Download Carbon cycling through the pelagic foodweb in

ICES Journal of Marine Science, 61: 572e584 (2004)
doi:10.1016/j.icesjms.2004.03.021
Carbon cycling through the pelagic foodweb in the
northern Humboldt Current off Chile (23(S)
H. E. González, R. Giesecke, C. A. Vargas, M. Pavez, J. Iriarte,
P. Santibáñez, L. Castro, R. Escribano, and F. Pagès
González, H. E., Giesecke, R., Vargas, C. A., Pavez, M., Iriarte, J., Santibáñez, P., Castro,
L., Escribano, R., and Pagès, F. 2004. Carbon cycling through the pelagic foodweb in the
northern Humboldt Current off Chile (23(S). e ICES Journal of Marine Science, 61:
572e584.
The structure of the zooplankton foodweb and their dominant carbon fluxes were studied in
the upwelling system off northern Chile (Mejillones Bay; 23(S) between October 2000 and
December 2002. High primary production (PP) rates (1e8 gC m2 d 1) were mostly due to
the net-phytoplankton size fraction (O23 mm). High PP has been traditionally associated
with the wind-driven upwelling fertilizing effect of equatorial subsurface waters, which
favour development of a short food chain dominated by a few small clupeiform fish species.
The objective of the present work was to study the trophic carbon flow through the first step
of this ‘‘classical chain’’ (from phytoplankton to primary consumers such as copepods and
euphausiids) and the carbon flow towards the gelatinous web composed of both filterfeeding and carnivorous zooplankton. To accomplish this objective, feeding experiments
with copepods, appendicularians, ctenophores, and chaetognaths were conducted using
naturally occurring plankton prey assemblages. Throughout the study, the total carbon
ingestion rates showed that the dominant appendicularian species and small copepods
consumed an average of 7 and 5 mgC ind 1 d 1, respectively. In addition, copepods
ingested particles mainly in the size range of nano- and microplankton, whereas appendicularians ingested in the range of pico- and nanoplankton. Small copepods and appendicularians removed a small fraction of total daily PP (range 6e11%). However, when the
pico- C nanoplankton fractions were the major contributors to total PP (oligotrophic
conditions), grazing by small copepods increased markedly to 86% of total PP. Under these
more oligotrophic conditions, the euphausiids grazing increased as well, but only reached
values lower than 5% of total PP. During this study, chaetognaths and ctenophores ingested
an average of 1 and 14 copepods ind 1 d 1, respectively. In terms of biomass consumed,
the potential impact of carnivorous gelatinous zooplankton on the small-size copepod
community ( preferred prey) was important (2e12% of biomass removed daily). However,
their impact produced more significant results on copepod abundance (up to 33%), which
suggests that carnivorous gelatinous zooplankton may even modulate (control) the
abundance of some species as well as the size structure of the copepod community.
Ó 2004 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.
Keywords: coastal foodweb, gelatinous zooplankton, Humboldt Current system, trophic
carbon flow.
Accepted 23 March 2004.
H. E. González, R. Giesecke, and P. Santibáñez: Universidad Austral de Chile, Instituto de
Biologı́a Marina, Casilla 567, Valdivia, Chile. H. E. González and R. Escribano: Centro de
Investigaciones Oceanográficas del Pacı́fico Sur-Oriental (COPAS), Concepción, Chile.
C. A. Vargas, M. Pavez, L. Castro, and R. Escribano: Universidad de Concepción,
Departamento de Oceanografı́a, Concepción, Chile. J. Iriarte: Universidad Austral de
Chile, Instituto de Acuicultura, Puerto Montt, Chile. F. Pagès: Institut de Ciències del Mar
(CSIC), Barcelona, Catalunya, Spain. Correspondence to H. E. González: Universidad
Austral de Chile, Instituto de Biologı́a Marina, Casilla 567, Valdivia, Chile; e-mail:
[email protected].
1054-3139/$30.00
Ó 2004 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.
Carbon cycling in the northern Humboldt Current
Introduction
The frequent upwelling of cold, nutrient-rich equatorial
subsurface water (ESSW) along the coast off Antofagasta in
the northern region of the Humboldt Current system during
most of the year (Rodrı́guez et al., 1991; Marı́n and
Olivares, 1999) supports a highly productive phytoplankton
assemblage (dominated by chain-forming diatoms) that in
turn sustains a large pelagic commercial fishery. In this
coastal ecosystem, the main flux of material and energy is
assumed to flow through the ‘‘classical food chain’’ (sensu
Ryther, 1969; Steele, 1974). In contrast, systems dominated
by small-size phytoplankton components (less than 23 mm)
fuel the microbial foodwebs within the photic layer.
The ESSW is nutrient-repleted and stimulates primary
production (PP) in a narrow band (ca. 20 nmi) from the
coast (Escribano et al., 2002), which in turn promotes the
presence of copepods and their predators, such as ctenophores, fish larvae, cnidarians, and chaetognaths. A less
studied component of this trophic flux scenario is the role
played by the gelatinous components or the ‘‘gelatinous
foodweb’’. Gelatinous carnivorous zooplankton groups are
common in most pelagic trophic webs and they are key
components in the pelagic system (Båmstedt, 1990). They
seem to be opportunistically positioned to utilize secondary
production that is ordinarily consumed by fish (Mills,
1995). Because of the rapid population growth of most
gelatinous species (Hopcroft et al., 1998), high density of
these organisms often occurs during the periods of high PP.
573
However, the potential role of the gelatinous groups modulating the seasonal zooplankton abundance in upwelling
areas is still unclear, partly because there are too few estimates of their production rates and partly because estimates
of predation rates of these gelatinous groups are almost
non-existent to date in upwelling systems off Chile.
