Journal of Plankton Research VoL19no.6pp.693-702, 1997
Effects of temperature, salinity and food level on the life history
traits of the marine rotifer Synchaeta cecilia valenrina, n. subsp.
Rafael Oltra and Rafael Todolf
Area de Ecologia, Facultad de Ciencias Bioldgicas, Universitat de Valincia, 46100
Burjassot (Valencia), Spain
Abstract A strain of the marine rotifer Synchaeta cecilia valentina, n. subsp., isolated from the Hondo
of Elche Spanish Mediterranean coastal lagoon at 22%o salinity, was cultured in the laboratory in 20
ml test tubes and fed with the alga Tetraselmis suecica. The effect of two temperatures (20 and 24°C),
four salinities (20,25,30 and 37%o) and two food levels (15 000 and 25 000 cells ml-1) on the life history
traits of this rotifer were studied in life tables performed with replicated individual cultures. Temperature and salinity had a significant negative effect (P < 0.001) on the average lifespan (LS) and on the
number of offspring per female (RQ). The effect of food level on LS is unclear, whereas R$ is greater
at 20°C with the lower concentration of algae and at 24°C with the higher algal concentration. The
maximum values of LS and RQ, 5.6 days and 9.2 offspring per female, respectively, were recorded at
20°C, 25%o salinity and low food concentration. There is also a clear negative effect on the intrinsic
growth rate (r) due to salinity. The effect of temperature depends on the food level and, as occurs
with RQ, the maximum values of r occur with the lower algal concentration at 20°C, whereas at 24°C
they are obtained with the higher algal concentration. These r values, from 1.04 to 1.10 day-', were
reached at 24°C, salinities of 20-25%o and with high food concentration.
Introduction
Even though the culturing of freshwater rotifers is relatively simple, and has been
achieved with various species (Pourriot, 1965; May, 1987), the same cannot be said
of marine or brackish water species. In fact, with the exception of the euryhaline
Brachionus plicatilis, it has been possible to culture only a few such species, some
examples of which are Encentrum linnhei (Scott, 1974; Schmid-Araya, 1992),
Synchaeta cecilia (Arndt et ai, 1985; Egloff, 1986,1988) and Synchaeta hutchingsi
(Brownell, 1988).
The culturing of another species of this group would be of interest because it
could provide further information about the biology of marine species, which is
currently based primarily on B.plicatilis. It is also of potential interest for the areas
of ecotoxicology and marine aquaculture in which the only rotifer used at present
is the aforementioned B.plicatilis (Lubzens et al, 1989; Snell and Janssen, 1995).
This species is used in the feeding of larvae of fish such as the gilthead sea bream
{Spams aurata) in marine aquaculture, although the cultures have to be enriched
with polyunsaturated essential fatty acids, since the natural levels are insufficient
to ensure the survival of the larvae (Lavens et al, 1995). This problem, together
with the fact that recently hatched sea bream larvae prefer small prey with a width
of between 30 and 70 urn (Lubzens et al, 1989), has led to other species of rotifers
being tried, such as E. linnhei in the feeding of larval turbot Scophthalmus
maximus (Schmid-Araya, 1989), or species of the genus Synchaeta from natural
blooms in the feeding of sea bream larvae (Divanach and Kentouri, 1983). The
latter rotifer genus, Synchaeta, can be found in brackish and marine waters
throughout the world (Rousselet, 1902; Ruttner-Kolisko, 1974; Nogrady, 1982), the
cultivation of some species being practicable in seawater.
© Oxford University Press
693
R.Oftra and R-Todolf
The aim of the present work has been to culture a strain of the marine rotifer
S.cecilia valentina, n. subsp. (Hollowday et al, in preparation), from the coastal
lagoon Hondo of Elche (Spanish Mediterranean). This rotifer is known to be
capable of living under a wide range of conditions, since it was found in the lagoon
throughout the summer and beginning of autumn of 1995 at salinities from 18 to
36%o, temperatures of 18-28°C, and densities of up to 4800 bid. I"1 (ArmengolDfaz and Oltra, unpublished results).
