
4
3
Ammonia beccarii
Elphidium excavatum
Haynesina germanica
Elphidium williamsoni
Elphidium oceanensis
Fissurina lucida
Nonion depressulus
Aubignyna hamblensis
Quinqueloculina dimidiata
Buliminella elegantissima
Stainforthia sp.
Brizalina sp.
Textularia tenuissima
Bolivinellina pseudopunctata
Hopkinsina pacifica
Elphidium margaritaceum
Elphidium sp.
Bolivina variablilis
Stainforthia fusiformis
Eggerelloides scaber
Paratrochammina (L.) haynesi
Bulimina gibba/elongata
Ammobaculites balkwilli
calcerous unindentified
Miliammina fusca
16
ALVE AND MURRAY
the sediment (microhabitat partitioning: within the surface
0–1 cm from all 27 months and down to 4 cm during the
first 14 months) and biodiversity.
VOLUME VERSUS AREA FOR REPORTING NUMERICAL
ABUNDANCE?
FIGURE 6. Number of stained individuals of the more abundant
subsidiary species (surface 0.25 cm).
of 29 in May 1995 with no new occurrences after that. The
maximum number of species recorded in any one core at a
single sampling event was 22.
There is no obvious pattern in the number of species over
time in the single sediment layers (Fig. 9). However, when
considering all the species present in each core (0–4 cm)
through time, there is a comparable pattern at both stations
with a progressive increase from April through to November. The mean number of species over each year was highest
in the surface 0.25 cm and showed a slight decrease downcore (Table 2). However, within each sediment interval the
figures were essentially the same at both stations.
DOWN-CORE DEPTH DISTRIBUTIONS (4–12
CM)
Two to four species were present (including the three
dominant forms) in each 2 cm section and there was an
average of 4 and 8 individuals per 10 cm3 at sta. 1 and 2
respectively.
DISCUSSION
In a previous paper relating to the present study (Murray
and Alve, 2000) the results from the bulk surface 0–1 cm
showed that the assemblages were dominated by three species: Haynesina germanica, Ammonia beccarii, and Elphidium excavatum. Patchiness occurred on a scale of a few
centimeters and had a major impact on tracking temporal
changes in the standing crop. The seasonal cyclicity was not
always well shown by the foraminiferal numerical abundance but was better shown by species diversity and biomass. In this paper, we focus on depth distributions within
As pointed out by Alve and Olsgard (1999), numerical
abundance can be presented in two fundamentally different
ways: as number of individuals per unit area summed for
the whole down-core section, and as number of individuals
per volume of one particular core slice. In the former, the
true numerical abundance for the unit area will be attained
only if the core length is at least equal to the down-core
distribution of living individuals. In the latter method, the
numbers will to a much stronger extent depend on the thickness of the slice analyzed. Several studies have shown that
the majority of foraminifera live in the surface one to two
cm of sediment. In such cases, if the numerical abundance
values are presented per unit area, the figures will not
change dramatically if individuals from sections deeper than
the zone of high abundance are included. However, if the
numerical abundances are given per unit volume, the figures
will strongly depend on the thickness of the sediment slice.
For instance, in this study the majority of forms live in the
surface 0.25 cm. If the results are averaged for a 1 cm thick
slice of unit volume, then the numerical abundance is much
lower than that of the thin surface layer. Of course, if the
sediment slice is standardized at 1 cm thickness then for the
surface 1 cm, the results per unit area and unit volume are
identical. Consideration of the method of presenting the results is important when comparing data from different studies.
MICROHABITAT PARTITIONING
In order to obtain a high resolution record of infaunal
depth distribution, the surface 0–1 cm was sampled in four
0.25 cm slices. The most striking features of this extensive
dataset are that three species dominated at all depth levels
throughout the investigation period, that the maximum
standing crop of all species (dominant and subsidiary) was
in the surface 0.25 cm throughout most of the 27 months,
and that there was a general lack of seasonal change in the
vertical distribution of the foraminifera. However, at times
of low standing crop in the surface layer, the relative abundance increases down-core (Figs. 4 and 5). The lack of a
consistent seasonal pattern for both stations (Fig. 3) indicates that seasonality is not a controlling factor for the vertical distribution of individuals in this area.
