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Downward flux of organic matter and
pigments in Lake Kinneret (Israel):
relationships between phytoplankton and
the material collected in sediment traps
Y. Z. YACOBI* AND I. OSTROVSKY
ISRAEL OCEANOGRAPHIC AND LIMNOLOGICAL RESEARCH LTD., YIGAL ALLON KINNERET LIMNOLOGICAL LABORATORY, PO BOX
447,
MIGDAL
14950, ISRAEL
*CORRESPONDING AUTHOR: [email protected]
Received April 9, 2008; accepted in principle June 12, 2008; accepted for publication June 26, 2008; published online June 28, 2008
Corresponding editor: William Li
Sedimentation rates of organic materials and algal pigments were measured by near-bottom traps
in Lake Kinneret (Israel) throughout 2006. Pigment composition in the epilimnion and in the
traps was compared by trap-to-water indices (TWIs) based on the proportion of a given pigment
to the concentration of b-carotene. The appearance of particular pigment in traps was associated
with its ability to decompose and be transferred to the trap. The relative lability of pigments
increased in the following order: b-carotene. lutein+zeaxanthin. Chlorophyll b. Chlorophyll
a. echinenone. fucoxanthin. Chlorophyll c. peridinin. A seasonal variability, pertaining to
the thermal stratification in the lake was observed in the TWI; it showed highest values during
holomixis, and lowest after an establishment of anoxic conditions in the hypolimnion.
Bacteriochlorophyll e was one of the dominant pigments in traps from mid-July to mid-September,
when the green sulfur bacterium Chlorobium phaeobacteroides formed dense populations in the
metalimnion. Using chlorophyllous pigments as a proxy for biomass, we evaluated the possible
contribution of Ch. phaeobacteroides to the total sedimentation flux of all photosynthesizing organisms on an annual basis. The proportion of freshly fixed carbon in the downward flux changed
seasonally, depending on the composition of the phytoplankton and thermal stratification, and was
on average 22% of primary productivity at the lake centre.
I N T RO D U C T I O N
Sedimentation is a major route for removal of suspended particles from the water column, and its rate
depends on the physicochemical properties of the particles (shape, specific gravity and lability) and ambient
conditions they are exposed to (e.g. water density, viscosity, turbulence, pH, redox potential, temperature and
bacterial activity). Morphology of lakes, their thermal
structure, exposure to winds, current patterns, affect
particle distribution in the entire aquatic system (Hilton
et al., 1986), and can affect the spatiotemporal variability
of particle flux near the bottom (Hakanson and
Jansson, 1983). Planktonic organisms and their products
(e.g. feces and mucous excretions) are perpetually
produced in the aquatic environment and removed
from the water column towards the bottom sediments
by sedimentation, and also by grazing, decomposition
lysis and other biological processes. The fate of organic
components of seston is more complex than that of
minerals, as organisms and their debris may be consumed by bacteria, invertebrates and fish and decompose to soluble compounds. Organisms or their residues
leave a signature that can be traced and provide important information about processes that occurred prior
sedimentation or throughout its occurrence (Smol,
2002). The persisting fraction of settling particles can be
doi:10.1093/plankt/fbn070, available online at www.plankt.oxfordjournals.org
# The Author 2008. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]
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a microscopically identifiable cellular component (e.g.
dinoflagellate cysts and diatom frustules), or a biochemical marker. Liphophilic components of biological
membranes are particularly useful as taxon-specific
compounds, such as sterols, chlorophylls and carotenoids and are known to persist in sedimented material
for a time scale that spans from ,1 year to more than
105 years, and are, therefore, used for tracing phytoplankton (Leavitt, 1993; Leavitt and Hogdson, 2001).
The absolute rate of pigment export from the water
column towards the sediment depends on the differential rates of phytoplankton biomass production and the
rate of algal biomass decomposition, such that the
pigment suite archived in the sediment is not directly
proportional to all pigments produced in the water
column (Bianchi et al., 2002).
Chlorophyll a is common to all oxygenic phototrophs
and, therefore, can be used for the identification of
bulk of such organisms. Other chlorophylls are more
restricted in their taxonomic distribution, and therefore
can be used as signatures of some algal and bacterial
divisions. In some aquatic ecosystems, anoxygenic bacterial phototrophs may play a detectable role, and they
may be traced by the measurement of specific
pigments—primarily the bacteriochlorophylls (Imhoff,
1995). In Lake Kinneret, some anoxygenic organisms
develop dense populations in the metalimnion (Bergstein
et al., 1979; Eckert et al., 1990) and produce large
enough concentrations of pigments to be monitored by
the pigment analysis (Yacobi et al., 1990; Ostrovsky and
Yacobi, 1999). All chlorophylls are complex molecules
that upon cell death are prone to a variety of degradation steps, and formation of a whole array of degradation products (Eckard et al., 1991; Louda et al., 1998;
Matile and Hörtensteiner, 1999). These chlorophyll
degradation products absorb light in the visible range
of the spectrum and may be spectrophotometrically
identified during HPLC separations (Mantoura and
Llewelyn, 1983). The presence of chlorophyll degradation products has the potential to indicate the
occurrence of events leading to phytoplankton cell
degradation, such as grazing or cell disruption (Hurley
and Armstrong, 1990).
