Limnol.
Oceanogr.,
26(6), 1981, 1045-1056
@ 1981, by the American
Society of’ Limnology
and Oceanography,
Loss rates from sedimentation,
the growth, nutrient limitation,
D. H. Jewson, B. H. Rippey,
Limnology
Laboratory,
Inc.
parasitism, and grazing during
and dormancy of a diatom crop
and W. K. Gilmore
New University
of Ulster,
Traad Point, Maghcrafelt,
Co. Derry,
N. Ireland
Abstract
Factors controlling
the growth and decline of a diatom crop were measured in well mixed
Lough Ncagh, Northern Ireland. Net population increase in spring was interrupted
for a short
period, due to stormy weather causing changes in the underwater
light climate. The increase
in chlorophyll
ceased when soluble reactive phosphorus was dcplctcd, while biomass continued to increase until silica reached undetectable
lcvcls. Losses due to washout (between
0.25 and 0.5% of the crop per day), parasitism (4% infestation
by chytrids), and grazing by
zooplankton
(mainly Cyclops ubyssorum Sars) were small in relation to the net population
growth rate of 4% per day. Sedimentation
rate showed a rapid incrcasc during cahn weather
at the time of nutrient limitation,
with over 00% of the population
of Melosiru itulicu (Ehr.)
Kutz. and Stephunodiscus
ustrueu (Ehr.) Grun reaching the sediment. Changes in internal
morphology
and a drop in the adenylatc energy charge from 0.81 to 0.55 indicated that these
cells formed resting stages. Decay was limited until 4 weeks later when, in association with
increased activity of the benthic fauna, 75% of the chlorophyll
a was consumed in the next
40 days. This resulted in only 1% of the population
surviving through to the following
year.
Some of the complexity
with which
aquatic ecosystems work has been ovcrlooked in recent years due to a tendency
to emphasize the role of a single factor,
such as nutrient limitation of phytoplankton. For instance, relatively
small shifts
in components further up the food chain
can have important repercussions
for algal population
dynamics
(Porter 1973,
1976; Duncan 1975; Covency et al. 1977).
So while nutrients
may give important
clues to the size of final yields, more comprehensive
information
is needed if we
wish to understand why certain species
are present and others not, why they
grow and decline when they do, and how
much is produced and to where it goes.
These questions were asked somc years
ago (e.g. Lund 1965, 1967) but, despite a
large increase in studies of production,
the success at answering them has been
somewhat
limited
(see Yentsch 1974).
This can be partly attributed to our more
limited knowledge of loss rates (see Kalff
and Knoechel
1978). These need to bc
considered
in conjunction
with factors
likely to limit both the rate of growth and
final yield (e.g. light, temperature,
nutrients, etc.).
This approach has been applied to the
growth and decline of a population of diatoms in a large (383 km2) eutrophic lake,
Lough Neagh, Northern
Ireland.
The
water is well mixed with a mean depth
of 8.9 m and a maximum of 29 m (Gibson
et al. 1971). Sampling time was reduced
to 2- or 3-day intervals during March and
April to help give an accurate timing of
events. In addition, the fate of the diatoms in the sediment was investigated,
as
the strategy of some species in forming
resting stages may be nullified
if they are
eaten by benthic invertebrates.
The resting stages were investigated
both visually, by using the descriptions
of Lund
(1954), and metabolically,
by adenylate
energy charge measurements
(Karl and
Helm-Hansen
1978).
We thank A. Fitzsimmons
for the zooplankton
counts and C. E. Gibson for
many discussions
during this work, as
well as II. McGrogan and B. Gillan for
help with the sampling and analysis.
Methods
The homogeneity
of the Lough Neagh
water column has been established (Gibson ct al. 1971; Stewart 1975), so a site in
the northwestern
corner of the lake was
chosen to permit frequent sampling. The
site was in 8 m of water; samples were
taken at 1, 3, 5, and 7 m and brought to
the laboratory for immediate analysis.
