1
Seasonal variation in the abundance and grazing rates of the first
2
stages of copepods in a temperate sea.
3
4
Running head: Copepods abundance and grazing rates
5
6
Eva López*, Leticia Viesca, Ricardo Anadón
7
Área de Ecología, Departamento de Biología de Organismos y Sistemas, Universidad de
8
Oviedo, C/ Catedrático Rodrigo Uría, s/n, CP 33071, Oviedo, Spain.
9
*E-mail address: evalop.uo@uniovi.es
10
11
12
Abstract:
13
The understanding of the role of copepods populations in oceanic ecosystems and carbon fluxes is limited
14
by the scarcity of information about their smallest size fraction and first developmental stages. Here, we
15
present an study that includes the whole copepod population, but with special emphasise on copepods <
16
200 µm and nauplii. Abundance of the different stages of copepods, and ingestion rates of nauplii,
17
copepods and copepodites belonging to the size fraction < 200 µm, were measured during an annual cycle
18
in three stations off Cudillero (Southern Bay of Biscay). Nauplii were the most abundant group in the
19
metazooplankton, with densities ranging between 1 - 48 individuals l-1. The highest abundances have
20
been found during late summer and autumn, with differences in the time between stations. Ingestion rates
21
on phytoplankton showed a significant trend of increase with chlorophyll-a concentration in the water,
22
with a saturation response at around 240 µg C l-1. Specific ingestion rates ranged between 0.04-2.05 µg C
23
µg-1 nauplii C day-1 and 0.04-3.38 µg C µg-1copepod C day-1.
24
25
Key words:
26
Copepod nauplii, ingestion rates, gut fluorescence, Cantabrian sea
1
1
INTRODUCTION
2
In the present scenario of general concern about climate change, the need to
3
understand the biogeochemical cycles in the oceans and quantify the importance of all
4
the processes that take part in them is becoming more and more urgent. Research
5
programs on this topic are mostly focused on coastal zones due to their accessibility and
6
special characteristics. Coastal zones are generally very sensitive to any external
7
forcing, so climate changes are therefore likely to have the greatest impact and be
8
experienced first in them, whereas spatio-temporal buffering in the oceans may delay
9
evidence of climate change for decades or even centuries (Sündermann et al. 2001).
10
From 1993, a monthly sampling has been conducted in the Central Cantabrian
11
Sea (North of Spain). During this period, several studies relating physical and chemical
12
parameters have been carried out in this area (eg. Llope et al. in press, Stenseth et al.
13
submitted). It has also been evaluated the numerical importance and feeding impact of
14
different taxonomical groups, such as, fish larvae (González-Quirós & Anadón 2001),
15
appendicularians (López-Urrutia et al. 2003), mesozooplanktonic copepods (Huskin et
16
al. 2006), protozoa (Quevedo & Anadón 2000), and bacteria (Serret et al. 1999,
17
González et al. 2003). This means a significant amount of reference data, allowing us to
18
establish an observation strategy and detect future changes in the coastal zone. There is
19
available information about most of the main zooplanktonic groups in the area, being
20
maybe the major deficiency the lack of studies dealing with small copepods and nauplii.
21
Copepods are the most abundant group in the metazooplankton and they have
22
been one of the main focuses of oceanographic studies during last decades. In our study
23
area, mesozooplanktonic copepods abundance and feeding rates on phytoplankton have
24
been estimated during an annual cycle by Huskin et al. (2006), but this study did not
25
include the fraction <200 µm (mostly nauplii and copepodites). In fact, we are aware of
2
1
very few studies of ingestion rates for the naupliar phase (reviewed in López et al.
2
2006). And most of the published data come from studies with cultures of copepods and
3
phytoplankton in laboratory, so results are difficult to extrapolate to natural conditions.
4
Nauplii have received relatively little attention despite the fact that they are more
5
abundant than copepodites and copepods in the field and that their success in the
6
plankton will ultimately determine recruitment into the copepodite phase and,
7
consequently, the population dynamics (Torres & Escribano 2003). To our knowledge,
8
there are no studies in the literature regarding the seasonal changes in nauplii feeding
9
rates. However, seasonal changes in their abundance have been reported for other zones
10
(reviewed in Turner 2004), although data are still rather scarce due to the common use
11
of 200 µm mesh nets to sample metazooplankton. The bias produced by the use of such
12
large pore nets to sample copepods assemblages has been reported several times (e.g.
13
Calbet et al. 2001, Turner 2004), as they seize inefficiently nauplii, copepodites and
14
adult copepods from the smallest species. This lack of information about copepod
15
nauplii (and small copepods) makes it impossible to correctly evaluate the importance
16
of copepods in the oceanic carbon cycles.
17
The scarcity of data about nauplii ingestion rates in natural communities can be
18
explained by the methodological difficulties to work with such small organisms. In a
19
previous work (López et al. 2006), it has been described a series of adaptations for the
20
gut fluorescence method (Mackas & Bohrer 1976) so it can be used with copepod
21
nauplii. In that work, it has been discussed the choice of the gut fluorescence method to
22
measure nauplii ingestion rates on phytoplankton and the advantages and weaknesses of
23
this technique.
24
In this study, it has been used the previous mentioned methodology to measure
25
herbivory ingestion rates of nauplii, copepods and copepodites from the <200 µm
3
1
fraction during an annual cycle. The functional responses of this fraction feeding on
2
phytoplankton were studied, calculated the impact caused on phytoplankton stock and
3
compared with data obtained for larger copepods by Huskin et al. (2006). It has also
4
been studied the seasonal changes in the abundance of the main metazooplankton
5
groups and related to phytoplankton abundance and water temperature.
6
7
MATERIALS AND METHODS
8
The study took place in a transect of 3 stations (E1, E2 and E3) off Cudillero in
9
the southern Bay of Biscay (Figure. 1). This zone exhibits a very dynamic hydrography
10
(described in Llope et al. in press) and the stations show significant differences in spite
11
of their proximity. E1 (65 m depth) is a coastal station influenced by freshwater
12
discharges, tidal currents and frequent wind-driven upwelling during summer. E2 (130
13
m) is located on the continental shelf and as such is also affected by upwelling events
14
although less intensively than E1. E3 (850 m) is on the slope and is the most oceanic as
15
it is only marginally affected by coastal processes except for the occasional appearance
16
of the Iberian Poleward Current and the indirect effect of upwellings, probably by
17
offshore advection (Stenseth et al. submitted).