Although extensive work has been carried out on
pigment transformations in cultures (Spooner et al.,
1994, 1995; Louda et al., 1998, 2002), few studies have
been made in natural systems, where pigments extracted
from material collected in sediment traps were analyzed
(Hurley and Armstrong, 1990; Repeta and Gagosian,
1982). The accumulation rates of seston in sediment
traps in Lake Kinneret have shown large temporal
and spatial variability (Koren and Ostrovsky, 2002;
Ostrovsky et al., 2006). The studies on photopigments in
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the lake were focused manly on material accumulated
in surface sediments (Ostrovsky and Yacobi, 1999;
Yacobi and Ostrovsky, 2000). We, therefore, undertook
a seasonal study of dynamics of pigments in water and
sedimentation traps to understand the fate of photosynthetically produced organic material in Lake Kinneret,
with a focus on phytoplankton biomass and lability
(degradability) of different photopigments in specific
seasons.
The lake
Kinneret is a warm monomictic lake, in which homothermy occurs between late December and early March
with minimum water temperatures usually ,158C. The
lake is stably stratified from about April to September,
when the thermocline is at a depth of 15 m, and
maximum epilimnetic temperatures reaching 29 –308C.
The thermocline starts deepening in September, and
usually vanishes completely in late December, or the
beginning of January. With the onset of stratification,
the hypolimnion rapidly becomes anoxic with high concentrations of sulfide. Comprehensive description of the
light climate in Lake Kinneret, its relation to phytoplankton standing stock and productivity has been published in the past (Dubinsky and Berman, 1979). Light
attenuation coefficient, Kd, is relatively high 20.627 +
0.231 m21, and the euphotic depth of 9.27 + 2.18 m is
lower than the location of the thermocline, throughout
most of the stratified period (Yacobi, 2006). The large
centric diatom Aulecoseira granulata occasionally forms
high densities in January and February. The dominant
phytoplankton from February through May is often the
dinoflagellate Peridinium gatunense Nygaard, which forms
dense blooms and comprises more than 90% of the
algal biomass during the bloom and 59 –90% on an
annual basis. In the recent decade, however, this bloom
has not always occurred and other algae were prominent in the phytoplankton assemblage, e.g. Microcystis,
Ankistrodesmus, Carteria, Debarya. In 2006, no Peridinium
bloom was detected. Nanoplanktonic forms of chlorophytes, diatoms, cyanophytes and dinoflagellates normally dominate the assemblage from June through
January. A detailed description of the lake phytoplankton was published by Zohary (Zohary, 2004). The
annual average of chlorophyll a (Chl) concentration in
the epilimnion is 14.3 mg m23, with highest values in
April – May, and minima from August throughout
December. The annual average of primary productivity
is 1650 mg C m22 day21, and temporal variation
characterized by relatively high values in March– April
(Yacobi, 2006). The spatial variability of Chl and
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primary productivity in Lake Kinneret are small, except
for periods of P. gatunense domination (Yacobi, 2003a).
METHOD
Sediment traps were deployed in Lake Kinneret in the
deepest point of the lake (station A) where the mean
bottom depth was about 41.5 m throughout the current
study. Two sets of traps were deployed: “low” traps were
positioned approximately 1.5 m above the bottom (Alow)
and “upper” traps were deployed 9 m above the
“low” trap (Aup). Each trap set consist of four plastic
cylinders with a diameter of 5 cm and a height 50 cm.
A detailed description of the traps and their set up are
outlined elsewhere (Koren and Klein, 2000). The four
sub-samples of material collected at each time and position were pooled and subjected to further analysis.
Traps were deployed from 5 to 15 days, with the exception of the period from 11 July to 15 August 2006 when
war in the area prevented field work and forced an
exposure that lasted 35 days. Both trap sets were located
within the hypolimnion when the lake was thermally
stratified.
Water samples for pigment analysis were collected at
station A from the depth of 1 m, as representative for
the entire epilimnion because the distribution of phytoplankton in Lake Kinneret is mostly uniform, unless
Peridinium dominates the phytoplankton (Yacobi, 2006).
Taking into account that Peridinium did not form dense
populations in 2006, the same sampling procedure was
applied throughout the year. Water and sediment trap
samples for pigment analysis were prepared by filtration
of several hundred milliliters onto GF/C filters of
material collected in sediment traps and from the water
column and storage in the dark at 2188C. Using GF/
C filters for collection of particles in Lake Kinneret
0.02– 0.15% of chlorophyllous pigments were lost in
comparison to GF/F filters. However, by using GF/C
filters, we accumulate a larger concentration of particles
and thus increase the signal-to-noise ratio of the peaks
showing on the chromatogram. We, therefore, prefer
the benefit of the increased precision of the HPLC
analysis, which outweighs the issue of material loss. The
particulate material collected on the filters was processed within a week, following collection; frozen filters
were ground in 3 mL of cold 90% acetone, an
additional 3 mL of acetone was used to flush leftovers,
and the pooled extract was left overnight in the dark at
48C. Subsequently, the acetone extract was filtered
through a GF/C filter and the extract separated by a
reverse-phase HPLC, detailed description of which has
been given elsewhere (Yacobi et al., 1996). Extracts were
PIGMENT ACCUMULATION IN TRAPS
run in two rounds: one with the detector tuned at
436 nm, to enable maximal detection of all thylakoidbound pigments, and the other at 640 nm. Overlapping
of pigments is not a rare phenomenon, and our intention to gain maximal information possible on chlorophyllous pigments guided us in our decision to use
detection at 640 nm, as we have realized that small
peaks of chlorophyllous pigments often co-elute with
carotenoids. Approximately one-half of the chlorophyllous pigments appeared in minor quantities and the recognition of their presence is based on the fact that they
are detectable in the red range of the electromagnetic
spectrum. Peaks that were large enough were spectrally
analyzed on-line, and their absorption maxima and tentative identity are shown in Table I.