Although in this study vertical depth distribution is not
really developed, in other environments there is a clearer
habitat partitioning. The first reliable record of infaunal foraminifera is that of Richter (1961) based on cores from the
intertidal zone in the southern North Sea. He recognized a
relationship between maximum depth of life and the thickness of the surface oxidized zone. Since then, a large number of studies of vertical distributions have been made on
environments ranging from high marsh to hadal ocean. The
results sometimes appear contradictory and certainly there
is no global pattern of specific taxa occupying one particular
subsurface depth zone. The reasons for this are partly ex-
TEMPORAL VARIABILITY IN VERTICAL DISTRIBUTIONS
17
PLATE 1
SEM micrographs. Scale bar 100 ␮m. 1 Ammonia beccarii (Linné) forma tepida Cushman, juvenile. 2 Haynesina germanica (Ehrenberg),
juvenile. 3 Elphidium excavatum (Terquem), juvenile. 4, 5 Nonion depressulus (Walker and Jacob). 6, 7 Fissurina lucida (Williamson). 8, 9
Elphidium oceanensis (d’Orbigny). 10, 11 Elphidium margaritaceum Cushman. 12, 13 Stainforthia fusiformis (Williamson). 14, 15 Stainforthia
sp.
18
ALVE AND MURRAY
PLATE 2
SEM micrographs. Scale bar 100 ␮m. 1 Buliminella elegantissima (d’Orbigny). 2 Bolivina pseudoplicata Heron-Allen and Earland. 3 Bulimina
gibba/elongata Fornasini. 4 Cuneata arctica (Brady). 5, 6 Brizalina variabilis (Williamson). 7–9 Bolivinellina pseudopunctata (Höglund). 10, 11
Hopkinsina pacifica Cushman. 12, 13 Quinqueloculina dimidiata Terquem. 14, 15, 16 Aubignyna hamblensis Murray, Whittaker and Alve. 17
Ammonia beccarii (Linné) forma tepida Cushman.
19
TEMPORAL VARIABILITY IN VERTICAL DISTRIBUTIONS
FIGURE 7. Time/depth distributions of standing crop for selected
subsidiary species.
FIGURE 9. Number of stained species in the surface 0.25 cm and
0.75–1.00 cm sediment slices and in the 0–4 cm interval combined.
plained by Buzas and others (1993): ‘Because each core
captures a variety of individuals found together in one instant of time, we are simply observing a transient phenomenon of a group of animals with a three dimensional aggregated spatial distribution’, by De Stigter and others (1998):
‘microhabitats of benthic foraminiferal species are not static,
but may be highly variable from place to place, as determined by local environmental conditions’ and finally, as
stated by Jorissen and others (1998): ‘‘The vertical zonation
of foraminiferal species in the sediment shows a close correspondence with the depth distribution of oxic respiration,
nitrate and sulphate reduction’’.
From the mass of data collected over four decades, the
main conclusions to emerge are:
● that benthic foraminifera have been recorded living infaunally from ⬍1 cm down to at least 40 cm (the latter
in marsh environments Akers, 1971, perhaps in part due
to open burrows, Goldstein and others, 1995)
● typically the highest numbers are found in the surface 0–
1 cm layer (e.g., Gooday, 1986; Mackensen and Douglas,
TABLE 2.
Depth (cm)
FIGURE 8. Cumulative number of species versus cumulative number of counted individuals (each entry on the x-axis represents one
sampling event, i.e., one month, starting from January 1994).
Sta.
Sta.
Sta.
Sta.
1
1
2
2
(yr
(yr
(yr
(yr
1)
2)
1)
2)
Mean number of species in each sediment slice.
