Download Distribution and trophic ecology of chaetognaths in the western

Journal of Plankton Research Vol.22 no.2 pp.339–361, 2000
Distribution and trophic ecology of chaetognaths in the western
Mediterranean in relation to an inshore–offshore gradient
Alícia Duró and Enric Saiz
Institut de Ciències del Mar, CSIC, Departament de Biologia Marina i
Oceanografia, Ps. Joan de Borbó s/n, 08039 Barcelona, Catalunya, Spain
Abstract. This study examines the distribution patterns and feeding ecology of chaetognaths in the
Catalan Sea in relation to mesoscale features along an inshore–offshore gradient. The study was
conducted during two different periods of the year: late spring of 1995 and late summer of 1996. The
two periods differed in hydrographic conditions and mesoscale processes, which affected the distribution patterns of the different species of chaetognaths found. The diet of the chaetognaths was
mainly composed of copepods and differed between species. Prey size was not always strongly related
to chaetognath size and for certain species, there was an overlap in prey size spectrum. Trophic niche
breadth (on a ratio scale) appeared to be constant with growth. Ingestion rates and predation pressure
by chaetognaths did not follow a clear trend related to the mesoscale features in the area, such as the
presence of a density front. The impact of chaetognaths on copepod standing stock appeared to be
extremely low (<1%), but it became more relevant when the species and prey size specificity of the
chaetognaths was taken into account.
Introduction
The role of predation as a decisive factor determining the structure of the marine
planktonic food webs was not emphasized until quite recently (Verity and
Smetacek, 1996). Within carnivorous zooplankton, chaetognaths play a major
role both in their biomass contribution [up to 30% of the biomass of copepods in
the global oceans (Reeve, 1970)], and also in their impact on zooplankton
communities as one of the main predators of copepods (Pearre, 1980; Stuart and
Verheye, 1991).
Predator–prey interactions are largely determined by the characteristics of the
prey and among these characteristics, prey size has proved to be particularly
relevant [(Pearre, 1974) and references therein]. The study of foraging patterns
in relation to prey size appears necessary in order to establish patterns of food
selection, trophic niche and, eventually, food limitation and competence.
Although these topics have been addressed in marine fish larvae (Pearre, 1986;
Pepin and Penney, 1997), previous work on chaetognaths has concentrated
largely on prey selection and predator–prey relationships (Pearre, 1980; Kehayias
et al., 1996) and less so on aspects such as trophic niche breadth and niche overlap.
Chaetognaths have another characteristic that makes them particularly interesting from the oceanographic point of view. They have proved to be good indicators of water masses (Pierrot-Bults, 1982) and consequently, appear to be
especially suitable for the study of the effects of physical processes acting at the
mesoscale on the dynamics and variability of zooplankton populations.
It is less known, however, how physical processes at the mesoscale, which can
affect the distribution and abundance of zooplankton populations, reflect
processes at smaller scales, such as feeding and reproductive performance, as well
as predation pressure and, eventually, growth of the zooplankton populations.
© Oxford University Press 2000
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A.Duró and E.Saiz
Mesoscale singularities, such as density fronts and eddies might affect not only
the distribution and abundance of zooplankton, but also modify the encounter
rates between predator and prey due to the presence of associated small-scale
turbulence [(Kiørboe, 1997) and references therein].
The objective of this study was twofold: first, we addressed the distribution of
chaetognaths in the northwestern Mediterranean in relation to mesoscale physical processes occurring across an inshore–offshore gradient; second, we determined the trophic ecology of co-existing chaetognath species, and attempted to
determine their feeding impact on other zooplankters along the mentioned
gradient.
The study was carried out in the Catalan Sea (northwestern Mediterranean) in
June 1995 and September 1996. In the northwestern Mediterranean, there is a
semi-permanent density front associated with the Liguro–Provençal–Catalan
current, that flows SW along the shelfbreak. This area is characterized by high
variability at the mesoscale (Font et al., 1988). The cruises corresponded, respectively, to the periods of stratification and hydrographic transition in the western
Mediterranean, and we expected to find differences in the types and intensity of
mesoscale physical processes between both periods. Previous studies in the area
had shown that some groups of zooplankton tended to concentrate in the vicinity of the hydrographic front, while their distribution was more heterogeneous in
coastal waters (Boucher, 1984; Sabatés et al., 1989; Saiz et al., 1992; Sabatés and
Olivar, 1996). The accumulation of zooplankton in the frontal area, either active
or passive, might lead to the development of characteristic zooplankton
communities more stable and of higher productivity than in the surrounding
waters.
Method
Cruises
Sampling was conducted during two cruises in the Catalan Sea on board the B/O
García del Cid: FRONTS-95 (18–23 June 1995) and FRONTS-96 (16–21 September 1996). The area surveyed in the second cruise was located further to the north
than in the first cruise (Figure 1).
In each cruise a grid of three transects perpendicular to the shoreline, with four
stations each, was sampled. The stations were located, respectively, in coastal
waters, shelf waters, at the frontal system and in oceanic waters (Figures 2a and
3a). The station at the frontal system was located at the shelfbreak in FRONTS95, while it moved offshore in FRONTS-96. In each cruise the grid of stations was
surveyed two times consecutively, each survey taking about 3 days. The three
transects and both surveys for the respective coastal, shelf, frontal and oceanic
stations, were pooled as replicates within a cruise when we attempted to determine statistical differences along the transects.
At each station, routine CTD casts (Neil Brown) were conducted for temperature and salinity profiles. Chaetognaths were sampled with a BONGO net (60
cm diameter) fitted with 500 µm netting. The net tows were performed obliquely
from 200 m depth to the surface at the frontal and oceanic stations, and from 10 m
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Trophic ecology of chaetognaths
Fig. 1. Map of the sampling area in cruises FRONTS-95 and FRONTS-96.
above the bottom to the surface when shallower. During the tow, the ship was
kept at 2 knots and the towing speed was 20 m min–1. The volume filtered during
the tow was estimated by means of a flow meter. Samples were preserved in 5%
formalin buffered with borax.
