Introduction
In the marine environment, zooplankton fecal pellets constitute a main
vehicle for transporting biogenic elements to the sediments, although a
substantial proportion of this flux is recycled or repackaged in the water
column by microbial decomposition and zooplankton coprophagy (Turner, 2002,
2015). Diatoms are among the most abundant phytoplankton, and they represent
a main component in the diet of zooplankton in marine environments. Studies
show that zooplankton with a diatom diet usually produce fecal pellets that
sink faster than those on other diets (Feinberg and Dam, 1998). Dagg et al. (2003) reported that the contribution of fecal pellets to the flux of
particulate organic carbon (POC) and biogenic silica (bSi) is higher during
the spring diatom bloom than during the summer within the Antarctic Polar
Front region. Similarly, Goldthwait and Steinberg (2008) reported an
increase in mesozooplankton biomass and fecal production and flux inside
cyclonic and mode-water eddies. However, González et al. (2007) reported
a negative correlation between the vertical carbon flux of diatoms and the
production of fecal material in a time-series study in the upwelling waters
off Chile.
The quantity and characteristics of the fecal pellets produced by
zooplankton depend on several factors. The pellet production rate is
reported to be affected by the rate of ingestion and assimilation efficiency
(Butler and Dam, 1994; Besiktepe and Dam, 2002). It has also been
demonstrated that the type of diet can affect the characteristics of the
fecal pellets produced – including size, density and sinking rates (e.g.,
Feinberg and Dam, 1998, and references therein). In addition, the decomposition
rate of pellets varies with water temperature, as well as with both
microbial and metazoan activity (Poulsen and Iversen, 2008; Svensen et al.,
2012). Factors that contribute to the sinking velocity of the pellets
include size, density and shape, all of which can vary dramatically both
among different zooplankton species and within the same zooplankton species
feeding on different types of prey (Fowler and Small, 1972; Turner, 1977;
Feinberg and Dam, 1998). Turbulence in the water column, the presence or
absence of a peritrophic membrane, and the production of microbial gas
within a peritrophic membrane might also affect the sinking rate of pellets
(Honjo and Roman, 1978; Bathmann et al., 1987). Indeed, the sinking rate and
decomposition rate are the two most important parameters used, to determine
whether a pellet will or will not be successfully transported into deeper
water before its contents are degraded. For example, a slowly sinking pellet
is more likely to decompose and become part of the recycled materials before
it exits the euphotic zone (Dagg and Walser, 1986).
The cell wall (frustrule) of diatoms is composed of two silicate shells,
which are believed to act as a defense mechanism to prevent ingestion by
grazers (Pondaven et al., 2007); thus different levels of silicification of
the frustrule might affect the grazing rate of copepods (Friedrichs et al.,
2013, Liu et al., 2016). The silica content of the cell wall of
diatoms is not only species-specific, but it is also affected by
environmental parameters such as light, temperature, salinity, pH, nutrients
and trace metals (Martin-Jézéquel et al., 2000, and references therein;
Claquin et al., 2002; Vrieling et al., 2007; Herve et al., 2012; Liu et al.,
2016). Although the frustule has no nutritional value for
zooplankton, it is thought to provide ballast, which is especially
advantageous when the fecal pellets are sinking. Hence, pellets with a high
diatom biomass generally exhibit higher levels of export of POC (Armstrong
et al., 2002; François et al., 2002; Klaas and Archer, 2002). Thus, the
content of the zooplankton diet (and therefore the type and concentration of
ballast minerals ingested) might strongly affect the sinking velocity of the
fecal pellets produced, and hence the vertical flux of biogenic silica and
carbon.
