Journal of Foraminiferal Research, v. 30, no. 3, p. 177–191, July 2000
MAJOR ASPECTS OF FORAMINIFERAL VARIABILITY (STANDING CROP AND
BIOMASS) ON A MONTHLY SCALE IN AN INTERTIDAL ZONE
JOHN W. MURRAY1
AND
ELISABETH ALVE2
press). Because time series studies are labor-intensive, there
have been relatively few on benthic foraminifera and none
involving monthly sampling has lasted for more than two
and a half years.
Temperate intertidal environments are subject to cyclic
climatic seasonality, and the biota should respond to this.
In common with other environments, they are sensitive to
environmental impact and to environmental change. They
therefore serve as good areas for investigation. Also, they
are readily accessible for sampling. However, there is a potential problem of evaluating the results if variability masks
any underlying cyclicity (Murray, in press). Several time
series studies have been based on monthly sampling and by
far most of them are from intertidal to shallow subtidal environments (Table 1).
Samples were collected monthly over more than two
years (27 months), with two replicate cores from each of
two stations. Major faunal features, such as temporal variability of the standing crop, dominant species, and species
diversity of the assemblages in the top 1 cm of sediment,
the size distribution and biomass of the three dominant species, and the recognition of cyclicity are discussed in this
paper. The focus is on the top 1 cm of sediment because
from the data presented by Alve and Murray (in press), it
can be seen that over a one year period, on average 77–79%
(leave as is of the living fauna of the top 4 cm of sediment)
was found in this interval.
In a separate paper, Alve and Murray (in press) discuss
the temporal variation of the foraminiferal depth distribution
patterns in the top 4 cm of sediment (with 4 slices in the
0–1 cm interval, and 1 cm slices down to 4 cm) based on
monthly sampling over a period of 15 months. This includes
a very detailed analysis of seasonal microhabitat partitioning
with respect to depth in the sediment (0.25 cm slices in top
1 cm, then 1 cm slices to 4 cm), the ephemeral colonization
of the area by species not permanently living in the area,
and compilation of a complete list of species found living
in the area during the survey period. The dominant species
in the study area were Ammonia beccarii (Linné) (forma
tepida Cushman), Elphidium excavatum (Terquem) and
Haynesina germanica (Ehrenberg). They are illustrated in
Alve and Murray, 1994, plate 1, figs. 1–2, 4, and 5 respectively.
ABSTRACT
Temporal and spatial variability of intertidal benthic
foraminiferal assemblages in the surface (0–1 cm) sediments have been determined by a time series survey (27
months) of the Hamble estuary, southern England. One
pair of replicates was collected each month from two
stations at different elevations in the intertidal zone. The
assemblages were dominated by three species, Haynesina
germanica, Ammonia beccarii (forma tepida), 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 study clearly
shows the need for replicate sampling in order to obtain
reliable information especially on absolute abundance
data. The absence of juveniles is due to loss through drying the samples prior to picking. The results show that
it is not possible to determine the lifespan of continuously reproducing species (i.e., young individuals always
present) where it is impossible to follow the growth of
cohorts, and for the same reason it is not possible to
make production calculations. While there is a cyclicity
in standing crop at station 2 (mid intertidal zone), this
is not the case at station 1 (lower intertidal zone). Species
diversity showed reasonable annual cyclicity at both stations. At neither station is there any correlation between
the size of the standing crop and the chlorophyll a content of the surface sediment. There was some cyclicity in
the peaks of biomass (only determined for sta. 1) in all
three species and considerable variability from one year
to the next. Thus this area is extremely variable, there
is no obvious annual pattern in standing crop, and the
best measures of seasonality seem to be species diversity
and biomass.
INTRODUCTION
The aim of ecological studies is to determine the relationship between the biota and the environment. Most ecological studies of benthic foraminifera are spatial (samples
collected over a geographic area once or a few times) and
give an instantaneous or arbitrary picture of the environmental conditions in an area. Other studies are temporal
(samples collected regularly from one or a few sites over an
extended period of time) and show dynamic, often seasonal
change. The aim of such studies is to measure variability
and cyclicity of the environment and the biotic response
through time. This is important in contributing not only to
ecological understanding but also to such features as environmental impacts and environmental change (Murray, in
DESCRIPTION OF THE ENVIRONMENT
The study area is the intertidal zone of the Hamble estuary at Warsash, Hampshire, England (Alve and Murray,
1994, Fig. 1, W5–W8). The diurnal tidal pattern is unusual:
the flood tide has a duration of around 6 hours, then there
is a period of around 3 hours when the tide remains high
followed by a 4 hour ebb tide. The extreme tidal range is
around 4.9 m but mean spring tides are 4 m and neap tides
2 m (Kent and Ridge, 1994). The sample sites have different
1 School of Ocean and Earth Science, Southampton Oceanography
Centre, European Way, Southampton SO14 3ZH, England.
2 Department of Geology, University of Oslo, PO Box 1047 Blindern, N-0316 Oslo, Norway.
177
178
MURRAY AND ALVE
TABLE 1.
Long term (ⱖ1 yr) studies of live (stained) benthic foraminifera.
Environment
Duration
of study
(months)
Time
Japan
Japan
Nova Scotia
Baltic
1450 m
1450 m
Intertidal
1–30 m
36
46
38
31
1991–1993
Mar. 91–Dec. 94
Sep. 75–Aug. 78
Dec. 64–Jun. 67
England
Argentina
Argentina
Bahrain
California, USA
Intertidal
Intertidal
Intertidal
Intertidal
3.2 m
31
26
26
25
24
Jan. 79–Jul. 81
Apr. 61–May 63
Feb. 64–Mar. 66
Feb. 91–Feb. 93
Sep. 75–Aug. 77
13 times
19 times
irregular
monthly,
bimonthly
monthly
weekly
weekly
monthly
weekly
Baltic
Spain
Cape Cod, USA
Adriatic
Chesapeake Bay, USA
Jamaica
Washington, USA
England
Subtidal
Intertidal
Intertidal
3–35 m
7–10 m
0–3 m
Intertidal
Intertidal
23
21
14
14
12
12
12
12
Jul. 73–May 75
Apr. 84–Dec. 85
Aug. 56–Sep. 57
Sep. 67–Oct. 68
Dec. 65–Nov. 66
Nov. 69–Oct. 70
Apr. 76–Mar. 77
Sep. 59–Aug. 60
monthly
monthly
bimonthly
monthly
monthly
monthly
2 monthly
3 monthly
Area
lengths of subaerial exposure (sta. 1, 1.5 m above chart datum, exposed 561 times per year; sta. 2, 2.2 m above chart
datum, exposed 700 times and for around 1 hour more per
tidal cycle than sta. 1). The low discharge from the River
Hamble has very little effect on the salinity at Warsash
which is commonly ⬎30‰ (Webber, 1980). 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 on the mid to upper intertidal zone
when the tide is out; this affected sta. 2 but not sta. 1. The
area is moderately well sheltered from severe wave activity
and there is no evidence of contemporary erosion. Although
the estuary has a large number of yacht berths, the water
quality is ‘good’ according to EC standards (monthly data
for the duration of sampling were posted on the quayside at
Hamble-le-Rice). A more comprehensive outline of the environment is given in Alve and Murray (1994). A survey
of nutrients in Southampton Water from March 1995 until
February 1997 showed elevated levels of nitrate and phosphate which were described as hypernutrification (definition:
an increase in nutrient concentrations within a body of water
should be termed hypernutrification, while the term eutrophic has come to be applied to those waters where the increase is considered likely to produce deleterious changes
in the ecosystem) (Hydes and Wright, 1999). Short-lived
blooms of phytoplankton (⬍ two weeks and developed only
at neap tides) utilized some of the nitrate and phosphate but
oxygen depletion during periods of high organic productivity did not take place due to vigorous tidal mixing. The
nutrient-rich plume affected not only Southampton Water
itself but also adjacent areas such as the Hamble estuary.