The spectral data of the separated peaks and their
retention times were used as the parameters for peak
identification using published data (Rowan, 1989; Jeffrey
et al., 1997). Lutein and zeaxanthin were not separated
in our HPLC system; we designate the peak as “luteinþ
zeaxanthin” throughout the current paper. Bacteriochlorophyll e was detected from July to October. This
pigment, composed of three spectrally identical
Table I: Pigments identified in samples
collected from sediment traps in Lake Kinneret,
in 2006
Retention time (min)
10.9
11.4
12.4
13.6
14.1
15.6
16.2
17.2
19.7
20.3
18.2
18.9
19.8
20.2
20.4
21.0
21.1
25.2
26.0
27.0
27.5
27.7
32.6
35.3
37.8
Peak location (nm)
433,
418,
422,
426,
434, 667
448, 634
474
467, 669
451
409, 666
409, 666
409, 666
474, 658
409, 666
442, 470
447, 477
450, 479
447, 474
474, 658
409, 666
474, 658
455, 646
430, 664
430, 664
430, 664
459
411, 664
452, 479
409, 666
Identification
Chlorophyllide a
Chlorophyll c
Peridinin
Pheophorbide a-like
Fucoxanthin
Pheophorbide a-like
Pheophorbide a
Pheophorbide a-like
BChl e2
Pheophorbide a-like
Dinoxanthin
Diadinoxanthin
Diatoxanthin
Lutein+ zeaxanthin
BChl e3
Pheophorbide a-like
BChl e4
Chlorophyll b
Chlorophyll a-allomer
Chlorophyll a
Chlorophyll a-epimer
Echinenone
Phaeophytin a
b-carotene
Pyropheophorbide a
The pigments were isolated on-line from HPLC analysis. They are,
therefore, dissolved in the HPLC eluents. Both solvents used in the
system are 70% methanol (Yacobi et al., 1996). The other components
are 1 M ammonium acetate and ethyl acetate, and show in varying
proportions, according to the time-point in the elution program.
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homologous components is a signature for the presence
of the green sulfur bacterium Chlorobium phaeobacteroides
(Imhoff, 1995; Borrego et al., 1997). The quantification
of the chromatograms was facilitated by injection of
standards of known concentrations into the HPLC
system, and calculating the response factor based on the
area under the peak. The quantification of degradation
products of Chl a was done using the same response
factor calculated for pheophorbide, since no standards
for most of those pigments were available. All pigment
concentrations were normalized on an organic matter
(OM) basis. All Chl a degradation products combined
were defined as “Total degraded Chl a” (Chl_DP).
Primary productivity is routinely monitored at station
A by the radio-carbon isotope method. Methodological
details of this measurement have been specified in detail
elsewhere (Yacobi, 2006). Transformation to values of
carbon and Chl produced were done, assuming that
carbon consists 50% of OM (Ostrovsky et al., 1997;
Eckert and Parparov, 2006).
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conditions. Thus, the pigment suite found in the Aup
traps probably best represents the population of directly
sinking particles from the euphotic zone (Ostrovsky
et al., 2006). Combination of the ratios indicated in
equations (1) and (2), led to the development of
trap-to-water index (TWI):
TWI ¼
PItrap
PIwater
ð3Þ
Pigment indices
This dimensionless index enabled direct comparison
of the relative contribution of pigment flux (using trap
material) to the relative pigment concentration in
the euphotic zone, where any specific pigment was
produced. It is important to note that the cell
( pigment) population sampled in the water column is
not necessarily identical with the population that
reaches traps at the same period of time. Still, keeping
in mind the aforementioned shortcomings of the
indices, persisting temporal patterns of their variations
can be indicative for pigment diagenesis and vertical
transport associated with given ambient conditions
and specific algal phyla.
For the sake of comparison of pigment abundance in
the water column and in the traps, we use the following
pigment indices (PI):
R E S U LT S
PIwater ¼
PItrap ¼
Cx
; mgL1 ðmgL1 Þ1
Cbcarotene
Fx
Fbcarotene
ð1Þ
; mgm2 day1 ðmgm2 day1 Þ1 ð2Þ
where PIwater is the ratio of pigment concentrations in
the water column, PItrap is the ratio of pigment fluxes
in the traps, Cx is the concentration of a given pigment in
the water column, and Fx its flux in the trap, Cb-carotene
and Fb-carotene are the concentration and flux of
b-carotene, respectively. b-Carotene was chosen for
normalization being characterized by its high stability
in the aquatic environment (Leavitt and Carpenter,
1990). Additionally, b-carotene is present in most algal
phyla (Rowan, 1989). The caveat of using b-carotene
for normalization is the uncertainty associated with the
relative cellular concentration of different pigments,
which can be species specific and prone to some variations in response to changing environmental conditions
(Mackey et al., 1996). We used pigment fluxes recorded
in the Aup traps located in the middle of the hypolimnion and at the same time above the turbulent benthic
boundary layer (BBL) to avoid the possible impact of
re-suspended material trapping under turbulent
Productivity and pigment dynamics
in the epilimnion
During 2006, primary productivity was the lowest in
January with ,700 mg C m22 day21 and peaked in
May, with 3250 mg C m22 day21 and subsequently
declined to 1000 mg C m22 day21 in November–
December (Fig. 1). Chl a content in the epilimnion
showed a limited variation, not surpassing a ratio of
1:2.4 between the lowest and highest record. The temporal variation of b-carotene was virtually synchronous
Fig. 1. Chlorophyll a content (Chl a) in the epilimnion (0–15 m
water column) and daily primary productivity (PP per day), measured
at a central station (Stn A) in Lake Kinneret in 2006.