Most of the studies describing the production rates and characteristics of
copepod fecal pellets have focused on aspects such as food types (Feinberg
and Dam, 1998), or the different periods of phytoplankton blooms (Butler and
Dam, 1994). There are currently no reports that describe the effect of the
silica content of diatoms on the production, degradation and sinking of
fecal pellets. Liu et al. (2016) recently demonstrated that the diatom Thalassiosira weissflogii, when
grown at different light levels, contains varying amounts of silica and that
the small calanoid copepod Parvocalanus crassirostris, when fed diatoms containing high levels of
silica, exhibited a reduced feeding rate and stagnant growth, as well as low
egg production and hatching success. In this study we used the same diatom
species with different silica content as prey to study the characteristics
of the fecal pellets produced by the herbivorous copepod, Calanus sinicus.
Materials and methods
Copepod and prey culture conditions
The herbivorous copepod Calanus sinicus was collected
from the coastal waters around Hong Kong in February 2013. Copepods were
maintained on a 14 h light : 10 h dark cycle at 23.5 ∘C in 2 L glass
containers with 0.2 µm filtered seawater. The copepods were fed a mixed
algal diet consisting of Rhodomonas sp. and Thalassiosira weissflogii at a concentration of ∼ 5000 cells L-1;
this food suspension was supplied to the cultures twice a
week and the whole culture seawater was replaced every week. The copepods
were maintained for more than 1 month prior to the start of the experiment
to ensure that all the adults were grown in approximately the same
conditions and were of approximately the same age.
The diatom T. weissflogii was maintained in exponential growth in f/2 medium (Guillard,
1975), under light intensities of either
15 or 200 µmol photons s-1 m-2 to generate cells
with different cellular silica contents (Liu et al., 2016). The diatom
cultures were transferred every 4 or 8 days for the high- and low-light
batches, respectively. After two transfers the amount of biogenic silica in
the diatom cells was measured using a modified version of the method
described by Paasche (1980), following the procedures described more
recently by Grasshoff et al. (1999). Cells were collected on a 1 µm
polycarbonate filter (47 mm diameter) and washed with 10 mL autoclaved
seawater and 0.01M HCl during filtration to remove the intercellular
silicate pools. The folded filter was immediately placed into a 15 mL
polypropylene tube and stored at -80 ∘C. Hydrolysis was carried
out using 4 mL of 5 % NaOH, digested at 85 ∘C for 2 h. After
cooling, 0.72 mL of 1.0 M HCl was added to each tube, lowering the pH to
3–4. Silicic acid concentration of samples was determined colorimetrically,
through the formation of blue-colored silica complexes.
Summary of the concentration and cellular silica content of the
diatom prey in each experiment.
Experiment
Measurements
[Prey]
Silica
Initial prey density
Cellular silica
level
(cells mL-1)
(pg SiO2 cell-1)
1
Fecal pellet
High
High
8194 ± 166.9
55.7 ± 1.7
production
High
Low
7976 ± 8.5
38.2 ± 1.4
2
Low
High
1640 ± 28.3
51.7 ± 1.9
Low
Low
1490 ± 84.9
31.4 ± 6.6
3
Fecal pellet
High
High
8194 ± 166.9
55.7 ± 1.7
degradation*
High
Low
7976 ± 8.5
38.2 ± 1.4
4
High
High
7499 ± 63.6
58.9 ± 2.4
High
Low
7344 ± 169.7
33.4 ± 4.3
5
Low
High
1640 ± 28.3
51.7 ± 1.9
Low
Low
1490 ± 84.9
31.4 ± 6.6
6
Fecal pellet
High
High
8114 ± 138.0
56.5 ± 5.9
sinking
High
Low
7904 ± 124.7
27.0 ± 0.6
7
Low
High
1790 ± 48.1
52.1 ± 1.3
Low
Low
1545 ± 75.0
30.3 ± 3.1
* The incubation time of the three fecal pellet degradation experiments can be
found in Table 3.
Experimental design
Active adult female Calanus sinicus specimens with intact appendages were
selected and starved for 24 h before an experiment. A total of seven
experiments were conducted to determine fecal pellet production, degradation
and sinking, and in each experiment these parameters were measured both at
low and high food concentrations, and at high and low levels of silica
contained in the diatom prey (Table 1). In each experiment, the copepods
were fed the same species of diatom (i.e., T. weissflogii), at either ca. 1600 cells L-1 (low concentration)
or ca. 8000 cell L-1 (high
concentration), the latter being above the food saturation level according
to Frost (1972). The abundance and volume of diatoms were measured
(triplicate subsamples) using a Beckman Coulter Z2 particle counter and size
analyzer.