0.00–0.25 0.25–0.50 0.50–0.75
15
15
13
12
12
11
11
11
9
8
10
9
0.75–
1.00
9
8
9
9
1.00–2.00 2.00–3.00 3.00–4.00
10
—
10
—
‘10
—
9
—
10
—
8
—
20
●
●
●
●
●
●
●
●
●
●
ALVE AND MURRAY
1989; Bernhard and Reimers, 1991; Barmawidjaja and
others, 1992; Murray, 1992; Rathburn and Corliss, 1994;
Bernhard and Alve, 1996; Hannah and Rogerson, 1997;
Castignetti and Manley, 1998; De Stigter and others,
1998, 1999; Jorissen and others, 1998)
there is no clear pattern of depth stratification from one
area to another
several authors have pointed out the control of the redox
boundary (availability of oxygen) as the lower limit of
life in the sediment (e.g., Richter, 1964; Shirayama, 1984;
Ohga and Kitazato, 1997; Langer and others, 1989) or
oxygen availability as a major control (e.g., Hohenegger
and others, 1993; Jorissen and others, 1992; Mackensen
and Douglas, 1989). However, Rathburn and Corliss
(1994) specifically stated that there was no oxygen control on depth distribution in the Sulu Sea and according
to Jorissen and others (1998) ‘‘foraminiferal microhabitats are only indirectly controlled by pore water oxygen
concentrations’’
others have pointed to the role of availability of food
(Corliss and Emerson, 1990; Jorissen and others, 1992;
Hohenegger and others, 1993; Linke and Lutze, 1993;
Wollenburg and Mackensen, 1998)
biotic controls on depth stratification in the deep-sea were
favored by Gooday (1986) and Hohenegger and others
(1993) considered that specific food requirements were
responsible for patchiness in the surface layer and in limiting vertical distributions for those taxa feeding on live
microalgae
observations of living forms show that they are highly
mobile (e.g., Kitazato, 1981; Severin and Erskian, 1981;
Severin, 1987; Wetmore, 1988; Langer and others, 1989)
and can migrate through the sediment in search of food
or more favorable oxygen conditions (e.g., Jorissen and
others, 1992; Linke and Lutze, 1993; Alve and Bernhard,
1995)
experimental studies have shown that infaunal taxa become epifaunal as the availability of oxygen decreases
(Alve and Bernhard, 1995) and this confirms field observations (Barmawidjaja and others, 1992; Linke and Lutze,
1993)
some taxa live in anoxic sediments and may be facultative
anaerobes (e.g., Bernhard, 1989, 1992, 1993; Bernhard
and Reimers, 1991)
some authors have promoted the view that different morphotypes live at different levels in the sediment (Corliss,
1985, 1991; Corliss and Chen, 1988; Corliss and Emerson, 1990; Corliss and Fois, 1990) but De Stigter and
others (1998) pointed out that ‘so-called epifaunal morphotypes may also be common in subsurface microhabitats’ and they cautioned against oversimplistic interpretations of morphotypes (p. 56)
the TROX model proposed by Jorissen and others (1995)
links the interplay of food and oxygen as the principal
controls; this is essentially based on the conclusions
reached by Corliss and Emerson (1990) although not formalized by them into a model
the essence of the TROX model is that in oligotrophic
environments the infauna is shallow due to the limiting
control of food (adequate oxygen); in eutrophic environments the infauna is limited by availability of oxygen
(superabundance of food); while in mesotrophic environments the infauna may penetrate deeply into the sediment
according to the availability of food with oxygen not usually being a limiting factor
● the TROX-2 model was introduced to take into account
other geochemical changes (apart from oxygen depletion)
and the role of competition for labile organic matter (Van
der Zwaan and others, 1999)
● combining the TROX models with the experimental evidence that forms change their depth in the sediment in
response to oxygen gradients, then the concept of different morphotypes for different depths in the sediment
(Corliss and Fois, 1990; Corliss, 1991) is loose (Van der
Zwaan and others, 1999) and meaningless on a global
scale although it might apply locally if the environment
remains constant
In this study, the sediments at both stations had a brown
layer which rarely exceeded 1 cm and the minimum was
about 0.2 cm. At station 2, below the brown layer it turned
directly to dark gray/black, whereas at sta. 1 there was a
transition from brown into medium gray. It is established
that the base of such a brown layer does not necessarily
coincide with the redox-boundary, meaning that the lower
part of the brown layer may be anoxic (Revsbech and others,
1980). Microelectrode measurements performed once at
each station (March, 1994) indicated that the redox boundary had a shallower position at sta. 2 (⬃0.3 cm) as compared to a more transitional boundary at sta. 1 (⬃1.2 cm).