This culturmg has presented some difficulties. Initial attempts at feeding with
the algae Nannochloropsis ocidata, Pavlova lutheri and Isochrysis galbana were
unsuccessful, despite the latter having been used successfully in the feeding of the
closely related S.cecilia (Egloff, 1988). The use of the chlorophycean Tetraselmis
suecica, which has previously been used in the feeding of S.cecilia, did, however,
produce good growth despite being found to be extremely sensitive to excessive
algal concentrations. As a first step towards our proposal, in this paper we study
the life history traits of this strain of S.cecilia valentina cultured at different temperatures, salinities (up to 37%o) and food levels.
Method
Synchaeta cecilia valentina was isolated from the Hondo of Elche in September
1995 when water salinity and temperature were 22%o and 20°C, respectively.
Several clones from single isolated females were cultured in sterilized seawater,
which was diluted to 20%o and enriched with nutrients and vitamins of the
Guillard and Ryther (1962) f/2 medium. The clones were kept in 20 ml test tubes
at 20°C, at a light intensity of 12 uE cm"2 s"1 with a 12:12 h light:dark photoperiod,
and fed with T.suecica which had been cultured under similar conditions, but with
a light intensity of 80 uE cm"2 s"1.
Life table analyses were performed with individual rotifer cultures at two temperatures (20 and 24°C), four salinities (20,25,30 and 37%o) and two food levels
(15 000 and 25 000 T.suecica cells ml"1) which correspond to 2.10 and 3.49 ug ml"1
dry weight, respectively (Temprano et al., 1994). The experimental light intensity
and photoperiod were as described above.
The procedure used for each of the 16 experimental assays was as follows. Preexperimental cultures were maintained under the 'experimental' conditions for
at least 1 week in 20 ml test tubes at low population density (<5 ind. ml"1). From
these cultures, -100 egg-bearing females were selected at random and placed in
glass wells (2 females ml"1). After 12 h,72 newborn females were isolated and cultured individually throughout their lifetime in plates of 24 wells with 1 ml of fresh
culture medium in each well. The offspring were counted every 24 h and the
mothers were transferred to new trays with freshly prepared medium and food.
Algal concentrations in exponentially growing cultures at the same salinities as
the experimental assays were determined with a haemocytometer and diluted to
the desired food level.
The following demographic parameters were calculated from the survival and
fecundity schedules: average lifespan (LS), mean fecundity per female lifetime
), average age of offspring production (Tc), intrinsic rate of population increase
694
Life history traits of S.cecilia Valentino, n. subsp.
(r) calculated as r = ]nR(/Tc (Krebs, 1985), age-specific survival (he) and agespecific fecundity (jnx - newborns per female) (Carey, 1993).
The effects on LS and ^?0 included in the factorial design (temperature X salinity X food level) were evaluated using univariate F-tests from the MANOVA
program of SPSS (Norusis, 1986). Previously, the logarithmic transformation was
applied to the LS variable and the + 0.5 square root transformation to the Ro variable (Sokal and Rohlf, 1995).
Results
The effects of salinity, temperature and food level on the survivorship and agespecific fecundity of S.cecilia valentina are shown in Figure 1. Lifespan is a little
longer when the temperature is lower. At 20°C, it varies from 10-11 days at low
salinity (20 and 25%o) to 6-8 days at higher salinities, whilst at 24°C lifespan varies
from 8-10 days at 20%o and to <7 days at the other salinities.
The age-specific fecundity also varies with temperature since, when the latter
is increased, reproduction finishes earlier. In this case, although the maximum
values obtained at each temperature, slightly more than two progeny per female
per day, are similar, the reproductive peaks appear earlier in the trials carried out
at 24°C (first and second day of life) than in those at 20°C, except at 20%o salinity when the reproductive maximum also occurred at the age of 1 day.
Salinity has a marked negative effect both on lifespan, which falls by almost
half with the change from 20 to 37%o, and on maximum prolificity whose values
undergo an even greater reduction.
The effect of food concentration on survivorship is less clear, except for the
low-salinity (20%o) assays. In these, the survival and lifespan are greater with the
lower algal concentration (15 000 cells ml"1) when the temperature is 20°C, and
with the higher algal concentration at a temperature of 24°C. For higher salinities, there are hardly any differences which can be attributed to the feeding (tests
at 25%o), or there are variations which follow no clear pattern. At 24°C, the agespecific fecundity is at a maximum with the highest concentration of algae, whilst
at 20°C there are barely any differences due to alimentation.
