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Biological Responses of Tropical Cladoceran,

Ceriodaphnia Cornuta to Different Algae Diets

Hasnun Nita Ismail Faculty of Applied Sciences/Universiti Teknologi MARA (Perak) Kampus Tapah, 34500 Tapah Road, Perak, Malaysia

Email: [email protected]

Umi Wahidah Ahmad Dini and Chia Chay Tay Faculty of Applied Sciences/Universiti Teknologi MARA (Perlis), 02600 Arau, Perlis, Malaysia

Email: [email protected]; [email protected]

Abstract—The biological responses of tropical cladoceran,

Ceriodaphnia cornuta fed on different algae diets were

investigated under laboratory conditions. Two types of

microalgae, Chlorella (C) and Scenedesmus (S) were given

as mono-algal diet and multi-algal diet (CxS). The different

types of algae diets have significantly altered the biological

responses of C. cornuta. Diet contained Chlorella alone

promoted high longevity, fast egg development, early

maturation, increased egg clutch number and increased egg

and offspring production. As a result, animals showed

higher survival, faster development and greater

reproductive output. On the other hand, diet with

Scenedesmus alone supports for higher growth rate more

than Chlorella. Despite of the opposite algal effect, diet

combination of both algal (Chlorella x Scenedesmus)

enhanced all biological responses. Therefore, this study

suggests that the diet combination of both algae is the

optimum diet to boost up the survival, development and

reproduction of C. cornuta. This outcome has provides the

guideline to choose the suitable algal species which can

maximize the biological performance of C. cornuta.

Index Terms—tropical cladoceran, algae diets, growth rate,

development, reproduction, survival

I. INTRODUCTION

Cladoceran forms the most dominating group of

micro-crustacean in tropical freshwaters especially in

lakes, ponds and rivers. Although microscopic in size,

cladoceran plays a dual role in food web as a primary

consumer and a prey for higher consumers [1]. They

influence energy and organic matter transfer from

primary producers to the highest consumers [2]. As a

primary consumer, most cladoceran are herbivorous.

They have the ability to control the production of

producer species in aquatic systems especially the

microalgae [3]. In fact, microalgae have been the primary

diet chosen by the aquatic systems especially the

microalgae [3]. In fact, microalgae have been the primary

diet chosen by the herbivorous cladocerans beside of

alternative diets like bacteria, debris, unicellular fungi

and humus.

Manuscript received August 19, 2014; revised December 1, 2014.

Tropical region such as Malaysia is well known to

support growth of many species due to it warm

environments [4]. Indeed, tropical cladoceran should be

more diverse with many selections of food diet here.

However, reported studies on tropical cladoceran in

South East Asia especially from Malaysia are limited [5].

Many studies are restricted to taxonomy, distribution and

zoogeographic analysis [6], [7]. Thus far, none of the

studies reveal the important parts related to biological

and ecological requirements in the life history of

Malaysian cladoceran.

The genus Ceriodaphnia is classified under the family

of Daphniidae [8]. In their life cycle, Ceriodaphnia

displays cyclic parthenogenesis which is typical in nearly

all groups of cladoceran. Cyclic parthenogenesis consists

of alternation between asexual and sexual reproduction

[9]. Asexual reproduction is the major mode of

reproduction conducted under favourable conditions by

means of parthenogenesis. Meanwhile, sexual

reproduction begins as the environments start to

deteriorate and challenge the population’s survival. The

outcome from sexual reproduction is the resting eggs

which are resistant under harsh environment and hatch

once the environments back to favourable conditions.

In many diet studies, the biological responses of

cladoceran vary when fed to algae of different taxa. The

cladoceran, C. silvestrii lived longer when fed on

Chlorella lacustris but showed the shortest longevity

when fed on Scenedesmus bijugus [10]. The growth of

euryhaline cladoceran, Daphniopsis australis grew faster

when fed on Nannochloropsis oculata than fed to

Tetraselmis suecica [11]. Other euryhaline cladoceran,

Moina mongolica matured earlier with N. oculata but

maturation was delayed by Dunaliella salina [12]. The

reproductive performance of freshwater cladoceran,

Simocephalus vetulus was significantly higher when fed

to Scenedesmus acutus then fed to other algae such as

Microcyctis and Planktothrix [13]. In general, the life

responses of cladoceran are species-specific and likely

dependent on the types of algae.