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with that of Chl a, whereas other pigments showed
somewhat different patterns (Fig. 2). Chl a degradation
products (Chl_DP) could have been detected in the water
column mostly throughout the holomixis, from January
to March, and during that period showed a similar
pattern of temporal variability to Chl a (Fig. 2A). Chl c
and peridinin occurred in high concentration from
February to April, and subsequently their concentration
declined, following thermal stratification (Fig. 2B). The
same pattern was seen in the temporal variability of
fucoxanthin, but the peak in the winter was lower and
the concentration in the summer months was lower than
of peridinin and Chl c. Chl b and lutein+zeaxanthin,
and echinenone showed a similar pattern of temporal
change, and both showed a relatively stable concentration throughout the entire sampling season (Fig. 2C).
Representatives of four major phyla (chlorophytes,
diatoms, dinoflagellates and cyanophytes) contributed in
most measurements .90% of the algal biomass.
Chlorophytes developed relatively high concentrations
in April, reached the highest values in the beginning of
May and subsequently declined rapidly in the last week
of May. The large centric diatom A. granulata formed a
small bloom in January – February, and small pennate
diatoms prevailed in August and September. Between
April and June, several species of the dinoflagellate
genus Peridiniopsis formed small blooms in the lake.
Cyanophytes comprised a significant proportion of the
PIGMENT ACCUMULATION IN TRAPS
phytoplankton biomass (.20%) from July until the end
of November.
Sedimentation traps
Gross sedimentation rates (GSR) spanned from 0.23 to
6.24, and from 0.82 to 9.53 g dry weight m22 day21, in
the upper and lower traps, respectively. GSR showed
high values in January and from March throughout
June, and was systematically higher in the lower traps
(Fig. 3A). Organic matter content (OMC, i.e. the proportion of OM in of the total material accumulated in
sediment traps) was, on average, slightly higher in the
lower traps, but statistically not different from OMC in
the upper traps (39.1 versus 37.7%), and ranged from
17.4 to 81% in Alow, and from 15.5 to 68.4% in Aup
(Fig. 3B). There was a conspicuous reduction in the
OMC between April and June and a higher OMC in
September– November. The reduction in OMC in
April – June period is apparently associated with a dramatic increase in calcium carbonate precipitation, following increase in pH, as a result of high algal
photosynthetic activity (Koren and Ostrovsky, 2002).
The sedimentation rate of organic matter showed
similar temporal trend seen in GSR, with higher values
in the lower traps (Fig. 3C).
Chlorophyll a (Chl a) sedimentation rates varied in
Alow from 0.95 to 7.53, and in Aup from 0.32 to
Fig. 2. Concentration of pigments in the epilimnion. (A) common pigments, (B) pigments of diatoms and dinoflagellates and (C) pigments of
green and blue–green algae.
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Fig. 3. Sedimentation of particulate matter in traps positioned at a central station A in Lake Kinneret in 2006. Traps positioned 1.5–2.5 m
above the bottom are designated by the suffix “low”, and the traps deployed 9 m above the lower trap are designated by the suffix “up”. (A)
Gross sedimentation rate (GSR), (B) organic matter content (OMC) and (C) sedimentation rate of the organic material (OM).
5.35 mg m22 day21, and were consistently higher in the
lower traps. The sedimentation rates of Chl a increased
from January until mid May and then gradually declined
until December (Fig. 4). The annual average of Chl a
sedimentation rate was 3.56 and 1.69 mg m22 day21, in
the lower and higher traps, respectively. Sedimentation
rates of chlorophyll b, chlorophyll c, peridinin, fucoxanthin, lutein+zeaxanthin, echinenone and b-carotene
mostly followed the pattern showed by Chl a, i.e. higher
values in the low traps (Fig. 4). Chl b, lutein and
b-carotene were found in all samples in the traps, but
Chl c, fucoxanthin, peridinin and echinenone did not
show in the traps on all occasions (Fig. 4).
Chlorophyll a degradation products were found
mostly from January throughout March, to a smaller
extent in June – July, and still lower otherwise (Fig. 5).
The number of different Chl_DP detected on chromatograms varied from 0 to 27 and was usually higher in
the lower traps than in the upper traps and the lowest
in the water column samples (Fig. 5A). The proportion
of Chl_DP to chlorophyll a (mass-to-mass ratio) altered
temporally likewise the number of peaks of Chl_DP
(Fig. 5B), i.e. larger concentrations of Chl_DP were
associated with higher number of those compounds,
and the two variables were positively correlated, with
r 2 ¼ 0.68 (n ¼ 197, P , 0.01).