The widespread development of carpets of Ulva and Enteromorpha during the summer months must also be controlled
by the nutrient supply. Floating and drifting macroalgal
masses are considered by some as indicators of coastal eutrophication (Sundbäck and others, 1996, and references
Sampling
frequency
Sediment
thickness
(cm)
Reference
15
15
1
5
Kitazato & Ohga, 1995
Ohga & Kitazato, 1997
Scott & Medioli, 1980
Lutze, 1968
1
not stated
2
1
not stated;
plus algae
not clear
1
1
1
2
4
15
1
Murray, 1983
Boltovskoy, 1964
Boltovskoy & Lena, 1969
Basson & Murray, 1995
Erskian & Lipps, 1987
Wefer, 1976
Cearreta, 1988
Parker & Athearn, 1959
Daniels, 1970
Buzas, 1969
Buzas and others, 1977
Jones & Ross, 1979
Murray, 1968
therein). There are no published data on the annual contribution of organic carbon to the sediment.
METHODS
CHOICE
OF
SAMPLING SITES
From the preliminary faunal studies carried out by the
authors in 1992 (Alve and Murray, 1994), two sites were
selected for time series study. Station 1 (⫽ W5, close to
neap low water) was selected because it is the furthest down
the intertidal zone that it is possible to sample every month
including at times of neap tides. Station 2 (⫽ W8) in the
mid intertidal zone was selected because it showed a peak
standing crop value (more than twice that of any of the other
stations) in the 1992 survey. Thus, the two stations seemed
to have contrasting features which we considered to be
worth exploring through time series studies. Both stations
lie to the south of the ferry slipway which provides a safe
way of crossing the intertidal zone as well as a stable work
area suitable for dividing up the cores immediately after
they were collected.
SAMPLING PROCEDURE
At the beginning of the survey, the position of each of
the two stations was marked with a wooden post hammered
into the sediment. Samples were collected as the tide ebbed.
At every sampling visit to each station, 2 foraminiferal and
3 chlorophyll samples were collected in short core tubes and
the area disturbed by sampling was defined with markers.
In this way monthly samples were always taken from the
adjacent untouched area. When sampling, the core tubes
were placed close together to minimize disturbance of the
surrounding area. Over the period of the study, the total area
sampled around each post was about one meter in each direction. At the higher site (sta. 2), the macroalgae resting
on the sediment surface were removed prior to sampling.
The presence/absence of this algal cover was recorded every
month.
179
MONTHLY SCALE VARIABILITY
Sediment samples for foraminiferal analysis were collected in the following way. A short core tube was pushed
into the sediment to a depth of around 6 cm. An aluminium
plate was then inserted under the core tube to slice off the
sediment. The core tube with the plate beneath was lifted
out of the sediment and the core tube carefully slid into a
core carrier where it was held in an upright position with
the bottom held against the base. The cores were carried to
the slipway where they were divided into slices as follows:
a retort stand was set up with an upward-pointing plunger
having the internal diameter of the core tube. A core in its
tube was carefully slid from the carrier onto the plunger and
the sediment slowly pushed to the top of the tube. A short
section of core tube, marked with graduations of 0.25, 0.5
and 1.0 cm was placed on top of the core tube and the
sediment core extruded into it to the desired thickness (0.25
cm, etc.). The plate was then inserted between the the core
tube and graduated tube to slice off the sample. The plate
and sample were slid off from the top of the core tube, the
graduated core tube removed, the sediment carefully transferred to a labelled wide-mouthed container, and the plate
was cleaned. The process was repeated down core until all
the required sections had been taken. All foraminiferal samples were immediately preserved in 99% ethanol.
The area studied for each sample at each station was 66.4
cm2 for January to March 1994 and 45.4 cm2 thereafter. In
January and February 1994, each core was divided into two
0.5 cm slices in the top 1 cm and three 1 cm slices from
1–4 cm. From March 1994, the top cm was always divided
into four 0.25 cm slices. Because living foraminifera were
rare deeper than 1 cm (the mean numerical density at 1–4
cm is about one order of magnitude lower than for the surface 0–1 cm of sediment), examination of deeper samples
ceased after March 1995. A similar procedure was followed
for the sediment samples used for determining the chlorophyll content. The major differences were that the core tube
was inserted only 2–3 cm into the sediment, just the top 1
cm slice was taken, and it was placed in a pot without any
preservative. From each station, a single core was collected
for sediment grain size analysis.
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.
Staining with 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. 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, only a
portion (generally ⬎300 individuals) was picked and the
standing crop numbers calculated for the whole. Species diversity was calculated for samples with ⬎100 individuals
using the Fisher alpha index (Fisher and others, 1943) and
the information function, H(S) (see Murray, 1991). A single
sample from sta. 2 (March 1995) was seived on a 38 ␮m
sieve and wet-picked for juveniles.
TABLE 2.
Conversion factors for different measures of biomass.
Measure
Unit for top 1 cm of sediment
Conversion
factor
Organic carbon
Ash free dry weight
Wet weight of organic matter
Volume
ATP
␮g 10 cm⫺2 or mg m⫺2
␮g 10 cm⫺2 or mg m⫺2
g m⫺2
mm3 10 cm⫺3
ng ATP mm⫺3
1
2
10
10
0.0033
BIOMASS
Biomass can be expressed as wet weight of organic matter
(i.e., soft body), ash free dry weight, weight of organic carbon, weight of ATP, or volume of the test. It is clearly difficult, if not impossible, to determine the wet weight of the
organic matter of foraminifera because of the test, and likewise dry weight values are too high for the same reason
(Gooday and others, 1992). Organic carbon can be determined using an infrared analyzer (Altenbach, 1987). The
volume of the test can be calculated by approximating the
shape to a sphere, oblate or prolate spheroid, cone, cylinder,
etc. according to shape (Murray, 1991). Ideally the volume
of the chambers rather than of the whole test should be used,
but this is rarely attainable with any accuracy. It is known
that the cytoplasm does not always fill all the chamber space
(Altenbach, 1987) and within the cytoplasm there are vacuoles. For this reason, DeLaca (1986) used ATP as a measure of biomass.
