1
Effect of the Ankistrodemus gracilis and Scenedesmus quadricauda
microalgae on the growth of zooplankton species.
Carla Fernandes Macedo1 & Ricardo Motta Pinto-Coelho2
1
Centro de Ciências Agrárias, Ambientais e Biológicas, Universidade Federal do
Recôncavo da Bahia (UFRB), Campus de Cruz das Almas, Centro, 44380-000, Cruz das
Almas, BA, Brasil. E-mail: cfmacedo@ufrb.edu.br
2 Instituto de Ciências Biológicas, Departamento de Biologia Geral, Universidade Federal
de Minas Gerais, 31270-901, Belo Horizonte, MG, Brasil. E-mail: rmpc@icb.ufmg.br
Abstract
The effect of the microalgae on two zooplankton species (Daphnia laevis and Moina
micrura) was evaluated throughout variables related to the somatic (biomassa) and
population growth. All the animals derived from a single female, in order to avoid genetical
variation between treatments. The zooplankton microalgae diet, were the chlorophycean
Scenedesmus quadricauda and Ankistrodesmus gracilis. Cultures were mantained under a
11 hours light photoperiod, illumination ranged from 800 to 1400 Lux and temperature was
21 ± 3°C. Ankistrodesmus grew more than Scenedesmus with the same CHU12 medium and
the two growth curves were significantly different (F=1,47, gl=38, p <0,001).
Ankistrodesmus showed larger carrying capacity (K) for Daphnia than Moina. Daphnia
population exponential growth was larger than Moina, which grew slowly. Daphnia laevis
neonate had 0.62 mm in length and adults reached 1.50 mm and 1.06 mm with
Ankistrodesmus and Scenedesmus, respectively, as source of food. Moina micrura neonate
and adults reached 0.52 mm and 0.97 mm, respectively, for any microalgae studied. The
2
present work shows that cultures of Ankistrodesmus and Moina can be indicated for fish
growth in ponds, because both grow faster and the time for Moina egg production could be
short.
Key-word: microalgae; cladoceran; growth; experiments; aquaculture.
Resumo
O efeito das microalgas sobre duas espécies de zooplâncton (Daphnia laevis e Moina
micrura) foi avaliado através das variáveis relacionadas ao crescimento somático
(biomassa) e da população. Todos os animais foram derivados de uma única fêmea, a fim
evitar a variação genética entre tratamentos. As microalgas utilizadas na dieta do
zooplâncton foram as clorofíceas Ankistrodesmus gracilis e Scenedesmus quadricauda. As
culturas foram mantidas sob um fotoperíodo de 11 horas de luz, a iluminação variou de 800
a 1400 Lux e a temperatura foi de 21 ± 3°C. Ankistrodesmus cresceu mais do que
Scenedesmus com o mesmo meio CHU12 e as duas curvas de crescimento foram
significativamente diferentes (F=1,47, gl=38, p <0.001). Ankistrodesmus apresentou maior
capacidade suporte (K) com Daphnia do que Moina. O crescimento exponencial da
população de Daphnia foi maior do que de Moina, que cresceu lentamente. Os neonatos de
Daphnia laevis tiveram comprimento médio de 0,62 milímetros e os adultos alcançaram
1,50 e 1,06 milímetros tendo como fonte de alimento Ankistrodesmus e Scenedesmus,
respectivamente. Os neonatos e os adultos de Moina micrura alcançaram 0,52 milímetros e
0,97 milímetros, respectivamente, para as duas microalgas estudadas. Foi observado com o
presente trabalho que a cultura de Ankistrodesmus com Moina pode ser indicada para
crescimento de alevinos em tanques de peixes, porque ambas crescem mais rápido e o
momento para produção do ovo de Moina poderia ser curto.
3
Palavras-chave: microalgas; cladóceros; crescimento; experimentos; aqüicultura
Introduction
The strong demand for phytoplankton and zooplankton in larviculture systems of
intensive production of aquatic animals is recognized. Microalgae have important paper in
the feeding of larvae of crustaceans, bivalves in the different periods of training,
zooplankton and fish (Shamsudin, 1997; Wikfors & Ohno, 2001; López Elías, 2003;
Martínez-Fernándes, 2004). The zooplankton diet of high nutritional, essential value is
considered for fingerlings and juveniles of many fish that prefer to ingest organism livings
(Watanabe et. al., 1983; Morris & Mischke, 1999). The quality of zooplankton used as food
for larvae of fish, also it is related to the taxonomic group, the conditions of culture and the
phase of life of the animal. In this way, the use of a good food in the initial periods of
training of development of the fingerlings can guarantee success in the production of fish
(Tacon, 1993; Sánchez-Salvedra & Voltolina, 1996).