Soluble reactive phosphorus and solu-
1045
1046
Jewson et al.
ble silicon were determined in duplicate
that it was rapid enough not to change
for each sample (Golterman et al. 1978). the adenylate energy charge of the sample. These were carried out according to
The average analytical
standard deviation (Youden 1959) was 16 mM P (range the methods of Karl and Holm-Hansen
1745) and 0.7 ,uM Si (range 0.4-3.6). No (1978) with the ratio
chemical gradients in the column were
[ATP] + 1/2[ADP]
Energy =
found during sampling, so the four samcharge
[ATP]
+ [ADP] + [AMP] ’
ples were meaned. This gave standard
deviations
of 6-147, average 36 mM P,
Chlorophyll
a and pheopigments
were
extracted from 500 ml of filtered
lake
0.4-5.4, average 1.4 PM Si, and 0.5-12,
water and from 1 ml of the surface sedifor ATP analysis, average 4 pug Chl a.
ment layer (O-l-cm depth), using disposliter-l.
1061s) with
Undisturbed
sediment cores were tak- able l-ml pipettes (Sterilin
widebore
tips, into 90% methanol,
aden in duplicate with a Kajak-Brinkhurst
corer (Brinkhurst
et al. 1969), with
justed to allow for the water content of
the sample. Duplicates were taken from
monthly checks on six cores. The most
satisfactory
method
of sampling
the
two cores. The chlorophyll
a and pheomud-water
interface was to remove the
pigments were determined by the method of Riemann (1978) using acid below
water above the sediment by extruding
2 mM and neutralized
with magnesium
the core until it reached the top of the
tube. Fifty-microliter
samples were takcarbonate. All samples were scanned been immediately
with a transfer pipette,
tween 350 and 750 nm before and after
on a Perkin Elmer model
with the disposable tips cut shorter so as acidification
124. Degradation
of chlorophyll
a only
to enlarge the opening and thus avoid
became important in the surface layers
preferential
sucking up of interstitial
water. The samples were injected into 8 after the period described here.
ml of boiling McIlvaine
phosphate buffer
Estimates of grazing by Cyclops abys(Bulleid
1978) in 50-ml beakers and ex- sorum Sars were based on experiments
in which the animals were collected by
tracted for 1 min. Samples were then
net haul from the lake and
made up to 10 ml with distilled water and a vertical
centrifuged,
allowed to cool, and assayed
placed in five sets of flasks (100 ml) at
for ATP using peak height determinaconcentrations
ranging from 0 to 20 anitions (Karl and Holm-Hansen
1978) on an mals per flask. These were incubated in
S.A.I. Technology,
model 2000 ATP phothe dark at the temperature of the lake on
tometer. Five replicate samples were tak- a gently circulating
wheel (10 rpm) for
en, with ATP standards added to two to about 3 days and the decreases in numbers, filament lengths, etc. of the diatoms
check recovery. This method gave almost
compared to the control (zero animals).
complete
recovery (99%) and reduced
the variability
found with the other ex- Adjustments
were made for any loss of
traction methods tried, such as boiling
animals due to death or cannibalism.
Retris buffer and cold sulfuric acid/EDTA
suspension of cells is unlikely
as both
(Karl and LaRock 1975). The reduced
species studied enclosed their fecal pellets in peritrophic
membranes.
variability
is partly due to the saturation
of phosphate-absorbing
sites by the buffPhotosynthesis
was measured according to the in situ method of oxygen light
er (Bulleid 1978) and partly to the nature
of the sediment, which is very easily disand dark bottle technique
described by
persed, having a water content of 86% Jewson (1976), and the depth of the euphotic zone was determined
as by Jewand consisting
mainly of small organic
particles, so that thermal gradients are son (1977).
avoided (Karl and Holm-Hansen
1978).
As with all ATP extractions attention to
Results and discussion
detail is important to avoid possible inThe main factors affecting the waxing
tracellular changes in the ATP pool. The
extraction method was checked to ensure
and waning of spring diatom crops are
Diatom
growth
1047
and losses
Om
iI
9m
B
A
IO’
I
r
I
JAN
FEB
1
I
MAR
APR
Fig. 1. Increase in chlorophyll
a during spring
growth of diatoms in L. Neagh. Insets show illuminated
depth (1% light level) to mixed depth
of lake on 14 and 19 February. Left arrow indicates
date of maximum cell volume of M. it&w
and
(see Fig. 2).
right arrow maximum of S. astrueu
Units on ordinate should read pg. liter-‘.