At sta. 2 at the time of measurement there was a clear transition from brown to dark gray/black at 1.1 cm, whereas no
clear color change was obvious at sta. 1. Despite this difference between the two stations in depth of the redox
boundary, the average relative abundance of the standing
crop over 14 months was nearly the same in the surface
0.25 cm layer (sta. 2 ⫽ 59%; sta. 1 ⫽ 60% as a proportion
of the total number of stained individuals down to 4 cm).
Comparable results were found by Castignetti (1996) in an
11 month survey of the Plym estuary, UK, where 93% of
the foraminifera (in 8 cm long cores) occurred in the top
0.3 cm and 97% in top 1 cm. There the brown layer was
0.2–0.6 cm thick but the depth of the redox boundary was
not given.
The fact that the redox boundary at sta. 1 seemed to be
situated at about 1 cm or deeper, yet the large majority of
individuals lived in the surface 0.25 cm, indicates that the
redox boundary is not the main factor limiting their downcore abundance. Indeed, several of the common species are
known to survive dysoxia or anoxia (e.g., Ammonia beccarii and Elphidium excavatum, Moodley and Hess, 1992)
and many of them have been recorded living in reasonable
numbers (as compared to their surface abundance) down to
25 cm sediment depth (Moodley, 1990). All the dominant
and some of the subsidiary species have been shown to
sequester chloroplasts (see Bernhard and Bowser, 1999, and
references therein) or feed on benthic microalgae (e.g.,
Knight and Mantoura, 1985; Hohenegger and others, 1989).
As these algae are obviously dependent on light, it seems
reasonable that the maximum abundance of foraminifera in
the surface few millimeters is primarily due to this irrespective of the position of the redox boundary. When the
TEMPORAL VARIABILITY IN VERTICAL DISTRIBUTIONS
tide was out during daylight, a golden-brown layer of epipelic diatoms developed on exposed sediment. They
emerged from the sediment within a few minutes in response to light (see Paterson, 1986, for discussion) and we
have observed this under the microscope in the laboratory
on freshly collected surface sediment. The foraminifera
were not observed to do this but their pseudopodia probably
penetrated to the surface of the sediment. Similarly, on tidal
flats in the southern North Sea, the upper surface of mud
and muddy sand is covered with a dense mucilaginous layer
of diatoms. Langer and others (1989) considered that the
living foraminifera were embedded within this layer in order
to protect themselves against disturbance by tidal currents.
The mucilaginous material is a biofilm and recent studies
show it to consist of carbohydrate-rich exopolymers (EPS)
produced by the epipelic diatoms during locomotion. This
is utilized as a food source by bacteria which in turn also
produce EPS (Underwood and Smith, 1998). The bacteria
are a potential source of food for the foraminifera and the
EPS helps to bind the sediment and reduce erosion. Both of
these attributes are potentially beneficial to shallow infaunal
foraminifera.