In this study, estimates of biomass have been made
through calculations of test volume for the three dominant
species Ammonia beccarii, Elphidium excavatum, and Haynesina germanica. The tests were almost entirely filled with
cytoplasm; although the final chamber was often empty, this
could have been the result of cytoplasm contraction during
preservation with ethanol. Size measurements from 25
monthly samples (March 1994–March 1996) from sta. 1
were made using an eyepiece micrometer on a Zeiss microscope and calibrated with a metric scale. Each unit on the
micrometer scale represents 18.2 ␮m for the magnification
used. The number of individuals measured each month
were: A. beccarii 52–337, mean 164; E. excavatum 82–336,
mean 193; H. germanica 97–623, mean 220. The three taxa
are roughly oblate spheroids. Measurements were made of
the greatest diameter for all specimens. The thickness was
measured on ⬃10 individuals of each species to calculate
the ratio between diameter and thickness. From these measurements the unit volume of specimens of each 18.2 ␮m
size class has been calculated. For each species the unit
volumes have been multiplied by the number of individuals
in each size class and summed to give biomass in mm3 per
10 cm3 for the top 0.25 cm of sediment.
In order to compare results from different studies it is
necessary to use conversion factors (Table 2). Gerlach and
others (1985) converted volume to wet weight assuming a
cytoplasm density of 1.13 g cm⫺3. They converted wet
weight to organic carbon assuming that foraminiferal cytoplasm contains 10% carbon. In this study, because of the
inherent inaccuracy of the various methods, a volume of 1
mm3 organic matter is taken as equivalent to 1 mg of organic matter; therefore, mm3 10 cm⫺3 ⫽ g m⫺2 for the top
1 cm of sediment (i.e., g 0.01 m⫺3). This is in agreement
180
MURRAY AND ALVE
FIGURE 2. Chlorophyll a measured in the top 0.5 cm of the sediment at both stations.
with Korsun and others (1998) who gave the conversion
factors as ‘wet weight of soft parts 10: ash free dry weight
2: organic carbon 1: ATP 0.0033’.
cm2), and l is the path length (1 cm) of the cuvette (container) (equation from Baker and Wolff, 1987). For each
station, two samples were measured each month. The values
used are the average of each sample pair at each station.
Sediment size analysis was carried out using the standard
sieving technique. Total organic carbon (TOC) was determined using a Carlo-Erba EA-1108 elemental analyser.
ENVIRONMENTAL VARIABLES
RESULTS
The chlorophyll content of the top 0.5 cm of sediment
was measured as a possible proxy for food for foraminifera.
The value of chlorophyll as a biomass indicator of oceanic
microscopic marine plants has been recognized for more
than 40 years (Jeffrey and Mantoura, in Jeffrey and others,
1997). Chlorophyll a is universally present in plants (Jeffrey
and Vesk in Jeffrey and others, 1997).
Each sample comprised the top 5 mm section of a core
having an area of 16 cm2. As soon as possible after collection, the sample was washed with seawater into a 50 ml
centrifuge tube, centrifuged at 3000 rpm for 10 minutes, and
the water decanted. Then 10 ml of 90% acetone/10% distilled water was added to the sediment, mixed thoroughly,
kept at 4 ⬚C in a refrigerator for 24 hours, and centrifuged
again at 3000 rpm for 10 minutes. The liquid was placed in
a spectrometer cuvette (path length 1 cm). The uv spectrophotometer was zeroed using the 90% acetone/10% distilled
water blank in a cuvette. Then the sample was measured for
the following wavelengths: 750, 664 (chlorophyll a); two
drops of 10% HCl were added to the sample and measurements made at 667 (chlorophyll a) and 750 nm. The measurement at 750 nm is a turbidity blank. It is subtracted from
the readings in order to give a more accurate reading of
absorption by pigments. Measurement after acidification allows a correction to be made so that active chlorophyll a
can be distinguished from the pheopigments of detrital plant
material.
The calculation for ‘‘active’’ chlorophyll a (i.e., corrected
for the pheopigment degradation products) in mg m⫺2 is:
ENVIRONMENTAL VARIABLES
FIGURE 1. Salinity and temperature measured between stations 1
and 2 on the ebb tide.
chlorophyll a ⫽
26.7(664o ⫺ 667A )10V
sl
where 26.7 is a constant (absorption coefficient of chlorophyll a in acetone), 664o is the absorption at 664 nm minus
that at 750 nm, 667A is the absorption at 667 nm after acidification minus that at 750 nm, V is the volume of extractant
(10 ml), s is the surface area of the sediment sampled (16
The water temperature ranged from 4.0 to 22.5 ⬚C and
salinity from 25–35 ‰ (mean 32; SD 2.8 ‰) (Fig. 1). In
the mid to upper intertidal zone, a cover of seaweeds (Ulva,
Enteromorpha) was present from late spring to autumn at
sta. 2 but not at sta. 1. The sediment was uniform downcore
(0–4 cm) and very similar at the two stations (median diameter 4.3 ␾ at both, clay and silt content 63–74%, sorting
0.8 sta. 1, 0.9 sta. 2, TOC (average for 0–4 cm) ⫽ 1.4%
and 1.5%, respectively). The sediment surface layer was
brown and varied in thickness from 0.25 to 1.0 cm at both
stations. The boundary between the brown layer and the
dark grey sediment beneath was invariably sharp at sta. 2
but commonly transitional at sta. 1. When the tide was out,
a golden-brown layer of 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. No foraminifera were observed to do this. The range of values of
active chlorophyll a was from 0 to 49 mg/m2, but most
values were in the range 0 to 10 (sta. 1) and 0 to 20 mg/
m2 (sta. 2) while the means were 8.35 (SD 10.19) and 13.35
(SD 13.68) mg m2, respectively (Fig. 2). Station 1 showed
a spring bloom in all three years (April 94, May 95, Feb.
96) while sta. 2 had it only in 1994 and 1995 (April). However, sta. 2 also showed a further bloom period from July
to November 1995.
FORAMINIFERAL SIZE FRACTIONS
No living individuals ⬍90 ␮m in diameter were recorded
in any of the replicates (dry picked). However, juveniles
were found in the 38–63 ␮m fraction which was wet-picked.