/”
/
0’
,
first considered separately to show how
their relative
importance
varies with
time. One factor not included is temperature as changes were small, rising from
3°C at the start to 5°C by the end of the
study.
Growth and light limitation-The
cxponential
increase
in chlorophyll
a
shown in Fig, 1 is due to two diatoms,
Melosira
italica
(Ehr.) Kutz. and Stephanodiscus astraea (Ehr.) Grun (Fig. 2).
The other diatoms present were Asterionella formosa Hass and several small
Cyclotella
and Stephanodiscus
species,
but their total contribution
was never
more than 10% of the cell volume. There
were also two species of filamentous
blue-greens,
Oscillatoria
redekei Van
Goor and Oscillatoria
agardhii
Gom
(Fig. 2), but net population increase only
started in these after the diatom crop had
declined.
In a turbid lake, like L. Neagh, the initiation of net population
growth in the
spring depends on fixing sufficient energy in the euphotic zone to cope with the
metabolic
demands of being circulated
for long periods in the dark (see Jewson
1976; Jcwson and Taylor 1978), as well
as overcoming any losses of cells through
I
I
MARCH
APRIL
Fig. 2. Seasonal growth of phytoplankton
in L.
Ncagh. a. Melosiru itulicu (0) and number of cells
infected (ml-‘) by chytrids (x); note scale change,
1,000 cells *ml-’ equals about 0.6 mm3 *liter-‘.
b.
Stephunodiscus
ustrueu. c. Blue-greens
Oscillutoriu ugurdhii and 0. redekei.
sedimentation,
grazing, etc. However,
even when conditions
are good enough
to allow a net increase to start, if incoming solar radiation declines, then the increase may slow down or even stop. Such
conditions
are usually combined
with
stormy weather which leads to further
stress by decreasing
light penetration
(Jewson 1976,1977). This is the case here
where growth began in early February
with an overwintering
crop of 19 pg Chl
a *liter-l
but was checked between 19
and 23 February (see Fig. 1) when the
euphotic zone was reduced from 3.2 to
2.2 m and so the light:
dark (or
photic : aphotic) ratio of the water column
changed from 1:1.8 to 1:3.2, which precludes net population growth at this time
of year (see Jewson 1976, 1977).
More favorable conditions
rapidly returned as the suspended material settled
out and radiation increased, allowing
a
Jewson et al.
1048
MARCH
APRIL
Fig. 3. Seasonal changes of (a) chlorophyll
a,
(b) soluble phosphorus, and (c) soluble silica in L.
Neagh.
net increase to resume. The increase in
chlorophyll
a returned to the previous
rate of about 4% per day (or a doubling
time of about 2 weeks) up until maximum
crops were reached at 97 mg Chl a *rnm3.
A full analysis of the factors controlling
primary production at this season is given
elsewhere (Jewson 1976) but it is worth
considering
here the amounts of carbon
fixed for energy flow estimates and to
show the relationship
between production and standing crop. For instance at
the time of light limitation just discussed,
the gross photosynthesis
was between
0.2 and 0.3 g C *rnT2 *d-l and, presumably,
losses were just exceeding
the energy
fixed. Near the time of the peak crop (13
March 1980) the gross primary production was 1.99 g C *me2 *d-l. This was an
increase of nearly 10 times, whereas the
total biomass in the water column had
shown less than a threefold
increase
(297-801 mg Chl a.mm2). Thus the production to biomass ratio in the water column had shifted from a limiting
one, of
0.67 mg C-mg Chl a-l, to a more favorable one of 2.48.
Nutrient
limitation-The
role of nutrients in controlling
algal growth has
been outlined for L. Neagh by Gibson et
al. (1971), with more detailed reports on
the silica budget of diatoms by Dickson
(1975) and Rippey (1976) and on the effect of phosphorus limitation on the bluegreen algal population
by Gibson and
Stevens (1979). In the present study, the
depletion
of the soluble reactive phosphorus to undetectable
levels coincided
with the cessation of the chlorophyll
a
increase (Fig. 3). However, diatom biomass continued to increase (Fig. 2), and
this was reflected in further declines in
silica concentration
(Fig. 3). Melosira
italica reached its maximum population
size 10 days later when silica levels were
reduced to 11 FM. This is similar to the
situation found by Lund (1954, 1955) in
the English
Lake District
where the
same species stopped growing
before
most others. An interesting
addition to
this is that S. astraea had a faster growth
rate (doubling
time 6.8 days) and although it started off with a smaller inoculum it finished up with a population size
similar to that of M. italica
(doubling
time 12.6 days) (Fig. 2). After phosphate
became undetectable
there was no further increase in chlorophyll
a, although
the cell volume continued
to increase.