Despite the fact that the most optimal conditions for the
present intertidal species are within the surface few millimeters of sediment, Moodley (1990) recorded 8 of them to
be living in reasonable numbers (as compared to their surface abundance) down to 25 cm in subtidal southern North
Sea sediments. He concluded that their vertical distribution
was governed primarily by the burrowing activities of macrofauna. As opposed to other intertidal areas, where higher
abundances of the present species have been recorded at
greater sediment depths (e.g., Langer and others, 1989), only
a few small worms and crustaceans (e.g., Corophium) and
no typical estuarine infaunal bivalves (e.g., Scrobicularia)
were recorded in the present study area. Consequently, the
low abundance of foraminifera below the surface few millimeters throughout the investigation period probably reflects low bioturbation activity (e.g., as compared with the
intertidal area of outer Jade Bay studied by Langer and others, 1989) causing sparcity both of oxygenated burrows and
labile food at depth. However, the few stained individuals
in the deeper sediment layers (recorded down to 12 cm, the
limit of sampling) still indicate some bioturbation activity.
When infaunal foraminifera live to a considerable depth
in the sediment, then estimates of the standing crop based
on the surface 1 cm will be too low. For instance, Buzas
(1974) pointed out that in the Rhode River, USA, estimates
of standing crop based on the 0–2 cm interval represent
barely one fifth of the true number. In the present study, this
is not the case since such a high proportion live in the surface 1 cm. The implications of this are that in designing an
ecological survey, it is essential to carry out a pilot study
to determine the depth to which sampling needs to take
place.
BIODIVERSITY
AND
COLONIZATION
SPECIES
BY
SUBSIDIARY
In surveys based on a single period of sampling the number of stained (living) species recorded will be those present
at that time only. The Hamble estuary is a region of low
21
diversity with 5–22 species per sample according to season.
In this study, the total number of hard shelled stained species found over the 27 month sampling period was 35 (plus
at least three soft shelled taxa). It is evident from the time
series data that certain species colonized the area ephemerally (Figs. 6 and 7) and therefore the number of species
recorded varied from one month to another (Fig. 9) and
never exceeded 22 (sta. 1, Sept. 1994). The cumulative increase in species from the start of the study reached a plateau earlier at sta. 2 than at sta. 1 (Fig. 8) which is probably
related to their positions relative to the main (seaward)
source. No doubt over a longer period of time other species
might be ephemerally introduced into the area. The pattern
of cumulative increase obviously depends on the starting
point of the survey. Had the study commenced in the autumn, the initial number of species would have been much
higher at both stations although the cumulative total would
have remained the same. On the other hand, temporal cumulative diversity increase should be much higher in the
overall more stable and diverse offshore environments.
Forms such as Elphidium williamsoni and Quinqueloculina dimidiata were probably sourced from nearby tidal
marshes where we have observed Q. dimidiata living attached to filamentous algae. Other forms, such as the bolivinids, Buliminella elegantissima, Bulimina gibba/elongata, Nonion depressulus, and Fissurina lucida, were most
probably sourced from the nearby marine shelf as these are
more stenohaline taxa (Alve and Murray, 1994). Indeed, the
same holds true for Stainforthia fusiformis which is a wellknown opportunistic species in European waters (Alve,
1994). In the earlier study, Quinqueloculina spp. and Fissurina sp. were recorded only as unstained (dead) individuals and were considered to have been transported into the
area in suspension. It is now clear that the reason why we
did not record them living at that time is because they are
ephemeral colonizers which reproduced there especially
during the summer and autumn. This is probably linked to
the greater penetration of the salt wedge during the drier
summer months. A similar pattern was recorded for Quinqueloculina dimidiata in Christchurch Harbour (Murray,
1968). At least three species show blooms following summer colonization: E. williamsoni, F. lucida and Q. dimidiata and when they were present they occurred in both replicates showing that their occurrence was not patchy.