This study covers the Malaysian cladoceran species, C.

cornuta isolated from wild freshwater environments. C.

cornuta is a small tropical cladoceran with a body size

less than 0.50 mm [8]. The first objective is to examine

482014 Engineering and Technology Publishing

Journal of Life Sciences and Technologies Vol. 2, No. 2, December 2014

doi: 10.12720/jolst.2.2.48-54

the biological responses of C. cornuta fed to different

types of microalgae; Chlorella and Scenedesmus. The

second objective is to determine the optimal food for C.

cornuta cultured under laboratory conditions. The finding

will show the impact of algal diet to the survival,

development and reproduction and provide a guideline in

feeding selection of this cladoceran under man-made

conditions. Overall, it might shed light in introducing this

species as an alternative live food in fish aquaculture.

II. MATERIALS AND METHODS

A. Culture of Algae

The freshwater green algae used in this study include

Chlorella and Scenedesmus. Both algal species were

cultured in BBM medium in 2 L glass bottle provided

with aeration. The air was filtered using Nylon air filter,

0.45 µm pore size. Light was continuously provided at

1900 lux with 12 h light: 12 h dark photoperiod.

Temperature was controlled at 25°C. Algae were

harvested for every two days at exponential growth phase

to feed the stock culture of C. cornuta.

B. Stock Culture of C. Cornuta

C. cornuta was obtained from Biological Research

Laboratory, Universiti Teknologi MARA (Perlis),

Malaysia. Originally, the species was collected from

freshwater Tasik Elham around the campus in July, 2013.

Since then, the animals have been cultured for more than

100 generations under laboratory condition. C. cornuta

have been maintained in aged tap water in 5L beaker.

The stock culture condition was maintained at 25 oC

under 12 h light:12 h dark regime at 1900 lux. The

population was fed on Chlorella and Scenedesmus

separately at the density of 106

algal cells/mL. The

population density of C. cornuta was maintained below

1000 individual/L to reduce overcrowding.

C. Experimental Design

The response of C. cornuta to different diet was tested

with two mono-algal diets which were Chlorella (C),

Scenedesmus (S) and one multi-algal diet which was the

mixture of both Chlorella and Scenedesmus (CS). Algal

cells were harvested at exponential growth phase for

feeding regimes. Enumeration of algal density was

carried by using Improved Neubaeur haemocytometer

under the light microscope (Olympus) at 400

magnifications. Since the size of two algae was highly

variable, the biovolume measurement was used to

standardize the concentration of food [14].

Experiment on the life cycle of C. cornuta was started

by isolating a single parthenogenetic female from the

stock culture and acclimatized in a culture bottle

containing 5 mL medium from each corresponding food

diet Chlorella, Scenedesmus and a mixture of them

respectively. The parthenogenetic females were left until

the appearance of the third generation. During

acclimatization, the medium was renewed daily to avoid

confounding effects from dead microalgae. The

acclimatization procedure is important and is a standard

procedure to offset the maternal effect [15]. Only the

animals after the third generation and above were used

for observation on the life cycle responses.

In the life cycle experiment, the animals younger than

24h were individually inoculated into a bottle containing

5mL of medium for each food treatment. Temperature

and photoperiod was maintained similar to the culture

stock condition. 25 replicates were conducted for each

food treatment and the culture media were renewed on

daily basis. The life cycle parameters recorded for each

individual include longevity (day), growth rate (mm/day),

age at first reproduction (day), egg development time

(day), total clutch (female/life time), total egg per clutch

(female/life time) and total offspring (female/life time).

Daily observation was conducted until the death of the

last individual. The Olympus SZ51 zoom

stereomicroscope (up to 80x total magnification) was

used for observation on the individual response to each

different diet.