The large variability
between biomass
indicators at times of nutrient limitation
(e.g. Sakshaug and Helm-Hansen
1977)
stresses the importance of having more
than one measure.
Washout-The
retention
time of the
lake is estimated to be between 1.2 and
1.4 years (Stewart 1975). However this is
a mean figure for all seasons and so during periods of heavy rainfall the losses
from washout will be increased. For instance during
January an average of
0.57% of the total volume was lost down
the outflow every day (equivalent
to a
turnover time of about 6 months). In the
next 3 months this dropped to 0.24, 0.23,
and then 0.25% per day. Although the last
figures are unlikely to be important when
the crop is increasing by 4% per day, the
losses in washout may contribute to delays in the onset of growth on other occasions. For example, in January the rate
of increase was only about 2% per day
Diatom
growth
(see Fig. I), due to the prevailing
light
conditions, and so loss rates of 0.5% leave
the crop liable to limitation
as the result
of small shifts in grazing, sedimentation,
or increased turbidity.
Parasitism-Frequently
overlooked are
losses due to fungal parasites such as chytrids. During this study M. italica was
parasitized by Zygorhixidium
melosirae
Canter (see Canter 1967); the number of
cells infected is shown in Fig. 2a. From
early March when only 85 cells *ml-l
were infected (or 2% of total M. italica
volume) the numbers of parasitized cells
increased to over 400 cells *ml-l or 4-5%
of cell volume. This meant about every
third filament was infected, but it was
rare to find more than one infected cell
per filament, and this was usually an end
or dividing
cell. The chytrid infestation
was lower in the season reported here
than in previous years (C. E. Gibson pers.
comm.). Infestation
rates for the other
diatoms were very much lower, so it is
unlikely
that in this year losses due to
parasitism
significantly
affected succession, However, in other lakes under certain circumstances
significant
modifications of seasonal patterns
have been
found. Canter and Lund (1953) showed
up to a 79% infestation
on the diatom
Asterionella
formosa
and more recent
examples have been given by BaileyWatts and Lund (1973), Reynolds (1973),
and Youngman et al. (1976).
Zooplankton
grazing-Another
potentially important component is grazing by
zooplankton.
During the period of this
study the predominant
species were
Diaptomus
gracilis
Sars and Cyclops
abyssorum Sars (Fig. 4). Diaptomus gra&is is a recognized
herbivore,
but C.
abyssorum is usually classed as a carnivore (Fryer 1957) and the structure of the
gut as well as the nature of the mouth
parts tends to confirm this. However during the immature stages C. abyssorum
has been reported to feed hcrbivorously
(W. J. P. Smyly pers. comm.). In L. Neagh
both adult and copepodite
stages were
found during winter
and spring with
their guts full of diatoms but little or no
evidence of animal remains. To investi-
1049
and losses
&VIIO
Cabyssorum
I
I
0.grach
0
,
I
MARCH
1
APRIL
4. Seasonal
changes
in zooplankton
Fig.
ubyssorum adult fe(No:m-“).
Al Jove-Cyclops
males, adult males, and juvenile females. BelowDiuptomus
grucilis juvenile females.
gate the possible quantities
of diatoms
consumed,
we did a series of experiments in which the decrease in M. italica
concentration
was recorded over a period
of about 3 days in vessels containing
increasing numbers of adult C. abyssorum.
Figure 5 shows such an experiment.
At
this time (19 January 1979) M. italica
made up 75% of the gut contents. Estimates of the consumption rate were 1,550
cells *ind-l *d-l. This is based on the assumption that the decrease in cell numbers is linear with time, with the animals
unaffected by cell densities and limited
only by handling time, because the method of food capture is not through filter
feeding but by seizing (Fryer 1957). For
instance, in this experiment
the mean
length of filaments for the highest concentration of animals fell from 99 to 39
pm, which is a drop from about 5 to 2
cells per filament. The lake population
normally has a mean between 4 and 8
cells per filament, with some individuals
up to 20 cells. The way in which C. abyssorum feeds on M. italica has not been
determined but it is rare to find filaments
of more than 2 cells in the gut, although
up to 33% may be intact. It seems likely
that cells are “bitten”
off from the filaments but not precisely enough to rupture all the cells.