Five research cruises (GEMINIS IeV: GElatina Marina:
Inicio de Nuevas Investigaciones del Sistema): Austral
spring 2000 (19e23 October), Austral summer 2001 (2e11
February), Austral winter 2001 (1e11 August), Austral
spring 2001 (20e30 October), and Austral spring 2002 (30
Novembere8 December: only experimental work with ctenophores) were conducted at a 130-m-deep permanent
station (23(00.15#S; 70(26.43#W), located at ca. 8 nmi
from the coast on the continental shelf. Simultaneously
with the cruises, experimental studies on feeding behaviour
of principal crustaceans and both gelatinous carnivores and
filter-feeders were carried out at a coastal marine laboratory
in Mejillones Bay (Figure 1).
The main objectives of this study were twofold. The first
objective was to estimate the carbon flux through the first
step of the ‘‘classical’’ foodweb in a coastal marine system
from PP to dominant crustaceans grazers (copepods and
euphausiids). The second objective was to estimate the
fraction of PP consumed by appendicularians and the fraction of the small-size copepod standing stock consumed by
gelatinous carnivores, such as chaetognaths and ctenophores (Figure 2).
10
22.8
0
22.9
10
Pacific
Ocean
23
Exp
20
30
23.1
Mejillones
40
23.2
23.3
70.7
50
70.6
70.5
70.4
Longitude (W)
70.3
90
80
70
60
Longitude W
Figure 1. The study area Mejillones Bay (23(S) showing the position of the permanent station (*exp.).
Latitude S
Latitude (S)
Lat. N
22.7
574
H. E. González et al.
“Classical” Food Chain
Phytoplankton
Primary Production
“Herbivores”, Omnivores
(PP)
?
(Copepods, Euphausiids)
Small pelagic
fishes
Heterotrophs
(1)
“leakage” (2)
“leakage” (3)
Filter-feeders
Carnivores
(Appendiculareans, Salps)
(Chaetognaths, Ctenophores
Siphonophore
Other Pathways
Microbial loop
Microplankton respiration
Vertical flux
Lateral advection
?
Fish larvae - eating
Siphonophores)
“Gelatinous” Foodweb
Figure 2. A conceptual model of carbon flow through the ‘‘classical’’ pelagic foodweb in Mejillones Bay including losses (‘‘leakage’’)
toward the ‘‘gelatinous’’ foodweb. Numbers in parentheses indicate the three trophic pathways estimated in the present study: (1) Grazing
impact (as %PP) exerted by metazooplankton (copepods + euphausiids). (2) Grazing impact (as %PP) exerted by filter-feeding gelatinous
zooplankton (appendicularians). (3) Predation impact (as percent small copepod standing stock) exerted by carnivorous gelatinous
zooplankton (ctenophores and chaetognaths).
Materials and methods
Phytoplankton fractionated biomass (PB) and PP
Water samples for PP experiments were collected using 5-l
PVC Go-Flo bottles at three depths within the euphotic zone:
surface, subsurface chlorophyll a (Chl a) maximum and 2%
light penetration depth. Water samples (two replicates for
each depth) were incubated in 100-ml bottles (two clear
and one dark) and placed in a natural-light incubator for
4 h (mainly between 10:00 and 14:00). Temperature was
regulated by running surface seawater over the incubation
bottles. For the subsurface samples, the light intensity was
attenuated using a screen to replicate levels similar to those
at the depth where the water was collected. Sodium bicarbonate (40 mCi e NaH 14CO3) was added to each bottle. The
extent of light (PAR) penetration was determined using
submersible sensors (QSP 200-D, Biospherical Instruments). PP was measured using the method described by
Steemann Nielsen (1952). Phytoplankton size fractionation was carried out in three consecutive steps: (1) for the
Carbon cycling in the northern Humboldt Current
nanoplankton fraction (2.0e23 mm), seawater was prefiltered using 23-mm Nitex mesh and collected on a 2.0-mm
Nuclepore; (2) for the picoplankton fraction (0.7e2.0 mm),
seawater was pre-filtered using a 2.0-mm Nuclepore and
collected on a 0.7 mm MFS filter; (3) for the whole phytoplankton community, 100 ml of seawater was filtered through
a 0.7 mm MFS filter. The micro-phytoplankton fraction was
obtained by subtracting the production estimated in steps (1)
and (2) from the production estimated in step (3).
Samples were handled under attenuated light conditions
during pre- and post-incubation periods. The contents were
filtered according to the fractionation procedures mentioned
above. Filters (0.7 and 2.0 mm) were placed in 20-ml
scintillation vials, kept at 15(C until reading (15 d later).
To remove the excess inorganic carbon, filters were treated
with HCl fumes for 4 h. Scintillation cocktail (10 ml,
Ecolite) was added to vials and radioactivity was determined in a scintillation counter (Beckman).
Fractionated Chl a measurements were taken at the same
stations and at depths where PP experiments were performed. Seawater samples (150 ml) were filtered and
analysed using a digital Turner AU-10 fluorometer, as recommended by Parsons et al. (1984). The size-fractionated
procedure was the same as that for PP. Additional water
samples (250 ml) to estimate flagellate and ciliate abundance were collected from 50-m depth (the middle point of
the zooplankton water column sampled) and processed
according to Utermöhl (1958).
Vertical flux and phytoplankton carbon
The vertical flux of particulate matter was measured using
paired drifting, cylindrical-shaped sediment traps (modified
from Gundersen, 1991) with a 122 cm2 catchment area and
a height:diameter ratio of 8.3. Traps were deployed at 50
and 100-m depths for periods ranging between 1 and 2 d.