The great difference in number of species present during
different times of the year is evident in Fig. 9. Similar records are available for a few other areas in which time series
studies have been carried out for at least one year: Bottsand
lagoon, Germany 2–8 species (Lutze, 1968), Samish Bay,
USA, a maximum of 10 species but only 2–5 present at any
one sampling event (Jones and Ross, 1979), 28 species
found living in 1961 samples but by 1970 the number had
increased to approximately 65 (Boltovskoy and Lena, 1970),
an increase in H(S) from 0.1 to 1.6 in the intertidal zone,
Bahrain (Basson and Murray, 1995). Unfortunately, in most
studies temporal variation in diversity is not discussed, yet
it is clear from these few results that the variability is very
large. For studies where sampling is so infrequent that the
temporal variabilities in species diversity are not recorded,
only a partial record will be obtained and the season of
sampling will have a significant influence on the number of
22
ALVE AND MURRAY
species found. This partly explains why, in most environments, the species diversity of the (time-averaged) dead assemblage invariably exceeds that of the living assemblage
recorded at any one time.
The mechanisms of colonization of azoic environments
have been shown to be passive dispersion (either physical
or biological disturbance of the source area) and transport
(in suspension at various growth stages) with the transit time
dependent on the current energy of the environment (Alve,
1999). The same processes must operate even when the environment is already inhabited by a range of taxa. In this
area, tidal currents are vigorous as the area is meso-macrotidal. It might be assumed that the transit time would be
short (days) and colonization fairly rapid once conditions
were favorable.
Species diversity is one of the principal univariate methods used to assess both natural variability and possible human impacts on marine soft bottom ecosystems (e.g., Coull
and Chandler, 1992). In any particular environment, human
impacts tend to reduce the species diversity. For example,
the ranges of the Shannon-Wiener index and Hurlbert’s index for soft bottom macrofauna are included in the assessment of Norwegian environmental quality on a scale from
very good to very poor (Molvær and others, 1997). Similar
ranges have not yet been established for benthic foraminifera but in setting them up account would have to be taken
of the large seasonal variability such as that recorded in the
present study.
COMPARISONS
WITH OTHER
AREAS
What attributes of the Hamble Estuary make it suitable
for the three species, H. germanica, A. beccarii and E. excavatum to become dominant? In adjacent estuaries the
combinations of dominant species differ and may include
one or more of E. williamsoni, Nonion depressulus, Miliammina fusca and Reophax moniliformis (Murray, 1968).
Elphidium williamsoni may not be dominant here because
of a combination of the generally high salinity (mainly ⬎30
psu) and the high mud content of the sediment (63–74%)
as elsewhere it has been found not to tolerate mud values
⬎60% (Langer and others, 1989; Alve and Murray, 1999).
Miliammina fusca is very euryhaline (Murray, 1991) but
occurs on a wide range of substrates (Alve and Murray,
1999). Nonion depressulus is an inner shelf species common only on sandy substrates and is not tolerant of very
reduced salinities (Murray, 1983). Off southern Norway it
occurs on sandy sediment with ⬍12% mud and ⬍1% TOC
(Alve and Murray, 1999). Other studies have shown that
there is no direct correlation between individual environmental variables and species distributions (e.g., Buzas and
Severin, 1993). Thus, the combination of dominant taxa in
each area depends on the local, often subtly different, environmental characteristics.
CONCLUSIONS
The distribution of live (stained) foraminifera has been
determined with respect to abundance, depth of life in the
sediment (down to 4 cm), and species diversity in replicate
samples from two intertidal stations sampled 0–1 cm
monthly over 27 months and 0–4 cm over the first 14 of
these months. The following conclusions can be drawn
based on the combined results from the pairs of replicates:
● The same three species (Haynesina germanica, Ammonia beccarii (tepida), Elphidium excavatum) were dominant at both stations, the maximum abundance of all species
(dominant and subsidiary) was in the surface 0.25 cm, and
there was a general lack of seasonal change in the vertical
distribution of the foraminifera. The absence of a consistent
seasonal pattern for both stations indicates that seasonality
is not a controlling factor for the vertical distribution of
individuals in this area.
● In contrast to many subtidal areas none of the foraminifera in this intertidal environment showed high subsurface abundances.