Another factor contributory
to the lin-
1050
Jewson et al.
1
6
1;
C. abyssorum (No. /lOOmI I
16
i0
Fig. 5. Decrease over 3.5 days in M. italica cell
volume with increasing concentrations
of C. abyssorum. Calculated
regression line is y = 0.837 0.028x,
?- = 0.97.
ear decrease was the relatively high density of filaments
over this period, between 227 and 1,475.mll.
This makes it
unlikely
that encounter time was limiting. There were also considerable
numbers of blue-green
filaments
present
(2,000-4,000~ml-‘),
which might be expected to interfere with the selection process, but these rarely appeared in gut
contents. As diatom numbers decline and
blue-greens increase later in the year this
may become a more significant factor.
The data from experiments such as the
one illustrated in Fig. 5 also confirms other work based on 14C labeled material
(Gilmore
unpubl.)
using gut passage
times of 40 min, which gave estimates of
a mean of 43 cells per gut “food pellet.”
In the lake, average values were 36 with
maximum
values of 129 per adult C.
abyssorum. Gut analyses also confirmed
that both the later copepodite stages (IV
and V) as well as the adults were feeding
on diatoms.
There is less information
available for
D. gracilis but the high filtering rates of
similar species (see Haney 1970) means
that they may also be important.
Numbers in the lake were low (Fig. 4), as the
maximum
population
density
reaches
over 10,000*m-3 (A. Fitzsimmons
pers.
comm.). Gut analyses showed that diatoms formed only a part of their diet but
in a control experiment with 10 D. gracilis per 100 ml, carried out at the same
time as the experiment
in Fig. 5, M.
italica
decreased to 0.48 mm3 * liter-‘.
This figure is not enough to give a precise
estimate, since in filter feeders the decline in cell numbers will be related to
cell density and is, therefore, likely to be
nonlinear (see Edmondson and Winberg
1971). However,
the fact that it is of a
similar order to the C. abyssorum consumption means that, at lake population
concentrations
(Fig. 4), D. gracilis feeding is probably responsible for losses under a half of those for C. abyssorum.
If these figures are now applied to the
situation in the lake, then at the beginning of the diatom increase (27 February
1979) a total of 1.57 X 10’ cells *mm2 or
0.05% of the population were consumed
by C. abyssorum; for comparison, the figure for the time when the diatoms were
on the decline
(30 March 1979) was
11.4 x lo7 cells .rne2. d-l or 0.15% of the
M. italica. Even with the possibility
that
D. gracilis doubled these losses, it is unlikely that grazing had much effect on the
timing of this crop. By contrast, in 1980,
when over-wintering
diatom populations
were lower (144 cells*ml-l),
grazing
probably contributed
to delaying the net
population
increase by over a month. It
seems that for at least 4 months (December-March)
diatoms form an important
element of the C. abyssorum diet.
Sedimentation
and dormancy-The
sedimentary
story is shown in Fig. 6.
This illustrates changes in chlorophyll
a,
pheopigments,
ATP, and energy charge
in the surface layers of the sediment. The
figures represent mixed samples down to
1 cm into the mud. Evidence from vertical profiles of chlorophyll
a, ATP, redox
profiles, etc. show that at this time of year
there is a sharp change between the first
and second centimeters.
Details will be
reported elsewhere (Rippey and Jewson
unpubl.), but values of ATP from l-2 cm
down in the mud are included in Fig. 6b
Diatom
gmwth
for comparison. Later in the year there is
evidence for greater mixing in the top 3
cm of sediment, but at the time of this
study the increases represent inputs from
the overlying water column only. The alternative-algal
growth in the surface
layers of the mud-is
unlikely,
since the
euphotic zone (1% light level) was never
>3 m, whereas the sample site was in a
depth of 8 m. This was chosen to be near
the mean depth of the lake (8.9 m). At
greater depths the surface layers of the
mud can become suboxic but at 8 m and
above they remained oxygenated.