In this paper we refer to individuals ⬍150 ␮m as ‘‘young
individuals’’. There were young individuals of all three species present throughout all months (Fig. 3). Large individ-
MONTHLY SCALE VARIABILITY
181
FIGURE 4. Standing crop and standard deviation of the whole living assemblages (0–1 cm) at stations 1 and 2.
FIGURE 3. Cumulative percent of size fractions (in ␮m) at station
1 of Haynesina germanica, Ammonia beccarii, and Elphidium excavatum.
uals (⬎400 ␮m) were most common during late spring and
early summer.
STANDING CROP
AND
data for the remaining 25 months are presented as means of
the replicates for each station together with standard deviation bars (Fig. 4). The standing crop was generally higher
at sta. 2 than sta. 1 (means 469 and 274 respectively, 27
months) and there was considerable overlap between the SD
bars of neighboring months.
At sta. 1 there was no repeated annual pattern in the mean
standing crop. The lowest values were present in June–July
1994, and maximum values occurred in September to November 1994. At sta. 2 it is possible to see a broad annual
pattern with low values in summer, building up through the
winter to a maximum in the spring (Fig. 5, as a 2 point
rolling average). The mean standing crops of the two sta-
BIOMASS
Although data were collected for January and February
1994, these cores were divided into 0.5 cm slices in the top
1 cm as opposed to 0.25 cm slices for all other months.
Therefore, year 1 runs from March 1994 to February 1995
and year 2 from March 1995 to February 1996. Mean values
for the whole investigated period are from January 1994 to
March 1996 inclusive (27 months). Foraminiferal data
(mean for replicates, surface 0–1 cm) are given in the Appendix. Biologists define standing crop as biomass per unit
area but we follow common practice among those studying
foraminifera in using the term for numbers of individuals
per unit volume (or area) of sediment.
With the exception of the first two months, when only
one sample was collected at each station, the standing crop
FIGURE 5. Two point rolling average for standing crop of the
whole living assemblages (0–1 cm) for both stations.
182
FIGURE 6.
MURRAY AND ALVE
Standing crop of the three main species at both stations.
tions showed a very good positive linear correlation for
1994 (r ⫽ 0.8496, p ⬍ 0.01). However, because there was
no correlation between the two stations for 1995 (r ⫽
0.0179), the overall correlation for the whole time period
was weaker (r ⫽ 0.4853, p ⬍ 0.05).
Both stations were strongly dominated by the infaunal
taxa Haynesina germanica, Ammonia beccarii and Elphidium excavatum. At sta. 1 the dominance changed from H.
germanica throughout winter/spring to E. excavatum during
the summer/autumn (Fig. 6). Ammonia beccarii basically
followed the pattern for H. germanica but with generally
lower values. The mean standing crops (individuals per 10
cm3) over the whole investigation period for stations 1 and
2, respectively, were H. germanica 92 and 187, A. beccarii
65 and 179, and E. excavatum 82 and 66. At sta. 2, H.
germanica dominated from January to July 1994. It was
then exceeded by A. beccarii which dominated until May
1995. After this the two species were co-dominant. Elphidium excavatum was consistently of lower abundance than
the other two and showed no regular pattern of abundance.
For H. germanica at sta. 1, the peaks in relative abundance and biomass in general were out of phase with the
peaks in those larger than 400 ␮m. All three species showed
a pattern with highest relative abundances of individuals
→
FIGURE 7. Biomass of young individuals (⬍150 ␮m) and adults
(⬎400 ␮m) at station 1 (0.25 cm) for Haynesina germanica, Ammonia
beccarii, and Elphidium excavatum.
183
MONTHLY SCALE VARIABILITY
TABLE 3. Biomass (mm3/10 cm3) of the three dominant species for
the top 0.25 cm of sediment.
Species
Overall range
Overall mean
Mean yr 1
Mean yr 2
A. beccarii
E. excavatum
H. germanica
Sum of 3 spp.
0.16–2.62
0.15–2.90
0.26–3.20
0.71–7.60
1.02
1.17
1.60
3.80
0.69
0.97
1.52
3.18
1.32
1.35
1.55
4.22
DISCUSSION
FIGURE 8. Biomass of Haynesina germanica, Ammonia beccarii,
and Elphidium excavatum, and the total of the three species at station
1 (0.25 cm).
⬎400 ␮m in spring to early summer: H. germanica in
April–May, A. beccarii in May–June, and E. excavatum in
April–July (Fig. 7). The biomass for H. germanica ⬎ 400
␮m showed pronounced peaks from March to May in both
years. For the two other species the peaks were poorly developed in the first year but were clearly developed in the
second year (A. beccarii: May–June; E. excavatum: May–
July). Haynesina germanica made the greatest contribution
to the biomass for both years and the values were essentially
the same (Fig. 8). For A. beccarii year 1 biomass was only
half that of year 2, and for E. excavatum the difference was
less pronounced (Table 3). The overall range of biomass
(sum of three species) was very broad (an order of magnitude). All three species show a significant linear correlation
(p ⬍ 0.01) between standing crop and biomass over the 25
month period (A. beccarii r ⫽ 0.632, H. germanica r ⫽
0.716, E. excavatum r ⫽ 0.639). However, the correlation
between assemblage standing crop and combined biomass
of the three dominant species is less good (r ⫽ 0.432).
In most time series studies of benthic foraminifera the
changing abundance of taxa through time has been documented primarily to provide information on temporal variability rather than to seek causes of the observed changes
(see Table 1 for examples and source references). It is commonly implicitly assumed that the changes are controlled by
seasons, recognizing that these provide cyclic changes of
temperature, of food supply (in temperate areas there is
commonly a spring and an autumn bloom in sediment microalgae), sometimes of salinity, and sometimes in environmental energy. Seasonal effects (pulses of food) are known
even from deep water (Kitazato and Ohga, 1995; Ohga and
Kitazato, 1997). In the case of Glabratella ornatissima, the
species reproduces during spring and summer (times of in-
SPECIES DIVERSITY
Overall, the species diversity (surface 0–1 cm) was somewhat higher at sta. 1 compared to sta. 2. The H(S)-values
ranged from 1.08 to 1.94 (mean 1.45) at sta. 1 and from
0.66 to 1.74 (mean 1.28) at sta. 2 (data from individual
replicate cores, i.e., not means for pairs of replicates). The
number of species and the alpha-index showed a more varied pattern with values in the range 7–20 (mean 14) and
1.4–3.7 (mean 2.5), respectively, at sta. 1, and 5–20 (mean
13) and 0.7–3.3 (mean 2.1), respectively, at sta. 2. There
was a complete lack of a cyclic pattern for H(S) when expressed as mean values of the replicates for each station
(Fig. 9). For the number of species and the alpha-index, a
broad pattern can be detected with minimum values in the
spring to early summer and maximum values in the autumn.
There is a good positive, linear correlation between the
number of species and the alpha-index at both stations (sta.