From the end of July to the end of September, when
the lake was strongly chemically stratified and H2S was
found in the low metalimnion, high fluxes of bacteriochlorophyll e (Bchl e) were measured. Bchl e appeared in
the sediment traps a short time after its appearance was
detected at the top of the metalimnion (Rimmer et al.,
2008). Temporal change in Bchl e sedimentation rate
was similar in the lower and upper traps, but different
from that of Chl a (Fig. 6). Like other organic compounds, higher sedimentation rates of Bchl e were
detected in the lower traps.
DISCUSSION
Pigment diagenesis
The varying proportion between pigments seen in sediment traps may be accounted for by several independent processes: (i) the dynamics of phytoplankton
development in the lake, (ii) stability of cells once eliminated from the euphotic zone, (iii) differential rates of
preservation/decomposition of pigments and (iv) the
effect of re-suspension, focusing and the effects of translocation and re-disposition. We are addressing the
second and third issues by examination of the TWI,
based on normalization of pigment concentrations and
fluxes to that of b-carotene.
TWI for Chl a was mostly close to 1, and showed a
slight decrease from the end of holomixis, in March,
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PIGMENT ACCUMULATION IN TRAPS
Fig. 4. Sedimentation rates of pigments in traps positioned at a central station A in Lake Kinneret in 2006. Traps positioned 1.5–2.5 m above
the bottom are designated by the suffix “low”, and the traps deployed 9 m above the lower trap are designated by the suffix “up”.
until December (Fig. 7A). Chl c, on the other hand,
showed in most cases TWI much lower than 1, indicating rapid decomposition of this pigment on the way
from the euphotic zone to the traps. Relatively high rate
degradation of Chl c was observed in freshwater cultures
(Louda et al., 1998), and may be indirectly inferred
from measurements in natural systems (Hurley and
Armstrong, 1990; Ostrovsky and Yacobi, 1999) where
carotenoids harbored by Chl c-containing algae, are
found but Chl c is missing altogether in particles collected in sediment traps. However, it should be noted
that relatively fast degradation of Chl c is not a universal
phenomenon, as it was shown in marine cultures that
Chl c maybe less degradable than Chl a (Louda et al.,
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Fig. 5. Chlorophyll a degradation products (Ch_DP) in Lake Kinneret in 2006 epilemnetic water and sediment traps: (A) the number of
different peaks of chlorophyll a degradation products. (B) Mass ratio (mg mg21) of chlorophyll a degradation products to Chl a.
2002). Peridinin in our work displayed the same pattern
of degradability as Chl c (Fig. 7B) indicating a rapid
decomposition of dinoflagellates in the water column.
Peridinium gatunense cells in Lake Kinneret mostly decompose in the euphotic zone of the water column, although
sometimes they may reach traps intact (Zohary et al.,
1998). In our study, species of Peridiniopsis comprised the
majority of the dinoflagellate population, but there is no
reason to suspect that they are less degradable than
Peridinium (Viner et al., 1999). Fucoxanthin in our
samples was contained mainly by diatoms, which formed
relatively high concentrations in February, in June-July
and in September-November. Abrupt appearance and
disappearance is typical in the winter months in Lake
Kinneret of the large centric diatom A. granulata. This
species sinks towards the sediment rapidly, and at least
part of the sinking population includes intact cells,
which readily revive once brought to the light (SickoGoad et al., 1986; Yacobi, unpublished data). Rapid
degradation of fucoxanthin was recorded in senescing
cells in cultures (Louda et al., 2002) and in natural
systems (Repeta and Gagosian, 1982), and fucoxanthin
may be fully degraded passing through the digestive
tract of certain grazers (Descy et al., 1999). The dominant diatoms in the summer and autumn in Lake
Kinneret are small pennate forms (Zohary, 2004).
Fig. 6. Sedimentation rates of chlorophyll a (Chl a) and
bacteriochlorophyll e (Bchl e) in Lake Kinneret, from the last week of
July to the last week of September 2006.
Those small diatoms may be consumed in the upper
water column, and undergo decomposition, as seen in
the relatively low TWI of fucoxanthin from May
onwards (Fig. 7B).
TWI for Chl b and lutein/zeaxanthin showed a prominent peak in March – April (Fig. 7C), when relatively
dense populations of chlorophytes were eliminated from
the euphotic zone. During that period, the relative concentration of cyanophytes was low; therefore, we
assume that lutein was the major component of the
lutein+zeaxanthin assemblage. The high TWI of Chl b
and lutein indicates that chlorophytes, or debris originating in chlorophyte cells, accumulated in the traps
relatively to other phytoplankton that occur simultaneously in the epilimnion. During the stratified
period, the pattern changed as the TWI for Chl b and
lutein approached a value of 1, indicating preservation
of the relative proportion of chlorophyte cells of the
total phytoplankton at that time. Echinenone TWI was
mostly ,1 during the holomixis and consistently when
the lake was stratified (Fig. 7C), indicating that it is less
stable than the signature pigments of the chlorophytes.