In Table I, the average lifespan and average number of offspring per female
are shown for each of the 16 assays. It can be seen that the effects of temperature and salinity are highly significant for both parameters (Table II), and that
they follow the same pattern as for survivorship and age-specific fecundity. In
the trials at low temperature (20°C) and salinity (20 and 25%o), the average lifespan (3.8-5.6 days) and the average number of offspring (5.6-9.2) are greater
than in those carried out when these are increased. The effects of algal concentration on average lifespan are uncertain, but/the influence on the average
number of offspring is clear (Tables I and II). At 20°C, the greatest number of
offspring per female occurs at an algal concentration of 15 000 cells ml"1 for all
salinities, whilst at 24°C it is highest at a concentration of 25 000 cells ml"1.
Figure 2 shows these variations in R^ with respect to the experimental conditions, along with those of reproduction time Tc and the intrinsic rate of population increase r.
695
R.OItra and R-Todoh
24°C
20°C
0,1 -
20%,
0.01 -
0.001
0,001
0
1 2 3 4 5 6 7
8 9
10 11 12
x(d)
m(x)
25 %o
0,01-
0,01-
0
I
2 3 4 5 6 7 8 9
X(d)
10 11 12
0,001
m(X)
0,1 -
30%.
0.01
0,01 •
0.001
0,001
0
1 2
3
4
0 1 2 3 4 5 6 7 8 9
X(d)
5 6 7 8 9 10 11 12
x(d)
m(x)
0,1
10 11 12
m(x)
0,1 -
37%,
0.01
0.001 **-*—
0 1
2 3 4 5 6 7 8 9
X(d)
0.01-
10 11 12
F j | L Age-speciflc survival [l(x), dashed line), and fecundity [m(x),\ for S-cccilia valcntina grown at
S n i < « » P ™ ^ « (20 and 24°C), salinities (20,25, 30 and 37*!) and food l e v e f ^ e f c ^ l
l-'; open circles, 25 000 cells mH). Age (x) in days (d).
The variations in Tc are comparable to those observed for the average number
of days of life: the generation time tends to shorten when temperature and salinity (>25%o) increase since life expectancy also diminishes. At 20°C, life expectancy
696
life history traits otS.cedlta valattina, a. subsp.
Table L Average lifespan (IS), average number of descendants per female (/?o) and their respective
standard errors (SE) of S.cecilia valentina grown at the indicated temperature, salinity and food level
Temperature
(°C)
Salinity
(*•)
Food level
(cells ml-')
20
20
15 000
25 000
15 000
25 000
15 000
25 000
15 000
25 000
15 000
25 000
15 000
25 000
15 000
25 000
15 000
25 000
25
30
37
24
20
25
30
37
n
LS
SE
*b
SE
72
68
72
72
72
72
72
72
70
70
•72
72
72
72
72
72
5.3
4.0
5.6
3.8
3.1
3.2
3.2
3.2
3.2
4.7
3.7
33
3.1
2.6
2.0
2.5
03
03
0.4
0.4
0.2
0.2
02
02
0.2
0.2
0.2
02
02
0.1
0.1
0.1
7.9
5.6
92
6.1
2.7
2.3
1.5
1.5
2.1
6.2
2.9
5.4
1.8
2.9
0.8
1.1
0.6
0.5
0.6
0.7
03
03
02
0.2
0.2
0.3
0.2
02
0.2
02
0.1
0.1
varies between 2.3 and 3.1 days, and at 24°C from 1.3 to 2.3 days. Once again, the
effect of algal concentration is unclear, but it does seem that at 24°C, Tc is generally at its lowest with the highest concentration.
The intrinsic growth rate, r, which summarizes all life parameters since it combines survival, fecundity, and the timing of development and reproduction, clearly
varies according to experimental conditions. On the one hand, it decreases along
with salinity, and on the other hand it rises together with temperature if the food
level is high, but falls if this is low (Figure 2). At 20°C, the maximum value is 0.76
day 1 and the minimum is 0.15 day 1 , with the differences at 20 and 25%o salinity
being slight irrespective of the algal concentration. At 24°C, the differences due
to food level are significant: the maximum value at greatest algal concentration is
1.10 day 1 (at 20%o salinity) and the minimum is 0.06 day 1 (at 37%o), which is less
than the lowest value at 20°C. The values decrease markedly in the lowest algal
concentration, reaching a negative value (-0.21 day 1 ) at 37%o salinity owing to a
value for the mean fecundity of less than one (0.75 descendants per female).