Before deployment, 1 ml of saturated HgCl2 solution was
added per 250 ml of sample solution (GF/F-filtered seawater) to retard bacterial activity in the trap material (Lee
et al., 1992). Subsamples from the traps were taken for
estimations of dominant microplankton taxa and faecal
material using standard microscopic methods (Utermöhl,
1958). Phytoplankton carbon, based on cell volume, was
estimated after counting and sizing the different species
according to Edler (1979). Faecal material carbon was
estimated after counting and sizing the undamaged faeces
and their fragments. The faecal volume was estimated assuming that copepod and euphausiid faeces have a cylindrical shape and the appendicularian faeces have an
elliptical shape. The faecal carbon content was estimated
from the relationship proposed by González and Smetacek
(1994): mgCfaecal ¼ 0:076 Volfaecal ðmm3 Þ.
Zooplankton
Vertical net hauls were taken using a WP-2 net towed
vertically (0.25 m2 opening and mesh size of 200 mm;
575
UNESCO, 1968) and equipped with a closing mechanism
that allowed sampling at three different depth strata: 0e25,
25e50, and 50e100-m depth. A TSK flowmeter was
mounted between the middle and the ring of the net
opening to quantify the water volume filtered by the net.
Euphausiids ( juvenile and adults), as well as large copepods that may have avoided the WP-2 net, were counted
from samples collected using bongo net (300 mm) tows.
Metazooplankton was divided into four classes: small
copepods (!1500 mm), large copepods (O1500 mm), euphausiids (juvenile and adults), and appendicularians.
Twice a day, profiles of temperature and oxygen were
recorded at selected depths using a CTD. The animals were
fixed immediately after collection in 5% sodium tetraborate
buffered formaldehyde seawater.
In order to estimate in situ zooplankton abundance,
whole samples were subsampled using a Folsom splitter
and all specimens were counted under a stereomicroscope.
Subsample size depended on the abundance of zooplankton
in the sample: in cases where the samples were too
concentrated, the analysed fraction ranged between 1/32
and 1/128 of the total. In cases where the samples were less
concentrated, the whole sample was analysed.
Zooplankton collected for experiments
Experiments to estimate digestion time and ingestion rates
were conducted using animals collected from the upper
30 m by vertical net hauls (0.3 m s1) with a large nonfiltering codend of approximately 25 l. This codend reduced
individual damage during the sampling (Feigenbaum and
Maris, 1984). Immediately after collection, the codend
content was transferred into a thermo box in order to
maintain the animals in good condition during their transport to the coastal laboratory (approximately 20 min).
Chaetognaths
In the laboratory, single Sagitta enflata of 12:6G1:7 mm
in length were sorted with a wide-bore pipette, placed in
600-ml bottles containing 50 mm filtered seawater, and kept
for at least 24 h at in situ (17(C) temperature. Surviving
chaetognaths were fed with small-size copepods !1000 mm
in numbers ranging between 160 and 460 ind l 1. Each of
the 600-ml bottles containing S. enflata was observed every
15 min to determine the digestion time (DT), where DT was
the time between food ingestion and defecation.
The experiments were carried out under 12-h low light
and 12-h darkness conditions to simulate a natural environment and to minimize stress for the individuals. After 24 h,
the animals, their faecal pellets, and the remaining food were
preserved in 5% formaldehydeeseawater buffered with
sodium tetraborate. Afterwards, the size of each S. enflata
was measured and the number of copepods was counted.
More details on these methods are provided elsewhere
(Giesecke and González, submitted for publication).
In order to account for codend feeding, prey found in
the foregut (upper quarter of the gut) were recorded, but
576
H. E. González et al.
omitted for the analysis (Feigenbaum and Maris, 1984).
Partially digested copepods in the chaetognath guts were
identified by means of their mandible morphology (unpublished data). The daily feeding rates (FR) of S. enflata were
estimated using the formula proposed by Bajkov (1935):
FR ¼ ðNPC=DTÞ!24
where NPC is the number of prey per chaetognath and DT
is the digestion time (h).
Ctenophores
Individuals of the species Pleurobrachia sp. (7e10 mm
oraleaboral length) were sorted and placed in 6-l incubation jars. The ctenophores were maintained in these
jars filled with filtered seawater (37 mm) at the same field
temperature for 6 h to allow gut emptying. They were then
placed in new jars under the same conditions and the
dominant copepod species in the field for each year were
added as prey. The utilized copepod densities corresponded
to the normal range of natural densities observed in the field
in the study area (Escribano and Hidalgo, 2000). In spring
2000, the dominant Acartia tonsa were used as prey and the
experiment was run at 12(C. In 2001 and 2002, the dominant Paracalanus parvus were used as prey and the experiments (two sets in 2001 and three sets in 2002) were
conducted at 15(C. The duration of the predation experiments varied from 6 to 8 h, after which the water from the
jars was filtered (37-mm mesh), the live remaining
copepods were counted and the carcasses on the jar bottom
were also quantified. The predation rate (Pr; copepods*
ctenophore1*d 1) was estimated from the clearance rates
following Buecher and Gasser (1998):
Pr ¼ nm C
C ¼ ðlnðni Þ lnðnf ÞÞ V=NT
where C is the clearance rate (litresctenophore1d 1), ni
is the initial density of prey in the jar (copepodsl 1); nf is
the final density of prey in the jar (copepodsl 1); V is the
jar volume (l), N is the number of predators, T is duration
of the experiment (days), Pr is predation rate (copepods
ctenophore1d 1), and nm is the mean number of prey in
the experimental jars (copepodsl 1).
