Journal of Plankton Research Vol. 18 no.7 pp.1123-1135.19%
Seasonal variations in the zooplankton and in the population
structure ofAcartia tonsa in a very eutrophic area: La Habana
Bay (Cuba)
Juan Diaz Zaballa and Raymond Gaudy1
Instituto de Investigaciones del Transporte, Apanado 17029, zona postal 17,
Ciudad de La Habana, Cuba and 'Centre d'Ocianologie de Marseille, Station
marine d'Endoume, rue de la Batterie des lions, F-130007 Marseille, France
Abstract. Seasonal changes in the abundance of total zooplankton and of main components were
studied at a fixed station in La Habana Bay. Special attention was given to the dominant species. Acania
tonsa. which constituted 89% of the total number of zooplanktonic organisms. The variations in some
of its population parameters (eggs, nauplii. copepodites. adults, sex ratio, number of eggs per female)
were analysed in relation to temperature, salinity and chlorophyll. The abundance of eggs was independent of the environmental factors, particularly of chlorophyll which was always present in excess. The
number of eggs per female showed several peaks, but was also independent of environmental factors.
Nauplii were poorly correlated with egg numbers, but depended on the abundance of chlorophyll in
particles of size <55 \im. This suggested that the part of edible food suitable for them in size or quality
was not always in excess in the available seston. provoking a temporary increase in naupliar mortality.
The temporal evolution of the following successive stages was nearly synchronous: thus, the changes
observed in their abundance were not caused by fluctuations in the reproductive potential of females,
but appeared to be related to a periodic decrease in the total zooplankton density due to the flushing
effect of inland water in the bay.
Introduction
Coastal regions which display a high degree of urban or industrial activities are
often characterized by eutrophication. These conditions are generally more
marked in semi-closed areas such as lagoons or bays poorly connected with the
open ocean. In such environments, particularly in tropical regions, the wide range
of temperature and salinity variations also contributes to affect the stability of the
pelagic ecosystem. The Bay of Habana (Cuba) corresponds to this type of semiclosed ecosystem. In the present study, we analyse, during an annual cycle, the
quantitative and qualitative variations in the mesozooplankton, and particularly
the main species, the copepod Acartia tonsa, in relation to the environmental factors. This work, which is based on high-frequency data acquisitions, completes the
preliminary study of Diaz Zaballa and Rodriguez (1984).
Method
The Bay of La Habana is located on the north coast of Cuba (23°08'N; 82°20'30"E).
It is a semi-land-locked area of 5.1 km2 and 9.2 m average depth, composed of three
coves (Marimelena, Atares and Guasabacoa) with a river outlet in each of them
(Figure 1).
The sampling station is located at the north of the bay, near the canal connecting
with the sea, over 4 m depth. The samples were taken between 26 March 1991 and
30 April 1992, with an average frequency of 14 days, always in the morning
© Oxford University Press
1123
J.Oiaz Zaballa and R.Gaudy
N
Coif of Mexico
Fig. 1. Map of the Bay of La Habana and location of the reference station
(08:40-11:20 h). Zooplankton were collected by three successive vertical hauls
between the bottom and the surface, with a Juday net (opening diameter 40 cm,
mesh size 55 u,m). Temperature was measured in surface water. Samples of this
water were taken for salinity measurements (salinometer E-202, Tsurumi Seiki)
and filtered on Whatman GF/C for chlorophyll pigments (Turner fluorometer
Model 111; method of Yentsch and Menzel, 1963). The abundance of pigments was
measured on a screened fraction (<55 jim) of the water and on the total water, to
separate the contribution of phytoplankton (<55 (xm) and detritus (fragments of
macroalgae), which were generally abundant in the total sample.
The different species of zooplankton were counted. For the copepod A.tonsa,
which was the most abundant form, eggs, naupliar stages (counted together), copepodite stages (C1-C5) and adults (males and females) were separated.
The data were compared using the Spearman correlation technique (Table I).