18
Sampling was done monthly during 2003. At every station, physical and
19
chemical parameters were measured and samples were taken to determine, chlorophyll-
20
a (chl-a) concentration, mesozooplankton biomass, micro and mesozooplankton
21
taxonomy and nauplii and copepodites gut contents. In station E2 samples were taken
22
also for phytoplankton taxonomy and primary production.
23
24
Vertical profiles of temperature and salinity were obtained with a CTD from a
depth of 50, 100 and 500m in E1, E2 and E3 respectively.
4
1
Chl-a concentration was determined fluorometrically. Water samples were
2
collected with 5 l Niskin bottles at 6 - 10 different depths from surface to the end of the
3
photic layer. Samples were carried to the laboratory in cold conditions and filtered onto
4
GF-F filters. Filters were frozen and extracted in 5 ml 90% acetone during 24 h in dark
5
and cold conditions. Chl-a concentration was measured with a Turner Designs 10
6
fluorometer following the method of Yentsch & Menzel (1963).
7
Primary production was determined by incubating with
14
C water from 3
8
different depths (surface, chlorophyll maximum and limit of the photic layer). Water
9
samples were inoculated with 370 kBq (10 µCi NaH14CO3) and incubated for 2 h. Three
10
light bottles and one dark bottle (control) were incubated for each depth. Temperature
11
and light for each treatment were simulated following preliminary study of the CTD
12
casts. After incubation, samples were filtered onto GF-F filters, exposed for 12 hours to
13
concentrated HCl fumes to remove inorganic
14
scintillation counter. Quenching was corrected by the internal standard method. There
15
was a problem with primary production experiment during August so there is a gap on
16
data.
14
C, and counted in a Wallac 1409
17
Water samples for phytoplankton species identification were collected at 3
18
different depths (surface, chlorophyll maximum and limit of the photic layer); they were
19
preserved with 2% final concentration Lugol´s iodine solution. Subsamples (100 ml)
20
were settled (Utermöhl method) and counted with an inverted microscope.
21
At every station, one WP2 net (37 cm diameter, 200µm mesh) was deployed to
22
50 (station E1), 100 (station E2) or 200 m (station E3) to sample mesozooplankton for
23
biomass quantification. Cod end contents were kept in 250 ml plastic bottles and carried
24
to the laboratory where they were screened through 200, 500 and 1000 µm meshes to
25
create three different size fractions. Each fraction was filtered onto GF-A pre-
5
1
combusted and pre-weighed filters, maintained for 48 h at 60ºC and weighed. Biomass
2
was expressed as mg dry weight m-3.
3
Two net tows were carried out at every station with a 53µm mesh net to collect
4
zooplankton from the upper 50 m. The first net tow was devoted to metazooplankton
5
taxonomic composition and the second to gut fluorescence analysis. Some net samples
6
from October, November and December were lost so there is some gaps on data. The
7
cod end content from the first tow was screened through 200 and 30 µm meshes and
8
both samples were fixed with 4 % buffered formaldehyde and determined under a
9
stereomicroscope to the level of main taxonomic groups. The cod end content from the
10
second tow was fractionated in the same way and samples from the <200 µm fraction
11
were filtered onto mesh filters, frozen in liquid nitrogen and kept frozen until analysis.
12
Gut fluorescence was measured for nauplii and copepods <200 µm (cop <200 µm,
13
includes copepodites and copepods from the <200 µm, as we did not distinguish
14
between both of them) following Mackas & Bohrer (1976) and the adaptations
15
described in López et al. (2006). For each station, 3 groups of 20 nauplii and 6 groups
16
of 10 cop <200 µm were analysed. The samples were extracted in 120 µl of acetone (90
17
%) for 24 h at 4 ºC and measured with a Turner Designs 700 fluorometer with a
18
minicell adapter kit.
19
Ingestion rates were calculated with the formula:
20
I=kG
21
where k is the gut clearance coefficient and G is gut content (expressed as ng chl-a eq.
22
ind-1).
23
24
25
To calculate k we use the empirical relationship with temperature (T) proposed
by Dam & Peterson (1988) for adult copepods:
k = 0.0117 + 0.0018 T
6
1
A previous study with copepod nauplii (López et al. 2006) found no differences
2
between gut evacuation rates obtained with nauplii in the laboratory and the rates
3
obtained with the previous equation.
4
Groups of at least 40 nauplii and 40 copepodites from every sample were
5
measured by taking photographs of the sample under the stereomicroscope and using
6
image analysis software. Average dry weight was estimated for each sample using the
7
following relationships:
8
Log dry weight (µg) = 2.1034 log nauplii total length (µm) - 5.2105
9
Log dry weight (µg) = 2.6757 log copepodite prosome length (µm) - 6.7625
10
As relationships found in the literature are usually obtained for only one species
11
(reviewed in Mauchline 1998), we calculated the above mentioned ones with data from
12
the study of Klein Breteler et al. (1982), for four species of copepods very abundant in
13
our study area. Their graphs were scanned, all data from them were obtained with image
14
analysis software and new relationships were obtained by plotting all data together.
15
They were used to calculate dry weight for the mix of copepods found in our samples.
16
They were compared with relationships presented in Mauchline (1998) and it was
17
checked that parameters were in the same range as others from different studies.
18
19
To convert chlorophyll concentration in C units, as an index was not available
for each station and date, a value of 50 was used for all samples (Taylor et al. 1997).