Sample analysis
All chaetognaths present in the samples were counted and identified to the
species level. Their sexual developmental stage was determined according to the
degree of ovary development [stage I: ovaries not evident; stage II: ovaries well
developed, but no mature oocytes; stage III: presence of mature oocytes (Zo,
1973)]. Stages I and II correspond to juvenile individuals; stage III are adults.
The gut contents were analyzed only for the three most abundant species in
each cruise. All individuals in the samples were considered except for Sagitta
setosa where, due to their high abundance, only 100–200 individuals were
analyzed per sample. The number of chaetognaths examined in FRONTS-95 and
FRONTS-96 were, respectively, 150 and 547 individuals of S.bipunctata, 1602 and
594 of S.setosa, 930 and 302 of S.lyra, and 1113 and 521 of S.enflata.
Prior to dissection for the study of gut contents, total length and head width of
each individual were measured under the stereomicroscope. Contents of the gut
were classified according to their location and degree of digestion. The gut was
divided into foregut (including prey items in the mouth), midgut and hindgut
(Øresland, 1987). The degree of prey digestion was divided into three classes: (i)
undigested; (ii) digested but identifiable; and (iii) unidentifiable remains. Prey
items were identified to genus or species when possible, and their width
measured.
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Fig. 2. Horizontal distribution of salinity (‰) at 5 m depth during the first (a) and second (b) surveys
of the FRONTS-95 cruise. The location of the stations is also indicated (• physical, o biological; C:
coastal, S: shelf, F: front, O: oceanic). (c, d) Vertical profiles of temperature (°C) and density for the
central transect of cruise FRONTS-95.
Feeding activity was expressed as FCR (food containing ratio, or percentage of
individuals with contents in their guts) and NPC (number of prey per chaetognath). The prey located in the foregut were not used for the calculation of FCR
and NPC values because they might have been artifacts due to cod-end feeding.
Overall, the number of prey located in the foregut was relatively low (2–36%)
except for Sagitta enflata (72%). In the case of S.enflata, for some individuals, the
location of the prey in the gut was not determined. In order to use those samples,
we corrected the NPC and FCR values of those individuals according to the
percentage of prey in the mid- and hindgut observed for the same species in other
stations.
Samples where a chaetognath species was represented by less than 10 individuals per sample were not considered for feeding studies.
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Fig. 3. (a, b) Horizontal distribution of salinity (‰) at 5 m depth during the FRONTS-96 cruise. The
location of the stations is also indicated (• physical, o biological; C: coastal, S: shelf, F: front, O:
oceanic). (b, c) Vertical profiles of, respectively, temperature (°C) and density for the central transect
of cruise FRONTS-96.
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Data analysis
Predation pressure was estimated as the summation of the products of the abundance of each chaetognath species times their ingestion rates.
Ingestion rates (I, prey ingested per chaetognath and day) were calculated
according to a modified version of the equation of Feigenbaum:
2 3 NPC
I = –––––––– 3 24
DT
where DT is digestion time (in hours) and NPC is the average number of prey
per chaetognath (Feigenbaum, 1991). The factor 2 in the equation accounts for
the loss of prey in the gut due to sampling and preservation (Baier and Purcell,
1997b).
Digestion time was estimated from Baier and Purcell (Baier and Purcell,
1997b) taking into account the temperature at the depths where the different
species of chaetognaths were distributed. Thus, for Sagitta bipunctata, S.enflata
and S.setosa a digestion time of 5.5 h was estimated [0–50 m layer, temperature:
15–20°C (Furnestin, 1962, 1970; Pearre, 1974; Andréu, 1979, 1992; Kehayias et al.,
1994)]. Sagitta lyra inhabits deeper waters [50–200 m, temperature: 14–15°C;
Furnestin, 1962; Pearre, 1974; Andréu, 1979, 1990)] and a digestion time of 6.6 h
was used.
Comparisons between stations were conducted by analysis of variance
(ANOVA). When the requirements of homoscedasticity were not fulfilled, data
were transformed. In those cases where no suitable transformation was found,
non-parametric tests were used instead.
The study of foraging strategies between the different species of chaetognaths
had to be conducted within cruises because the number of individuals examined
within stations was not sufficient to allow comparison among stations. Thus, data
from the whole cruise were pooled for each species. Predator–prey size relationships were studied by comparing the predator head size with the prey width
(Pearre, 1980). Although chaetognath body length must also be related to prey
size, we preferred to use head size because it is more directly related to ingestion.
Regarding prey size, we used prey width instead of prey length because chaetognaths swallow prey whole and endwise.
Dependency of prey size on predator size was studied by linear regression on
log transformed prey data. Prior to analysis, data were binned according to predator size (head width) in 50 µm classes. Only classes with two or more items were
used. Mean prey size (and standard deviation) of the logarithmically transformed
data were computed for each predator size class. Both mean prey size and its standard deviation were regressed against chaetognath size after weighing by the
number of observations for each predator size class. Although Pearre (Pearre,
1980) found the best fit for the mean predator–mean prey size relation in chaetognaths using a power function, for our dataset the exponential model rendered
equally good fits and was chosen for simplicity. The standard deviation of the log
transformed prey sizes is an estimator of the trophic niche breadth [defined as
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Trophic ecology of chaetognaths
the width of the size spectrum of ingested prey, on a ratio scale (Pearre, 1986)]
and it was regressed against predator size in order to determine whether or not
it changed as the chaetognath grew.
Trophic niche overlap was estimated by comparing the prey size distributions
of the different co-existing species. Although we were not able to determine
patterns of prey selectivity because we lacked data on the field prey size spectrum, we estimated the prey size eligibility by comparing the relative ingested
prey size spectrum (i.e. prey size/predator size) for the different species studied.
Results
Hydrography
In the FRONTS-95 cruise (late spring), the area studied was characterized by a
thermocline at 40 m depth and the presence of a density front at the shelfbreak
(Figures 2c and 2d). The first survey of the grid of stations showed the presence
of a water mass of continental origin (<19°C and <37.5‰), detected in surface
(down to 30 m depth) in the northern and central transects (Figure 2a). This water
mass was associated with the Liguro–Provençal–Catalan current flowing southward along the shelfbreak front.