1:r ⫽ 0.95, sta. 2:r ⫽ 0.96).
COLOR
OF THE
CYTOPLASM
Each of the dominant species has a different color: Haynesina germanica pale yellow through yellowish-green to
intense green, Ammonia beccarii pale yellow, Elphidium
excavatum greenish brown. The latter two have a brownish
tint due to a relatively thick organic lining.
FIGURE 9. Variation in species diversities (Alpha-index, H(S),
number of species) expressed as mean values for each pair of replicate
samples (0–1 cm) throughout the investigation period at both stations.
184
MURRAY AND ALVE
creased food supply) and the juveniles attach to algae, but
during the winter the species is dormant and seeks refuge
in the sediment to avoid death and destruction through increased wave activity (Erskian and Lipps, 1987). However,
although the physical attributes of environments may show
repetitive annual cyclicity, in other examples the biological
response is rarely so well ordered (Murray, in press). The
benthic foraminifera have ‘good’ and ‘bad’ years for reasons
that can rarely be explained (e.g., Bottsand lagoon, Baltic,
Lutze, 1968, Miliammina fusca showed modest variation
throughout the study period, whereas ‘Cribroelphidium articulatum’ had a good year followed by a bad year). In this
case, the standing crop of the assemblage followed the pattern of C. articulatum because that was the dominant species. Also, there are sometimes significant faunal changes
for which no obvious environmental cause can be given
(e.g., a sudden increase in the abundance of certain taxa and
of species diversity in the intertidal zone in Bahrain, Basson
and Murray, 1995). These results show that the biological
response to environmental change, even to natural seasonality, is complex and, as yet, poorly understood.
PATCHINESS
Both the spatial distribution and the relative and absolute
abundances of benthic organisms are affected by patchiness,
i.e., the organisms are aggregated and not uniformly distributed, and this occurs on a variety of spatial scales (Valiela,
1995). An awareness of this is particularly important when
dealing with living assemblages, as compared to fossil assemblages where the samples represent time averages. With
few exceptions (e.g., Buzas, 1968, 1970) investigations of
living assemblages have not considered possible impacts of
patchiness, as they have not analyzed replicate samples.
Here, the pairs of replicates collected each month were used
to monitor patchiness. The standard deviation of the standing crop in each pair of replicates can be considered as a
measure of patchiness in foraminiferal abundance. For some
months the SD was very small but there were some extreme
differences, for example at sta. 1, Sept. 1994 (Fig. 4A). Considering that the replicate samples were generally taken adjacent to one another, it shows that substantial spatial variability may occur on a very small scale (within cm).
There is an increase in aggregation as the abundance of
individuals increases (Buzas, 1968) and also as the size of
the study area increases (Buzas, 1970). In Rehobeth Bay,
USA, the three dominant species (the same as in this study,
A. beccarii, Elphidium clavatum (a variant of E. excavatum) and E. tisburyensis (⫽H. germanica) all showed inhomogeneous distributions with no simple pattern of high
or low abundance (Buzas, 1970). Yet the assemblage as a
whole was homogeneous over an area of 1500 m2 suggesting that the abundance of one species compensates for that
of another to give the most efficient use of habitat space.
The causes of spatial distributions are complex and poorly
understood but for small organisms they include factors
such as grazing and predation (Valiela, 1995). The meiofauna (Giere, 1993), including foraminifera, are potential food
for a variety of organisms (summarized in Murray, 1991;
Gooday and others, 1996). The main cause of pre-reproductive deaths (perhaps as much as 80%) is considered to be
predation (Buzas and others, 1989; Murray and Bowser,
2000, and references in both). Another possible cause of
variability might be the feeding activities of birds. As the
tide goes down, they walk along the water’s edge poking
their beaks into the mud searching for food. Even if they
do not eat foraminifera they undoubtedly cause sediment
disturbance and mixing.
FOOD
In the past, TOC has been commonly used as an indication of food availability but, as pointed out by Altenbach
and Sarnthein (1989), there is a better correlation between
the benthic biomass and organic material such as that derived from primary production cycles. This is because such
organic material is labile and more obviously metabolizable.
As an illustration of this, the Danish slope of the North Sea
Skagerrak basin is a region of low TOC (⬍1.5%). Nevertheless, the standing crops are high (⬎1000 ind./10 cm3)
due to abundant particulate organic detritus (Alve and Murray, 1997).
It is known that many shallow water foraminifera feed on
microalgae and bacteria (Frankel, 1975; Lee, 1980). It is
therefore reasonable to use chlorophyll a as a measure of
food availability (e.g., Erskian and Lipps, 1987). Where organisms are feeding at the same trophic level, the most obvious source of species diversity within an assemblage is
through specialization (Lee and others, 1969). Although in
this study no data were gathered on food preferences of the
foraminiferal taxa, each of the three dominant species has
different colored cytoplasm. These color differences suggest
that they have resource partitioning for food and this is supported by published observations. For example, Lopez
(1979) isolated algal chloroplasts from the cytoplasm of E.
excavatum and H. germanica and considered that these foraminifera were performing ‘chloroplast symbiosis’ where
they utilized products from photosynthesis. This was confirmed for H. germanica by Knight and Mantoura (1985),
and they also showed that Ammonia tepida, a variant of A.
beccarii, does not contain chlorophyll or husband chloroplasts. Ammonia tepida shows a strong preference for blue
green algae and avoids certain abundant diatoms, whereas
H. germanica avoids areas with ‘‘high’’ amounts of blue
green algae (Hohenegger and others, 1989). However, Goldstein and Corliss (1994) reported that the food vacuoles of
Ammonia beccarii tepida most commonly contain parcels
of sediment including organic detritus and bacteria. The bacteria are digested only in the final chamber. Minor food
elements include diatoms and other algal cells. It is speculated that the maximum abundances of big individuals of
the respective species H. germanica April–May, A. beccarii
May–June, and E. excavatum April–July (Fig. 3) reflect increased growth at particular times due to resource partitioning.
APPARENT LACK
OF
JUVENILES
In other size distribution studies of stained planispiral/
trochospiral tests, individuals smaller than about 100–120
␮m (diameter) are found to be rare even though the samples
were processed through a 63 ␮m sieve. This is the case, for
example, from areas in temperate latitudes such as the Baltic
185
MONTHLY SCALE VARIABILITY
Sea (Haake, 1967; Lutze, 1968; Wefer and Richter, 1976),
England (Murray, 1983), Japan (Matsushita and Kitazato,
1990), and from near tropical latitudes such as Bahrain
(Basson and Murray, 1995). The same pattern is recorded
here as the smallest individuals were 90 ␮m in diameter.
The absence of juveniles is due to loss during sample processing since they were present in wet-picked 38–63 ␮m
fraction. Likewise, samples washed on a 28 ␮m sieve and
dried at 50 ⬚C yielded hardly any individuals smaller than
100 ␮m (Ohga and Kitazato, 1997), and we suspect that
destruction due to drying applied here too.