D. Statistical Analysis

All data were analyzed using statistical software, SPSS

version 20.0. In prior, data were explored for

homogeneity variance and assessing normality

assumptions. Only data for longevity were inversely

transformed to achieve the normality assumption. One-

way analysis of variance (ANOVA) will be used to test

the treatment effects on each life cycle variable to find

the significant difference among treatments. The

difference between groups will be compared using

Tukey’s test. All significant level will be set at P<0.05.

III. RESULTS

A. Longevity

The individuals longevity significantly differed

between the diet treatments (ANOVA, P<0.05; Table I).

Further analysis revealed that individuals fed on the

combination of Chlorella and Scenedesmus showed the

longest longevity rather than those fed on other diet

treatments (Tukey's HSD, P<0.05; Fig. 1a). The

longevity was significantly shortened as individuals fed

on the Scenedesmus alone (P<0.05). However, no

significant difference in longevity was found when

individuals fed on Chlorella alone and fed on

combination of Chlorella and Scenedesmus (P<0.05).

B. Age at First Reproduction (AFR)

The age at first reproduction (AFR) was significantly

affected by the diet treatments (ANOVA; P<0.05; Table

I). Specifically, Scenedesmus alone significantly

prolonged the AFR of individuals (Tukey's HSD, P<0.05;

Fig. 1b). In comparison, individuals significantly

shortened the AFR when fed on combination of

Chlorella and Scenedesmus (P<0.05). However, AFR

was not significantly different between individuals fed on

Chlorella alone and fed on the combination of Chlorella

and Scenedesmus (P<0.05). Regarding the diet treatments,

the time to reach maturity is significantly faster for those

individuals fed on the combination of Chlorella and

Scenedesmus than those fed on the Scenedesmus.



C. Egg Developmental Time (EDT)

The egg developmental time (EDT) was significantly

dependent on the diet treatments (ANOVA, P<0.05;

Table I). Chlorella alone significantly reduced the EDT

of individual (Tukey's HSD, P<0.05; Fig. 1c). In contrast,

Scenedesmus alone significantly lengthened individuals

EDT (P<0.05). ). However, EDT was not significantly

different between individuals fed on Chlorella alone and

fed on the combination of Chlorella and Scenedesmus

(P<0.05). Regarding the diet treatments, the eggs hatched

faster when individuals were fed on single diet of

Chlorella than those fed on Scenedesmus (P<0.05).

Figure 1. Responses of life history parameters to different diet treatments: (a) Longevity b) Age at first reproduction (AFR), (c) Egg development time (EDT), (d) Total clutch, (e) Total egg and (f) Total offspring, (g) Growth rate



D. Total Clutch

Diet treatments significantly affected the total number

of egg clutch of individuals (ANOVA, P<0.05; Table I).

The highest number of egg clutch occurred in females fed

on combination of Chlorella and Scenedesmus (Tukey's

HSD, P<0.05; Fig. 1d). Meanwhile, Scenedesmus alone

significantly lowered the total egg clutch of individuals

(P<0.05). However, no significant differences were

observed on the number of egg clutch between females

fed on Chlorella alone and fed on mix diet of Chlorella

and Scenedesmus (P<0.05). Analysis revealed that food

affected significantly on the reproductive frequency of C.

cornuta.

TABLE I. RESULTS OF ANOVA FOR LIFE CYCLE PARAMETERS OF C. CORNUTA FED ON DIFFERENT DIET TREATMENTS

One-way ANOVA df SS MS F P

AFR (day)

Diet treatment

Error

2

57

8.63

13.95

4.32

0.24

17.64

0.000*

EDT (day)

Diet treatment

Error

2 57

4.90 12.75

2.45 0.22

10.95

0.000*

Total egg clutch

(no.female-1 lifetime-1)

Diet treatment

Error

2

57

12.03

42.55

6.02

0.75

8.06

0.001*

Total egg

(no. female-1 lifetime-1 )

Diet treatment

Error

2

57

45.30

268.30

22.65

4.71

4.81

0.012*

Total offspring

(no. female-1 lifetime-1)

Diet treatment

Error

2

57

58.23

188.75

29.12

3.31

8.79

0.000*

Longevity (day)

Diet treatment

Error

2

57

0.00

0.16

0.00

0.00

7.90

0.001*

Growth rate

(mm day-1)