20
The equations for the different types of functional responses (Holling 1965)
21
were fitted by the least-squares criterion to the ingestion data. For the type I fit
22
(rectilinear model) we followed the procedure by Rothhaupt (1990) to calculate where
23
the deflection point should be, and then we obtained the fit for the combination of the
24
two linear regressions:
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I  aC , when C  Cd
7
I  Im ax , when C  Cd
1
2
where I is the specific ingestion rate (µg C µg-1 nauplii C d-1), a is a constant, C is the
3
phytoplankton concentration (mg chl-a m-3), Cd is the C at the deflection point and Imax
4
is maximum I, calculated as the I average value for C > Cd.
5
For type II we used the Ivlev (1961) equation:
I  Im ax1  exp  aC Im ax
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7
where I is the specific ingestion rate, Imax is asymptotic maximum I, a is a constant and
8
C is the phytoplankton concentration.
9
And the logistic equation for type III model:
I  Im ax 1  expKc  C  a
10
11
where Imax is asymptotic maximum I, C is the phytoplankton concentration, Kc is a
12
constant defined as the food concentration for I  Im ax 2 , and a is a constant.
13
To compare between models, minimization of the mean-square error (MSE) was
14
used as the criterion for goodness of fit. The significance of differences in variances
15
among regressions was tested by a two-tailed F-test on the MSE (Rothhaupt 1990,
16
Mullin et al. 1975).
17
18
RESULTS
19
Vertical profiles of temperature and chl-a concentration are shown in figures 2
20
and 3 respectively. The hydrographic features of the study area are those of a typical
21
temperate sea, being the main characteristic the transition from the winter-spring mixing
22
to the summer-autumn stratification with the development of a thermocline at about 40
23
m. A more detailed description about physical and chemical characteristics is presented
24
in Llope et al. (). As a special feature, it has been observed during February in E3, the
25
appearance of a low salinity water mass in the upper 50 m of the water column (salinity
8
1
profile not shown). In this water, a winter bloom developed reaching the highest
2
chlorophyll concentration for the whole annual cycle.
3
Metazooplankton and phytoplankton abundance
4
Copepods have been the most numerous group of the metazooplankton in both
5
fractions (Table 1 and 2). They represented on average the 72,5 % of the total
6
abundance in the >200 µm fraction and the 93 % including both fractions. The 81 % of
7
the total copepods belonged to the <200 µm fraction. Only cirripeds larvae have
8
outnumbered them in the fraction >200 µm during April in E1 and February in E2.
9
Appendicularians have also presented really high abundances during most of the year
10
and doliolids during late summer and autumn, reaching the highest value during
11
October in E3.
12
As copepods represented the majority of the mesozooplankton, we can interpret
13
changes in the relative biomass of each fraction (Figure 4) as changes in copepod
14
community size structure. It is necessary, however, taking into account the cases in
15
which cirriped larvae have been rather abundant (February in the three stations and
16
April in E1). Cirriped larvae would be mostly comprised in the 200 - 500 µm fraction.
17
There was a significant increase in the biomass of this fraction during February in E2
18
when it was found the highest cirriped larvae abundance. The other more abundant
19
groups were those belonging to the gelatinous zooplankton, that with their high water
20
content were not expected to account for a significant amount of sample dry weight.
21
Observed changes in copepods number were not directly related with changes in
22
biomass. The highest mesozooplankton biomass was found in spring, when a shift in the
23
community size structure was observed, increasing the abundance of large sized
24
copepods, and resulting in a lower total number than that of periods when small species
25
dominate. Another point is the different kind of sampling used for both parameters. Net
9
1
tows have been deployed to 50 m in the three stations for taxonomic analysis and gut
2
contents, while they have been deployed to 50, 100 and 200 m in E1, E2 and E3 for
3
mesozooplankton biomass. So in E2 and E3 a non-homogeneous distribution of
4
copepods in the water column would lead to non comparable results with both methods.
5
This can be the reason why in February in E3 we have found the highest number of
6
copepods for the whole cycle and it does not match with the data obtained for biomass.
7
Seasonal changes in the abundance of the whole copepod community (Figure 5),
8
were mainly due to changes in nauplii numbers. There are different patterns for the
9
three stations. In the coastal one it was observed a significant increase in the number
10
during June, while it did not occur until August in E2 and September in E3. Afterwards,
11
the number remained high until December in the three stations.
12
It was analysed the relationship between nauplii abundance and: (1) temperature
13
and (2) chlorophyll concentration in the water, by linear regression. The objective of
14
these analyses was to identify the variables that are driving copepods population
15
dynamics. The increase in nauplii abundance during favourable conditions is also
16
dependant on the number of adult copepods; so, apart from the total nauplii abundance,
17
we have also performed the analyses with the relationship “number of nauplii/ number
18
of copepods” (nau/cop) for each period. It was found a significant effect for temperature
19
in total nauplii (r2 = 0.277, p = 0.001) and nau/cop (r2 = 0.126, p = 0.039), which
20
affected positively their number. Chlorophyll concentration in the water only showed a
21
significant relationship with total nauplii (r2 = 0.224, p = 0.005), showing a decrease in
22
the density of nauplii at high chlorophyll concentrations.
23
The highest phytoplankton abundance in E2 was reached during spring bloom
24
(Figure 6), when diatoms were dominant in the community. A second peak in the
25
abundance was reached in late summer (August and September), when the most
10
1
numerous groups were diatoms and crysophyceae. It was possible to compare the
2
pattern of integrated chl-a concentration with that of abundance of phytoplankton cells
3
in E2, as both data were available. Both patterns did not coincide; while the summer
4
increase in phytoplankton started in August for abundance, it was not until September
5
for chl-a concentration.
6
Copepod abundance followed a different pattern than chlorophyll concentration
7
and phytoplankton abundance in the three stations. However, there was a
8
correspondence in E2 between August increase in number of phytoplankton cells and
9
increase in number of copepods.
10
Grazing rates and functional responses
11
Nauplii and cop <200 µm gut contents ranged between 0.004 - 0.082 ng chl-a
12
eq. ind-1 and 0.003 - 0.315 respectively. Carbon ingestion rates of nauplii and cop <200
13
µm (Figures 7 and 8 respectively) translate into a grazing of 0.3 - 9.6 % of
14
phytoplankton stock daily and 0.49 – 19.9 % of primary production in E2 (Figure 9).