During the second survey of the FRONTS-95 cruise, this water mass moved
SW and was evident in the southern transect (Figure 2b). The distribution of
surface salinity suggests the intrusion of shelfbreak waters into the shelf, probably in relation to the SW movement of the water mass mentioned above.
During the cruise FRONTS-96 (late summer), the mesoscale physical structures were clearly different. In both samplings the thermocline was well developed at about 50 m depth, and the front appeared further offshore and weakly
defined (Figures 3b and 3c, only one survey shown). Surface salinity and temperature were quite uniform, with no significant gradients. The high salinity observed
in surface waters (~38‰) suggests the intrusion of open sea waters towards the
shelf. The contribution of waters of continental origin was probably limited to
coastal areas.
Abundance and distribution of chaetognaths
In both cruises the stations were sampled irrespective of time of day. Day and
night samples have been used indiscriminately in this work. We are confident
about this procedure because (i) in coastal and shelf stations, almost the whole
water column was sampled, and (ii) for the frontal and oceanic stations, there
were no significant differences in abundance estimates between day and night
stations in any of the cruises (ANOVA tests, P > 0.1) and consequently, if
chaetognaths performed vertical migration, its extent was within the strata
sampled.
In the FRONTS-95 cruise, the abundance of chaetognaths (per m2, mean ± SE)
varied between 26 ± 11.5 for the coastal stations, 77 ± 16.3 for the shelf stations
and, respectively, 169 ± 26.0 and 113 ± 9.5 for the frontal and oceanic stations.
There were significant differences between stations (one-way ANOVA test,
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A.Duró and E.Saiz
P < 0.01). In the FRONTS-96 cruise, the differences were less marked (coastal:
113 ± 53.3; shelf: 37 ± 7.8; front: 27 ± 8.4; oceanic: 59 ± 13.4), and not significant
(P > 0.1, after log transformation).
Seven species of chaetognaths were identified in the cruise FRONTS-95.
Sagitta setosa was the dominant species (69.7% of the abundance of chaetognaths); S.lyra and S.enflata contributed 12.7% each, S.minima 3%, and the
remaining 1.9% included S.bipunctata, S.serratodentata and Pterosagitta draco. In
the FRONTS-96 cruise, the specific composition changed slightly. Sagitta setosa
and S.enflata constituted the bulk of the community, contributing, respectively,
59.5 and 16.8% to the chaetognath abundance, followed by S.bipunctata (12.1%),
S.minima (6.2%), S.lyra (5.4%). Sagitta decipiens and S.serratodentata made up
the rest. In further analysis only the most abundant species on both cruises
(S.setosa, S.lyra, S.bipunctata and S.enflata, which comprised 95% of the total
abundance of chaetognaths) will be considered.
With regard to differences in distribution between species, during the
FRONTS-95 cruise all species tended to be more abundant at the front and
oceanic stations (Table I) except for S.setosa, which was more abundant at the
shelf and front stations. In the FRONTS-96 cruise several patterns were observed
(Table II). Thus, S.setosa was almost restricted to coastal waters, and S.enflata and
S.minima also tended to be more abundant in coastal and shelf waters. Sagitta
bipunctata and S.lyra presented a broader distribution.
Tables I and II also show the stage composition of the populations studied.
Some differences were observed between species and cruises. Thus, while in
FRONTS-95 (late spring) S.setosa was represented by both juveniles and adults,
this species was mainly represented by juveniles in FRONTS-96 (late summer).
Sagitta lyra presented only juveniles in both cruises, while S.minima was
composed mainly of adults in both cruises.
No common trend was observed in the stage composition of chaetognaths in
relation to the inshore–offshore gradient. Thus, while some species showed no
trend, others presented either a higher proportion of juveniles at the oceanic
stations (i.e. S.bipunctata in FRONTS-95), or the opposite pattern (i.e. S.lyra in
FRONTS-95 and S.enflata in FRONTS-96).
The horizontal distribution of the chaetognath species did not differ conspicuously between surveys except for S.setosa and S.lyra in FRONTS-95 (Figures 4
and 5), where the distribution of stages I and II of S.setosa and stage I of S.lyra
seemed to follow the movement of the water mass of continental origin along the
shelfbreak mentioned above.
Trophic ecology
In general, the gut fullness was low (Table III), the lowest values for S.enflata
(FCR 2–10%) and the highest for S.bipunctata and S.lyra (FCR 14–37%). When
the guts were full, usually only one prey was present, exceptionally 2 or 3 (in
1–4% of individuals with full guts).
NPC values (Table III) for night samples were significantly higher than day
samples (128%) in the cruise FRONTS-96, irrespective of the species (two-way
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Trophic ecology of chaetognaths
Table I. Abundance (as individuals per m2 and individuals in 1000 m3) and stage composition (as %)
of the chaetognath species in the FRONTS-95 cruise. Data for the different transects and surveys have
been pooled (n: number of stations). Abundances are expressed as average ± standard error. Sampling
depths were 200 m to surface at the front and oceanic stations; 30 m (range: 20–35) to surface at the
coastal stations; and 66 m (range: 50–100) to surface at the shelf stations
Coastal
(n = 7)
Shelf
(n = 7)
Front
(n = 7)
Oceanic
(n = 7)
Pterosagitta draco
ind per m2
0.02
ind in 1000 m3
1 ± 1.1
% Stage I
0
% Stage II
0
% Stage III
100
Sagitta bipunctata
ind per m2
0.04
ind in 1000 m3
1 ± 1.2
% Stage I
0
% Stage II
0
% Stage III
100
Sagitta enflata
ind per m2
ind in 1000 m3
% Stage I
% Stage II
% Stage III
1.6 ± 1.37
46 ± 39.0
20
44
37
3.9 ± 0.90
59 ± 16.1
12
58
30
20.9 ± 14.14 46.5 ± 11.46
104 ± 70.7
232 ± 57.3
9
17
39
46
52
36
Sagitta lyra
ind per m2
ind in 1000 m3
% Stage I
% Stage II
% Stage III
0.4 ± 0.21
13 ± 5.9
91
9
0
6.5 ± 2.04
71 ± 9.9
85
15
0
32.1 ± 7.56
161 ± 37.8
73
27
0
39.7 ± 8.72
198 ± 43.6
61
39
0
Sagitta minima
ind per m2
ind in 1000 m3
% Stage I
% Stage II
% Stage III
0.2 ± 0.15
7± 4.7
0
17
83
3.5 ± 0.99
45 ± 12.1
4
12
84
2.4 ± 0.64
12 ± 3.2
7
0
93
10.0 ± 4.72
50 ± 23.6
4
12
84
0.2
0.9 ± 0.88
0
0
100
0.4 ± 0.22
2 ± 1.1
0
0
100
0.4 ± 0.19
2 ± 1.0
0
0
100
Sagitta serratodentata ind per m2
ind in 1000 m3
% Stage I
% Stage II
% Stage III
Sagitta setosa
0
0
—
—
—
ind per m2
23.6 ± 10.37
ind in 1000 m3 742 ± 316.1
% Stage I
18
% Stage II
31
% Stage III
52
0
0
—
—
—
0.07
1 ± 1.1
0
0
100
0
0
—
—
—
0
0
—
—
—
1.7 ± 0.80
9 ± 4.0
13
28
59
7.9 ± 2.80
39 ± 14.0
47
43
11
85.8 ± 25.72 111.5 ± 24.40
1085 ± 292.5
557 ± 122.0
27
22
26
29
47
49
8.5 ± 2.79
43 ± 14.0
25
21
54
ANOVA on square root transformed data, P < 0.015). However, in the cruise
FRONTS-95 no significant difference appeared between day and night NPC
values (two-way ANOVA on log transformed data, P > 0.1).