REPRODUCTION
In a broad sense, size in foraminifera is an indication of
age. Consequently, measurements of test size should reveal
periods of growth and reproduction represented by polymodal size curves. In reality, this simple pattern is not always present, because for any one species, reproduction
may be more-or-less continuous. It may occur at different
stages of maturity (reproduction at various tests diameters,
Haake, 1967), and there must inevitably be variation in
growth between individuals which will cause overlap in age
groups. All these cause size distributions to be unresolvable
into age classes (Gage, 1995). The presence of young individuals (90–150 ␮m) throughout most of the year suggests
that reproduction is continuous rather than seasonal, although the rate may be slower during the winter months.
Notwithstanding this, several authors have sought reproduction patterns in these types of data although realizing that
reproduction is nearly continuous. Other studies in which
reproduction was inferred to be essentially continuous
throughout the year are those of Murray (1983) for Nonion
depressulus, Boltovskoy (1964) and Basson and Murray
(1995) for A. beccarii, Haake, (1967) and Wefer (1976) for
E. excavatum, and Cearreta (1988) for both A. beccarii and
H. germanica.
Many seasonal studies suggest that reproduction occurs
once or a few times per year (e.g., Lutze and Wefer, 1980;
Erskian and Lipps, 1987; Cearreta, 1988; Kitazato and Matsushita, 1996). In the western Baltic Sea, the life cycle of
Elphidium excavatum has been reported to last at least 20
days with reproduction throughout the year (Haake, 1967)
and about three months (Wefer, 1976). Under optimum conditions an agamont Spirillina vivipara may reproduce soon
after the 12th day, or there may be a delay of several weeks.
Both phases of the life cycle can be completed in as little
as 18 days (Myers, 1936). In the extreme case of Rotaliella
elatiana, reproduction occurred just a few hours after the
gamonts left the reproductive cyst (Pawlowski and Lee,
1992). In all these cases, there are co-ocurring individuals
at different stages of their life cycle because there is no
synchronization of reproduction. By contrast, Elphidium
crispum reproduces over a short period in March/April so
that the asexual and sexual phases each take one year (Myers, 1943). All species are influenced by a plexus of factors
which define the niche. Two factors commonly cited as important in controlling the onset of reproduction are temperature (e.g., Bradshaw, 1955, 1957; Schnitker, 1974) and
availability of food (Myers, 1943; Bradshaw, 1955; Lee and
others, 1969; Gooday, 1988). However, field studies provide
only circumstantial evidence, and experiments are known to
be influenced by culture conditions. Basically, at present it
is speculative about what controls the onset of reproduction.
In this study, the overlapping generation times and variable duration of reproductive cycles resulted in no clear pattern of a cohort of juveniles produced in one month showing
progressive size increase over the following months. Instead, young individuals were present throughout the year.
However, there was a very clear cycle in the largest individuals (⬎400 ␮m). They were nearly absent during the
winter months (dormant, or slow rate of growth?) but peaked in spring-early summer (Fig. 3). This may have been a
response to increased food availability leading to the onset
of reproduction. Rapid activation of metabolic and feeding
processes following periods of starvation has been shown
for bathyal (Altenbach, 1992; Linke, 1992; Linke and others, 1995) and probably abyssal foraminifera (Gooday,
1996). It is reasonable to assume that the same holds for
shallow water taxa (as in the present study), and these processes might initiate reproduction. The largest individuals
probably represent a delay in reproduction relative to the
last major food pulse. Such a delay was reported by Myers
(1943), who indicated that 10–22% of the megalospheric
individuals (Elphidium crispum) failed to reproduce at the
end of the first year and continued to live and grow through
the next year.
PRODUCTION CALCULATIONS
In previous studies, different approaches have been used
to calculate reproduction rates in foraminifera (see Murray,
1991 and references therein). However, estimates of production can be made only if the species present in an area
reproduce solely at certain seasons so that age classes can
be readily separated by size. Consequently, since in this area
(and probably most other areas, see cited seasonal studies),
the dominant species appear to reproduce continuously, reliable calculations of production cannot be made. Fluctuations in standing crop represent the interplay of a population
increase due to reproduction (births, B) and a decrease due
to death (D, however it is caused, including reproduction).
When B⬎D there is an increase in standing crop, and the
latter peaks when B approaches D. When D⬎B, the standing
crop decreases, and the lowest value is where D approaches
B. The methods of estimating test production depend on the
interpretation of changes in standing crop. However, it is
possible to demonstrate that the estimates of changes in
standing crop size are also dependent on the frequency of
sampling. Furthermore, they are strongly influenced by
patchiness. It follows that calculations of production (addition of dead tests to the sediment) are likewise influenced
by the frequency of sampling. Consequently, true absolute
figures can not be determined, and the figures summarized
in Murray (1991) are not not likely to be correct.
CYCLICITY
In both years macroalgae were present at sta. 2 from
April/June to September. Whereas water temperature
showed the expected annual cyclicity, other environmental
variables, for instance salinity (Fig. 1) and chlorophyll (Fig.
2), did not.
186
MURRAY AND ALVE
Annual cyclicity
Both stations showed similar patterns of variation in
standing crop in 1994, and at sta. 2 the pattern was repeated
in 1995 but this was not the case at sta. 1. There were no
obvious environmental changes at sta. 1 that explain this
difference. At sta. 2, the minimum standing crop values occurred in June when the area became covered with macroalgae, many of which were decaying. However, their presence
did not seem to be the cause of the low standing crops, as
they subsequently increased while the algae were still present (i.e., from July/August). Such algal mats do not even
seem to have a negative impact on the biomass of lightdemanding microorganisms (e.g., Sundbäck and others,
1996).
A similar pattern was found in our initial survey of the
area when there were low standing crop values throughout
the intertidal transect in June compared with the those of
March, the latter being an order of magnitude higher (Alve
and Murray, 1994, Fig. 3). The new results show that the
decrease in standing crop from March to June is repeated
each year, and therefore this is a characteristic feature of
this area. However, ordination of the monthly standing crop
data by non-metric multidimensional scaling did not produce an orderly pattern of progressive changes which would
be indicative of seriation throughout even a single year.
Thus, standing crop does not show either structured change
or cyclicity. Likewise, in a nine-month study of two stations
10 m apart in the Indian River, Florida, USA, Buzas and
Severin (1993) found that there was no overall difference in
the density of the abundant species but the periodicity was
different at each.