In the fecal pellet production experiments, five replicate bottles
containing one copepod per bottle and two control bottles without a grazer
were used. All the bottles were filled with 100 mL freshly prepared media
consisting of 0.2 µm prefiltered seawater and suspensions of the
respective prey for each treatment. All incubations were conducted at
23.5 ∘C and in the dark for 24 h. At the end of the incubation
period, a 2 mL sample was collected from each bottle and fixed with acid
Lugol's
at a final concentration of 2 %, for subsequent diatom
quantification. The remaining water was collected in a 50 mL polypropylene
tube and fixed with glutaraldehyde at a final concentration of 1 %, for
further quantification of the fecal pellets.
Degradation rate of the fecal pellets produced by C. sinicus after they were
fed diatoms with different silica content.
Prey
Incubation
Silicon status
n
Degradation
concentration
period
of prey
rate (day-1)
High
48 h
HSi
3
0.21 ± 0.15
LSi
3
0.91 ± 0.17
High
24 h
HSi
4
0.03 ± 0.04
LSi
4
0.15 ± 0.02
Low
24 h
HSi
3
0.08 ± 0.04
LSi
2
0.38 ± 0.03
Note: HSi: high silica content, LSi: low silica content.
In order to obtain fresh pellets for the degradation experiments, two
plastic beakers were prepared for the high- and low-silica content prey.
Each beaker contained 7–8 copepods and 700 mL culture medium, prepared as
described for the production experiments. After 12 h of incubation
(except for experiment 3, which was incubated for 18 h), the medium
was sieved through a 40 µm mesh to collect the fecal pellets and then
rinsed with autoclaved 0.22 µm filtered seawater. At least 20 intact
fecal pellets were selected using a glass Pasteur pipette under a
stereomicroscope and poured into a 250 mL polycarbonate bottle containing
200 mL of 2 µm pre-filtered sea water taken from the field. The number
of replicate bottles and the incubation period of each experiment are shown
in Table 2. All the bottles were put on a roller at 0.4 rpm in the dark at
23.5 ∘C; then at the end of the respective incubation times,
the whole water of each bottle was collected in a plastic bottle and fixed
with glutaraldehyde at a final concentration of 1 % for further fecal
pellet analysis.
Experiments to estimate the fecal pellet sinking rate were conducted by
obtaining fecal pellets using the degradation experiment procedure
(described above) but with an incubation time of 24 h. After collecting
all the fecal pellets from the beakers, 50 intact pellets were selected and
suspended in 260 mL 0.2 µm prefiltered autoclaved seawater. The fecal
pellet sinking rate was measured using a SETCOL chamber (49 cm height, 2.6 cm inner diameter) made by 4 mm Plexiglas (Bienfang, 1981), filled with
well-mixed pellet-containing seawater. The chamber was allowed to settle for
6 min, and then the whole column of water was collected from outflow tubes
in a top-to-bottom order. The water was collected in a plastic bottle and
fixed with glutaraldehyde as described above, for subsequent fecal pellet
analysis.
Determining the number and size of fecal pellets
The water samples containing the fecal pellets in the 50 mL polypropylene tubes were allowed
to settle for 24 h. The upper water was then removed smoothly and the
remainder was poured into the well of a six-well plate and the number of
pellets was counted using an inverted microscope (Olympus IX51) at
100 × magnification. Only intact fecal pellets and fragments with
end points were counted. The total number of fecal pellets was then
calculated to include all of the intact fecal pellets plus half of the
pellet fragments. Images of at least 30 intact fecal pellets were acquired
with a CCD camera (Model 4.2, Diagnostic Instrument Inc., USA), after which
the length and width of each fecal pellet were measured, and the volume was
calculated assuming that they are cylindrical in shape.