Appendicularians and small copepods
Undamaged copepods were sorted under a stereomicroscope,
and appendicularians with intact houses were carefully
isolated with a wide-mouthed pipette and transferred to
500 ml acid-washed polycarbonate bottles with ambient
water and filled to the top to avoid bubbles. Three control
bottles without animals and three bottles with 3e5 animals
each were placed on a plankton wheel (0.2 rpm) in darkness
and in situ temperature for approximately 15e20 h. Initial
control bottles were immediately preserved with 2% Lugol’s
acid and a subsample was preserved in glutaraldehyde (6%
w/v). After incubation, subsamples from all bottles were
taken and preserved in glutaraldehyde for bacterial biomass
(5 ml) and nanoflagellate counts (20 ml) and preserved in
Lugol’s acid (60 ml) for cell concentration. Phytoplankton
were counted under a Leica LEITZ DMIL inverted microscope according to standard procedures (Utermöhl, 1958).
Plasma volume and carbon content were estimated for
diatoms, dinoflagellates, and autotrophic flagellates (Edler,
1979). Ingestion rates were estimated in accordance with
Frost (1972). Ingestion rates by large copepod and euphausiids were estimated from previous work in the study area
(González et al., 2000).
Results
Hydrography
The upper boundary of the oxygen minimum zone (OMZ,
!1 ml O2 l 1) associated with the ESSW was located at
about 30e40-m depth in spring and summer (Geminis I, II,
and IV). In winter (Geminis III), upwelling became more
intense due to increasing southerly winds and the OMZ
occurred at a depth of nearly 10 m (Figure 3). In spring, the
thermocline was located at a depth of ca. 20 m during day
and night. In summer, a shallowing of the thermocline was
observed between the first and the second sampling dates.
Because of the strong upwelling events in winter, the
normal mixture of Sub-Tropical Water (STW) and SubAntarctic Waters (SAAW) at the surface layer did not occur
and the surface layer was dominated by ESSW, characterized by low temperatures. This condition prevented the
formation of a marked thermocline due to displacement of
cold water to the surface, as shown in Figure 3.
Phytoplankton biomass and PP
During the cruises Geminis IeIII, long-chain-forming diatoms (O23 mm) such as Chaetoceros spp., Guinardia
delicatula, Rhizosolenia spp., Detonula pumila and Eucampia cornuta constituted more than 70% of the total
phytoplankton abundance. Autotrophic and heterotrophic
cells contributed equally to the nanoplankton (2e23 mm)
pool.
High values of Chl a and PP were measured with a
predominance (O50%) of the net-phytoplankton fraction
(O23 mm), represented mainly by diatoms (Tables 1 and 2).
Unexpectedly, the vertical particulate flux was low, ranging
between 0.2% and 3.1% of total PP in February and
October 2001, respectively. Phytoplankton cells contributed the bulk of POC sedimentation (ca. three-fourth of total
sedimentary POC), while faecal material contributed only
ca. one-fourth of total carbon sedimentary matter.
Copepods and appendicularians
The highest abundances of copepods were found in the upper
layer (50 m), where the !1500 mm prosome length
Carbon cycling in the northern Humboldt Current
Temperature (ºC)
Temperature (ºC)
12
13
14
15
16
17
18
12
13
14
2
3
4
5
6
0
7
0
0
-20
-20
-40
-40
Depth (m)
Depth (m)
1
-60
-80
16
1
2
3
4
17
18
6
7
l-1)
5
-60
-80
-100
-100
October 2000
February 2001
-120
-120
Temperature (ºC)
12
13
14
15
16
Temperature (ºC)
17
12
18
13
Oxygen (ml l-1)
0
1
2
3
4
5
14
15
16
17
18
Oxygen (ml l-1)
6
0
7
0
0
-20
-20
-40
-40
Depth (m)
Depth (m)
15
Oxygen (ml
Oxygen (ml l-1)
0
577
-60
-80
-100
August 2001
-120
1
2
3
4
5
6
7
-60
-80
-100
October 2001
-120
Figure 3. Vertical distribution of temperature (continuous line; (C) and dissolved oxygen (broken line; ml l 1) at the permanent station in
Mejillones Bay during October 2000, February 2001, August 2001, and October 2001.
copepods Paracalanus parvus, Centropages brachiatus,
Acartia tonsa, Oithona spp., Oncaea spp., and Corycaeus
spp. were the most abundant on all cruises, reaching 80e91%
of the entire copepod community. No clear evidence of
diel changes in vertical distribution was found in either
year. Estimation of average ingestion rates for small
copepods ranged from 4.1 and 6.3 mgC ind 1 d 1 for
October 2000 and August 2001, respectively (range of
2e8 mgC ind 1 d 1) (Table 1). The contribution of heterotrophic prey to small copepod rations varied from 15% in
August 2001 to 35% in October 2000. The appendicularian
community was dominated by Oikopleura dioica, except in
August 2001 when O. longicauda were more abundant.
Appendicularian ingestion rates fluctuated between 4.4 and
6.5 for O. dioica, and 8.8 mgC ind 1 d 1 ( for O. longicauda) and for both species almost a quarter of their rations
were obtained from heterotrophic prey (Table 1). Metazooplankton showed a combined grazing impact (as % PP
removed daily) that ranged between 7.5% (February and
August 2001) and 115% (October 2001) (Figure 4).
The gelatinous zooplankton was dominated by ctenophores and chaetognaths.
Chaetognaths
Five species of chaetognaths were collected. Sagitta
enflata, the most abundant species, represented up to 65%
of all chaetognaths by number followed by Sagitta bierii
(34%). S. enflata was mainly distributed above the OMZ,
while the bulk of S. bierii remained below this zone.