Table IV shows the different prey types found in the guts of the chaetognaths.
Guts with unidentified remains always made a relevant contribution. The most
frequently identified prey were copepods. There were conspicuous differences in
the type and degree of digestion of gut contents for the different chaetognath
species. Thus, S.bipunctata presented essentially prey items in advanced digestion
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A.Duró and E.Saiz
Table II. Abundance (as individuals per m2 and individuals in 1000 m3) and stage composition (as %)
of the chaetognath species in the cruise FRONTS-96. Data for the different transects and surveys have
been pooled (n: number of stations). Abundances are expressed as average ± standard error. Sampling
depths were 200 m to surface at the front and oceanic stations; 47 m (range: 40–60) to surface at the
coastal stations; and 158 m (range: 130–175) to surface at the shelf stations
Coastal
(n = 6)
Sagitta bipunctata
ind per m2
ind in 1000 m3
% Stage I
% Stage II
% Stage III
2.1 ± 1.46
51 ± 36.9
11
42
47
Sagitta decipiens
ind per m2
ind in 1000 m3
% Stage I
% Stage II
% Stage III
0
0
—
—
—
Sagitta enflata
ind per m2
ind in 1000 m3
% Stage I
% Stage II
% Stage III
17.9 ± 4.67
393 ± 109.9
31
49
21
Sagitta lyra
ind per m2
ind in 1000 m3
% Stage I
% Stage II
% Stage III
Sagitta minima
ind per m2
ind in 1000 m3
% Stage I
% Stage II
% Stage III
Sagitta serratodentata
ind per m2
ind in 1000 m3
% Stage I
% Stage II
% Stage III
Sagitta setosa
ind per m2
ind in 1000 m3
% Stage I
% Stage II
% Stage III
Shelf
(n = 6)
14.0 ± 2.98
91 ± 21.5
22
45
32
9.2 ± 2.23
68 ± 23.4
41
28
31
Oceanic
(n = 6)
45.2 ± 12.70
239 ± 80.3
19
33
47
0
0
—
—
—
0
0
—
—
—
12.3 ± 3.37
83 ± 26.2
16
32
51
2.4 ± 1.30
16 ± 6.9
19
24
57
7.1 ± 1.82
35 ±11.7
7
53
39
1.1 ± 0.59
21 ±10.9
35
65
0
8.2 ±2.42
53 ±18.1
60
40
0
15.1 ± 5.39
74 ± 22.1
51
49
0
6.9 ± 1.63
27 ± 3.2
47
53
0
7.7 ± 3.40
172 ± 80.9
0
34
66
1.8 ± 0.69
12 ± 5.3
0
24
76
0.8 ± 0.63
3 ± 2.6
0
0
100
0
0
—
—
—
83.6 ± 47.08
1816 ± 981.8
26
33
41
0.2
1 ± 1.3
0
100
0
Front
(n = 6)
0
0
—
—
—
0
0
—
—
—
0.3
2 ± 2.1
25
75
0
0
0
—
—
—
0.2
1 ± 1.0
0
0
100
0.1
0.7 ± 0.72
0
0
100
0
0
—
—
—
stage (unidentified); unidentified prey items contributed only 36–46% of the full
guts of S.enflata and S.setosa, while the rest (>48%) were basically copepods.
Chaetognath species differed in the copepod prey found in their guts (Table
V). Differences were also evident between cruises. The copepods Pleuromamma
sp., Calanus sp. and Euchaeta sp. were the main copepod prey found in the guts
of S.lyra. Sagitta setosa and S.enflata showed the main copepod prey items to be
Centropages typicus and Temora stylifera. For S.bipunctata, identifiable prey were
only present in the cruise FRONTS-96, and then Corycaeus sp. was the main
copepod found in the guts.
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Fig. 4. Abundance and horizontal distribution of Sagitta setosa in cruise FRONTS-95. Left panel
corresponds to the first survey; the right one to the second survey. Crosses indicate that no specimens
were caught.
Mean prey size was not consistently dependent on chaetognath size (Figure 6).
Thus, while prey size increased with chaetognath size for S.lyra in 1995 and 1996
(linear regression analysis, respectively, r2 = 0.35, P < 0.02, n = 80 and r2 = 0.76,
P < 0.01, n = 60), S.enflata in 1995 (r2 = 0.38, P < 0.05, n = 49, or r2 = 0.74, P < 0.01
n = 42 after removing a predator size class which exhibited unexpectedly small
prey) and S.bipunctata in 1996 (r2 = 0.92, P < 0.04, n = 11), this trend was not
significant in the other cases (S.setosa in 1995: P > 0.1, n = 130; S.enflata in 1996:
P > 0.1, n = 17; S.setosa in 1996: P > 0.1, n = 57). Niche breadth was independent
of predator size for all chaetognath species (linear regression analysis, P > 0.05).