One of the critical points in any station of fish culture is the maintenance of supplies of
zooplankton of good quality and enough amounts, available in the certain time so that it
makes possible to feed the fingerlings adequately. Although exist simple culture media, as
the Chu12, used predominantly for diatomaceas and green algae (Vijverberg, 1989), one of
the main problems of the microalgae culture on a large scale for feeding of fingerlings and
juveniles of fish is the cost of the used chemical reagents for preparation of the culture
media. However, culture in laboratory is desirable under point of view of feed quality, since
if it can choose the organism that desires to cultivate and, with this, significantly to improve
the quality of the food offer the fingerlings. Animals of the cladocerans and rotifers groups
4
can be used for massive production in fish culture stations. The fingerlings of fish consume
animals of small weight, as rotifers, and the juveniles, bigger animals of zooplankton,
mainly cladocerans and copepods (Threlkeld & Choinski, 1987; Morris & Mischke, 1999).
Cladocerans is preferred, in view of some alometrics characteristics, as well as its
nutritional quality (De Bernardi & Giussani, 1975). Moreover, due to parthenogenetic
reproduction, the culture of cladocerans, under excellent conditions of temperature, food
and water quality, can generate a great number of individuals in a short period of time.
The nutritional composition of zooplankton varies in accordance with factors such as:
conditions of culture and food quality. The food quality depends on the culture conditions
and is a function of the content biochemist of the canine tooth and the ability of the predator
to assimilate the nutrients of the canine tooth. Different zooplankton species, despite from
related groups, can differ considerably in its nutritionals requeriments or its abilities to
assimilate the nutrients proceeding from the microalgae (Stutzman, 1995). Limitations for
choice of the diet exist, related mainly with quality, availability and acceptability of the
food together to the nutritionals markers of the animal such as digestibility and ratio
storaged energy/nutrient consumed (Watanabe & Kiron, 1994).
Diverse microalgae can be used as food for zooplankton species (Giani, 1991; Arnold,
1971; Porter, 1977; Repka, 1997). The unicells or cenobios Chlorophyceae are selected for
culture on a large scale for presenting finer cellular wall and high amount of total organic
carbon in relation to the dry weight (Sipaúba-Tavares & Rocha, 1994). The
Chlamydomonas globosa e Scenedesmus obliquus Chlorophyceae have been used as food
and they are considered good food resource for zooplankton (Boersma & Vijverberg, 1996).
Crisoficea and diatomacea are ideal for culture, in comparison with cyanobacteria and some
5
chlorophycea, that are considered of low and intermediate nutritional quality, respectively
(Ahlgren et al., 1990).
The quality of the microalgae as food also depends on its nutritional state, as well as of
the size, digestibility of the cell wall, toxicity and chemical composition (Ahlgren et al.,
1990; Rothhaupt, 1990; Giani, 1991; Sterner at al. 1993). Variations in the productivity of
Daphnia, with different microalgae species, are registered in literature for Giani (1991) and
Lundstedt and Brett (1991).
In relation morphologic characteristics, colonial forms are less favorable as food
(Infante & Litt, 1985). Size assimilable and absence of morphologic defenses, as thorns,
hard surface or gelatinous sheath, can indicate foods of high quality for zooplankton
herbivore (Sterner et al., 1993).
The good performance of the microalgae Ankistrodesmus as food for zooplankton can
be verified by means of experimental studies, focusing filtration rates (Macedo & PintoCoelho, 2000), aspectos bioquímicos (Macedo & Pinto-Coelho, 2001) and demographics
(Sipaúba-Tavares, 2001). However, Scenedesmus quadricauda possess composition better
biochemist, in terms of lipid, carbohidratos and proteins, of that Ankistrodesmus gracilis
when cultivated in the media Chu12 (Oliveira, 1999).
Considering the importance of the microalgae as food for zooplankton, this study
objectived to test the effect of the Ankistrodesmus gracilis and Scenedesmus quadricauda
diets in the growth of two cladocerans, Daphnia laevis and Moina micrura. For being a
chlorophycea with not adjusted morphologic characteristic, due to presence of thorns,
expects that the Scenedesmus microalgae is optimum food for cladocerans D. laevis and M.
micrura.