Results
Variation in the environmental factors
The temperature ranged between 22 and 31°C, but most values were between 26
and 30°C. Maximum values occurred from May to September (Figure 2) and the
minimum, in February. Salinity varied between 28 and 34.6, with a low-salinity
period during summer and a high-salinity period from the beginning of October to
1124
Table 1. Matrix of correlations. Spearman coefficient values
Temperature Salinity Chi a
total
Oil a
Zooplankton A.toiiso
<55 M.m total
total
Eggs
Nauplii
C\
C,
Males
Females
Eggs
per
female
Salinity
-0.177
Chi a total
0.328
Chi a <55 \isn
0.203
Zooplankton total 0 . 4 4 1 "
A.tonsa total
0.266
Eggs
0.197
024«
Nauplii
C,
0.257
0.567"
C:
C,
0311
0.074
C,
0.140
C,
0.259
Males
-0.063
Females
Eggs per female
0.115
Sex ratio
0.517*
0.0847
0J39
0.629**
- 0 189 -0.021
0.006
0.057
0.064 -0.005
0.057
0.046
-0.285
0.135
-0.354 -0.064
-0.441"-0.018
-0.243 -0.093
0.047
-0.100
0.059
-0.129
-0.007 -0.043
-0.242 -0.084
-0.139
0.208
0.233
0.468*
-0.022
0.497"
0.157
-0.417
-0.145
-0.241
-0.165
-0.138
- 0 157
-0.256
0.041
0.875"
0 530"
0.871"
0 380
0.648"
0 245
0.158
0.038
0.284
0.082
-0.016
0.032
•Significant at /><0.05.
••Significant at P<0.01.
n = 27 except for eggs per female (;i •= 24) and sex ratio (n = 22).
0 266
0.990"
0 4«8"
0.240
0 234
0.159
0.090
0.255
0.026
0 093
0.431*
0 464*
(1.307
0.389*
0.056
0 058
0.001
0.121
0 129
0.038
0.188 -0 031
0.264
0 140
0 238 - 0 080
0 496* -0.1 OX
-0.007
0.291
0.559"
0.669"
0.625"
0.619
0 679"
0 470*
0.008
0 329
0814"
0 729"
0.609"
0.5 4 8 "
0.508"
-0.030
0.109
0 715"
0.603"
0.687"
0.444*
-0.042
0.339
0.871**
0.817"
0.743"
-0.129
0.265
0.889"
0 . 8 4 1 " 0.734"
-0.182 -0.164 -0.405
0.231
0.314 -0.302
0.3K3
J.Diaz Zaballa and R.Gaudy
Temperature
32
30
28
26
24
22
20
Salinity
35
33
31
29
27
25
Chlorophyll (total particles)
700
600
500
400
300
200
100
0
Chlorophyll (particles < 55 ftm)
M
A
M
J
J
A
S
O
N
D
J
F
M
A
Fig. 2. Seasonal variations in temperature, salinity, chlorophyll (particles <55 p.m) and total
chlorophyll.
1126
Seasonal variations in zooplankton of La Habana Bay
the end of March. During this last period, temporary decreases in salinity were
observed, particularly on 7 February, after a period of strong rains caused by a
tropical depression.This minimum salinity value also corresponded to the minimal
temperature. The chlorophyll of thefine(<55 u.m) sestonic fraction displayed very
high values (up to 150 jig I1), with a succession of rapid changes in abundance
(seven peaks during the studied period). The total chlorophyll showed a parallel
evolution, but with 2- to 6-fold higher values, except during the hurricane period of
February when the chlorophyll concentrations of the total and <55 p.m fractions
were similar, because of the scarcity of large detritus in the seston.
Quantitative and qualitative variation of zooplankton
The abundance of total zooplankton was very high, from 15 000 to 255 000 ind. nv\
with a main maximum in June-July and several other secondary peaks during the
rest of the year (Figure 3). A positive, but relatively low correlation was observed
with temperature (Table I).
The zooplankton were dominated by the copepod A.tonsa (89% of the total
number of organisms, in annual average). Other notable taxa were the appendicularian Oikopleura sp. (5.8%) and the rotifer Brachionus plicatilis (3.5%). The
remaining taxa were cirriped nauplii, polychaete larvae, lamellibranch larvae,
other copepods and amphipods.
As a consequence of its dominance, the seasonal variation in abundance of
A.tonsa was parallel to the evolution of total zooplankton, with a succession of six
peaks (Figure 3). Correlations of total Acartia (swimming stages) with temperature and salinity were not significant, but a positive correlation appeared with
chlorophyll <55 (xm.