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A.Duró and E.Saiz
Fig. 5. Abundance and horizontal distribution of Sagitta lyra in cruise FRONTS-95. Left panel corresponds to the first survey; the right one to the second survey. Crosses indicate that no specimens were
caught.
Table III. Gut fullness of chaetognaths (FCR and NPC; average ± standard error) as a function of day
and night time in the cruises FRONTS-95 and FRONTS-96. Data for the four more abundant species
are shown
1995
––––––––––––––––––––––––––––
n
FCR ± SE NPC ± SE
Sagitta bipunctata Day
Night
1996
––––––––––––––––––––––––––––––––
n
FCR ± SE
NPC ± SE
5
37.1 ± 8.88
––
0.37 ± 0.089
––
13
4
14.1 ± 3.02
35.8 ± 8.68
0.14 ± 0.031
0.36 ± 0.088
Sagitta enflata
Day
Night
12
4
4.0 ± 0.87
2.2 ± 0.50
0.04 ± 0.009
0.02 ± 0.006
8
6
5.9 ± 2.42
9.7 ± 1.17
0.06 ± 0.024
0.10 ± 0.011
Sagitta lyra
Day
Night
9
8
31.0 ± 5.11
28.1 ± 4.59
0.32 ± 0.053
0.30 ± 0.046
7
4
16.8 ± 7.32
28.6 ± 12.43
0.18 ± 0.082
0.31 ± 0.129
Sagitta setosa
Day
Night
13
11
10.7 ± 2.68
16.9 ± 3.35
0.11 ± 0.027
0.17 ± 0.035
2
3
8.2 ± 1.20
18.3 ± 4.32
0.08 ± 0.010
0.19 ± 0.050
n, number of stations.
With regard to trophic niche overlap between co-existing species (Figure 7),
in the 1995 cruise, prey size spectra did not differ significantly between S.enflata
and S.setosa (two-sample Kolmogorov–Smirnov test, P > 0.05; geometric mean
prey sizes were, respectively, 327 and 312 µm). However, there was not much
trophic niche overlap between S.lyra (geometric mean prey size: 540 µm) and
the former two chaetognath species (respective Kolmogorov–Smirnov tests, P >
0.05). In the 1996 cruise, geometric mean prey sizes were 484, 435, 389 and
350
Trophic ecology of chaetognaths
Table IV. Composition of the gut contents of the four most abundant chaetognaths in cruises
FRONTS-95 and FRONTS-96. Values are expressed as percentage
FRONTS-95
––––––––––––––––––––––––––––––––––––––––––
Species
Contents
%
FRONTS-96
–––––––––––––––––––––––––––––––––––––––––
Species
Contents
%
Sagitta bipunctata
Unidentified
Sagitta bipunctata
Unidentified
Copepods
Chaetognaths
88.6
10.5
0.9
Sagitta enflata
Unidentified
Copepods
Cladocerans
Other crustaceans
Chaetognaths
36.3
54.0
4.0
4.8
0.8
Sagitta enflata
Unidentified
Copepods
Cladocerans
Other crustacean
Chaetognaths
36.4
53.5
3.1
6.2
0.8
Sagitta lyra
Unidentified
Copepods
Euphausiids
Other crustaceans
Chaetognaths
Cephalopod larvae
Fish larvae
81.8
13.0
0.4
3.9
0.4
0.4
0.4
Sagitta lyra
Unidentified
Copepods
Euphausiids
Other crustaceans
Chaetognaths
49.1
40.0
1.8
3.6
5.5
Sagitta setosa
Unidentified
Copepods
Cladocerans
Other crustaceans
Chaetognaths
45.9
48.2
2.7
2.0
1.2
Sagitta setosa
Unidentified
Copepods
Cladocerans
Other crustaceans
Chaetognaths
43.1
50.0
4.9
1.0
1.0
100
‘Unidentified’ stands for prey remains not identified.
252 µm for, respectively, S.lyra, S.enflata, S.bipunctata and S.setosa. While the
first three species did not differ significantly in their prey size spectra
(Kolmogorov–Smirnov tests, P > 0.05), S.setosa appeared to ingest different
(smaller) prey (Kolmogorov–Smirnov tests, P < 0.01).
The differences in mean prey size between 1995 and 1996 cannot be explained
by differences in chaetognath size (Table VI). Furthermore, it appears that the
chaetognaths presented specific electivity for certain prey sizes. Figure 8 shows
the frequency distribution of prey sizes standardized to the size (head width) of
the predator. Sagitta enflata, S.lyra and S.bipunctata showed a preferred prey size
(the median) of about 30–50% of their own head widths. Sagitta setosa, which is
the species with the smallest head, showed an optimum at about 70%.
Daily ingestion rates (Table VII) were computed from NPC values. In the
cruise FRONTS-95, no significant differences were found in ingestion rates along
the inshore–offshore gradient for any of the species (one-way ANOVA tests, P >
0.1). In the case of the cruise FRONTS-96, where there was a significant diel
feeding rhythm, we corrected NPC values by taking into account the number of
hours of daytime and night, and also the 128% higher gut fullness found at night.
Except for S.enflata, in FRONTS-96 ingestion rates did not change between
stations along the transect (one-way ANOVA and Kruskal–Wallis tests, P > 0.3).