The digestion time of small copepods ingested by
S. enflata at 17(C was estimated in nine experiments and
578
H. E. González et al.
Table 1. Average values of chlorophyll a and vertical flux rate and abundances and ingestion rates of dominant metazooplankton both
chitinous (copepods and euphausiids) and gelatinous (ctenophores, chaetognaths, and appendicularians) in Mejillones Bay between
October 2000 and 2001. Integrated values for the upper 50-m water column. n.d. Z no data.
Geminis 1
(October 2000)
Geminis 2
(February 2001)
Geminis 3
(August 2001)
Geminis 4
(October 2001)
Chlorophyll a conc. (mg m2)
Vertical flux rate (mgC m2 d 1)
89
n.d.
585
10
695
61
47
35
Abundance (ind. m2)
Copepods O1 500 mm
Copepods !1 500 mm
Chaetognaths
Ctenophores
Euphausiids
Appendicularians
6 900
224 150
916
493
200
n.d.
2 800
44 900
962
311
50
7 679
2 000
57 650
180
311
400
3 881
11 600
196 100
1 000
129
500
835
Appendicularians
23.7
4.1y H ration = 35%;
A ration = 65%
n.d.
95.1
23.7
6.3z H ration = 15%;
A ration = 85%
8.8{ H ration=22%;
A ration=78%
95.1
23.7
4.9x H ration = 23%;
A ration = 67%
4.4k
Euphausiids*
23.7
5.0z H ration = 25%;
A ration = 75%
6.5k H ration = 25%;
A ration=75%
95.1
95.1
Ingestion rate (copepods
predator1 d 1)
Chaetognaths
Ctenophores
0.9
11.5
0.7
14.3
1.1
14.3
0.9
15.5
Grazing rate (mgC ind.1 d 1)
Copepods* >1 500 mm
Copepods !1 500 mm
%P + Nplank. = % of pico- + nanoplankton-PP with respect to total PP. H ration = heterotrophic fraction (%) of total ration; A
ration = autotrophic fraction (%) of total ration.
*
From González et al. (2000).
y
Dominated by Acartia tonsa and Centropages brachiatus.
z
Dominated by Acartia tonsa and Paracalanus parvus.
x
Dominated by Paracalanus parvus and Centropages brachiatus.
k
Dominated by Oikopleura dioica.
{
Dominated by Oikopleura longicauda.
ranged between 0.85 and 3.5 h, with an average of 2:2G1 h.
A total of 786 guts were analysed and their contents
identified (233 in spring 2000, 464 in summer, and 89 in
winter 2001). Mean average values of NPC obtained for
austral spring, summer, and winter were not significantly
different, corresponding to 0.088, 0.086, and 0.093 prey
chaetognath1, respectively (t-test, p!0:005). Feeding rates
were relatively constant within the upper layer (0e25-m
depth) on each sampling date (w1.2 prey S. enflata d 1),
decreasing with depth. The predation was centred principally on small copepods, with higher chaetognath-feeding
activity at night. The daily predation impact over the total
standing stock of small copepods varied seasonally between
6% in spring and 0.4% in winter. At prey generic level, S.
enflata consumed a daily average of 16, 5, 9, 3, 7, and 2% of
Corycaeus, Acartia, Centropages, Oncaea, Oithona, and
Paracalanus populations, respectively (Table 3).
In spring and winter, the predation impact was mostly on
the cyclopoid community with a high impact on Corycaeus
sp. In summer, the highest predation impacts were on the
calanoid community, particularly on C. brachiatus, with
a daily removal of the standing stock of ca. 22%.
Ctenophores
Pleurobrachia sp. ( probably P. bachei) was the dominant
ctenophore in the area. The abundance of Pleurobrachia sp.
was much higher in spring 2000 (565 ind. m2) than in
spring 2001 (129 ind. m2). Peak densities of specimens
with copepods in their guts were 47.4 ind. m2 and
12.4 ind. m2 at the permanent station in October 2000
and 2001, respectively. Pleurobrachia sp. occurred mainly
in the upper 50 m and no evidence for diel vertical
migration was discerned in either year.
The oraleaboral length of 1111 Pleurobrachia sp.
ranged between 2 and 10 mm, with a dominance of small
sizes (2e3 mm). The most frequent prey in Pleurobrachia
sp. gut contents were copepods ranging between 0.5 and
Carbon cycling in the northern Humboldt Current
579
Table 2. Mean values of fractionated PP (mgC m3 h1) estimated from the photic layer and protozoan (ciliates and flagellates) abundance
(ind. l 1) collected at 50-m depth in the permanent station of Mejillones Bay.
PP picoplankton (mgC m3 h1)
PP nanoplankton (mgC m3 h1)
PP net-phytoplankton (mgC m3 h1)
Abundance (ind. l 1)
Athecate dinoflagellates
Thecate dinoflagellates
Ciliates (mainly
Strombilidiids)
Flagellates
Geminis 1
(October 2000)
Geminis 2
(February 2001)
Geminis 3
(August 2001)
Geminis 4
(October 2001)
1.61
12.29
20.39
1.28
1.27
15.30
3.26
8.65
26.26
1.29
0.21
0.29
100
982*
180
160
80
230
430
210
5 640y
100
40
440
60
120
80
120
*
Bloom of Prorocentrum micans.
High numbers of Myrionecta rubra.
y
1.5 mm prosome length. Among the copepods consumed,
the most frequent taxa were small calanoids that usually
dominated the copepod community off Mejillones (i.e.
Paracalanus parvus, Acartia tonsa) and small-size cyclopoids such as Oithona sp. and Oncaea sp.