6
Materials and methods
Culture and growth curves microalgae
The Ankistrodesmus gracilis and Scenedesmus quadricauda inoculation had been
gotten in the Phycology Laboratory of the Departmento de Botânica da Universidade
Federal de Minas Gerais, Belo Horizonte, MG. Strains had been kept in cultures of the type
batch under photoperiod of 12 hours of light, luminous intensity of 1000 to 1800 Lux and
temperature of ± 20°C. For the accompanying of the growth curve population was used
three replicas of culture of each microalgae. The culture media CHU12 (CHU, 1942) was
kept in pH alkaline of 8,0.
The growth curves of the microalgae were determined for maintenance of the
concentration of 104 céls.mL-1 or average carbon concentration 1,40µgC.mL-1, considering
the conversion factor 37,50pgC.cel-1 for Scenedesmus (Rocha & Duncan, 1984). Daily
samples of each replica had been collected always in the same hour and fixed with solution
of Lugol. For the quantification of the microalgae populations was used a chamber of
Fuchs-Rosenthal, being enumerated a minimum of 400 cells/sample (approximately 10% of
precision with 95% confiability limit). For each treatment the growth intrinsic rate (μ) was
estimed through linear regression (Statistica, versão 4.3) from the values of density in the
exponential phase of the culture (y), in function of the time (x), being μ equal to the
coefficient of the equation found, y = ax + b
Where,
x is the period in days
y is the ln of cell concentration
7
Experiments of individual and population growth
Daphnia laevis and Moina micrura were isolated of the reservoir of the Pampulha
(Belo Horizonte, MG) and clones kept in laboratory. The cultures were kept with
reconstituted water (CETESB, 1994) and the food was gave daily for one concentration of
4,5 x 104 cell.mL-1.
The experiments of individual growth had duration of six days. Three replicas per day
for each treatment were used, to a total of 72 bottles of 100 mL with neonates come out
with less 24-hour and water renewal to each two days. The duration of the experiment of
individual growth made possible the determination of the reproductive investment of M.
micrura through the egg number for female primipare. For determination of the total length,
the animals had been measured of the previous extremity to posterior (without including the
thorns or the any prolongations of carapace or the posterior part) and biomass were gotten
by the relation weight-length (Downing, 1984, Geller & Muller, 1985 e Pinto-Coelho,
1991).
For the experiment of population growth, 20 egg females of each species were isolated
in four bequeres of two liters, and were placed 10 females of one of the cladocerans. In each
one of the experimental units was added as food one of the microalgae, Ankistrodesmus or
Scenedesmus. The curve of growth of the animals was adjusted to the model of the logistic
equation (Krebs, 1978) for initial value of K as the average of the three last points of each
curve of the species. The curves of population growth D. laevis and M. micrura species had
been adjusted to the logistic model and the values of the parameters (rmáx= growth
8
instantanea rate and K= carrying capacity) calculated for the equations adjusted for the
species in the different treatments.
Covariance analysis to the level of 5% of probability was made, Statistic Program for
MS-Windows (Copyright, 1993), version 4.3.
Results
Curves of individual growth of the microalgae
Through the daily quantifications of the population, were estimated concentrations of
cells, curves of growth and intrinsic rate of growth (). The microalgae cultures were
initiated with average of 2.8 x 103 cell.mL-1 and 9.1 x 103 cell.mL-1 to S. quadricauda and
A. gracilis, respectively. The curve of population growth of Ankistrodesmus characterized
for the increase of cells until day 15 when the cell concentration was stabilized in more or
less 8.0 x 105 cell.mL-1 (FIG. 1A).
A similar standard for Scenedesmus was observed, with stabilization of the next frame
number to day 15, when the population reached 6.22 x 104 cell.mL-1 (FIG. 1B). In virtue of
the concentration of Ankistrodesmus to have stabilized in higher values of what
Scenedesmus (µ=0.44), as final density of cells as exponential growth rate had been
increased for Ankistrodesmus (µ=0.51). The covariance analysis demonstratedeen
significantly different (MS=632.59; F=3.03; p>0.001).
The average value of the length and width of the cells of A. gracilis were 19.64 µm and
1.01 µm. The measures of S. quadricauda were 19.46µm, 7.75µm and 15.13µm for length,
width and thorn of the cell, respectively.