Table H. Univariate F-test from MANOVA for the indicated factors and parameters
Effect
Temperature (T)
Salinity (S)
Food level (F)
T X S interaction
T X F interaction
S x F interaction
T X S X F interaction
d.f.
1,1128
3,1128
1,1128
3,1128
1,1128
3,1128
3,1128
LS
*o
F
P
F
P
6.6
14.8
2.4
35
31.8
6.4
6.2
0.010
0.000
0.121
0.014
0.000
0.000
0.000
4Z0
146.1
4.9
8.0
101.9
2.0
12.9
0.000
0.000
0.026
0.000
0.000
0.100
0.000
697
R-OHra and R-TodoK
20°C
24°C
Ro
5
Ro
20
2b
30
35
20
%
25
K>
30
3b
Tc
Tc
•-^
•
/
15
20
25
30
35
20
/—.
25
\
30
35
r
15
10
8
6
4
2
0
40
40
r
20
25
30
35
20
Salinity %.
25
30
35
40
Fig. 2. Effects of temperature, salinity and density of T.suecica (solid line,15 000 cells ml"1; dashed line,
25 000 cells mH) on net reproductive rate (RQ), cohort generation time (7"c) and intrinsic rate of population increase (r).
Discussion
The experiments reported here have allowed us to observe the response of a
strain of Sxecilia valentina in laboratory cultures to different conditions of
temperature, salinity and food concentration.
Synchaeta cecilia valentina grew in all of the salinities tested, including undiluted seawater. This is difficult to achieve in other rotifer species, apart from
B.plicatilis. Although growth was slow under these conditions, in seawater diluted
to 30%o it was notable, r = 0.78 day-1, with the appropriate temperature and food
concentration (24°C and 25 000 cells ml"1).
Table III contains the mean values of the parameters of the life table for the
temperatures, salinities and food concentrations analysed. Temperature has a
negative effect on both the average and maximum lifespan. This is a general effect
in rotifers and is due to an increase in the metabolic rate (Miracle and Serra, 1989;
Nogrady et aL, 1993). Temperature also affected the age-specific fecundity, bringing forward and shortening the reproductive period (Figure 1), one consequence
of which is a reduction in the time of generation (Table III). Similar responses
have been reported in Brachionus calycifiorus (Starkweather, 1987) and
698
Life history traits of S.cecilla Valentino, n. subsp.
Table EU. Mean values of the indicated demographic parameters for each experimental temperature,
salinity and algal concentration
n
LS
(SE)
«b
(SE)
n
Tt
(SE)
r
(SE)
572
572
3.9
3.1
(0.1)
(0.1)
4.6
2.9
(02)
(0.1)
8
8
2.6
1.6
(0.1)
(0.1)
0.49
0.51
(0.1)
(0.2)
280
288
288
288
43
4.1
3.0
2.7
(0.1)
(0.2)
(0.1)
(0.1)
5.4
5.9
2.4
1.2
(0.2)
(03)
(0.1)
(0.1)
4
4
4
4
2.0
2.5
2.1
1.9
(03)
(03)
(0.3)
(0.3)
0.78
0.71
0.45
0.05
(0.1)
(0.1)
(0.1)
(0.1)
574
570
3.7
3.4
(0.1)
(0.1)
3.6
3.8
(02)
8
2.2
2.0
(0.2)
(0.2)
0.40
0.60
(0.1
(0.1)
Temperature (°C)
20
24
Salinity (%o)
20
25
30
37
Algal concentration
15 000
25 000
(GT.2)
B.plicatilis (Serra et ai, 1994). In these species, however, the fecundity value
increased along with temperature which compensates for the negative effect that
the shortening of the reproductive period has on birth rate. For this reason, in the
B.plicatilis species, temperature variations affect time-dimensioned parameters,
but not the average number of offspring (Ro), which is similar at temperatures of
20,25 and 30°C (Serra et al, 1994).
In our case, the age-specific fecundity is not greater at the higher temperature,
as a result of which the average number of offspring is lower at 24°C (Table III).
Given that this temperature is not excessively high for the species, since S.cecilia
valentina has been detected in the lake at a temperature of 28°C in summer
(Armengol-Dfaz and Oltra, unpublished data), it leaves room for speculation that
the decrease in Ro at 24°C could be related to an insufficient food level.