Experimentally determined mean predation rates of
Pleurobrachia sp. on the dominant copepods reached
11.5 cop cten1 d 1 in October 2000, and 15.5 cop cten1
d 1 in October 2001 (Table 1). In December 2002 the
mean predation rates varied between 13.8 and 16.1 cop
cten1 d 1 (mean 14.8 cop cten1 d 1), and they did not
differ with other experiments (ANOVA, p ¼ 0:757) when
compared with those obtained during the previous two
years (ANOVA, p ¼ 0:513).
Ctenophores removed a low fraction (ca. 1%) of the
total small-size copepod biomass daily. However, during
October 2001, when the copepod preys were analysed at the
population level, Pleurobrachia sp. consumed a daily
average of 2.3, 3.5, and 0.3% of the Corycaeus, Acartia,
and Paracalanus populations, respectively (Table 3).
Discussion
In the sampling area there was a seasonal change in the
occurrence of the principal gelatinous species which was
associated with a shift of the predominant water masses in
the upper 100-m depth ( from SAAW and ESSW in spring to
a mixture of STW, SAAW, and ESSW in summerewinter).
During the springs of 2000 and 2001, Pleurobrachia sp. and
S. enflata were two of the most abundant gelatinous
predators and both occurred primarily in SAAW. Alternatively, and associated mostly with STW, the siphonophore
Bassia bassensis has been reported as the dominant gelatinous predator offshore in summer (Pagès et al., 2001).
The predatory impact of Sagitta enflata was more evident
in the upper 50 m water column, where this species was
more abundant. An average abundance of 19 ind. m3
was recorded in this layer during the summer 2001 and
4 ind. m3 during the winter 2001. Similar abundances
have been reported in the HCS off central Chile (1e20 ind. m3, Ulloa et al., 2000) as well as in the Benguela
Current system (3 ind. m3; Duró et al., 1994).
The distribution and predatory activities of chaetognaths
seem to be strongly influenced by the presence of the OMZ.
The most abundant species, S. enflata, was distributed
mainly in the well-oxygenated upper 25 m, and S. bierii
was found principally at depths below 50 m, in the OMZ.
Bieri (1959) characterized S. bierii as a species that is
normally associated with poor oxygen concentrations.
Chaetognath FR estimates (!1.3 prey ind.1 d 1) were
in the lower range of the observations in the literature. For
example, Øresland (2000) reported total FR estimates of
S. enflata between 4.7 and 1.3 prey ind.1 d 1, whereas
Kimmerer (1984) and Szyper (1978) reported between 10
and 12 prey ind.1 d 1 and 7.4 prey ind.1 d 1, respectively.
In Kanaobe Bay (Hawaii), Feigenbaum (1979) reported
ingestion rates between 1.7 and 2.9 prey ind.1 d 1. These
differences in our study are attributable to the low percentages of S. enflata specimens having gut contents
(4e18%) compared with the above-mentioned studies
(5e37%). The small proportion of individuals having gut
contents in our study could be attributed to the much lower
temperature in our sampling area (!17(C) (compared to
the other cited works), which could affect feeding rates of
S. enflata, since temperature has a direct effect on metabolism and, therefore, on ingestion rates; or it could have
been that chaetognaths had defecated or regurgitated during
sampling (Baier and Purcell, 1997). During laboratory
analysis of the samples, we observed a large number
of individuals with an expanded posterior gut containing big absorptive cells. This provided evidence of recent
defecation (Feigenbaum and Maris, 1984), and could have
led to an underestimation of predation impact.
The daily predation impact of chaetognaths on the small
copepods standing stock in the 0e50-m depth range varied
580
H. E. González et al.
a) October 2000
?
PP
8184
?
Vertical
flux
b) February 2001
?
PP
4622
?
Vertical
flux
c) August 2001
?
PP
6479
?
Vertical
flux
d) October 2001
?
PP
1116
Vertical
flux
?
Figure 4. Primary production (mgC m2 d 1), vertical flux of particles and carbon flow through the ‘‘classical’’ and ‘‘gelatinous’’
foodwebs at the permanent station in Mejillones Bay during October 2000, February 2001, August 2001, and October 2001.
Carbon cycling in the northern Humboldt Current
581
Table 3. Copepod abundance (ind. m3) and species-specific predation impact exerted by Sagitta enflata (Geminis 1e3) and
Pleurobrachia sp. (Geminis 4) (expressed as percent standing stock) on the most abundant small copepods at the permanent station of
Mejillones Bay.
Geminis 1
(October 2000)
Geminis 2
(February 2001)
Geminis 3
(August 2001)
Sagitta enflata
Species
Paracalanus
parvus
Centropages
brachiatus
Acartia tonsa
Oithona sp.
Oncaea sp.
Corycaeus sp.
Geminis 4
(October 2001)
Pleurobrachia sp.
Abundance
(ind. m3)
Predation
impact (%)
Abundance
(ind. m3)
Predation
impact (%)
Abundance
(ind. m3)
Predation
impact (%)
Abundance
(ind. m3)
Predation
impact (%)
252
3.9
575
0.6
167
0.1
997
0.3
131
5.7
36
21.5
6
0.0
35
0.0
220
57
19
5
11.2
13.8
1.7
32.9
321
134
239
61
4.2
0.9
1.2
9.6
98
123
51
16
0.4
4.8
4.8
4.2
48
408
196
118
3.5
0.0
0.2
2.3
between 4% in (spring) and 0.85% (in winter), percentages
that agree with previous reports. Øresland (2000) estimated
a predation impact of ca. 1% in the western Indian Ocean
and Terazaki (1996) estimated ca. 7.9% in the Central
Equatorial Pacific. But the daily predation impact increased
substantially when analysed at the species level. In summer, the major impacts were on the calanoid copepod
C. brachiatus, where daily removal of the standing stock
was about 21.5% (Table 3). Considering that this species
has a development time of ca. 30 d (unpublished data), the
population could be drastically reduced in numbers in
a short period of time (assuming that the daily predation
impact remains constant). During the spring, the major
impacts were on Corycaeus sp. when S. enflata ingested
daily ca. 33% of their standing stock. Acartia tonsa,
a species with a development time of ca. 20 d (Landry,
1983), could be drastically affected by the predation of
S. enflata in spring and summer when the daily removal of
the standing stock varied between 11% and 4%, respectively. In winter, due to the greater abundance of small
cyclopoid copepods, the bulk of the feeding pressure was
on this group, which had a relative impact around 4.6% of
the standing stock. Since small cyclopoids like Oithona sp.