Considering
the chlorophyll
a data
first, we see from Fig. 6a that during the
first half of March there was no increase
detectable in the sediments, suggesting
that losses due to sinking were minimal
during the main period of diatom biomass increase. The situation
changed,
however,
once silica bccamc limiting.
There was a major decrease in the total
phytoplankton
population
during two
very calm days (34 April), when 50% of
the M. italica
population
settled out.
There was only a 4% loss of S. astraea
during this period, followed
by a 34%
loss in the next 2 days (Figs. 2,6). Whether this was purely due to differences
in
physical settling properties of the cells or
was, perhaps, the result of a physiological
change is open to speculation and is discussed later.
It is also possible to make quantitative
estimates of the amounts of crop arriving
at the sediment surface and to compare
these with the losses from the water column ovef the same period, For instance
between 30 March and 16 April the drop
in concentration
of chlorophyll
a represents a loss of 424 mg Chl a .me2, The
increase in the sediment during this time
was 416 mg Chl a.me2. This means that
after nutrient
limitation
virtually
the
whole crop reached the bottom. This fits
in with the low loss rates in some of the
other categories, such as grazing, parasitism, and washout, at this time and also
confirms previous estimates from sediment trapping (Flower 1980).
The rise in ATP concentration
in the
sediment from late March to mid-April
1051
and losses
,
MARCH
APRIL
MAY
Fig. 6. Seasonal changes in surface layer (l-cm
depth) of sediment of L. Neagh. a. Chlorophyll
a
and pheopigments
(- - - -); vertical
bars
(-)
rcprcsent range of duplicate cores. b. ATP in surface layer (-)
with histograms denoting ATP concentration
in l-2 cm-layer;
vertical
bars denote
mean -+-SE. c. Energy charge of surface layer.
was at first believed to represent an increase in bacterial biomass. However this
is unlikely as the concentrations
of other
nucleotides,
such as GTP and UTP (see
Karl 1978), were lower than would be expected if such an increase in ATP had
been the result of bacterial growth (Jewson and Kelly in prep.). Also plate counts
made on 11 April 1979 just above the interface were low; e.g. aerobic hetcrotrophs were 550*ml-l (B. Gillan unpubl.).
Another important
indicator
was the
drop in adenylate
energy charge from
0.72 to 0.56 (Fig. 6c) as the algal material
was deposited,
although no equivalent
decrease was detected in the algal cells
still in suspension in the water, where
values remained at 0.81, within the range
(0.8-0.9) that energy charge is normally
maintained
in most healthy algal cells
1052
Jewson et al.
Fig. 7. Decline in chlorophyll
a (-)
in comparison to more stable pheopigment
levels (- - - -)
in surface sediments
of L. Neagh; vertical bars
represent range of duplicate cores.
(Karl and Holm-Hansen
1978). The fall to
between 0.5 and 0.6 may be associated
with a cessation of protein synthesis (Karl
and Holm-Hansen
1978), while lower
values still are usually indicative of a loss
of viability
(e.g. Saglio et al. 1979), with
a few exceptions (e.g. Ball and Atkinson
1975). The low values reported for L.
Neagh sediment suggest that most of the
adenylate pool is connected with a population under stress.
Another possibility
is that the value of
0.56 is the combination
of two crops of
which one has a low EC and the other a
high one. There is always a danger of this
in studies of mixed populations,
but one
final clue here is given by evidence from
the work of Lund (1954, 1955) on M.
italica in the English Lake District. He
described
the resting
stages of this
species with either two or four spherical
chromatophores
as the only readily visible cell contents. He found that if these
cells were illuminated
then recovery occurred within
2 days and cell division
was possible within 6 days. This is part
of a strategy which is very successful in
stratified conditions for the genus Melosira (Lund
1954, 1955; Stockner and
Lund 1970). It is likely that S. astraea
behaves in a similar fashion (Lund unpubl.). Cells in the mud of L. Neagh at
this time fitted Lund’s description
and
along with other evidence of no degradation of chlorophyll
and no further drop
in total adenylate pool over a period of 4
weeks, it seems likely that the diatoms
were in a resting or dormant stage.