Oikopleura sp. was present all through the year, with five peaks of abundance
not correlated with A.tonsa or total zooplankton abundances (Figure 3).
Brachionus plicatilis appeared only during summer, the period of the lowest
salinity values. Its two main peaks corresponded to two of the phytoplankton
peaks (Figure 3).
Variation in the population structure of Acartia tonsa
Acartia eggs showed a succession of eight peaks of similar size, all through the year
(Figure 4). The abundance of eggs was not correlated with temperature, salinity or
chlorophyll. Acartia nauplii were always present. They were positively correlated
with the chlorophyll contained in the fine fraction (<55 (xm) of seston (Table I;
Figure 6) and with the proximate stages, i.e. eggs and copepodite 1. The abundance
of the successive copepodites did not depend on the environmental factors, but
these stages were correlated between themselves and with adult males or females.
The sex ratio (males/total number of adults) varied markedly, even showing
periods of the total absence of one sex (Figure 5). It was correlated with temperature, but not with salinity or chlorophyll.The only other significant correlation was
found with the total number of Acartia (nauplii - copepodites - adults).
The number of eggs per female, which can be considered as a fertility index of
the population, presented 6-7 peaks during the study (Figure 5). No correlation
1127
J.Diaz Zaballa and R.Gaudy
Total zooplanktoo
ind./m3
300 000
200 000
100 000
0
Acartia tonsa
ind./m3
Oikopleura sp.
30 000 T
20 000
10 000
0
ind./m3
Brachionus plicatilis
60 000 T
40 000
20 000
0
M A M J
J
A
S
O
N
D
J
F M A
Fig. 3. Seasonal variations in abundance of total zooplankton. A.ionsa. Oikopleura sp. and B.plicaiilis.
1128
Seasonal variations in zooplankton of La Habana Bay
Eggs
Nauplii
ind./m3
200 000 T
150 000
100 000
50 000
0
Copepodites
Adults
M
A
M
J
J
A
S
O
N
D
J
F
M
A
Fig. 4. Acania tonsa: seasonal vanationsin abundance of eggs and nauplii, copepodites and adults.
1129
J.Diaz Zaballa and R.Gaudy
Eggs per female
Nb./female
120
100
80
60
40
20
0
/Vy
Sex-ratio (males/adults)
too
80
60
40
20
0
M
A
M
J
J
A
S
O
N
D
J
F
M
A
Fig. 5. Acartia tonsa: seasonal variations in sex ratio and number of eggs per female.
was found with temperature, salinity or chlorophyll. Contrary to the sex ratio, the
total abundance of Acartia had no significant effect on this parameter.
Discussion
In Habana Bay, the phytoplankton cycle has no significant effect on the recruitment of A.tonsa estimated from the eggs per female ratio, contrary to most previous observations on Acartia from other temperate or tropical regions (Deevey,
1960; Landry, 1978; Lee and McAlice, 1979; Uye, 1982; Sabatini, 1990; Gaudy,
1992a,b). As a matter of fact, previous in situ and experimental studies show that
the egg production of A. tonsa is narrowly related to the abundance of chlorophyll
or phytoplankton in a more or less extended range of concentration and that,
above a maximum food concentration (saturation level), egg production tends to
be constant (Durbin et al, 1983; Ambler, 1986; Beckman and Peterson, 1986;
Gaudy, 1992b). This maximum value depends on the area studied. It corresponds
to 20 jig m ' of chlorophyll a in the Berre lagoon, near Marseilles (Gaudy, 1992b),
to 16 jig I 1 in Narrangansett Bay (Durbin et al., 1983) and to only 5 u.g I1 in Long
Island Sound (Bellantoni and Peterson, 1987). The succession of several cohorts or
generations is often observed (when the sampling frequency is sufficiently high). In
A.tonsa, 3-11 generations can be separated according to the main temperature
conditions of the different studied areas (Conover, 1956; Woodmansee, 1958;
Deevey, 1960; Jeffries, 1962; Lee and McAlice, 1979; Sabatini, 1990; Gaudy,
1992a). They are generally generated by temporary increases in egg production
1130
Seasonal variations in zooplankton of La Habana Bay
Nauplii / m3
•
160 000 •
120 000 •
y = 455 Chi. + 24917
•
•
80 000 •
40 000 •
•
•
—~rT^
_
0-
•
•
• • •
•
20
™
•
40
^m
_
60
" "
•
•
1
1
1
1
1
80
100
120
140
160
Chlorophyll (particles < 55 ftm) ptg I 1
Fig. 6. Acartia tonsa: relationship between the density of nauplii and the abundance of chlorophyll
(particles <55|im).
provoked by changes in the chlorophyll concentration (Gaudy, 1992a), but during
summer, the increase in growth rate caused by temperature conditions leads to an
overlapping of generations which makes their analysis confusing.