Chl_DP (i.e. sum of chlorophyllide a, phaeophorbide
a, phaeophytin a, pyrrophaeophytin a and several unidentified compounds sharing spectral characteristics)
showed consistently TWI .1 (Fig. 7A). Chl_DP could
have been produced in the water column, and also
within traps, following sedimentation. The pattern of
degradation is also dependent on the taxonomic affiliation of the sinking phytoplankton, and on the period of
time during which degradation takes place (Louda et al.,
1998, 2002; Spooner et al., 1994, 1995). The usually
short interval used for the exposure of traps restricted
the effect of organic material degradation in the trap,
although degradation certainly went on, as seen by the
accumulation of Chl_DP, that were virtually absent in
water column during most of the study period. We did
not find any correlation between the time of sediment
exposure and the concentration of Chl_DP, indicating
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Y. Z. YACOBI AND I. OSTROVSKY
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PIGMENT ACCUMULATION IN TRAPS
Fig. 7. Trap-to-water index (TWI) calculated for various pigments in Lake Kinneret in 2006. The index was calculated for pigments, as a ratio
of the flux in the trap positioned in Aup normalized to the flux of b-carotene in the same sample, divided by ratio of pigment concentration in
the epilimnetic water normalized to the concentration of b-carotene in the same sample. (A) Chl a and Chl a degradation products; (B) Chl c,
peridinin and fucoxanthin; (C) Chl b, lutein+zeaxanthin and echinenone. HM, holomixis period.
that chlorophyll degradation (and presumably of other
organic compounds) occurred mainly on its way down
to the traps, but this is a complex process and susceptible to changes in the composition of organic matter
and the physicochemical environment in the lake.
Although TWI changed in the three defined periods
on the basis of oxygen abundance below the euphotic
zone, the stability of phytoplankton pigments appears
as follows: b-carotene. luteinþzeaxanthin. Chl b.
Chl a. echinenone. fucoxanthin. Chl c. peridinin
(Table I). That order of stability/degradation follows the
same pattern observed using a mass-balance approach
in Lake Mendota, WI, USA (Hurley and Armstrong,
1990). The latter did not include accessory chlorophylls,
but other sources indicate the relative high stability of
Chl b, and low stability Chl c (summarized in Leavitt
and Hogdson, 2001), as found in our study. This order
of pigment stability suggests also that in terms of the
phytoplankton phyla that were dominant in the current
study the order of algal preservation is: chlorophytes.
cyanophytes. diatoms. dinoflagellates, i.e. chlorophytes appeared the most enduring algal group while
dinoflagellates are the highly degradable one.
The high TWI of Chl_DP indicates preferential sedimentation of decomposed (or partially decomposed)
cells, probably by being integrated in large aggregates,
which may occur during termination of the algal
bloom. Chl_DP found in high abundance in sediment
traps in the period from January throughout March
when the water column became mixed, and also in July.
Throughout those periods Chl_DP appeared also in the
water column, and those were periods of the bloom of
Chl c containing algae crashed. On the other hand, a
sharp increase in Chl b concentration in traps in the
end of May was not accompanied by massive appearance of Chl_DP, neither in the water column nor in the
traps, indicating that chlorophytes, which harbor Chl b
may settle largely intact. This fundamental difference in
decomposition between dinoflagellates (and possibly
diatoms) and chlorophytes is probably the reason for
the good preservation of the latter in aquatic sediments
(Pollingher, 1986; Yacobi et al., 1991).
The temporal trend of TWI showed highest values
for most pigments during holomixis and lowest values
when the lake was thermally stratified and the hypolimnion was anoxic (Table I). We interpret this variation
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due to the degree of lability of different pigments and to
the capability of particles to be transported by advective
currents once removed from the euphotic part of the
water column. During holomixis, rapidly degraded pigments disappear in the fully oxygenated column once
the particles which they are associated with sink below
the euphotic zone, while slowly degraded pigments
remain and accumulate relative to their abundance in
the upper water column. In a stratified lake, the hypolimnion becomes anoxic and the suite of pigments that
originated in the epilimnion is largely preserved, as
negatively buoyant particles or cells, which pass through
the thermocline cannot be returned back by mixing
and continue their way down towards the bottom.
The contribution of green photosynthetic
bacteria to the sedimenting flux
Bchl e is a proxy for the biomass of the green sulfur
bacterium C. phaeobacteroides that inhabits strictly anoxic
environments. The average of Bchl e sedimentation rate
from mid-August to the end of September was 0.22 +
0.04 mg m22 day21. In order to evaluate the potential
role of sedimenting Chlorobium cells, we transformed
BChl e values into rates of organic carbon sedimentation. Taking into account that the photosynthetically
available radiation in the upper Lake Kinneret metalimnion does not exceed levels of 0.1 mmol photon m22 s21,
it is expected that the cellular content of photosynthetic
pigments is high, and in the calculation presented
herein we are using a ratio of 1:20 Bchl e: cellular
carbon. This number is based on the ratio between bacteriochlorophyll and protein in green sulfur bacteria
(van Gemerden, 1980; Oelze and Golecki, 1988), and is
used only as a rough estimate of the potential contribution of Chlorobium to the total budget of sedimenting
organic matter in the case of Lake Kinneret. Using the
ratio 20:1 we suggest that the contribution of Chlorobium
to the total mass of sedimenting OM, while the bacterium prevailed in the lake, was approximately 6% that of
algae. The overall annual contribution of Chlorobium to
the total pool of settling carbon associated with photosynthesizing cells in the traps, at Station A, was 1 –
1.5%. This suggests that anoxic phototrophs are not a
major component of the sedimenting organic matter in
the relatively large Lake Kinneret, in contrast to the
situation that may be found in small and shallow lakes
(Takahashi and Ichimura, 1968). In August– September,
the mean rate of decrease in BChl e content was
1.0 mg m22 day21 (Rimmer et al, 2008), i.e. about four
to five times higher than the measured sedimentation
rate in Aup. The large difference between the diminishing biomass and the biomass accumulating in the
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sediment traps indicates that Ch. phaeobacteroides could be
largely consumed by metalimetic predatory plankton
(Gophen et al., 1974), and thus be a major carbon
source that fuels the trophic chain in the metalimnion.