Sagitta enflata in the cruise FRONTS-96 exhibited significant differences between
351
A.Duró and E.Saiz
Table V. Specific composition and relative frequency (%, based on total number of copepod prey) of
the copepods found as prey in the chaetognath guts
FRONTS-95
FRONTS-96
–––––––––––––––––––––––––––––––––––––––––– –––––––––––––––––––––––––––––––––––––––––––
Species
Copepod
%
Species
Copepod
%
Sagitta bipunctata ––
Sagitta enflata
Sagitta bipunctata Centropages typicus
Corycaeus
Temora stylifera
Clauso/Cteno/
Paracalanus
20.0
40.0
20.0
20.0
Centropages typicus
Clauso/Cteno/
Paracalanus
Calanus
Temora
20.0
20.0
Centropages typicus
Oncaea
Calanus
Candacia armata
Candacia
Corycaeus
Euterpina
Microsetella
48.8
11.6
2.3
2.3
20.9
2.3
2.3
9.3
Sagitta enflata
Sagitta lyra
Centropages typicus
Candacia
Euchaeta
Calanus
Pleuromamma
Acartia
5.3
5.3
26.3
31.6
26.3
5.3
Sagitta lyra
Corycaeus
Euchaeta
Calanus
Pleuromamma
Temora stylifera
7.1
7.1
21.4
42.9
21.4
Sagitta setosa
Centropages typicus
Temora stylifera
Microsetella
Euterpina acutifrons
Clausocalanus
Clauso/Cteno/
Paracalanus
89.7
2.9
1.5
2.9
1.5
1.5
Sagitta setosa
Centropages typicus
Temora stylifera
Microsetella
Clausocalanus
Clauso/Cteno/
Paracalanus
29.0
54.8
6.5
6.5
3.2
20.0
40.0
Table VI. Average (± SE, mm) body and head sizes of the chaetognaths studied, and parameter
estimates (± SE) of the linear regression fit between their body and head sizes. The coefficient of
determination and sample size for the regression analysis are also shown
FRONTS-95 cruise
Sagitta bipunctata
Sagitta enflata
Sagitta lyra
Sagitta setosa
FRONTS-96 cruise
Sagitta bipunctata
Sagitta enflata
Sagitta lyra
Sagitta setosa
Length
Head
Intercept
Slope
r2
n
9.2 ± 0.21
11.0 ± 0.09
14.8 ± 0.19
7.5 ± 0.03
0.59 ± 0.016
0.89 ± 0.007
0.95 ± 0.014
0.40 ± 0.002
0.022 ± 0.0367
0.151 ± 0.0166
–0.059 ± 0.0138
0.132 ± 0.0077
0.062 ± 0.0038
0.067 ± 0.0015
0.068 ± 0.0009
0.035 ± 0.0010
0.64
0.66
0.87
0.43
148
1079
901
1590
9.6 ± 0.10
8.6 ± 0.15
15.9 ± 0.39
6.9 ± 0.06
0.67 ± 0.008
0.72 ± 0.012
1.06 ± 0.029
0.39 ± 0.003
–0.046 ± 0.0174
0.108 ± 0.0156
–0.079 ± 0.0222
0.097 ± 0.0106
0.074 ± 0.0018
0.070 ± 0.0017
0.070 ± 0.0013
0.042 ± 0.0015
0.77
0.78
0.92
0.57
544
500
275
587
stations (one-way ANOVA test, P < 0.001). A Tukey–Kramer HSD posteriori test
indicated that the oceanic stations were significantly higher (P < 0.05).
The predation pressure by chaetognaths was significantly lower at the coastal
stations during the cruise FRONTS-95 (Table VIII; one-way ANOVA on squareroot transformed data, P < 0.001 and Tukey-Kramer HSD posteriori test,
352
Trophic ecology of chaetognaths
Fig. 6. Relation between prey width (µm, geometric mean ± SD) and chaetognath head width (mm,
data binned in 50 µm classes) for the four chaetognath species studied in cruises FRONTS-95 and
FRONTS-96. Standard deviation values out of the range of the axes are shown by their values.
P < 0.05). In FRONTS-96 the predation pressure was more important at both the
oceanic and the coastal stations; in the latter case, this fact reflected the high
abundance of S.setosa in the coastal stations. In this cruise, however, the differences between stations were not significant (Kruskal–Wallis test, P > 0.05).
Discussion
Abundance, stage composition and distribution
The use of coarse mesh sizes (500 µm) in our study must be taken as a limitation
because overall, juvenile chaetognaths were not quantitatively sampled. In the
case of S.lyra, the fact that no adult stages were found is probably a consequence
of the deeper habitat of the adults (Furnestin, 1962; Pearre, 1976; Andréu, 1979,
353
A.Duró and E.Saiz
Fig. 7. Prey size distribution of the four chaetognath species studied. Prey size was log-transformed
and binned in twelve 0.1-wide intervals. The abcissae axis shows the prey size intervals in log scales.
Table VII. Ingestion rates (prey ingested per chaetognath and day; average ± standard error) for the
four most abundant species in the FRONTS-95 and FRONTS-96 cruises
Station
Sagitta bipunctata
Coast
Shelf
Front
Oceanic
Sagitta enflata
Sagitta lyra
Sagitta setosa
1995
–––––––––––––––––––––––
n
Ingestion rate
1996
––––––––––––––––––––––––––
n
Ingestion rate
1
4
––
––
3.76
3.13 ± 0.992
2
5
5
5
1.66 ± 1.110
1.96 ± 0.336
1.25 ± 0.447
2.92 ± 0.860
Coast
Shelf
Front
Oceanic
1
4
4
7
0.58
0.22 ± 0.062
0.13 ± 0.045
0.43 ± 0.106
5
5
1
3
0.51 ± 0.138
0.22 ± 0.097
0.58
1.93 ± 0.159
Coast
Shelf
Front
Oceanic
3
7
7
––
2.41 ± 0.654
1.83 ± 0.334
2.62 ± 0.437
1
4
3
3
2.99
0.82 ± 0.501
1.52 ± 0.223
3.26 ± 2.204
Coast
Shelf
Front
Oceanic
7
6
7
4
1.10 ± 0.385
1.75 ± 0.471
1.30 ± 0.263
0.46 ± 0.281
5
1.12 ± 0.168
––
––
––
n, number of stations.
Fig. 8. Frequency distribution of prey sizes (standardized to predator head size) for the four species
studied in cruises FRONTS-95 (a) and FRONTS-96 (b). Absolute prey size (geometric mean, µm),
median relative prey size (%) and sample size are also shown.