and Oncaea sp. have development times of ca. 20e30 d
(Paffenhofer, 1993; Sabatini and Kiørboe, 1994), this
predation impact may be almost negligible. All these estimates should be interpreted with caution, because the predation impact depends primarily on the in situ abundance of
the different items of prey.
In the predation experiments with ctenophores, prey
densities (8e16 cop. l 1) within and exceeding the upper
range of copepod densities observed in the field
(1e10 cop. l 1) were used in both years. Another factor
to consider in this type of study is the volume of the containers, since ctenophores tend to retract their tentacles and
hence cover a smaller area when they sense the container
walls (Buecher and Gasser, 1998; but see also Gibbons and
Painting, 1992, for Pleurobrachia sp.). To test for this effect
in this study, the container volume was increased by
a factor of 2 ( from 3 to 6 l volume). We did not observe
considerable differences in predation rates (14:2G2:6 and
14:8G1:2 cop. cten1 d 1) between the two containers.
Considering that the predator densities were maintained
similarly to field conditions and that similar results were
observed for all years, it seems likely that the predation rate
estimations are similar to those occurring at sea.
The vertical distribution of Pleurobrachia sp. was restricted to the top 50 m of the SAAW layer. Pagès et al.
(2001) have already proposed an apparent association of
this ctenophore with SAAW in the same area. Below this
layer, the presence of colder, oxygen-depleted ESSW may
have limited the vertical distribution of ctenophores, as has
been observed in other zooplankton (Escribano, 1998). No
evidence of diel vertical migration by Pleurobrachia sp.
was observed at any station.
The predatory impact of Pleurobrachia sp. over the
small-size copepod community off Mejillones was low
(!1.3% removed daily), but similar to estimations reported
from other areas. Miller and Daan (1989) reported a daily
predation impact of Pleurobrachia sp. of 1.6% on the
potential prey biomass off Germany, while Buecher and
Gasser (1998) reported a daily predation impact of 0.6% on
the copepod community in the Mediterranean Sea.
When the high ctenophore growth rates are compared
with the much lower growth rates of the copepod species,
the predatory impact of Pleurobrachia sp. might become
relevant. In October 2001 an analysis at species level
showed that the daily predatory impact of Pleurobrachia
sp. on Acartia tonsa and Corycaeus sp. was 3.5% and 2.3%
of standing stock, respectively.
H. E. González et al.
Trophic flow and foodweb structure
In the present study, the percentage of PP channelled via
vertical flux and metazooplankton grazing was highly
variable, accounting from 7% (August 2001) to O100%
(October 2001) (Figure 4). Previous studies conducted in
the northern Humboldt Current system reported that during
the 1997e1998 El Niño event, the vertical flux rate of POC
plus metazooplankton grazing removed a reduced fraction
( from 20% to 30%) of the photosynthetically produced
POC (González et al., 2000).
Using mesozooplankton (200 to 20 000 mm) and total PP
data from different areas in the world oceans, Calbet (2001)
reported an increase of the relative importance of mesozooplankton grazing impact with decreasing PP. In this study
we discuss this relationship by using both size fractionated
metazooplankton and PP to explore whether the increase in
metazooplankton grazing impact in more unproductive
systems was due to the specific effect of the small copepods
and appendicularians. In particular, we observed that the PP
dominated by net-phytoplankton (O23 m) was transferred
rather inefficiently (7e13%) to metazooplankton. On the
contrary, when PP was dominated by pico- C nanoplankton (!23 mm), a high percentage (86%) was channelled
through small copepods and in turn towards secondary
gelatinous consumers, principally chaetognaths and ctenophores. The flux through large copepods and euphausiids
seemed much smaller. However, this conclusion should be
viewed with caution, since ingestion rates for these zooplankton were estimated as averages from a previous study
(González et al., 2000) that provided a wide range of values
from a variety of oceanographic conditions in the area.
In the study area, phytoplankton biomass was usually
dominated by net-phytoplankton with a contribution of
pico- C nanoplankton PP to total PP that did not exceed
40% (cruises Geminis IeIII; see Table 2). Under these
conditions, the grazing impact based on PP utilization was
relatively low for small and large copepods, as well as for
euphausiids (combined grazing impact up to 13% PP)
(Figure 4). The dominance of the !23 mm phytoplankton
fraction usually occurs when total PP is low (oligotrophic
condition). This situation occurred in October 2001 when
small-size (!23 mm) phytoplankton contributed to 84% of
total PP (Geminis IV; see Table 2). Indeed, the grazing
impact exerted by the different zooplankton size classes
changed dramatically. The small copepods removed a much
higher fraction (86%) of total PP, indicating that their
relative grazing impact is more important under oligotrophic conditions (Figure 4), a conclusion also reached by
Dam et al. (1995). Alternatively, the grazing pressure of
large-size euphausiids, although also increased, remained
relatively low (!5% of the total PP), especially when
compared with that of the small copepods (Figure 5). Thus,
under this increased contribution of the picophytoplankton
to total PP (October 2001), the rapid incorporation of
picoplankton into heterotrophic flagellates, faecal material,
Grazing impact (as % daily PP removed)
582
100
80
Small copepods
60
40
20
Large copepods
Euphausiids
0
0
20
40
60
80
100
Percentage of Pico + Nanoplankton-PP from total PP
Figure 5. Grazing impact (as percent of PP removed daily) vs. the
relative (%) contribution of pico- + nanoplankton from total PP.