Benthic grazing-In
a stratified lake
the situation might remain stable until
fall overturn, when the cells would normally become resuspended, but in a shallow lake with a large benthic population
(see Carter 1978) this pattern is upset.
From mid-May until mid-June the chlorophyll a content in the surface l-cm layer decreases (Fig. 7). So do ATP and total
adenylates, but at a slower rate, due to a
rise in bacterial ATP. Associated with
these changes is an increase in sediment
respiration and a movement of the redox
profile lower in the sediment (Rippey in
prep.) as a result of animal activity, so
that by the time the algal biomass is consumed in mid-June the top 2 cm are almost completely mixed.
Another point notable from Fig. 7 is the
lack of evidence
for any increase
in
breakdown
products of chlorophyll
a,
either from animal feces or decomposition. In the case of the chironomids
it is
likely that the material is deposited lower
in the sediments
(M. Ripley
pers.
comm.). In fact from the end of the period
illustrated
in Fig. 7 there is an increase
in pheopigments
but, as this is associated
with a blue-green algal deposition, it becomes impossible
to follow any further
demise in the diatoms by using chlorophyll a alone. At this time about 25%
of the population remained, but visual inspection
of the sediment
showed
a
continuous
decline after this in depths
<15 m.
Recruitment
back to the water column-To
follow the fate of the cells further we looked at the deeper areas of the
lake. In July patches of intact diatoms
were found 1 cm below the mud surface
in water depths of 19 m but not in 8 and
15 m. The chlorophyll
a (674 5’ 195
mg*me2) showed little degradation
to
Diatom
growth
pheopigments
(31 -t’ 21 mg*mP2), although the material in the surface layer
above it did (250 +’ 10 and 118 +’ 7
mg*mB2). In the latter case this was mainly associated with blue-green algal decay
and probably
some movement
of sediment from shallower depths. The survival of these diatoms is likely to be linked
to the different
animal species present
(Carter 1978). The deeper water may act
as the reservoir for later recruitment
up-‘
ward. For instance as the area of lake bottom below 18 m is approximately
0.8% of
the total, there could have been sufficient
M. italica “stored” there to represent a
concentration
of 65 cells *ml-l if distributed throughout
the lake. This figure is
low but can be put into perspective
by
comparison with events in the water column.
On 20 September 1979 there occurred
the first major storm of autumn; SW gales
up to Force 9 were recorded. On the previous day 61 cells *ml-l were found in the
water; this increased to 132 the day after.
Of these cells, only about 1 in 20 were
dividing,
so the increase was not due to
growth, and about 1 in 10 showed the
characteristic
dormant stage (Lund 1954).
Some of these cells (24%) returned to the
sediment in the next 5 days but, despite
the frequent
resuspension
and deposition of material which occurs as the result
of windy weather in this lake, no further
significant
input of viable cells was recorded. The population
then remained
more or less static for the few months
(with the cell concentration
144 *ml-l at
the end of January 1980) before growth
began again in spring. These concentrations of cells were very low, representing
only 1.2% of the previous maximum crop
and <lo% of the previous year’s inoculum (1,736 cells *ml-l) at the same stage
of the season. This means that the population was much more susceptible
to
other factors and in fact the net increase
in population
was considerably
delayed
compared to that in 1979.
Factor interaction-The
formation
of
resting stages in the sediment of stratified lakes is a useful strategy for avoiding
unsuitable
conditions
and provides the
and losses
1053
possibility
of building
up a population
over several seasons (Lund 1954, 1955).
In lakes where the bottom is actively
populated
all year round (e.g. Carter
1978) the advantage is reduced. Certainly
large returns of populations,
such as occur in stratified lakes at times of overturn,
have not been recorded (C. E. Gibson
pers. comm.); yet M. italica and S. astraea during the last 10 years have been
among the most successful
in Lough
Neagh, and paleoecological
records suggest this has been so for much longer
(Battarbee
1978). In the year reported
here, it is probable that some of the inoculum
(43%) came from the deeper
water sediments, below 18 m. In other
years, when survival has been higher,
events in spring are likely to have been
influenced
by conditions
the previous
year, such as how much animal activity
there had been, how widespread
were
anoxic conditions,
etc. It is also possible
that survival in this lake requires opposite conditions
from those in stratified
lakes where success is linked to the resting stages on the bottom. In L. Neagh the
turbulent conditions mean that it is usual
to find some M. italica
in the water
throughout
the year, and it may be that
they are less likely to be grazed there
than in the sediment.