354
Trophic ecology of chaetognaths
355
A.Duró and E.Saiz
Table VIII. Predation pressure by chaetognaths on mesozooplankton in cruises FRONTS-95 and
FRONTS-96. Values for the different types of station are presented as arithmetic (± standard error)
and geometric means
Predation pressure (ingested prey m–2 day–1)
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
Average
Geometric mean
FRONTS-95
Coast
Shelf
Front
Oceanic
FRONTS-96
Coast
Shelf
Front
Oceanic
28.0 ± 12.20
138.4 ± 30.59
212.9 ± 40.22
152.5 ± 21.48
14.2
125.1
185.7
143.2
109.6 ± 54.99
37.1 ± 7.66
35.8 ± 10.80
168.0 ± 37.85
46.4
32.7
26.6
149.0
1990) being missed in our sampling. Thus, our abundance estimates are underestimates for the total community and must be considered with caution.
In spite of this, the chaetognath abundances (FRONTS-95, mean: 0.9 ind m–3,
range: 0.10–2.7 ind m–3; FRONTS-96, mean: 0.8 ind m–3, range: 0.03–6.8 ind m–3)
were generally similar to previous reports for the western Mediterranean [annual
average for the Catalan Sea: 1.5 ind m–3 (Andréu, 1990)]. The pattern of
dominance of the different species was in overall agreement with previous reports
for the western Mediterranean (Ibáñez and Dallot, 1969; Andréu 1979, 1985,
1990; Furnestin, 1970).
The distribution of chaetognaths appeared to be influenced by physical
processes at the mesoscale along the inshore–offshore transect, and some trends
can be detected. Thus, in FRONTS-95 the change in abundance of juvenile stages
of S.setosa at the frontal stations between the first and second surveys suggests
that they might follow the movement of the low salinity, cold water mass along
the shelfbreak. Similarly, the distribution of the stage-I S.lyra appeared to be
influenced by this cold water mass.
The distribution pattern of S.bipunctata in both cruises followed the displacement of offshore waters, in agreement with its oceanic character (Furnestin, 1952,
1962; Andréu, 1990). The confinement of S.setosa in coastal waters in FRONTS-96
(late summer) is probably related to the intrusion of oceanic waters onto the shelf.
Some authors have described S.enflata as a cosmopolitan (Alvariño, 1969) and
epiplanktonic species (Furnestin, 1962; Andréu, 1990, 1992). In spring
(FRONTS-95), the low abundance of this species at the frontal stations could be
influenced by the intrusion of low-salinity waters and their displacement southward. Camiñas observed that this species preferred saline (>36.5‰) and warm
waters (22–23°C) (Camiñas, 1983); this fact would agree with our observation that
S.enflata was more abundant in offshore waters.
356
Trophic ecology of chaetognaths
Trophic ecology and predation impact of chaetognaths in the northwestern
Mediterranean
The study of feeding rates of chaetognaths based on the analysis of the gut
content of specimens collected in nets is weakened by two main uncertainties:
first, the degree of over or underestimation of gut fullness due to either cod-end
feeding or to enhanced clearance of the guts during the towing of the net (Feigenbaum and Maris, 1984; Feigenbaum, 1991; Baier and Purcell, 1997a), and second,
uncertainties in the estimates of gut clearance rates and digestion times (Pearre,
1974; Baier and Purcell, 1997b).
In the estimation of gut fullness, we avoided some of the problems due to codend feeding by excluding analysis of prey located in the anterior part of the gut
(Pearre, 1973; Nagasawa and Marumo, 1972, 1976). Some authors also exclude
prey items located in other parts of the gut but which appear undigested (Szyper,
1978; Feigenbaum, 1982). We did not follow that procedure because they only
accounted for 3.1% of the contents. Furthermore, recent evidence suggests that
the evacuation of the gut might make a larger contribution to gut fullness than
cod-end feeding (Baier and Purcell, 1997a). Therefore, we have followed the
recommendation of Baier and Purcell to multiply NPC values by two in order to
take into account the clearance of the guts during long net tows (Baier and
Purcell, 1997a).
The low percentage of individuals found with full guts (FCR and NPC values)
in our study is similar to the values reported in other studies for the Mediterranean [(Kehayias et al., 1996) NPC: 0.029–0.370 for the eastern Mediterranean;
(Pearre, 1976) FCR: 6.5–47.2% for the western Mediterranean] and other seas
[(Baier and Purcell, 1997b), NPC: 0.02–0.2 for the Atlantic Ocean; (Stuart and
Verheye, 1991) NPC: 0.01–0.18 for the Benguela system].
Although the existence of diel feeding rhythms in chaetognaths is known and
has been well documented for a long time (Rakusa-Suszczewski, 1969; Pearre,
1973; Szyper, 1978; Feigenbaum, 1982; Bushing and Feigenbaum, 1984), in our
study chaetognaths did not always present such rhythms. Other studies with
similar results (Stuart and Verheye, 1991; Gibbons, 1992; Kehayias et al., 1996)
have attributed this variability in the presence of feeding rhythms to the coincidence in distribution of predator and prey throughout the day.
The diet of chaetognaths was composed mainly of copepods, as already
described in previous studies (Reeve, 1980; Pearre, 1980; Øresland, 1987). Other
plankters appeared sporadically in the diet, probably relating to their low abundance (Kuhlmann, 1977). There were differences in the species composition of
copepods found in the guts of chaetognaths. Some of these differences are due to
the seasonal changes in copepod species in the water column throughout the year.
Thus, the major contribution as prey of Centropages typicus in FRONTS-95 (late
spring) and of Temora stylifera in FRONTS-96 (late summer) must be related to
their seasonal peaks of abundance in the area (Saiz, unpublished data).
Prey size also plays an important role in determining the diet composition
(Rakusa-Suszczewski, 1969; Sullivan, 1980). There are obvious mechanical and
physical restrictions in the size of prey items related to the size and characteristics
357
A.Duró and E.Saiz
of the organ involved in food capture, in this case the mouth (Sullivan, 1980;
Pearre, 1980). Although our study showed a dependency of mean prey size on
predator size, this trend was not consistently significant in all cases and on some
occasions, explained only a small part of the variance of prey size. This poor (but
significant) or absent relationship between prey size (width) and predator size
(head size) has been also found by other authors (Pearre, 1980; Kehayias et al.,
1996). Although it can be partially explained by the narrow range of the independent variable in the regression analysis, it is very likely also due to speciesspecific differences in behaviour between potential copepod prey of similar size.