Calculating the fecal pellet degradation rate
The rate of degradation of the fecal pellets was calculated from the loss of fecal pellet equation,
described by
Nt=N0e-rt,
where N is the total number of fecal pellets in the incubation bottle at the
beginning (N0) and end of the experiment (Nt); t is the incubation
time (in days); and r is the degradation rate (d-1). The degradation
rate estimated in this study only considered the effect of microbial
organisms and assumed that the loss rate was exponential.
Calculating the fecal pellet sinking velocity
The rate that fecal pellets
sank was calculated from the formula reported by Bienfang et al. (1982),
which was originally used to measure the average sinking rate of
phytoplankton. Thus,
S=NsNt×Lt,
where S is the average sinking velocity; L is the height of the sinking
column; t is the duration of the trial; Nt is the total number of fecal
pellets within the settling water volume; and Ns is the total number of
fecal pellets that settled during the trial time.
In addition, the density of the fecal pellets was calculated using the
semi-empirical equation deduced by Komar (1980), as follows:
ws=0.0791μρs-ρgL2LD-1.664,
where ws is the sinking velocity of the fecal pellets; μ and
ρ are the fluid viscosity and density, respectively; L and D are the
length and diameter of the fecal pellets, respectively, assuming they are in
the cylindrical shape; g is the acceleration of gravity; and ρs is
the density of fecal pellet.
The cellular silica content of T. weissflogii grown under different light
intensities. The error bars show 1 standard deviation (n= 3).
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Results
Grazing response
The cellular silica content of first- and second-generation T. weissflogii when cultured at
high and low light intensities is shown in Fig. 1. After two transfers the
cellular biogenic silica content was significantly different (t test,
p < 0.05; Fig. 1) when comparing the high-light and low-light culture
conditions. The silica content of high- and low-silica diatoms used in all
the experiments was consistent, and the differences between the two
treatments were all statistically significant (Table 1). Other cellular
parameters, such as cell size and carbon and nitrogen contents, were also
measured for selected samples (data not shown), and the results were
consistent with those reported in a previous study (Liu et al., 2016), which
showed no significant difference between the two types of prey.
The grazing response of C. sinicus to diatoms with different silica contents showed
similar patterns between high (ca. 8000 cells mL-1) and low (ca.
1600 cells mL-1) prey concentration (Fig. 2). At high concentrations of
prey, C. sinicus grazed the diatoms with low cellular silica content 2 times faster
than when they had a high silica content (t test, p < 0.05). The same
trend was also observed at low concentrations of the prey, although in this
case the difference was not statistically significant. In addition, the rate
of clearance was significantly higher for the low-silica prey than for the
high-silica prey at both low and high prey concentrations (t test,
p < 0.05). These results indicate that the silica content of diatoms
can affect the grazing activity of copepods.
Grazing rate (a) and clearance rate (b) of C. sinicus fed high and low
concentration of diatoms with different silica content. HSi and LSi are high-
and low-silica diatom prey, respectively. The error bars show 1 standard
deviation (n= 5).
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Fecal pellet production
The rate of fecal pellet production varied both with the silica content and
the concentration of the prey (Fig. 3a). At a high prey concentration, C. sinicus that
were fed low-silica prey produced significantly higher amounts of fecal
pellets (192 ± 32 FP ind-1 d-1) than those fed high-silica
prey (113 ± 47 FP ind-1 d-1, p< 0.05), which
corresponds well with the rate of ingestion (Figs. 2a and 3a). At a low prey
concentration, however, the production of fecal pellets by C. sinicus fed the
low- and high-silica prey was not significantly different (Fig. 3a). In addition,
the size of the fecal pellets was only affected by the concentration of the
prey, and not by the silica content of the prey (Fig. 3b). Thus, the fecal
pellets produced in the high concentration of prey groups had a mean length
and width of 582.4 ± 98.7 and 72.5 ± 4.5 µm,
respectively, which are significantly larger than the size of those produced
in the low concentration of prey groups, which had an average length and
width of 352.4 ± 54.7 and 59.6 ± 6.8 µm, respectively
(ANOVA, p < 0.05).