9
Experiments of individual and population growth of the cladocerans
The growth of Daphnia was better with Ankistrodesmus. Moina grew equally with the
two foods, but the reproductive investment was faster with Ankistrodesmus. In the
experiment of individual growth the animals of Daphnia laevis species had grown better
with Ankistrodesmus and reached 25 µgDW biomass. However the adults of the Moina
micrura species had reached similar lengths and biomass with any one of foods
(6.8µgDW) (TAB. I and FIG. 2 and 3). However, about to reproductive investment of
Moina, the foods had not been equally efficient, eggs inside of the incubator chamber of the
females primipara had been found from the third day with the Ankistrodesmus microalgae,
but only about day 5 to Scenedesmus (TAB. II). In this way, Ankistrodesmus was better
food to Daphnia, and Moina grew equally with any one of foods.
About the experiment of population growth, Ankistrodesmus was the food most
efficient for the two studied cladocerans. The population growth of Daphnia, as well as of
Moina, was bigger with Ankistrodesmus of what with Scenedesmus. For the population
growth of Moina significant difference between two foods was found (TAB. III). The
standard of growth of the population of Moina micrura, with regard to some of the diets,
was adjusted well to the logistic model (r2=0,95 e 0,96) (FIG. 4 e 5).
In accordance with the parameters of the logistic model (K e rmáx), Ankistrodesmus
presented greater carrying capacity as to Daphnia as Moina, K = 49,36 e K = 289,73,
respectively. Moina grew more efficientle (rmáx = 0,55 e 0,50) than Daphnia (rmáx = 1,47 e
2,44) with any one of foods. The point of the curve where the growth stop of being
exponential and the density of the organisms reach carrying capacity (K) is day 4º e 10º to
Daphnia and Moina populations, respectively (FIG. 4 e 5).
10
Discussion
The experiments of individual and population growth demonstrated the efficiency of
the microalgae as food on the growth of the cladocerans. The cladocerans Daphnia and
Moina had grown well having as food the Ankistrodesmus microalgae, mainly in relation to
the population growth. The experiments had shown that species M. micrura invested in the
egg production having, consequently, reproductive advantage, while D. laevis invested first
in the somatic growth and accumulated greater biomass. The energy investment of
cladocerans in the reproductive period can occur in such way for somatic growth as for
reproduction, but in lower food levels D. obtusa places more energy in the egg production
than in the somatic growth (Manca & De Bernardi, 1987). However, in terms of individual
growth and fecundidade, the energy investiment of D. laevis can be similar between
reproduction and somatic growth (Fonseca, 1991).
As the quality of the food is relation with factors diverse and condiction in culture of
laboratory, S. acutus microalgae was considered a good food to Daphnia pulicaria and
Brachionus rubens (Rothhaupt & Lampert, 1992) and, moreover, others species of
Scenedesmus were inadequate for zooplankton (Taub & Dollar, 1968; Hart & Santer, 1994).
Generally, Scenedesmus can be considered a good food, but the population growth rate and
others parameters of life history to cladocerans, as Daphnia, vary in accordance with
different clones studied (Repka, 1997). S. quadricauda specie, used in the present work,
possess thorns, fact that contributes for reduction of palatability and a reply less favorable
in the individual and populational growth cladocerans.
The chemical composition of cultures microalgae can be modified by manipulation
such of environmental variable as composition in the culture medium (Fabregas et al.,
11
1986; Renaud et. al. 1995; Sánchez-Saavedra & Voltolina, 1996). Modifications in the
conditions of algae culture determined variations in the photosynthesis reply, growth rate
and cell metabolism and, consequentely these metabolisms variations determined protein,
carbohidrate and lipid concentrations (Sukenik et al., 1989).
The same chlorophyceae of the present study had grown better in the Chu12 medium of
that in others commercial medium, with concentrations highest of protein, lipid and
carbohidrate (% of dry weight without ashes) to S. quadricauda than in A. gracilis
(Oliveira, 1999). This fact indicates that in the present study chemical composition was not
determine food efficiency, since the results of the experiments indicate Ankistrodesmus as
better food.
The good performance of Ankistrodesmus microalgae as food to zooplankton also was
observed in diverse experiments, where were verified highest filtration rates (Macedo &
Pinto-Coelho, 2000), highest lipid concentration in cladocerans (Macedo & Pinto-Coelho,
2001) and highest growth in cladocerans (Sipaúba-Tavares, 2001).
Concentration decreases of food affect the growth of cladocerans population (Daphnia
magna, Daphnia galeata and Bosmina longirostris) (Goulden et al., 1982), being the
critical level of food was estimad in 0.1mgC.L-1, concentration in that reproduction was
stoped in several cladocerans (Lampert & Schober, 1980). In present study, the
concentrations of food were kept between the level considered intermediary (1 x 104) to
high (2,5-5,0 x 104), use in several experiments (Goulden et al., 1982; Porter et al, 1982;
Holm & Shapiro, 1984; Repka, 1997).