In other standing crop studies, some species showed a
repetitive annual cycle. For instance, intertidal Elphidium
gunteri showed cyclicity (Boltovskoy and Lena, 1969); Glabratella ornatissima showed cyclicity of gamonts on algae
and sediment and agamonts on algae (but less so on sediment) (Erskian and Lipps, 1987); in the intertidal Nonion
depressulus, cycles repeated for two years followed by a
change (Murray, 1983); and bathyal Textularia kattegatensis showed cyclicity (Ohga and Kitazato, 1997). In other
cases, the standing crop of species did not show annual cycles (Boltovskoy and Lena, 1969; Basson and Murray, 1995;
Ohga and Kitazato, 1997). When tested with analysis of
variance (single factor ANOVA, 5% confidence), the standing crop data for intertidal examples were shown to be statistically different from one year to the next (Murray in
press; data from Botsand, Baltic, Lutze, 1968; Deseado, Argentina, Boltovskoy, 1964, Boltovskoy and Lena, 1969;
Bahrain, Basson and Murray, 1995). The only example to
show repetition was the Exe estuary, England (Murray,
1983). Consequently, for most of the intertidal areas investigated so far, the standing crops were characterized by variability rather than cyclicity.
Although the pattern of reproduction is considered to be
continuous (although not necessarily at a constant rate) there
is nevertheless cyclicity in the abundance of adults with
highest values in the spring, especially in H. germanica
(Figs. 3 and 7). Species diversity, especially number of species and alpha index, showed a reasonable cyclicity at both
stations (Fig. 9). The broad trend with increasing number
of species during the summer and autumn indicates that this
temperate, intertidal area supported only a limited number
of taxa during the environmentally harsh winter months, and
that several, generally subtidal, species colonized the intertidal zone when conditions improved. Whether this occurred
in response to temperature (salinity did not show an annual
pattern) or other environmental conditions is not known, but
the data indicate that this is an annual event.
Variability
In addition to the data gathered in this survey, there is
additional information for March and June 1992 (Alve and
Murray, 1994). Whereas there was annual cyclicity in the
June values of standing crop at sta. 2 for the period 1992–
1996 as discussed above, this was not true for the March
values. These showed considerable variation (2288 per 10
cm3 in 1992 compared with mean values of 188, 587 and
764 for 1994–1996). Similarly, for sta. 1 the standing crop
figures were 695, 170, 253 and 399. Thus, not only do these
results show wide variation from one year to another, but
they also show that 1992 was an exceptionally good year
for the foraminifera in the study area.
There was considerable variability but no obvious cyclicity in the standing crop of the whole living assemblage at
sta. 1 (Fig. 4). The chlorophyll a data showed pronounced
peaks in March–May 1995 and February 1996 (Fig. 2), but
these were not matched by increases in standing crop as
might have been expected. However, these chlorophyll
peaks coincided with the periods of maximum biomass of
the three species combined (Fig. 8). This can be interpreted
as rapid growth in response to an increase in food availability, consistent with previous observations that foraminifera increase in size very quickly in response to increased
supply of food (Altenbach, 1992). However, this normally
leads to increased reproduction, but that is not obviously the
case here as the standing crop size did not increase. At sta.
2, there is a lack of correlation between chlorophyll and
standing crop (Figs. 2 and 4). Altenbach (1992) did not find
a general annual cycle in biomass for the populations of E.
incertum and E. excavatum clavatum in the Baltic.
The cyclic changes in standing crop observed in the intertidal zone at sta. 2 are remarkably similar to those described from 1450 m in Sagami Bay, Japan (Ohga and Kitazato, 1997), where there were low values in the summer
and high values in the winter/spring. Even though the standing crop at sta. 1 did not show this pattern, the biomass did
so very clearly. These observations demonstrate the overriding control of food supply on both standing crop and
biomass whether in shallow or deep water.
The underlying cause of the difference in standing crop
between the 2 stations is due to higher abundances in H.
germanica and A. beccarii at sta. 2 as the abundance of E.
excavatum was somewhat higher at sta. 1. Haynesina germanica was both abundant and dominant in the spring/early
summer at both stations followed by a major decline in
June, and the same pattern was found in the Plym estuary,
England (Castignetti, 1996). By contrast, it was abundant in
Christchurch Harbour, England, in the summer, while on the
east coast of the USA the major peak was in June (Parker
and Athearn, 1959, as Nonion tisburyense), and in both June
187
MONTHLY SCALE VARIABILITY
TABLE 4.
Environment
Intertidal
Intertidal (N. dep.)
Intertidal (A. becc.)
Intertidal (H. germ.)
Intertidal year 1 mean
Intertidal year 2 mean
Intertidal overall mean
Intertidal range
Subtidal—open (inside cages)
Lagoon
Lagoon
Shelf
Shelf
Shelf (E. incertum)
Shelf (E. excav. clav.)
Shelf
Shelf
Shelf
Shelf
Shelf
Shelf
Shelf
Shelf
Shelf
Summary of published biomass data.
Biomass
g m⫺2 (wet)
mm3 10 cm⫺2
0.31
0.1–1.77
3.37
1.32
3.18⬙
3.22⬙
3.8⬙
⬍1–7.6⬙
1–6 (2–15)
0–0.87
0.01–4.06
0.06–0.27**
0.02–2.58
0.02–2.99
0.54–16.31
0.43–4.91
8
0.32–0.49
0–0.35
0–0.62
0.01–0.31
0.04–1.41
0.32–0.8
0.13–0.35
Area
Reference
Puerto Deseado, Argentina
Exe estuary, England
Santoña estuary, Spain
Santoña estuary, Spain
Hamble estuary, England
Hamble estuary, England
Hamble estuary, England
Hamble estuary, England
Indian River, USA (experimental study)
Buzzards Bay, USA
Abu Dhabi, UAE
Arctic Sea
Baltic Sea
Baltic Sea
Baltic Sea
Kattegat
North Sea
North Sea
Vineyard Sound, USA
Off Long Island, USA
Off Cape Hatteras, USA
Celtic Sea, UK
Celtic Sea, UK
Bristol Channel, UK
Boltovskoy and Lena, 1969
Murray, 1983
Cearreta, 1988
Cearreta, 1988
This study 0–0.25 cm
This study 0–0.25 cm
This study 0–0.25 cm
This study 0–0.25 cm
Buzas, 1978
Murray, 1968
Murray, 1970b
Korsun, and others, 1998
Wefer and Lutze, 1976
Altenbach, 1992
Altenbach, 1992
Andrén and others in Gerlach, 1971
Gerlach and others, 1985*
Thomsen and Altenbach, 1993
Murray, 1969
Murray, 1969
Murray, 1969
Murray, 1979
Murray, 1970a
Murray, 1970a
* These authors measured the volume, converted it to wet wt by multiplying by 1.13, assumed that organic carbon ⫽ 10%. For the 0–6 cm
interval, they determined 4.0 mg C m⫺2. Only 20% of this was in 0–1 cm interval ⫽ 0.8 mg C m⫺2. This must be multiplied by 10 to give wet
wt ⫽ 8 g m⫺2.