The average intrinsic rate of population increase is similar at both temperatures
(Table III), since at 24°C the lower Rg is compensated for by a diminished Tc It
would, however, be somewhat higher at 24°C (r = 0.61 day 1 ) if the negative value
obtained at high salinity and low food concentration were not taken into account,
this value being seen to be due precisely to the lack of food, since under the same
conditions, but with a greater algal concentration, growth is positive.
Salinity has a marked negative effect on average lifespan, Ro and r (Tables II
and III), with the best results at the lowest salinities tested. At a salinity of 25%o,
the average Ro is higher than that obtained at 20%o, but Tc is also higher despite
the fact that life expectancy is shorter. This result can be explained in part by the
high initial mortality (38%, the maximum of all the tests) which affected the assay
at 20°C, 25%o and high algal concentration, causing LS to fall and Tc to rise. It
should be pointed out that although the growth of Scecilia valentina in seawater
at 37%o was limited, especially at 24°C, it was noteworthy in dilutions of up to 30%o
(r = 0.78 day 1 ) with adequate temperature and food concentration (24°C and
25 000 cells ml-1).
There are other marine or halophilous species which grow better at salinities
below that of seawater, e.g. the euryhaline B.plicatilis; although it is able to tolerate a wide range of salinities, it grows more quickly when salinity is moderate,
699
R.Ottra and R.TodoK
from 10 to 20%o, than when it is either higher or lower (Ruttner-Kolisko, 1972;
Lubzens, 1981; Pascual and Yufera, 1983; Lubzens et aL, 1985; Miracle and Serra,
1989). The marine species S.cecilia has been cultured at a range of salinities from
4 to 33.5%o (Arndt et al, 1985; Egloff, 1988). Synchaeta hutchingsi, another marine
species, has been cultivated at 34.5%o and, after a period of adaptation, is better
able to tolerate low salinities (up to 8%o) than either high ones (up to 50%o) or
seawater.
Food level has no significant effect on the average lifespan, whereas it does on
the number of offspring (Table II). Similar results have been obtained with the
species B.plicatilis and Encentrum linnhei cultured in seawater diluted to 50%
(Schmid-Araya, 1991). In both species, the production of offspring is at a
maximum at a given concentration of food, above and below which it falls. Stemberger and Gilbert (1985) also found a restriction in growth with high food doses
in different freshwater species, while Halbach and Halbach-Keup (1974) reported
a decrease not only in fecundity, but also in survival, at both high and low food
concentration in the B.calyciflorus species.
In our own tests, we have seen that the optimal food concentration depends on
the temperature. Thus, at 20°C, RQ and r are greatest when the food level is lower,
whereas at a temperature of 24°C they reach their maximum values when it is
increased. These findings are related to the acceleration in the metabolic rate
which accompanies the temperature rise, and the need for an increased food
intake that this generates (Serra and Miracle, 1989). The data provided by Starkweather (1987) on the interaction between food concentration and temperature
clearly illustrate this.
From our results, it seems logical to suppose that a concentration of 15 000 cells
ml"1 is more or less appropriate for cultures at 20°C given that a 66% increase (to
25 000 cells ml"1) provokes a decrease in fecundity and growth (Table II, Figure
2). We do not, however, know whether 25 000 cells ml"1 is the most convenient
dosage for a temperature of 24°C. Judging by the RQ and r values at 37%o, lower
than those obtained at 20°C, this may have been insufficient.
The possibility must also be considered that the results may have been different with another algae. Some preliminary trials carried out with Nannochloropsis oculata, Pavlova lutheri and even Isochrysis galbana, which has been used
successfully in the feeding of Scecilia (Egloff, 1988), were unsuccessful. Synchaeta
cecilia valentina has grown only with the chlorophycean T.suecica (also accepted
by S.cecilia as food) and even then it proved to be highly susceptible to excessive
algal concentration. In future experiments, tests will be carried out with cryptophycean algae, which are those that have given the best results in the cultivation
of species of the genus Synchaeta equally in freshwater (Pourriot, 1965; May, 1987)
as in saltwater (Egloff, 1988).
Acknowledgements
We thank Eric D.Hollowday for his valuable assistance in the recognition of specimens oiScecilia valentina, and Maria Rosa Miracle, Manuel Serra, Africa G6mez,
I.Costelo and an anonymous reviewer for their comments and suggestions.
700
Life history traits otS.ceeilia Valentino, n. subsp.
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Received on August 6,1996; accepted on January 23,1997
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