Diet treatment

Error

2 57

0.01 0.01

0.00 0.00

19.75

0.000*

df — degree of freedom, SS — sum of squares, MS — mean square

*significant different at P < 0.05

E. Total Egg

Diet treatments had a significant effect on the number

of egg production (ANOVA; P< 0.05; Table I). The

highest numbers of total number of egg were obtained by

the individuals fed on mix diet, Chlorella and

Scenedesmus whereas the lowest values were recorded in

those fed on Scenedesmus. alone (Tukey's HSD, P<0.05;

Fig. 1e). Total number of egg produced was influenced

significantly among each diet treatment (P<0.05).

Individuals fed Scenedesmus produced a total number of

egg that was significantly lower than that obtained with

single diet, Chlorella and combination of Chlorella and

Scenedesmus(P<0.05).

F. Total Offspring

There was a significantly effect of diet treatments on

the number of offspring production (ANOVA; P<0.05;

Table I). Total number of offspring production

significantly reduced when individuals fed on

Scenedesmus alone while the highest production of

offspring obtained by individuals fed on combination of

Chlorella and Scenedesmus (Tukey's HSD, P<0.05; Fig.

1f). However, total number of offspring production was

not significantly different between individuals fed on

Chlorella alone and combination of Chlorella and

Scenedesmus (P<0.05).

G. Growth Rate

Dietary types significantly affect the growth rate of C.

cornuta (ANOVA, P<0.05; Table 2). Growth rate

differed at each dietary treatment. Individuals fed on

Scenedesmus alone showed the highest growth rate while

the lowest growth rate was found in individuals fed on

Chlorella alone (Tukey's HSD, P<0.05; Fig. 1g).The

growth rate showed by single diet treatment is

significantly differ from those fed on multi-algal species

Chlorella and Scenedesmus (P<0.05).

IV. DISCUSSION

A. Longevity

In this study, the longevity of C. cornuta was

lengthened when fed on the multi-diet (Chlorella x

Scenedesmus) and the mono-algae, Chlorella. The

shortest longevity displayed when C. cornuta was fed on

Scenedesmus alone. The same finding was reported on

the other species of Ceriodaphnia, C. dubia where the

longevity was enhanced in similar combination algal diet

(Chlorella x Scenedesmus) and the longevity was

hampered with Scenedesmus alone [16]. Other study on

C. silvestrii reported that the highest longevity was

obtained with Chlorella alone rather than Scenedesmus

alone [10]. However, the longevity of C. rigaudi was the

shortest when fed on Chlorella alone [17]. Likely, the

longevity of Ceriodaphnia species is affected by the

types of diet and the addition of Chlorella in diet mostly

provides positive effect to their survival.

B. Development Performance

The development performance by C. cornuta was

evaluated by referring to their age at first reproduction

(AFR) and egg developmental time (EDT). The present

result showed that the fastest maturity observed in C.

cornuta fed on multi-diet (Chlorella x Scenedesmus) as

well as in Chlorella alone. The trend of eggs

development is also similar with AFR using the same

diets. However, C. cornuta matured later and their eggs

developed longer with Scenedesmus alone.

Correspondingly, study on other cladoceran, Daphnia

magna showed faster maturation when fed on Chlorella

than Scenedesmus alone [18]. Likewise, C. cornuta and

M. macrocopa matured at early age and showed fastest

EDT when fed on Chlorella alone [19]. Other study also

showed slowest AFR and longest EDT of C. dubia when

fed on Scenedesmus alone [20]. Therefore, the

development of most cladoceran species are supported by

Chlorella compared to Scenedesmus.

C. Reproductive Performance

In this study, C. cornuta obtained the maximum

reproductive output when fed on multi-diet (Chlorella x



Scenedesmus) and Chlorella alone. This showed by the

highest total number of egg clutch, egg number and total

offspring. However, less number of egg clutch, egg

number and total offspring produced in C. cornuta fed on

Scenedesmus alone. This finding is parallel when the

same diet was applied to C. dubia [16] and Daphnia

magna [18].Similarly, the other study showed that the

highest reproduction output displayed by M. macrocopa

[21] and M. micrura [22] fed on Chlorella alone rather

than Scenedesmus alone. Again, diet contained with

Chlorella supports reproduction of many tropical

cladoceran more than Scenedesmus.