** Values for 25–30 cm thick sample.
⬙ Sum of three dominant species.
and August/September for those living epiphytically but rare
on sediment (Matera and Lee, 1972, as Protelphidium tisburyensis).
Biomass
Biomass is a measure of the weight of organisms in a
given area or volume, but can also provide proxy information about the abundance of individuals with a known
weight/size range. Biomass is an important parameter because it is related to nutrient flux (Altenbach and Sarnthein,
1989), and foraminifera have a very rapid response to such
changes. Their response includes 1) increased bodymass
(e.g., mean values increased from 1.95 to 3.68 ␮g C in three
days for Cribrostomoides subglobosum and those of Elphidium excavatum increased from around 1.6 ␮g C before
to over 2 ␮g C just after the autumn phytoplankton bloom,
Altenbach, 1992) and 2) increased reproduction (e.g., Wefer,
1976; Gooday, 1988; Altenbach, 1992).
Although the results here show some cyclicity of peaks
of biomass for individual size fractions of the dominant species, there was variability from year to year (Fig. 8). Ammonia beccarii, and to a lesser extent E. excavatum, had a
poor year in 1994 compared with 1995, whereas for H. germanica, the two years were the same (Table 3). Overall,
1995 was much more favorable than 1994. The very low
biomass values in June 1994 were unusual because all three
species showed a synchronous rapid decline. No other
trough in biomass values was as extreme. The standing crop
values showed the same pattern (Fig. 4), but there was nothing unusual about the size distributions (Fig. 3). This was
probably a consequence of reproduction, but the juveniles
were not preserved in the dried ⬎63 ␮m fraction. Although
for all three dominant species there is a good correlation
between the standing crop and biomass, the correlation is
less satisfactory for the combined data because the peaks of
biomass and standing crop for each species are not always
in phase. Hence, sometimes peaks coincide and reinforce
one another. This illustrates that there is not obviously a
simple relationship between standing crop and biomass for
foraminiferal assemblages.
Summaries of published biomass values are given in
Murray (1973), Altenbach and Sarnthein (1989), and Gooday and others (1992), with a maximum value of 70 g m⫺2.
Most of the records are from the deep sea and most of the
high values are from depths greater than 500 m where analysis has been made of a relatively coarse size fraction and
often of predominantly agglutinated taxa. The results for the
top 1 cm of sediment for shallow waters, including the continental shelf, are summarized in Table 4. The ranges are
0.1–7.6 g m⫺2 for intertidal, 0.01–6 g m⫺2 for subtidal lagoon, and 1–16.31 g m⫺2 for the continental shelf. Compared with the normal subtidal environment, higher values
were obtained in screened cages which excluded predators
(Buzas, 1978). Warsash is comparable with other intertidal
areas listed in Table 4. The lack of pattern in biomass results
at Warsash is comparable with those for Elphidium incertum
and E. excavatum clavatum in the shallow waters of the
Baltic Sea (Altenbach, 1992). Not only were there big fluctuations from one month to the next but also differences
from one year to the next. Perhaps this is yet another indi-
188
MURRAY AND ALVE
cation of the inherent natural variability in intertidal and
shallow subtidal environments.
Size of Standing Crop and Elevation in the Intertidal
Zone
The data for 1992 showed an increase in standing crop
with increasing elevation in the intertidal zone (Alve and
Murray, 1994), and the same patterns occurred throughout
the present study period (with the exception of June 1992
and June–August 1995 when the standing crops were comparable). Thus, this is a long-term trend.
These results show that there is a consistent pattern of
increased higher standing crop from the lower part to the
upper part of the intertidal zone. One would expect this to
be explained by differences in availability of food, but this
is not the case here because the chlorophyll data for the two
stations are very similar (Fig. 2). The sediment grain size
and TOC are essentially the same, and the temperature and
pore water salinity regimes probably also do not differ between the two stations. However, there are differences in
subaerial exposure due to elevation (sta. 2 exposed for longer than sta. 1) and to physical disturbance from waves (sta.
1 more affected than sta. 2). These minor differences in
exposure are probably not important because the species are
infaunal.
If this increase in standing crop is a general trend, then
the significance for studies of Holocene successions, especially in relation to changing sea level, is that the middle/
upper part of the intertidal zone (below marsh level) should
produce deposits with a higher accumulation rate of foraminiferal tests in regions where the sediment is muddy.
CONCLUSIONS
A time series survey (27 months) of intertidal benthic
foraminiferal assemblages in the surface (0–1 cm) sediments of the Hamble estuary, southern England, was undertaken to determine temporal and spatial variability. Two
stations were selected at different elevations in the intertidal
zone and from each, a pair of replicates was collected each
month. This very large data set enables the following conclusions to be drawn:
The assemblages were dominated by three species: Haynesina germanica, Ammonia beccarii, and Elphidium excavatum.
Patchiness: this occurred on a scale of a few centimetres
and had a major impact on tracking temporal changes in
standing crop. This study clearly shows the need for replicate sampling in order to obtain reliable information especially on absolute abundance data.
Apparent lack of juveniles: the absence of juveniles is
due to loss through drying the samples prior to picking.
Species lifespan: from field based time series studies, it
is not possible to determine the lifespan of continuously
reproducing species (i.e., juveniles always present) where it
is impossible to follow the growth of cohorts.
Production: for the same reason it is not possible to make
production calculations.
Annual cyclicity: although there was no obvious cyclicity
in standing crop at sta. 1 (lower intertidal), species diversity
(especially number of species and alpha index) showed
some cyclicity at both stations. At neither station was there
any correlation between the size of the standing crop and
the chlorophyll a content of the surface sediment.
Biomass at sta. 1: there was some cyclicity in the peaks
of biomass in all three species and considerable variability
from one year to the next.
Although there was a positive linear correlation between
biomass and standing crop for each of the dominant species,
at assemblage level it was significant but weak.
Measures of seasonality: the best measures seem to be
species diversity and biomass.
ACKNOWLEDGMENTS
We are grateful to the following people for help: Duncan
Purdie and Leonie Dransfield for access to a spectroscope
(DP) and advice on the method of chlorophyll analysis
(both), to Daphne Woods for assistance in the field, carrying
out the chlorophyll determinations and sediment size analyses, Shir Akbari for TOC analyses, and Alexander Altenbach for discussion on the methodologies of determining
biomass. We are also grateful to the reviewers Martin Buzas
and Jan Pawlowski for constructive comments on the manuscript.
REFERENCES
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Received 12 August 1999
Accepted 19 November 1999
APPENDIX 1. Foraminiferal data in replicate samples (a, b) for surface 1 cm: standing crop (individuals per 10 cm3), biomass (mm3 per 10 cm3 for combined replicates), and diversity. NB.
Replicate samples not taken in Jan. or Feb. 1994.
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191