Fecal pellet degradation rate and sinking rate
The degradation rate of fecal pellets was significantly different when the
copepods fed diatoms with different silica content (Table 2). The
degradation rate of the fecal pellets produced from the low-silica prey was
approximately 4–5-fold higher than that of the pellets generated from the
high-silica prey, irrespective of the prey concentration or the period of
degradation incubation. In addition, the degradation rate of the fecal
pellets from low prey concentration was significantly higher than ones from
high prey concentration after an incubation period of 24 h (p < 0.05, ANOVA). Furthermore, the degradation rate obtained following 48 h
incubation was significantly higher than that following just 24 h incubation
(only high prey concentration experiments) for both the high-silica (p < 0.05, t test) and low-silica (p textless 0.01, t test) prey (Table 2),
indicating an acceleration of degradation on the second day of incubation.
Production rate (a) and average volume (b) of fecal pellet produced
by C. sinicus fed different concentration of diatom prey. HSi and LSi indicate
high-
and low-silica diatom prey, respectively. The error bars show 1 standard
deviation (n= 5).
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The sinking rate of fecal pellets was also different for the high and low
prey concentrations (Fig. 4). At a high concentration of prey, the sinking
rates of the pellets produced by the high- and low-silica prey (i.e., 3.05
and 3.13 cm min-1, respectively) were not significantly different.
However, at a low prey concentration, the sinking rate of pellets from the
high-silica-content prey (i.e., 2.59 cm min-1) was significantly
greater (t test, p < 0.01) than that of pellets from the
low-silica-content prey (i.e., 0.53 cm min-1). The average density of
the fecal pellets was calculated as being 1.093–1.095 g cm-3 at the
high prey concentration and 1.035–1.097 g cm-3 at the low prey
concentration. The variation in the calculated density of fecal pellets is
consistent with the pattern of sinking rate, with the lowest density
occurring in fecal pellets from low-silica prey at the low prey concentration
(Fig. 4).
Discussion
The grazing activity of copepods varies not only with the concentration of
the prey but also with the nutritional quality of the prey. In our study,
the grazing and clearance rates determined with varying food concentrations
followed a similar trend to that described in the literature (e.g., Frost,
1972). In addition, the grazing activity was affected by the cellular silica
content of the prey, as has been observed with other copepod species (Liu et
al., 2016). Silicification has been suggested to be one of the strategies
that is used by diatoms to protect them from ingestion by grazers (Pondaven
et al., 2007). Friedrichs et al. (2013) examined the mechanical strength of
the frustules of three diatom species and measured the feeding efficiency of
copepods on these diatoms. Their results showed that the diatom species with
the more weakly silicified frustules and the highest growth rate was the
least stable and was fed upon the most, whereas the species with the most
complex frustule exhibited the greatest stability and was fed upon the
least. Within the same species of diatom, different growth rates have
resulted in different amounts of silica in the frustule (Claquin et al.,
2002). This results in higher copepod ingestion and clearance rates for
diatoms with a low silica content when compared with those for diatoms with
a higher silica content (Liu et al., 2016). The results obtained in the
current study are consistent with those reported by Friedrichs et al. (2013)
and Liu et al. (2016).
The sinking rate (bars) and calculated density (open dots) of the
fecal pellets generated by C. sinicus following each treatment. HSi and LSi are
high- and low-silica diatom prey, respectively. The error bars show 1 standard
deviation (n= 3).