Both, conspicuousness of prey due to its motility, and its ability to escape, will
affect the attack rate and capture success of chaetognaths and introduce variability into any predator–prey size relationship.
We did not find naupliar and small juvenile copepod stages in the guts.
Although a short digestion time for small prey might help to explain this fact, if
they had been preyed upon, one would have expected to find some remains.
Therefore, it appears that predation was essentially concentrated on relatively
larger prey. This observation provides evidence of a lack of overlap in prey size
spectra for two of the main predators of copepods, chaetognaths and fish larvae
(Fortier and Harris, 1989; Sabatés and Gili, 1991; Sabatés and Saiz submitted).
Trophic niche breadth (on a ratio scale) did not change with predator size. This
invariability in niche breadth over chaetognath development is in agreement with
similar studies conducted with fish larvae (Pearre, 1986) and indicates a similar
use of trophic resources through development.
The degree of trophic niche overlap between co-existing species was relevant.
Thus, Sagitta enflata and S.setosa in the 1995 cruise were capturing prey of
similar size; for the 1996 dataset, and in spite of the small sample sizes of
S.bipunctata and S.enflata, these species were apparently competing for prey
items with S.lyra. However, this niche overlap does not seem to be a consequence of similarity in the sizes of the co-existing chaetognath species (see
Table VI). It is evident that there was a preference for certain prey sizes, and
that several factors were involved. If prey size was only constrained by a
mechanical limitation relative to predator size, the ‘optimum’ relative prey size
(standardized to the width of the head) would be expected to be common for
all species of chaetognaths. As this was not the case, it is expected that other
factors, such as behaviour and conspicuousness of prey, and the spatial coexistence of predator and prey on a small scale (i.e. prey availability), must play a
major role in determining the trophic interaction between chaetognaths and
their prey, and affect the observed prey selectivity.
One of the aims of this study has been to evaluate the predation pressure by
chaetognaths on zooplanktonic communities, and to determine how it could be
affected by physical variability at the mesoscale. Initially, we expected to find
differences in ingestion rates and predation pressure by chaetognaths along a
gradient in relation to the presence of the density front, and spatial differences
in prey concentration and turbulence. We do not know if the low intensity of the
gradients, or the lack of response to them, is responsible for the absence of differences observed along the gradient.
358
Trophic ecology of chaetognaths
Table IX. Average abundance (as geometric mean and range; individuals per m2) of the copepod
standing stock and of Centropages typicus in cruise FRONTS-95. Sampling was conducted with a
double WP-2 net (200 µm mesh size) towed vertically from 200 m to surface in the front and oceanic
stations, and from 60–100 m to surface in the shelf stations
Stations
Total copepods
C.typicus copepodites
C.typicus adults
Shelf
Front
Oceanic
134246 (112780–183912)
101765 (95493–109746)
90654 (58136–138452)
27646 (16864–41334)
18001 (10831–27327)
12401 (7074–21392)
6319 (3162–13563)
2964 (1709–5465)
2475 (1105–6536)
A final issue to consider would be the impact (as percentage of prey population removed daily) that chaetognaths might have on the copepod community.
We have been able to estimate this impact only in the cruise FRONTS-95, for
which data are available on copepod abundance at the same stations [Table IX
(Saiz et al., 1999)]. Our estimates must be taken carefully and considered as
tentative, as our digestion times are not direct measurements but literature
values, and also, the mesh size of the nets used (500 µm) did not retain the whole
chaetognath community. The impact on the copepod standing stock would be of
0.08% at the shelf stations, 0.15% at the frontal station and 0.12% at the oceanic
station. These values seem to be insignificant for the whole copepod community.
However, if the selectivity for copepod species and sizes shown by chaetognaths
is taken into account, the predation impact appears more relevant. Most of the
copepods found in the guts were adults or late copepodites of Centropages
typicus, Temora stylifera and, in the case of S.lyra, Calanus sp., Euchaeta sp. and
Pleuromamma sp. In the case of C.typicus, which was one of the most common
prey species in the cruise FRONTS-95, the impact by the chaetognaths would
range between 0.26 and 1.44% (based either on both copepodites and adults, or
only adults), 0.50 and 3.58% and 0.18 and 1.08% of the standing stock at, respectively, the shelf, frontal and oceanic stations. These values are comparable with
those found by Stuart and Verheye (Stuart and Verheye, 1991) in the Benguela
system (1–5.3% of the copepod standing stock consumed per day), or Drits and
Utkina (Drits and Utkina, 1988) in the Black Sea (0.3–6% of the standings stock
of Calanus (CV) and Pseudocalanus). Furthermore, the Centropages mortality
rates by the chaetognath community found in our study are comparable with,
although still lower than, the growth rates of adult C.typicus estimated by egg
production in the same cruise [respectively, 8.9, 9.0 and 2.7% (Saiz et al., 1999)].
It is consequently at the frontal and oceanic stations where the impact of
chaetognaths would appear to be more meaningful, accounting for roughly 30%
of the Centropages productivity. This high predation pressure by chaetognaths
must exert a significant control on the population of C.typicus in offshore waters
of the already food limited northwestern Mediterranean in summer (Saiz et al.,
1999). From our results we feel, as stated by Verity and Smetacek (Verity and
Smetacek, 1996), that a major effort should be put into ascertaining the importance of predation or ‘top-down’ trophic effects in determining the structure of
pelagic food webs, paying special attention to the particularities of different taxa
and their life histories.
359
A.Duró and E.Saiz
Acknowledgements
The authors thank M.Alcaraz, A.Calbet, J.-M.Gili, F.Pagès, A.Sabatés and J.Salat
for their useful comments during this study. Patricia Filipe and Magdalena
Jaskiewicz sorted the zooplankton samples. The authors also acknowledge the
comments by the unknown reviewers. This work has been supported by CICYT
AMB94-0853 and MAST MAS3-CT96-0051 grants.
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Received on March 3, 1999; accepted on September 2, 1999
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