Contribution of algae-associated organic
carbon (OC) to the total OC
sedimentation flux
The Chl a/OM ratio was on average 3.07 and
2.79 mg mg21, in the upper and lower trap, respectively
(Fig. 8). In spite of this, the flux of OM and pigments
was notably higher in lower trap, suggesting that enrichment of the sedimenting material in the lower traps
could be a result of particle focusing. The latter could
be related with lateral transport of matter along the
sloped BBL (Bloesh, 1995; Ostrovsky and Yacobi, 1999)
and or related with over-trapping of settling material
under the turbulent condition taking place in the BBL
(Buesseler et al., 2007). This suggests that lower traps
could contain older (more degraded) material and/or
that algal material underwent further decomposition on
its way down from the upper traps to lower traps. For
the evaluation, the contribution of freshly deposited
algal cells to the bulk of sedimenting organic carbon,
we used an average ratio between algal cellular (C)
carbon and Chl a of 67:1 (APHA, 2005), understanding
that in nature this ratio varies widely (e.g. Taylor et al.,
1997). Yet, the ratio we use is similar to C: Chl a of
naturally occurring phytoplankton in Lake Kinneret in
periods when P. gatunense dominates the lake (.90%
biomass), and then it is approximately 70:1, with only
slight variation from February through June. We also
did not find much vertical variation in the cellular Chl
a content, when Peridinium was the dominant phytoplankton (Yacobi, 2003b). Our calculations indicate that
the contribution of algae-associated OC to total OC
was on average approximately 41% in Aup and 37% in
Alow. This proportion was slightly higher during holomixis (51 and 41% in Aup and in Alow, respectively) and
Fig. 8. Seasonal dynamics of the ratio of chlorophyll a/organic
carbon (OC) in traps positioned at station A in lake Kinneret in 2006.
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Y. Z. YACOBI AND I. OSTROVSKY
j
conspicuously high in periods of rapid decline of phytoplankton in the epilimnion (84 and 78% in Aup and in
Alow, respectively).
The estimated ratio of algae-associated OC sedimentation flux to PP was relatively stable throughout the
study period (Fig. 9). On the other hand, the ratio of
the total OC flux to PP varied and showed a peak in
April, which coincided with the period of maximum
productivity and maximum precipitation of calcium carbonate in the lake (Fig. 10). The average rate of OC
sedimentation rate in trap Aup was 22% of PP. The
average ratio of OC sedimentation flux to PP in Lake
Kinneret was within an order of magnitude of that
found in other lakes where material flux was measured
in traps positioned below the euphotic zone, and also
within the range found in shallow marine environments
(Table II). The peak of the ratio of OC sedimentation
flux to PP occurred in Lake Kinneret in April –May,
when a relatively dense population of chlorophytes was
eliminated from the water column. A high proportion
of settling flux to PP is characteristic for events of
during decline of algal blooms and has been reported
for other aquatic ecosystems, although mostly associated
with dominance of diatoms in the phytoplankton
(Bloesch et al., 1977; Tilzer, 1984; Lignell et al., 1993;
Nodder and Gall, 1998). The ratio of OC flux to PP is
much lower in traps in the deep-sea (Table III), most
probably due to the long distance of downward particle
travel prior to reaching the anoxic environment, in
which degradation is slowed down (Jahnke, 1996). The
lack of Chl_DP from the water column when Lake
Kinneret was strongly stratified indicates that degradation occurred mainly in the upper, oxygenated layers
Fig. 9. Proportion of organic carbon (OC) found in trap Aup to the
intensity of primary productivity (PP) in Lake Kinneret in 2006. Left:
total organic carbon (OCtotal ); right: algae-associated organic carbon
(OCalgal ). Contribution of algae-associated OC to total OC sediment
flux. The algae-associated OC was calculated on the assumption of
OC=50% organic matter, and OC: Chl a ¼ 60.
PIGMENT ACCUMULATION IN TRAPS
Fig. 10. Temporal variation of organic carbon (OC) found in trap
Aup and the intensity of primary productivity (PP) in Lake Kinneret in
2006. Indicated is the period of intensive precipitation of calcium
carbonate (CaCO3), associated with the peak of primary productivity.
HM, holomixis period.
of the water column. Small differences in the Chl a/
OM ratio found in lower and upper traps (Fig. 8) indicate that the decomposition within the anoxic hypolimnion was low, in most cases, as is also indicated by the
lack of effect of time exposure of the traps, within the
limits provided in the current work. But, degradation
occurred, as indicated by the appearance of Chl a
degradation products, when they were absent altogether
in the upper water column.