15
Equations for the three models of functional responses were fitted to ingestion
16
data (Figure 10), and parameters were obtained by the least-squares criterion (Table 3).
17
Although the type III model showed the lower MSE, all of them were quite similar and
18
we did not find significant differences in explained variance between models (p > 0.3 in
19
all cases).
20
Both, nauplii and cop <200µm, showed a saturation response at around 2 - 4 mg
21
chl-a m-3. Calculated Imax could be significantly lower than the real one due to the
22
shortage of data in high chlorophyll concentrations. This problem is more evident in the
23
case of cop <200 µm; attending to Figure 10 we could expect an Imax of at least 2 µg C
24
µg-1 copepod C day-1.
25
11
1
2
DISCUSSION
3
Copepods abundance and seasonal changes in the community
4
During all the year, nauplii dominated copepods community in terms of
5
abundance (67 %). Similar results have been found by other authors in different areas;
6
nauplii accounted for 65% of the total copepods community in a coastal area of the NW
7
Mediterranean Sea (Calbet et al. 2001) and 63% in coastal waters off Jamaica (Hopcroft
8
et al. 1998). Nauplii densities during the annual cycle (on average 12 nauplii l-1) are in
9
the same range than others in coastal zones (Roff et al. 1995, Calbet et al. 2001,
10
Pedersen et al. 2005), but sometimes more than an order of magnitude lower than more
11
productive systems ones (Lucic et al. 2003, Uye et al. 1996). The high abundance of the
12
juvenile stages stresses the importance of including the fraction of copepods not
13
retained by the 200 µm mesh in the community studies. However, it is possible that
14
when using 53 µm mesh nets, nauplii are still being under sampled. Lucic et al. (2003),
15
studied nauplii abundance in the Adriatic Sea by sampling with Niskin bottles and
16
found that those belonging to the group with body length <80 µm could account for
17
30% of total nauplii. In our samples, such small nauplii are rather scarce, even though,
18
small sized copepod species such as Oithona nana and Oncaea media are abundant in
19
the study area. Thus, we suspect that nauplii from these species are not being kept
20
efficiently in the net. Lucic et al. (2003) working on the principle that they had found a
21
significant correlation between small nauplii and bacteria abundances, suggested that
22
they had a mainly bacterivorous diet, but they did not find this correlation with larger
23
nauplii. Although bacterivory had been previously described by Turner & Tester (1992)
24
and Roff et al. (1995), it is still not clear under what circumstances this occurs, as
25
Sommer et al. (2000) found that particles <2 µm escaped predation by copepod nauplii.
12
1
If smallest nauplii are actually feeding on bacteria, their under sampling would not
2
change the estimated impact on phytoplankton community. But, even in the case that
3
they were feeding on phytoplankton, we would not expect the real community ingestion
4
rate to be significantly higher, due to the smaller size of this possibly under sampled
5
fraction and consequently lower gut contents.
6
It would be logical to expect the number of copepods influenced by availability
7
of preys. In spite of this, we have found a negative relationship between nauplii
8
abundance and chlorophyll concentration in the water. It could be explained if
9
heterotrophic preys were more abundant when chlorophyll bearing preys decrease. We
10
have not measured the abundance of other potential preys, apart from phytoplankton,
11
but this option does not appear as probable. Other authors have suggested predation
12
(Calbet et al. 2001, Lawrence et al. 2004) and improved competitive advantage of
13
protozoans against metazoans at higher food concentrations (Uye et al. 1996) as causes
14
for the lack of relationship between copepods and nauplii abundances and chlorophyll
15
concentration in the water. Saiz et al. (1999) found an increase in copepods egg
16
production across the natural nutrient gradient from “oligotrophic” oceanic waters to
17
“eutrophic” shelf waters, which did not translate into an increase in the abundance of
18
copepods, and suggested that predation or advection may uncouple production from
19
abundance. Micheli (1999) evaluated bottom-up and top-down controls on consumers.
20
Their results suggest that these controls attenuate through marine food webs, and in
21
general, there may be a weak coupling between phytoplankton and herbivores.
22
On the other hand, the explanation that seems more accurate to us in sight of
23
phytoplankton and zooplankton annual cycles is that a combination of three factors
24
drives copepod population dynamics: (1) water temperature, (2) quantity and (3) quality
25
of available food. Some observations have shown that environmental temperature rather
13
1
than phytoplankton abundance controls egg production in copepods, so daily rates of
2
egg production increase with temperature to a maximum but then decrease with further
3
increases in temperature (Mauchline 1998). We have found a positive influence of
4
temperature in nauplii abundance and this latter could be used as an indicator of egg
5
production. Other studies have pointed out that quality as well as quantity of food
6
available is important; high quality encouraging production of successive egg masses
7
and clutches (see references in Mauchline 1998).
8
A recent study from Ianora et al. (2004) has found that dominant diatom species
9
impair the reproductive success of their grazers. Identifying the aldehydes that arrested
10
larval development in copepods, they have introduced a new light in the debate about
11
the positive or negative effect of diatoms in copepods populations. Although not all
12
bloom-forming species produce aldehydes, their findings provide a plausible
13
mechanism for the apparent poor timing between spring bloom development and the
14
arrival of the bulk of the copepod stock. When looking for a relationship between
15
nauplii abundance and chl-a concentration in the water (as an indicator of “quantity” of
16
available food) the interference of the “quality” factor would explain the impossibility
17
of finding a significant relationship.
18
These three factors acting together could shift the period of time most suitable
19
for breeding, from spring, with low water temperature and low food quality
20
(phytoplankton assemblages mainly composed by diatoms), although the highest chl-a
21
concentration, to the end of summer, with a higher water temperature and a second
22
increase in chlorophyll caused by growth of higher quality phytoplankton species. In
23
August, when the copepods abundance started to increase, diatoms were again abundant
24
in the phytoplankton, being their populations probably enhanced by the short-lived
25
upwellings that are a common event in the area during summer (Llope et al. in press).