Initiation
of a net increase in population size and the rate at which it progresses are largely controlled by the light
climate as has already been discussed,
but the factor controlling
cessation of
growth of the diatoms is the supply of silica. There have been many reports linking size of diatom crops with availability
of silica (see Gibson et al. 1971; Kilham
1975; Bailey-Watts 1976) since the classic
papers of Lund on the seasonal periodicity of diatoms in the English Lake District (e.g. Lund 1954, 1955, 1965). Lund
stressed the point that other factors may
modify
this relationship
and several
workers recently have illustrated
this by
attempting to quantify a range of environmental factors (e.g. Bailey-Watts
and
Lund
1973; Reynolds
1973; Smayda
1973; Knoechel and Kalff 1978; Youngman et al. 1976). One which has attracted
1054
Jewson et al.
a lot of attention
is sedimentation.
In
some situations, particularly
where silica
supplies are sufficient, it becomes a major determinant
of succession (Reynolds
1973, 1976u,b; Knoechel and Kalff 1975).
When considering sedimentation
it is important to distinguish
between sinking
rates of cells and loss rates from the population (see Titman and Kilham 1976). In
the present study high loss rates of about
50% of the M. italica in 2 days (Figs. 2,
6) indicated
even higher sinking rates
than the 1 m *d-l discussed
by Lund
(1954, 1959) for th is species, but it still
took nearly a month before the crop was
reduced to 5% of the maximum. In 1971
and 1972 (Jewson 1976), the population
declined at steady rates of cell loss of 6
and 3% per day; there was no sudden decrease as in 1979. This serves to illustrate
the importance of physical factors in controlling the loss rate, i.e. if turbulent conditions prevail then there is a steady loss
but in calm weather cells fall out much
more rapidly. However this only seems
to be the case after nutrient limitation;
if
calm periods occur during growth such
high losses are not recorded. The results of sediment trapping in the previous 2 years (Flower 1980) show this as
well and mean that changes in buoyancy
within cells can be important too. These
have been shown to occur in diatom cultures (e.g. Eppley et al. 1967; Titman and
Kilham
1976; Anderson
and Sweeney
1977) but their application to natural situations still has to be treated with some
caution (Lund 1959).
The possibility
of dormant or resting
stages in algae is frequently
overlooked,
mainly because of difficulties
of sampling
particularly
in the sediments. If dormancy is associated with intracellular changes,
as in some diatom species (e.g. Lund
1954), it can be relatively easily detected,
but in other groups where resting stages
may also occur (e.g. Kappers 1976), then
physiological
measures such as energy
charge may be more useful. However,
the specific conditions
need to be well
known to avoid problems in interpretation of energy charge values for the
mixed population
assemblages frequent-
ly present in sedimentary
systems (e.g.
Ulen 1976). The low activity of the benthos at the time of diatom sedimentation
in Lough Neagh was important
in our
ability to unravel the events here. The
persistence
of the algal biomass was a
surprise
as we had expected
a rapid
breakdown followed by bacterial growth.
The drop in energy charge during this
period suggested a cessation of protein
synthesis, but as it is probable that there
was some cell maintenance,
this still
needs to be confirmed by culture work.
It also means that dissolution
of the diatom frustules and a consequent buildup
of silica concentration
in the water (Dickson 1975; Rippey 1976) will not start until after the cells have been eaten.
Finally, the diversion of the major part
of the diatom population
through the
benthic rather than the planktonic
food
chain means that there are many more
possible interactions
controlling
the diatom population
than previously
supposed. The numbers, density, and distribution
as well as the activity
of the
benthic fauna will not only influence algal populations
directly, by determining
whether cells are trapped in the sediment or survive to return to the water column, but also indirectly
by influencing
the recycling of nutrients. This suggests
that improvements
in our ability to predict rather than just to interpret (see Kalff
and Knoechel
1978; Nilssen 1978) are
going to be closely linked to an increase
in integrated
sampling programs which
more closely reflect the interdependence
of trophic levels found in aquatic systems.
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Submitted:
Accepted:
10 June 1980
5 March 1981