The cladocerans studied can grow in fish ponds, in a generalized manner resist well to
the management involved in the culture and can be selected as food to fish larvae in relation
12
to some characteristics allometric and nutritional composition (De Bernardi & Giussani,
1975, Sipaúba-Tavares & Rocha, 1994). The logistic growth model character for a
association between the density of a population and its growth rate (Krebs, 1978), and in the
present study, value of parameter rmáx indicated for the growth rate that Ankistrodesmus was
better food to Daphnia than Moina.
In view of that demographic indicators had pointed A. gracilis as more efficient food
for cladocerans studied, that had been influenced by morphological characteristics of food
available, can be conclusion that the hypothesis searched was confirmed. Thus can be
recommend the cladoceran Daphnia to aquisition of higher biomass in less time in studies
of nutrition and production in large escale in laboratory and Ankistrodesmus as food.
Knowledments
We wish to thank Dr. Alessandra Giani for inocules of microalgae and Capes to
scholarship. This research was funded in part by FAPEMIG.
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19
Table I
Start and final length (mm) to neonates and adults of D. laevis and M. micrura with the A.
gracilis and S. quadricauda microalgae.
Daphnia
Moina
Ankistrodesmus
Scenedesmus
Neonate
0,62  0,17 (n=3)
0,62  0,12 (n=3)
Adult
1,50  0,08 (n=3)
1,06  0,04 (n=3)
Neonate
0,55  0,10 (n=3)
0,49  0,09 (n=3)
Adult
0,98  0,12 (n=3)
0,97  0,10 (n=3)
20
Table II
Average values of eggs gotten to Moina micrura with the microalgae from the third day of
experiment ( standard deviation; n=3).
Time (days)
Ankistrodesmus
Scenedesmus
3
7,3  0,6
0
4
7,3  0,6
0
5
7,0  2,6
8,0  1,0
6
7,7  1,5
7,0  1,0
21
Table III
Covariance analysis of Daphnia laevis and Moina micrura with Ankistrodesmus and
Scenedesmus food (gl=1).
MS
Daphnia
Moina
F
632,59
3,03
50189,10
85,91
P
0,13
0,000003
22
Figure 1. Growth curves of microalgae A: Ankistrodemus gracilis B: Scenedesmus
quadricauda
Figure 2. Populational growth curves in accordance with logistic model: D. laevis with the
microalgae. A: A. gracilis; B: S. quadricauda.
Figure 3. Populational growth curves in accordance with logistic model: M. micrura with
the microalgae. A: A. gracilis; B: S. quadricauda
Figure 4. Biomass growth of Daphnia laevis with the microalgae. A: A. gracilis; B: S.
quadricauda.
Figure 5. Biomass growth of Moina micrura with the microalgae. A: A. gracilis; B: S.
quadricauda.
23
15
n=19
A
14
13
ln cells.mL
-1
12
11
10
9
8
u = 0.51
7
0
2
4
6
8
10
12
14
16
18
20
Time (days)
15
n=20
B
14
Ln cells.mL
-1
13
12
11
10
9
8
u = 0.44
7
0
2
4
6
8
10
12
Time (days)
Fig.1.
14
16
18
20
24
30
A
Biomass (µg.DW)
25
20
15
10
5
Mean
0
0
1
2
3
4
5
6
7
Time (days)
30
B
Biomass (ug.DW)
25
20
15
10
5
Mean
0
1
2
3
4
Time (days)
Fig. 2
5
6
7
25
30
A
25
Biomass (ug)
20
15
10
5
Mean
0
1
2
3
4
5
6
7
Time (days)
30
B
Biomass (ug.DW)
25
20
15
10
5
Mean
0
0
1
2
3
4
Time (days)
Fig.3
5
6
7
26
100
Number of individuals
A
80
60
40
20
2
a=1,57 , k=49,36 , r=1,47 , r =0,71
0
0
2
4
6
8
10
Time (days)
Number of individuals
100
B
80
60
40
20
a=2,58 , k=40,10 , r=2,44 , r2=0,79
0
0
2
4
6
Time (days)
Fig. 4.
8
10
27
350
A
Number of individuals
300
250
200
150
100
50
0
a=2,47, K=289,73 , r=0,55 , r2=0,96
0
350
2
4
6
8
Time (days)
10
12
14
B
Number of individuals
300
250
200
150
100
50
0
a=3,30 , K=230,84 , r=0,50 , r2=0,95
0
2
4
6
8
Time (days)
Fig. 5.
10
12
14