● When measured, the redox boundary was at 0.3 and 1
cm at sta. 2 and sta. 1 respectively below the sediment surface yet the large majority of individuals lived in the surface
0.25 cm thus indicating that this boundary was not the main
factor limiting their down-core abundance. The generally
high dominance of individuals in the surface few millimeters was probably related to the presence there of microalgal
food.
● The total number of stained hard shelled species found
over the 27 month sampling period was 35 (plus at least 3
soft shelled forms) although the number recorded during one
sampling event ranged from a minimum of 5 to a maximum
of 22. Subsidiary species colonized the area ephemerally,
thus the number of species recorded varied from one season
to another. Over a longer period of time other ephemeral
species might be introduced into the area thus increasing the
total number of species recorded.
● The mechanisms of colonization include passive dispersion and transport from the source area, with the transit
time dependent on the current energy of the environment.
In this case, transit time is likely to be short (days), due to
the tidal currents, and colonization fairly rapid once conditions were favorable.
● Species diversity is one of the principal univariate
methods used to assess both natural variability and possible
human impacts on marine soft bottom ecosystems. Human
impacts tend to reduce the species diversity but, in assessing
the significance of diversity changes, caution should be exercised to take into account the large natural seasonal variability such as that recorded in the present study.
ACKNOWLEDGMENTS
We are grateful to Daphne Woods for assistance in the
field and to Helen Cussens for performing the microelectrode oxygen profiles.
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Received 29 November 1999
Accepted 19 June 2000
FAUNAL REFERENCE LIST
Generic names are in accordance with Loeblich and Tappan (1987).
The named species plus Stainforthia sp. are illustrated in Plates 1 and
2 (or in Alve and Murray, 1994; Murray and others, 2000).
Ammobaculites balkwilli Haynes, 1973
Ammonia beccarii (Linné) forma tepida Cushman ⫽ Rotalia beccarii
(Linné) var. tepida Cushman, 1927
Ammoscalaria runiana (Heron-Allen and Earland) ⫽ Haplophragmium runianum Heron-Allen and Earland, 1916
Aubignyna hamblensis Murray, Whittaker and Alve, 2000
Bolivina pseudoplicata Heron-Allen and Earland, 1930
Bolivinellina pseudopunctata (Höglund) ⫽ Bolivina pseudopunctata
Höglund, 1947
Brizalina variabilis (Williamson) ⫽ Textularia variabilis Williamson,
1858.
Bulimina gibba/elongata Fornasini, 1902/d’Orbigny, 1846
Buliminella elegantissima (d’Orbigny) ⫽ Bulimina elegantissima
d’Orbigny, 1839 Cassidulina obtusa Williamson, 1858
Cuneata arctica (Brady) ⫽ Reophax arctica, Brady 1881
Cornuspira involvens (Reuss) ⫽ Operculina involvens Reuss, 1850
Eggerelloides scaber (Williamson) ⫽ Bulimina scabra Williamson,
1858
Elphidium excavatum (Terquem) ⫽ Polystomella excavata Terquem,
1875
Elphidium margaritaceum Cushman, 1930
Elphidium oceanensis (d’Orbigny) ⫽ Polystomella oceanensis
d’Orbigny, 1826
Elphidium williamsoni Haynes, 1973
Fissurina lucida (Williamson) ⫽ Entosolenia marginata (Montagu)
var. lucida Williamson, 1848
Haynesina germanica (Ehrenberg) ⫽ Nonionina germanica Ehrenberg, 1840
Hopkinsina pacifica Cushman, 1933
Miliammina fusca (Brady) ⫽ Quinqueloculina fusca Brady, 1870
Nonion depressulus (Walker and Jacob) ⫽ Nautilus depressulus Walker and Jacob, 1798
Paratrochammina (Lepidoparatrochammina) haynesi (Atkinson) ⫽
Trochammina haynesi Atkinson, 1969
Quinqueloculina dimidiata Terquem, 1876
Stainforthia fusiformis (Williamson) ⫽ Bulimina pupoides d’Orbigny
var. fusiformis, Williamson, 1858
Textularia tenuissima Earland, 1933