14
1
But their relative abundance were not so high as in spring, and it has been pointed out
2
that a mixed diet serves to dilute the toxin causing lower effects on copepods
3
recruitment (Ianora et al. 2004). Another point is that timescale has been suggested as
4
very important in the negative effects of diatoms (Irigoien et al. 2002), and the shorter
5
period in which they were dominant during summer could not have been enough to
6
cause the same deleterious effects as during spring bloom.
7
As phytoplankton taxonomy is not available for E1 and E3, only chl-a
8
concentration can be used to compare copepods and phytoplankton annual cycles.
9
Although it has been observed for E2 that chl-a is sometimes an imperfect index of the
10
availability of phytoplankton, it gives us a guiding idea and we would expect that
11
succession follows a quite similar pattern than in E2. The copepod seasonal distribution
12
in E1 and E3 matches with the before explained theory. In E1 where chl-a concentration
13
remains high during all the year the breeding seasonality would be mainly controlled by
14
temperature and food quality for the majority of copepod species, while in E3 the lower
15
phytoplankton concentration during the beginning of summer would delay it until the
16
end of summer when chl-a increases and water temperature is still high.
17
During February in E3 it has been observed a water mass with special
18
characteristics. In the upper 50 m, water had lower salinity and higher chlorophyll
19
concentration than expected, which not correlated with data for E2. It had been
20
previously described the occurrence of slope fronts in the area (González-Quiros 1999,
21
González 2003). The presence of this kind of structure in outer waters could act as a
22
barrier for the surface transport of fresh water from Nalón River, justifying the
23
accumulation of this “low-salinity water” just before the front. During the previous days
24
to the sampling, the meteorological conditions in the area had been characterised by
25
weak winds (Llope, personal communication), which would have favoured the
15
1
formation and maintenance of this structure. Differences found during this month
2
between copepod abundance and biomass were possibly due to the majority of
3
copepods of the water column accumulated in the upper 50 m where the bloom
4
developed. Nutrients analysis (data not shown) indicated that the bloom was in an
5
advanced development stage.
6
Grazing rates
7
Ingestion rates obtained in this study should be considered as approximations as
8
the method used have some potential source of errors, such as calculation of gut
9
evacuation rate, and the possibility of copepods presenting diel feeding periodicities
10
which have not being assessed in this study. Also, values obtained with this method are
11
usually considered as minimum estimates due to the uncertainty about pigment
12
degradation in copepod guts (discussed in López et al. 2006). Although it is still not
13
clear under what circumstances and to what extend chlorophyll a is degraded to
14
colourless products, some authors apply an average value of 33 % destruction to correct
15
their estimates (Dam & Peterson 1988). Even though, gut fluorescence method provides
16
valuable results and allows measuring ingestion rates of small nauplii in the field.
17
When preparing samples to analyze gut fluorescence, nauplii were picked
18
without paying attention to development stage. Sorting only nauplii from feeding stages
19
would have been rather difficult and time consuming. Also, there is not a consensus
20
about which is the first nauplius stage to feed and it seems that, although most of
21
calanoid copepods start to feed during NIII, there are differences between species
22
(Mauchline 1998), cyclopoid and poecilostomatoid nauplii in contrast, could start to
23
feed immediately after hatching (Uchima & Hirano 1986, Paffenhöfer 1993). Thus,
24
when picking and counting all kinds of nauplii we were ensuring to obtain the real
25
community ingestion rate on phytoplankton, although individual rates would be
16
1
underestimated. Relationships between copepods and nauplii numbers give us an idea of
2
the high mortality rates during development (e.g. due to high predation on nauplii as
3
described in Liang & Uye, 1996). This implies that the first naupliar stages should be
4
much more abundant than the last ones, translating into a significant underestimation of
5
the individual ingestion rates.
6
Specific ingestion rates ranged between 0.03-1.71 µg C µg-1 nauplii C day-1 and
7
0.03-2.82 µg C µg-1copepod C day-1. As we could not find in the literature field studies
8
regarding nauplii grazing rates in temperate seas, we compare our data with the scarce
9
information available about this issue, coming from studies carried out in high latitudes
10
and mostly focused in the largest fraction of nauplii. Our data were in the same range
11
than values presented in those studies: 0.11 - 0.46 (Irigoien et al. 2003), 0 - 0.32
12
(Hansen et al. 2000), 0.28 - 0.52 (Tackx et al. 1990), 0.79 - 2.8 (White & Roman, 1992)
13
and 0.08 - 0.29 µg C µg-1 nauplii C day-1 (Uitto 1996). Ingestion rates found for cop
14
<200 µm are also in the same range, although sometimes higher, than those reported in
15
the literature. Mauchline (1998) made a review of copepod ingestion rates on
16
phytoplankton and reported mean values ranging between 0.02 - 1.83 µg C µg-1copepod
17
C day-1 for copepodites and 0.013 - 1.5 for adult copepods.
18
Functional responses
19
The study of functional responses provides a useful tool to predict the trophic
20
impact caused by copepods when specific experiments are not possible to conduct. Two
21
conceptual models (Lam & Frost 1976; Lehman 1976) pointed out that a type III
22
functional response (Holling 1965) is the one that maximizes the net gain of energy for
23
a copepod. They predict that below a critical food concentration the energy expenditure
24
of the feeding process is higher than the gain from the assimilation of the food
25
collected. Thus, an animal in this situation may reduce the feeding activity to minimize
17
1
the energy loss or even cease it. We have found that a type III model was the one that
2
best fit our data. However, differences between models were not significant, and in
3
Figure 10 we can observe type III plot have a positive “Y intercept”. Thus, it would
4
predict an unreal situation, individuals with chlorophyll in their guts when there is no
5
phytoplankton in the environment. Although López et al. (2006) observed a better fit to
6
a type III model with nauplii feeding on phytoplankton cultures; we think in this case
7
type II would be more suitable. The difference between type II and type III models is a
8
reduction in the ingestion at low food concentrations predicted by type III. We have
9
obtained the functional responses by studying only the ingestion on autotrophic preys,
10
but most copepods feed as omnivores (Turner 2004), and the abundance of
11
heterotrophic preys could explain the high data variability around the values predicted
12
by the model. During each sampling period, heterotrophic preys could be completing
13
copepods diet up to a different level. On the other hand, the presence of different
14
choices when phytoplankton abundance is low, would explain that we do not observe a
15
type III response, as copepods could continue filtering at the same rate, taking
16
advantage of all kinds of preys and not compromising their energy balance.