The import of organic matter to Lake Kinneret from
its tributaries is negligible, compared to the intensity of
primary production. The average autochtonous production of organic carbon in Lake Kinneret is approximately 10.5 105 ton year21, but provision of fixed
carbon by the River Jordan, the major lake channel of
water provision, is only 1.8 103 ton year21 (Kinneret
Limnological Laboratory Database, unpublished
results); therefore, the organic matter budget should be
close to balanced based on autochthonous organic
material and utilization (Hart et al., 2000). The upper
limit for the calculated export of the freshly fixed
carbon to the hypolimnion (22% of PP) is plausibly
close to the estimate of about 14 – 25% surplus of fixed
carbon over respired carbon in the 0 – 15 m euphotic
water layer of Lake Kinneret (Berman et al., 2004).
Our study indicates that the fate of OC and its phytoplankton component exported from the euphotic zone
is strongly determined by phytoplankton composition
and also depends on the thermal and chemical stratification of the lake. Lake Kinneret de-stratifies thermally
in late December or early January. This process is
characterized by nutrient enrichment imported from
bottom sediments, and is usually followed by an algal
bloom. During the earlier stage of thermal stratification
(i.e. when the hypolimnion is still suboxic), dinoflagellates were the dominant phytoplankton group, and
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Table II: Trap-to-water index (TWI) for different pigments, throughout three periods in Lake Kinneret
in 2006
Period and ambient conditions
Pigment
Signature
Chl b
Chlorophytes
Lutein/zeaxanthin
Chlorophytes+cyanophytes
Echineneone
Cyanophytes
Fucoxanthin
Diatoms
Chl c
Diatoms+dinoflagellates
Peridinin
Dinoflagellates
Degraded Chl a
All
Chl a
All
Dominant phytoplankton in the euphotic zone
January –March
Holomixis, oxic
April – June
Stratified, suboxic
September –October
Stratified, anoxic
2.6
2.6
1.2
2.4
0.3
0.5
2.9
1.3
Diatoms +chlorophytes
1.4
0.9
1.4
0.3
0.3
0.7
5.1
0.9
Dinoflagellates +chlorophytes
0.9
0.8
0.5
0.4
Not found in traps
Not found in traps
Not found in traps
0.7
Cyanophytes + chlorophytes
TWI was calculated as the ratio between a given pigment and b-carotene in traps, divided by the same ratio of pigments in the water column. The
definition of the oxic status in each period pertains to the situation below the euphotic zone of the water column.
Table III: Proportion of organic carbon delivered to sediment traps of primary production of various water
bodies
Location
Trap location beneath surface (m)
Sedimented OC/PP (%)
Source
Global oceans
Pacific Ocean
North Sea
Baltic Sea
Frobisher bay, Arctic Canada
Cariaco basin, Caribbean Sea
Lake Constance
Lake Lucerne, Switzerland
Rotsee, Switzerland
Lake Kinneret
.1000
100 –550
150
30
20
275 –1255
0.6 –2
0.5 –3.4
20 –35
72
31 –53
1 –2
30 –55
14
30
22
Fischer et al., 2000
Nodder and Gall, 1998
Davis and Payne, 1984
Lignell et al, 1993
Atkinson and Wacasy, 1987
Thunell et al., 2000
Tilzer, 1984
Bloesch et al., 1977
Bloesch et al., 1977
This study
15
5
25
those species showed a high decomposition rate prior
reaching the sediment traps. The decomposing cells left
OC in the euphotic zone, plus associated nutrients. The
nutrients, thus, maintain a quasi-stable stock in the
euphotic part of the water column and enable extensive
primary productivity in the stratified lake, despite the
restricted allochtonous supply of essential biogenic
elements and restricted recruitments from bottom sediment, following the formation of thermocline (Berman
et al., 1995). The “legacy” of nutrient retention by the
algal community in the euphotic zone from the beginning of thermal stratification to the following period
(July– December) apparently expressed by the positive
correlation between primary productivity of the average
from January to June to the average from July to
December in Lake Kinneret (Fig. 11). TWI for most
pigments decreased during period of thermal stratification with the transit from still oxidized water column
(April – May) to highly anoxic hypolimnion in October –
November, indicating enhanced degradation of pigments in the epilimnion (Table II). In the summer, the
phytoplankton is dominated by small algae (Zohary,
2004) that have lower sinking rate than the large phytoplankton cells dominating during holomixis and at the
start of thermal stratification. The phytoplankton that
prevails in the epilimnion during the summer months,
thus have a higher probability to decompose within the
epilimnion and release nutrients while being decomposed. Consequently, an almost stable level of primary
Fig. 11. The relationship between primary productivity semi-annual
(January–June versus July– December) averages in Lake Kinneret.
Data represent the period from 1972 to 2006.
1200
Y. Z. YACOBI AND I. OSTROVSKY
j
productivity prevails during the summer– autumn
months in Lake Kinneret.
PIGMENT ACCUMULATION IN TRAPS
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composition of downwelling irradiance in Lake Kinneret (Israel).
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AC K N OW L E D G E M E N T S
We thank Semion Kaganovsky and Nir Koren for field
and laboratory assistance. Dr William Louda and an
anonymous reviewer provided constructive criticism
that helped improving the clarity and quality of the
presentation.
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FUNDING
This work was partially supported by Lake Kinneret
Monitoring Program funded by the Israeli Water
Commissioner and by a research grant from the Israeli
Science Foundation (ISF Grant No. 932/04).
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