The succession of several peaks of numbers of eggs per female is not correlated
with chlorophyll abundance. It could result from changes in the quality of the available food, independently of its abundance. Ambler (1986) showed that the egg
production of A.tonsa in East Lagoon partly depended on the quality of algae.
Similar results were given in other areas by Cahoon (1981), Stottrup and Jensen
(1990), Kleppel (1992) or White and Roman (1992).
The absence of a correlation between chlorophyll and egg production in Habana
Bay is the consequence of the non-limiting trophic conditions prevailing all
through the year. Chlorophyll average values were 106 u,g I"1 for total seston and
40.62 u.g 1-' for seston of size <55 n.m, and values < 9 jig I"1 were encountered on only
three occasions over 27 seasonal samples. Thus, plenty of energy is available for
egg production most of the year. The number of eggs per female varied between
0.6 and 120, the average value being 31.8. The corresponding egg ratio values, calculated according Edmondson et al. (1962), were 0.57,133 and 32.6. These values
are in the range of most literature data. For example, Gaudy (1992b) found values
between 5 and 18 eggs female1 day1 in the Berre lagoon. Bellantoni and Peterson
(1987) cite values between 9 and 56 in Long Island Sound, and Durbin et al. (1983)
give an average value of 25.3 eggs female-1 day 1 in Narragansett Bay. Thus, the
very high trophic conditions prevailing in Habana Bay do not lead to exceptional
egg production rates. The relative constancy of the level of maximum egg production in various environments, characterized by very different chlorophyll richnesses, indicates that it must also depend on the physiological limit of the females,
e.g. the minimal time necessary for the maturation of oocytes.
The only correlation observed between chlorophyll concentration and zooplankton was observed with nauplii of A.tonsa, when the fine fraction of seston
1131
J.Diaz Zaballa and R.Gaudy
(<55 |xm) was considered. This result indicates that the survival of nauplii is probably related to the presence in sufficient abundance of edible particles of suitable
size for them, e.g. small phytoplankton cells. Even if naupliar stages are potentially
able to feed on a large range of particle sizes (Marshall and Orr, 1956; Fernandez,
1979), their highest filtration rate is observed on particles smaller than those
efficiently used by copepodites or adults. Berggreen et aL (1988) showed that the
optimum particle size and the upper size limit were 7-14 and 70 u.m for A.tonsa
NII-NIII, respectively, instead of 14-70 and 250 ^m for adults, respectively. The
quality of particles should also play a role. The effect of food quality on the egg
production of A.tonsa is well documented (Cahoon, 1981; Stottrup and Jensen,
1990; Kleppel, 1992; White and Roman, 1992). No information is available on this
subject for naupliar feeding, but it can be supposed that, compared with older
stages, they need a food containing proportionally more vitamins or oligoelements. Possibly, although the quality and quantity of algae present in seston are
never limiting for the feeding of the adults and for their egg production, the proportion in the seston of algae qualitatively favourable for the growth and survival
of nauplii must be relatively low, leading to a temporary lack of favourable food
when the seston abundance diminishes, with subsequent increases in the naupliar
mortality. Thus, the fluctuations in the survival of nauplii, which appear to be the
most sensitive developmental stage during the growth of Acartia (Heinle, 1966;
Landry, 1978; Uye, 1982), regulate the quantitative abundance of the less sensitive
older stages. Another hypothesis to explain the decrease in the naupliar population during low chlorophyll concentration periods could be the cannibalistic
behaviour of older copepodites and adult stages. Acartia tonsa is able to feed
efficiently on prey (Anraku, 1964; Lonsdale et ai, 1979; Robertson, 1983; White
and Roman, 1992). It could satisfy its protein requirement by feeding on its own
nauplii. Such a mechanism has been advanced to explain the high naupliar mortalities periodically observed in situ for Acartia clausi (Landry, 1978) and for
A.tonsa (Lonsdale etai, 1979).