17
Experiments involving all kinds of preys would be necessary to elucidate this aspect.
18
Both stages showed saturation responses at around 240 µg C l-1, although the
19
scarcity of samples at higher concentrations could have biased the calculation. Such
20
high concentrations can only be found in our study area during the beginning of the
21
spring phytoplankton bloom. Frost (1972) found a similar saturation concentration for
22
adult females. In contrast, experiments with nauplii in laboratory (López el al. 2006)
23
showed 2 to 3 times higher saturation concentrations. López et al. had already
24
suggested, that nauplii in natural conditions, where preys with more suitable sizes are
18
1
available, would probably reach saturation responses at lower chlorophyll
2
concentrations.
3
Nauplii vs. copepods
4
The study of Huskin et al. (2006) carried out during 1998 (same methodology
5
and area) for copepods >200 µm (cop >200 µm), gave us a valuable opportunity to
6
compare ingestion rates for the different sizes and development stages. Huskin et al.
7
found that cop >200 µm in stations E1 and E2 ingested on average 7 % of chlorophyll
8
standing stock daily, ranging between 0.36 and 25.5 %, and between 1 and 53 % for
9
daily primary production in E2. The ingestion rates we have found for the <200 µm
10
fraction averaged 2.8 % of chlorophyll standing stock and 5.7 % of daily primary
11
production. Thus, the total copepods ingestion on phytoplankton would never reach
12
100% of primary production, although during a few months in the year it would surpass
13
50%, having then a significant role in the control of phytoplankton populations. Not
14
including the fraction <200 µm when measuring copepods community ingestion rates,
15
would imply an underestimation of about 30 %. A similar proportion of C ingested by
16
the different stages of copepods was obtained by Sommer et al. (2000), as they found
17
that copepods ingestion on seston particles was four times higher than that of nauplii.
18
To compare individual ingestion rates between the different sizes and stages of
19
copepods, we have transformed ingestion rates reported by Huskin et al. to specific
20
ingestion rates. As copepods length and/or weight had not been measured in the
21
previous study, a sample was taken in station E2 with a WP-2 net (200 µm mesh) and
22
fractionated in the same way that they did (200-500 µm, 500-1000 µm and > 1000 µm).
23
In the laboratory, a sample of 60 copepods from each fraction was measured under a
24
stereomicroscope, obtaining an average length for each fraction and calculating C
25
weight with the same equation used for cop <200 µm. All the data from both studies
19
1
have been plotted in Figure 12. The data for cop >200 µm are only guiding values as we
2
made an error by using the same average size for all the samples. Previous studies have
3
suggested nauplii may have weight-specific ingestion rates 3 - 4 times higher than
4
adults (Lonsdale et al. 1996, Paffenhöfer 1971). We have calculated average specific
5
ingestion rates of 0.56 for nauplii, 0.71 for cop <200 µm, 0.42 for cop 200-500 µm, 0.29
6
for cop 500-1000 µm and 0.09 for cop >1000 µm. There is a trend of decreasing
7
specific ingestion rate with increasing body weight. The presence of non-feeding stages
8
in the nauplii assemblage would have lead to an underestimation of individual ingestion
9
rates that would explain the lower differences found between large copepods and nauplii
10
rates in comparison with previous studies, as to perform grazing experiments in the
11
laboratory only feeding stages are selected.
12
13
This study has allowed a deeper insight in copepods population dynamics in the
14
Cantabrian sea, by including the fraction < 200 µm for the first time. The study of the
15
whole community has been necessary for a better understanding of population
16
dynamics. However, when modelling carbon fluxes in the ocean, it is necessary to have
17
in mind that all stages of copepods must not be considered as an only group but as
18
different compartments. Due to the small size of their pellets, nauplii are not likely to be
19
important participants in the biological pump as adult copepods, but they may play an
20
important role in surface recycling processes (Green et al. 1992). They have also been
21
suggested to be critical intermediaries between “classical” and microbial food webs as
22
they can feed on pico and nanoplankton (Turner & Tester 1992, Roff et al. 1995) that
23
larger copepods may be unable to consume directly. We have found another important
24
zooplanktonic component in the area were appendicularians. Their grazing rates have
25
been estimated in a previous seasonal study (López-Urrutia et al. 2003), finding they
20
1
translated into, on average, 8 % of the daily primary production, reaching values as high
2
as 60 %. This means gelatinous zooplankton could be ingesting in some cases a higher
3
amount of phytoplankton than copepods. They are suggested to exploit the same size
4
fraction as nauplii, thus, they would also act as a nexus between both “classical” and
5
microbial food webs. In contrast, they produce larger fecal pellets which would not
6
participate in recycling processes.
7
Although the sparse information available on copepod nauplii makes it difficult
8
to assess their quantitative and ecological importance, this study has provided a first
9
approach of their impact on phytoplankton populations in temperate seas, which will
10
help us to reach an unbiased global view of the role of metazooplankton as consumers
11
of phytoplankton.
12
13
ACKNOWLEDGEMENTS
14
This work was funded by the collaboration specific agreement between
15
Universidad de Oviedo and Instituto Español de Oceanografia: “Control a largo plazo
16
de las condiciones químico-biológicas en la plataforma continental de Asturias” (SV97
17
IEO1), the CICYT project MAR1999-1072-C03-03, the FICYT project “Apoyo a
18
Grupos de Excelencia” and a FPU grant by MEC to E.L. We wish to thank the crew of
19
the R/V “Jose Rioja” for their help to collect samples. Thanks are also given to the
20
Group of Biological Oceanography of the Universidad de Oviedo for their help with the
21
sampling and I. Huskin and D. Fernández for their technical advice during the first
22
stages of this study. We are also grateful to J. L. Acuña for his useful comments on an
23
earlier version of the manuscript.