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Previous studies indicate that while there is a linear relationship between
the ingestion rate and the total number of fecal pellets produced per unit
time (Ayukai and Nishizawa, 1986; Ayukai, 1990), there is a high level of
variation among different diets (Båamstedt et al., 1999, and references
therein; Besiktepe and Dam, 2002). In addition, the size of fecal pellets
increases as the concentration of the food increases, such that they reach a
maximum size when the concentration of food is above the saturation level
(Dagg and Walser, 1986; Butler and Dam, 1994). Our results confirmed these
previous findings and demonstrated that the size of fecal pellets produced
was only affected by the concentration of prey, and fecal pellets did not
show any significant size differences when comparing prey of high and low
cellular silica content. Butler and Dam (1994) reported that when sufficient
food was available, the size of the fecal pellets varied with the
nutritional quality (e.g., the C : N ratio) of the prey. Since diatoms with
different silica content (generated by varying the light intensity) do not
differ in their cellular C : N ratio (Claquin et al., 2002; Liu et al., 2016),
these ratios did not affect the size of the pellets produced.
The relationship between degradation rates and surface : volume ratio
of fecal pellets from different experimental treatments. HSi and LSi are
high- and low-silica-content diatoms, respectively; high and low prey are
high and low prey concentrations, respectively; 48 and 24 h are the
incubation periods used for the degradation experiments. The error bars show
±1 standard deviation, and the dashed line shows the relationship
curve generalized by Olesen et al. (2005).
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The degradation rate and sinking velocity of the fecal pellets are highly
dependent on the characteristics of the pellets, which are in turn affected
by the quality and quantity of the food ingested (Feinberg and Dam, 1998;
Turner, 2002, 2015, and references therein). For example, it is known that
the decomposition rate of the fecal pellets is affected by diet, pellet size
and the producer of the pellets (e.g., Shek and Liu, 2010), but no research
has addressed the degradation rates of fecal pellets produced by prey under
different stoichiometric conditions. Hansen et al. (1996) estimated the
degradation rate of fecal pellets produced from diets of Thalassiosira weissflogii, a diatom;
Rhodomonas baltica, a nanoflagellate; or Heterocapsa triquetra, a dinoflagellate. Fecal pellets produced from a
diet of the diatom species presented the slowest rate of degradation when
compared with those produced from diets of the nanoflagellate or
dinoflagellate species. Similarly, Olesen et al. (2005) compared the
degradation rate of fecal pellets produced on a diet of the diatom,
Skeletonema costatum, or the nanoflagellate, Rhodomonas salina, and reported a similar trend but higher
degradation rates than Hansen et al. (1996). The relationship between the
surface : volume ratio and the degradation rate of fecal pellets was used to
explain the variation in the degradation rate of pellets produced with
different diets. Our results (Table 2) were higher than those reported by
Hansen et al. (1996), which were 0.024 d-1 for T. weissflogii, but our results showed
a similar trend to those summarized by Olesen et al. (2005) (dashed line in
Fig. 5), in that there was an increase in the degradation rate with the
increase in fecal pellet surface : volume ratio, although the degradation
rates that we measured exceeded the predicted rates in most cases,
particularly for fecal pellets produced with low-silica diatom prey (Fig. 5).
The generally higher rates in our study might be caused by the higher
temperature that we used when compared with the previous studies (i.e.,
23.5 ∘C in our study vs. 17 and 18 ∘C in Olesen et al., 2005, and
Hansen et al., 1996, respectively), but the differences in predator and prey
quality, particularly the cellular Si content in this study, cannot be
ignored.
The sinking rate of fecal pellets is usually considered to be related to
their size and density, which is in turn dependent on the concentration and
composition of the prey (Bienfang, 1980; Urban et al., 1993; Feinberg and
Dam, 1998). We also demonstrated that fecal pellet size, sinking rate and
density were correlated with the concentration of prey (Figs. 3b, 4),
especially in the low-silica diatom prey treatment. Using the ratio of
ingestion rate : fecal pellet production rate ratio as an index to compare
the diatom content per fecal pellet, no differences were found in pellets
produced from diets of the same silica content (Fig. 6), indicating that
prey concentration does not affect the package content of the fecal pellets.
On the other hand, copepods were shown to pack fewer hard-shelled (i.e.,
high-silica) diatoms into each fecal pellet in comparison to the soft-shelled
(i.e., low-silica) diatoms, although these data were not significantly different
statistically (Fig. 6).