The correlation between nauplii and Cl shows that the abundance of the first
copepodite logically depends on the abundance of the preceding stages. The temporal variations in the successive copepodite stages and adults of A.tonsa are more
or less synchronized, as demonstrated by the correlations existing between each of
them. The lack of correlation between their abundance and the egg production
cycle confirms that the variations in abundance of developmental stages do not
indicate the succession of different cohorts, contrary to some other regions (Sabatini, 1990; Gaudy, 1992a,b), but more probably reflect the occurrence of hydrographic instability events, such as dilution or partial replacement of the bay water
by riverine freshwater. The salinity variations can be used to indicate the importance of this process. For example, the large decrease in salinity observed in February corresponds to a strong decrease in the whole zooplankton population. The
same trend, although not statistically significant (r=0.34; P=0.08), is also observed
for chlorophyll abundance (<55 p.m), which is directly related to salinity changes.
The flushing effect of the freshwater in the bay is also illustrated by the disappearance of large detritus in seston, following the strong tropical rainfall event of
February. Another factor associated with salinity variations could be the
1132
Seasonal variations in zooplankton of La Habana Bay
temporary increase in the pollution level in the bay associated with strong freshwater discharges. We have no qualitative or quantitative data on pollutants for the
investigated period, but it is unlikely that the pollution impact would markedly
affect the abundance of the zooplankton, which are already chronically exposed to
high pollution conditions. The importance of predation by carnivorous organisms,
such as ctenophores, is emphasized in several previous studies to explain populations changes of A.tonsa (Conover, 1956; Heinle, 1966; Beckman and Peterson,
1986): In Habana Bay, the number of crustacean predators seems to be very low:
only a few amphipods and decapod larvae were collected. Gelatinous animals such
as Ctenophora were never caught. Thus, it is probable that predation by other
zooplankters must not be a determinant factor for the population changes.
Sex ratio variations observed in adults of A.tonsa could result from the greater
sensitivity of males to the hydrological instability of the bay: when the total population decreases, males diminish proportionally more rapidly than females, or even
disappear totally. However, this does not seem related to a particular sensitivity of
males to low salinity values because their abundance is not correlated with salinity,
as for females. Lee and McAlice (1979) observed in the Maine estuary that relatively more A.tonsa males were observed when the temperature decreased. In
Habana Bay, no correlation was found between temperature and males or
females, but the sex ratio was positively correlated to temperature, contrary to the
observations of Lee and McAlice. The possible effect of other factors not studied
there, particularly the pollutants, cannot be eliminated. The positive correlation
between the sex ratio and the density of the Acartia population can be interpreted
as a homeostatic mechanism for the regulation of the population. During periods
of low abundance, a higher proportion of females is available for egg production,
thus favouring a rapid recovery of the population level. Similar observations were
made on the same species by Heinle (1970) in the Patuxent River estuary region
and by Sabatini (1990) in the region of Bahia Blanca, and were also interpreted by
these authors as a compensatory mechanism for the regulation of the population.
To summarize our main results, in an exceptionally rich environment such as
Habana Bay, the short-term variations in abundance of A.tonsa cannot be
explained by changes in its reproductive potential in relation to phytoplankton
density, contrary to many other estuarine or marine coastal systems, because the
food is always in excess of reproduction needs. Most of the variations in abundance
mainly reflect the dilution of the total zooplankton population provoked by the
flushing effect of inland freshwaters in the bay. They also depend on the survival of
the naupliar stages, because nauplii numbers are directly correlated with the presence of edible phytoplanktonic particles. Thus, the importance of the quantity and
quality of food appears to be different if naupliar survival or adult fertility are
considered. As several other factors probably interact, it seems necessary to carry
out more experimental studies to progress knowledge of the processes acting on
the population dynamics in such eutrophic areas.
Acknowledgements
This work was carried out in the framework of the French-Cuban bilateral pro1133
J.Diaz Zaballa and R.Gaudy
gramme. The authors acknowledge the administrative and scientific authorities
of the two countries for their help and their financial assistance.
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Received on August 15. 1995; accepted on January 29.1996
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