The data from Tables 1 and 3 were plotted (exponential curve fit)
for the different metazooplankton size classes, namely small
copepods (dark circles, r2 ¼ 0:91), large copepods (open circles,
r2 ¼ 0:69), and euphausiids (triangles, r2 ¼ 0:64). Two points
obtained in the same area during January 1997 and July 1997
(unpublished data) are also plotted. For January 1997 the values
are: 67.3% pico- + nanoplankton-PP to total PP, and 25.7, 3.0, and
2.8% of grazing impact exerted by small and large copepods and
euphausiids, respectively. Similar values for July 1997 are: 66.4%,
and 14.2, 4.9, and 3.7%, respectively.
and organic matrices (Silver and Alldredge, 1981; Waite
et al., 2000) may have left this fraction quickly available to
zooplankton, and in particular to small copepods, which
seem to utilize more efficiently small-size detritus particles,
such as faecal material (González and Smetacek, 1994).
Feeding currents by flagellates (Fukuda and Koike, 2000)
and ciliates (Fenchel and Blackburn, 1999) may also produce aggregations of picoplankton of a size suitable for
small copepod manipulation. The high contribution of
picoplankton to total PP probably constitutes a recurrent but
transient situation in coastal upwelling ecosystems where,
according to the models of Moloney and Field (1990) and
Carr (1998), the early stages of a bolus of upwelled water
are dominated by picoautotrophs. The heterotrophic contribution to the small copepod diet in the incubation experiments was ca. a quarter of the total ration (Table 1),
indicating that the high abundance of ciliates and flagellates
in the area (Table 2) represented an important component
of their diet during both productive and unproductive
seasons.
The contribution of appendicularians to total metazooplankton grazing ranged from 0.3% to 15% (Figure 4), and
an increase in the percentage of pico- C nanoplankton PP
parallel to the increase in PP removed by appendicularians
was not observed as expected. Under oligotrophic conditions the fraction of PP removed by appendicularians may
increase (López-Urrutia et al., 2003), but we did not observe
this effect, probably because of the relatively low numbers
of appendicularians collected. Appendicularians contribute
Carbon cycling in the northern Humboldt Current
to vertical flux through the production of faecal pellets and
‘‘houses’’. Our results suggest that a significant proportion
of the chain-forming diatoms and dinoflagellates sink
attached to appendicularians mucopolysaccaride ‘‘houses’’.
In addition, they can also scavenge other particles while
sinking in the water column (Vargas et al., 2002).
The fact that the photosynthetically generated PP
dominated by net-phytoplankton (more usual situation)
was transferred rather inefficiently (7e13%) to metazooplankton and the surprisingly low vertical fluxes of particulates (see above), suggests two possible PP fates in the
studied area (Mejillones Bay). First, the microbial loop
seems to constitute a pathway preferred over the ‘‘classic
foodweb’’. Second, at least during part of the year, an
important fraction (up to 90% in February and August
2001; see Figure 4) of the photosynthetically generated
carbon might be exported seaward by mesoscale oceanographic features, such as filaments and eddies, since they
seem to be a recurrent physical feature in the study area
(Sobarzo and Figueroa, 2001). This seaward transport probably also occurs in other upwelling systems, such as
Monterey Bay, where the horizontal export by upwellinginduced advection was the dominant loss term for
phytoplankton PP (Olivieri and Chavez, 2000).
The impact of gelatinous predators on the copepod
community also varied between the more productive, netphytoplankton rich seasons and the less productive, picoplankton-rich conditions of the system. In particular, higher
biomass consumption of copepods by gelatinous predators
was observed during the more productive seasons (2.9e
11.4% of the copepod biomass daily). These results suggest that the potential impact of carnivorous gelatinous
zooplankton over the small copepod community (preferred
prey) may be significant. This percentage does not include
other abundant species, such as the siphonophore Bassia
bassensis that during January 1997 removed between 3%
(coastal) and 69% (offshore) of the total small-size copepod
community (Pagès et al., 2001). More importantly, at
a population level, predatory impacts were much higher and
may even modulate the population abundance and size
structure of some species when they are at low or medium
densities (i.e. 33% of Corycaeus spp. and 11% of Acartia
spp. standing stocks were ingested daily by S. enflata in
spring 2000) (Table 3).
Thus, the overall picture emerging from these results is
that the predatory impact of the carnivorous gelatinous
mesozooplankton on the copepod community may be large
and that, when accompanied with the impact of gelatinous
filter-feeders, such as Salpa fusiformis that in January 1997
removed up to 60% of the total PP (González et al. 2000),
the role of the ‘‘gelatinous foodweb’’ may become significant. Accordingly, future studies on the foodweb structure
and carbon flow of coastal upwelling systems should consider gelatinous filter-feeders and carnivores, as these may
be more relevant than the ‘‘classical’’ foodweb or microbial
loop under certain environmental conditions.
583
Acknowledgements
We thank all the researchers involved in the project for
their cooperation in the collection of samples: S. Palma,
P. Apablaza, P. Rosenberg, E. Herrera, D. Fernández, and
E. Menschel. H. Dam made suggestions that substantially
improved an earlier version of the manuscript. This work
was funded by Fondecyt Grant No. 1000419 to HEG, SP
and LC. Additional support was obtained from the
FONDAP-COPAS research programme No. 1501000072002.
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