24
21
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25
Figure Legends:
Figure 1: Location of sampling stations.
Figure 2: Vertical profiles of temperature in stations E1, E2 and E3 during JanuaryDecember 2003.
Figure 3: Vertical profiles of chl-a concentration (µg chl-a l-1) in stations E1, E2 and E3
during January-December 2003.
Figure 4: Seasonal variation in mesozooplankton biomass and copepod abundance in
the three sampling stations.
Figure 5: Seasonal variation in nauplii, cop <200 µm and cop >200 µm abundance and
integrated chl-a concentration in the water column.
Figure 6: Seasonal variation in phytoplankton abundance in E2. It was used the term
“other groups” for cells belonging to minority groups and those with such a small size
that were not possible to identify with the inverted microscope.
Figure 7: Nauplii ingestion rates and average chl-a concentration in the water column
during the annual cycle.
Figure 8: Cop <200 µm ingestion rates and average chl-a concentration in the water
column during the annual cycle.
Figure 9: Nauplii and cop <200 µm grazing impact on phytoplankton biomass (in E1,
E2 and E3) and primary production (in E2) during the annual cycle.
Figure 10: Nauplii and cop <200 µm specific ingestion rates as a function of chl-a
concentration in the water. Equations for functional responses are fitted to data. Type 1
is denoted by short dashed line; type 2 by long dashed line; and type 3 by solid line.
Figure 11: Specific ingestion rates for all the stages and size fractions of copepods in
the study area during the annual cycle. Data from Huskin et al. (in press) and this study.
Average values and sample standard deviations are plotted for each size class.
26
Figure 1
27
DEPTH (m)
E1
-25
-50
50
100
150
200
250
300
350
DEPTH (m)
E2
-50
-100
50
100
150
200
250
300
350
E3
DEPTH (m)
-50
-100
-150
50
100
150
200
250
300
350
JULIAN DAYS
Figure 2
28
0
DEPTH (m)
E1
-50
50
100
150
200
250
300
350
DEPTH (m)
0
E2
-50
-100
50
100
150
200
250
300
350
DEPTH (m)
0
E3
-50
-100
50
100
150
200
250
300
350
JULIAN DAYS
Figure 3
29
biomass 200-500 µm
biomass 500-1000 µm
biomass >1000 µm
copepod abundance
E1
12000
60
8000
40
4000
20
Ju
l
Au
g
Se
p
Oc
t
No
v
De
c
0
Ja
n
Fe
b
M
ar
Ap
r
M
ay
Ju
n
0
40
E2
6000
30
mg m-3
4000
20
2000
copepods m-3
mg m-3
80
16000
copepods m-3
100
10
Ju
l
Au
g
Se
p
Oc
t
No
v
De
c
0
E3
10000
8000
15
6000
10
4000
5
2000
0
0
Ju
l
Au
g
Se
p
Oc
t
No
v
De
c
20
Ja
n
Fe
b
M
ar
Ap
r
M
ay
Ju
n
mg m-3
25
copepods m-3
Ja
n
Fe
b
M
ar
Ap
r
M
ay
Ju
n
0
Months
Figure 4
30
nauplii
copepods <200 µm
copepods >200 µm
mg chl-a m-2
2500000
E1
160
120
1500000
80
1000000
mg chl-a m-2
individuals m-2
2000000
40
500000
0
Ju
l
Au
g
Se
p
Oc
t
No
v
De
c
Ja
n
Fe
b
M
ar
Ap
r
M
ay
Ju
n
0
3000000
E2
120
2000000
80
60
1000000
40
mg chl-a m-2
individuals m-2
100
20
Ju
l
Au
g
Se
p
Oc
t
No
v
De
c
0
Ja
n
Fe
b
M
ar
Ap
r
M
ay
Ju
n
0
4000000
E3
200
2000000
100
1000000
0
Ju
l
Au
g
Se
p
Oc
t
No
v
De
c
0
mg chl-a m-2
3000000
Ja
n
Fe
b
M
ar
Ap
r
M
ay
Ju
n
individuals m-2
300
Months
Figure 5
31
other groups
cryptophyceae
prymnesiophyceae
dictiochophyceae
crysophyceae
ciliates
diatoms
dinophyceae
2000000
1000000
c
De
v
No
t
Oc
p
Se
g
Au
l
Ju
n
Ju
ay
M
r
Ap
ar
M
b
Fe
n
0
Ja
number of cells cm-2
3000000
Months
Figure 6
32
E1
0.2
8
6
0.15
4
0.1
mg cl-a eq m-3
µg C nauplius-1 day-1
0.25
2
0.05
0
0
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
E2
0.2
8
6
0.15
4
0.1
mg cl-a eq m-3
µg C nauplius-1 day-1
0.25
2
0.05
0
0
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
E3
0.2
8
6
0.15
4
0.1
mg cl-a eq m-3
µg C nauplius-1 day-1
0.25
2
0.05
0
0
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Months
Figure 7
33
E1
8
0.6
6
0.4
4
0.2
2
0
0
mg cl-a eq m-3
µg C copepod -1 day-1
0.8
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
E2
8
0.6
6
0.4
4
0.2
2
0
0
mg cl-a eq m-3
µg C copepod -1 day-1
0.8
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
E3
8
0.6
6
0.4
4
0.2
2
0
0
mg cl-a eq m-3
µg C copepod -1 day-1
0.8
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Months
Figure 8
34
% chl-a stock ingested daily
nauplii
copepods < 200µm
10
8
E1
6
4
2
0
% chl-a stock ingested daily
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
8
6
E2
4
2
0
% chl-a stock ingested daily
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
10
8
E3
6
4
2
0
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
% pp ingested daily
25
20
E2
15
10
5
0
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Months
Figure 9
35
Specific ingestion (µg C µg-1 copepod C day-1)
Specific ingestion (µg C µg-1 nauplius C day-1)
2
1.6
1.2
0.8
0.4
0
3
2
1
0
0
2
0
2
4
6
8
mg Chl-a eq. m-3
4
6
8
Figure 10
36
Specific ingestion (µgC µg-1 ind C day-1)
3
nauplii
cop < 200 µm
cop > 200 µm
2
1
0
-1
0.01
0.1
1
Carbon weight (µg C ind-1 )
10
100
Figure 11
37
Table 1. Abundance (individual m-3) of the different taxonomic groups in the fraction >200 µm. COPE- Copepods, NAU- Nauplii, APPAppendicularians, CHA- Chaetognata, DECL- Decapod larvae, EUL- Euphausiids larvae, POL-Polychaeta, CIRRL- Cirripedes larvae, JELLJellyfish, FISHE- Fish eggs, FISHL- Fish larvae, CLA- Cladocerans, OST- Ostracods, SIPHO- Siphonophors, DOL- Doliolids, AMPAmphipods, PTER- Pteropods, ECHIL- Echinoderm larvae.