The grazing rate : fecal pellet production rate ratio of each
treatment. HSi and LSi are the high- and low-silica diatom prey,
respectively. The error bars show 1 standard deviation.
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The fecal pellets of copepods are formed in the midgut surrounded by a
peritrophic membrane, which is believed to protect the gut wall from the
sharp edges of the prey's cell wall. Moreover, the different sizes of fecal
pellets with similar prey content per fecal pellet are thought to result
from the decrease gut passage time with the increase of food
concentration. A high prey concentration results in the food passing through
the gut more quickly and results in incomplete digestion, whereas a low prey
concentration allows the food to be kept in the intestinal tract for a
longer time and therefore digestion is relatively more complete. We showed
that the silica content of the diatom cell wall determines the density and
sinking rate of the fecal pellets when the prey concentration was low due to
complete digestion. In addition, we showed that only the low concentration
of low-silica prey group resulted in a significantly lower fecal pellet density
and sinking rate. In previous studies, the sinking rate and density of the
fecal pellets of Calanus were shown to be 70–171 m day-1 and 1.07–1.17 g cm-3,
respectively (Bienfang, 1980; Urban et al., 1993), which are
considerably higher than our results (Fig. 4). We suggest that these
differences might be caused by the differences in methodology used (Griffin,
2000).
The L ratio (m-1), determined as the mean degradation rate
constant (t-1), divided by the mean sinking rate (m d-1), for each
treatment.
Prey silica
High food
Low food
content
concentration
concentration
High Si
3.91 × 10-4
7.56 × 10-4
Low Si
1.09 × 10-3
1.65 × 10-2
To compare the combined effects of sinking and degradation rates for each
treatment, the reciprocal length scale, or L ratio, which is the fraction of
pellet degradation per unit length traveled, was calculated (Feinberg and
Dam, 1998). The product of the L ratio multiplied by the depth of the mixed
layer can then be used to provide the degree of degradation of a pellet
within this layer. The results from such calculations suggest that some
diets might result in pellets that are substantially recycled within the
epipelagic layer whereas others result in pellets that are exported out of
the mixed layer in a relatively non-degraded manner. It should be pointed
out, however, that the degradation rates we calculated are likely to be
highly underestimated due to the absence of zooplankton activities. For
example, it has been reported that copepod ingestion of entire fecal pellets
(i.e., coprophagy) or only partial breakdown of fecal pellets might
dramatically reduce the overall downward transport of fecal material and
thus increase its retention in the epipelagic layer (Lampitt et al., 1990;
Gonzalez and Smetacek, 1994; Svensen et al., 2012). For the same reason,
plus the absence of turbulence in our experimental set-up, our sinking rate
measurements are likely to be overestimated. Nevertheless, the L ratio
provides a relative indicator of the export efficiency of the fecal pellets
produced on diatom diets of different silica content and can be used for a
comparison with copepod fecal pellets produced with other diets. Our results
also show that pellets produced from high-silica-content diatoms are more
likely to sink out of the mixed layer before being degraded, when compared
with pellets from low-silica-content diatoms. On the other hand, fecal
pellets produced from a low concentration of prey with low-silica content are
the most likely to be degraded in the mixed layer (Table 3). Our results
suggest that the grazing activity of copepods might result in organic matter
being mostly recycled in the mixed layer during the fast-growth period of
diatoms (e.g., at the beginning of the bloom), whereas it could accelerate
the export of POC to the deep ocean by producing fast-sinking fecal pellets
during the slow-growth period of diatoms (e.g., during the senescent stage
of the diatom bloom).
In conclusion, the silica content of the cell wall of diatoms can affect the
grazing activity of copepods and influence the rates of production,
decomposition and sinking of their fecal pellets. Our findings suggest that
it is not only the nutritional quality but also the digestion process of
copepods that can result in the different characteristics of the pellets
produced. In addition, it is a combination of both degradation and sinking
rates (which are affected by the abundance and cellular silica content of
the diatom prey among other physicochemical factors) that determines the
efficiency of the downward export of biogenic silica and organic carbon by
fecal pellets.