Station
E1
E1
E1
E1
E1
E1
E1
E1
E1
E1
E1
E1
Month
JAN
FEB
MAR
APR
MAY
JUN
JUL
AUG
SEP
OCT
NOV
DEC
COPE
268
1469
2456
782
2557
5596
8925
4625
12959
5317
3996
605
NAU
12
30
56
35
31
664
489
42
7
147
39
15
APP
218
305
1195
27
763
1027
265
265
10
63
14
5
CHA
3
3
3
63
38
77
21
56
3
-
DECL
14
9
10
65
42
45
42
24
7
3
1
EUL
2
7
14
1
POL
1
45
45
7
12
14
10
14
17
7
3
2
CIRRL
922
1058
5
14
416
-
JELL
1
49
13
12
21
87
21
3
3
-
FISHE
15
8
10
6
10
3
56
6
8
FISHL
1
7
5
14
3
1
CLA
1
77
155
252
615
59
42
49
49
-
OST
1
45
6
-
SIPHO
15
360
20
454
161
108
91
164
112
8
2
DOL
7
203
817
171
685
11
-
AMP
1
PTER
17
7
21
112
-
ECHIL
5
14
31
3
-
E2
E2
E2
E2
E2
E2
E2
E2
E2
E2
E2
E2
JAN
FEB
MAR
APR
MAY
JUN
JUL
AUG
SEP
OCT
NOV
DEC
1074
5117
1146
926
2826
3647
1923
2878
4087
4136
2227
460
6
608
48
80
45
734
63
84
73
618
126
13
179
28
35
423
299
587
59
440
265
150
70
17
2
28
12
21
21
7
6
1
16
28
14
21
28
21
10
21
21
3
5
14
17
10
6
-
66
1
7
7
7
3
7
17
3
8
-
16760
80
49
-
1
3
7
5
70
26
63
7
52
8
1
1
24
3
7
2
3
-
7
3
-
56
134
231
9
7
119
38
-
7
-
15
133
141
119
19
35
56
147
-
14
91
999
629
475
53
-
1
-
3
14
-
10
5
63
2
14
3
-
E3
E3
E3
E3
E3
E3
E3
E3
E3
E3
E3
JAN
FEB
MAR
APR
MAY
JUN
JUL
AUG
SEP
OCT
NOV
851
8251
3828
1058
3147
3376
2613
2417
3011
4464
2719
20
1816
286
119
35
84
234
56
63
482
117
1
70
576
318
3
171
161
398
517
447
162
4
7
9
10
21
21
28
3
45
21
11
17
10
9
3
3
1
7
14
10
3
21
7
21
6
161
10
10
7
10
14
-
1125
7
2
2
-
1
7
7
7
5
9
49
91
126
8
14
-
7
1
3
7
7
-
7
77
14
7
115
28
196
189
-
6
-
1
38
196
147
35
14
42
63
119
14
3
5
265
1188
314
2187
56
7
-
14
14
14
-
1
14
17
14
-
38
Table 2. Abundance (individual m-3) of the different taxonomic groups in the fraction
<200 µm. NAU- Nauplii, COPE- Copepods, APP- Appendicularians, CIRRLCirripedes larvae.
Station
E1
E1
E1
E1
E1
E1
E1
E1
E1
E1
E1
E1
Month
JAN
FEB
MAR
APR
MAY
JUN
JUL
AUG
SEP
OCT
NOV
DEC
NAU
2173
2480
2241
1062
4317
16306
12181
26715
18835
30271
12631
4692
COPE
391
548
1509
258
887
1146
1271
5882
145003
6239
3745
685
APP
295
108
267
42
112
279
28
140
35
70
49
8
CIRRL
189
14
-
E2
E2
E2
E2
E2
E2
E2
E2
E2
E2
JAN
FEB
MAR
APR
MAY
JUN
JUL
AUG
SEP
NOV
5669
5498
7769
1740
6658
8460
10263
17445
45780
15244
1235
1184
1921
545
814
2194
1446
4555
9334
4653
129
101
182
7
91
363
154
-
148
7
14
3
-
E3
E3
E3
E3
E3
E3
E3
E3
E3
E3
E3
E3
JAN
FEB
MAR
APR
MAY
JUN
JUL
AUG
SEP
OCT
NOV
DEC
4200
7140
14594
2522
12886
13106
9746
10249
21084
48666
17535
3138
813
1097
4443
660
1740
2746
831
5379
3577
8188
3486
1095
4
35
803
227
3
84
35
91
252
182
126
70
-
39
Table 3. Mean-square error (MSE) and parameters for each of the three types of
functional responses for nauplii and cop <200 µm. Imax expressed as µg C µg-1 nauplii C
d-1 and Cd and Kc as mg chl-a m-3.
Model
Type 1
Type 2
Type 3
Nauplii
Cop <200 µm
a
Cd
0.49
3.17
0.645
1.83
Imax
1.56
1.179
MSE
0.102
0.265
a
0.65
0.94
Imax
1.72
1.58
MSE
0.102
0.262
a
0.96
0.78
kc
1.72
1.29
Imax
1.60
1.63
MSE
0.097
0.243
40