D. Growth Rate Performance

In contrast to other life cycle parameters, the growth

rate of our species, C. cornuta was highly promoted

when fed on Scenedesmus alone. However, the mono-diet,

Chlorella resulted with the shortest growth rate andthe

intermediate growth rate was observed when C. cornuta

fed on multi-diet (Chlorella x Scenedesmus). The growth

rate of C. dubia also the fastest when fed on diet with

Scenedesmus alone while diet with Chlorella alone

produced the lowest growth rate [16], [21]. Likewise, the

growth rate of D. gessneri was the fastest using diet with

Scenedesmus alone [22]. Most of the Daphnia spp.

displayed the shortest growth rate with diet contained

Chlorella alone [23]. Hence, the growth rate of

cladoceran can be maximized with Scenedemus rather

than Chlorella.

In overall, our finding on C. cornuta found that

Chlorella seems to be the best diet for survival,

development and reproduction. However, Scenedesmus is

the best diet to promote for species growth. In many diet

studies, the life performance of cladoceran can be

improved when the diet contained combination of poor

algae and the good algae. For instance, the survival of

Daphnia pulicaria was shortest when supplied with

Cyclotella meneghiniana but the combination with

Scenedesmus resulted in better survival and development

of this cladoceran [24]. Moreover, Cryptomonas are

considered as the high-quality food for Daphnia pulex

due to high production of offspring but the production of

offspring was impeded when fed on Scenedesmus [25].

Interestingly, the combination of Cryptomonas and

Scenedesmus boosted the reproduction of the D. pulex.

Study on different cladoceran, Daphniopsis australis also

found that Tetraselmis suecica was the best diet to

improve growth while Nannochloropsis oculata was the

worst diet for growth. However, combination of these

algae increased the growth rate significantly [11].

Therefore, while Scenedesmus is suitable for growth and

Chlorella support more on development, survival and

reproduction, the combination of both algae managed to

improve all life parameters involved in the life history of

C. cornuta.

The positive results showed by Chlorella on the

development and reproductive performance of C. cornuta

may due to the highest lipid contents in comparison to

Scenedesmus [26]-[28]. The essential lipid content to

determine the cladocerans reproduction refers to the

group of PUFAs [29]. Many studies have shown that

Chlorella contained 43.37 to 47.12 % PUFAs while

Scenedesmus contained 29.56 to 30.17 % PUFAs [30]-

[32]. The higher amount of PUFAs in Chlorella than

Scenedesmus might be the reason that led to better

development and reproduction of C. cornuta in this study.

Specifically, the growth rate of cladoceran is related to

the amount of α-linolenic acid (α -LA) in algal diet where,

algae with high α-LA content contribute most to the body

growth [33], [34]. Previous studies have shown that

Scenedesmus contained 25.61 % of α-LA content while

Chlorella contained 2.28 to 4.21 % of α-LA content [35],

[36]. Therefore, the difference of α-LA composition in

both algal species could be considered as one of the

factor that affects the growth rate of this C. cornuta.

Overall, the variation in life cycle responses of C.

cornuta to different algal diets in this study may have

been caused by the differences in nutritional quality of

algal diet. The evidence for the effects of nutritional

quality comes from the experiment with multi-diet which

showed enhancement in all life cycle parameters. This is

because different algae can complement to each other

with respect to nutritional quality [37]. Hence, the

combination of different food quality of algal diets

contributed to the better life cycle performance of C.

cornuta.

V. CONCLUSION

Our results showed that different types of alga diet

significantly affect the life cycle of C. cornuta. Diet

contained Chlorella alone enhanced higher survival,

faster development and greater reproductive output in

comparison to Scenedesmus. On the other hand,

Scenedesmus supports for higher growth rate more than

Chlorella. Despite of opposite effects, combinations of

both algal enhanced all life cycle parameters. Therefore,

this study suggests that the combination of both algal

diets is the optimal food for C. cornuta. This study has

provides the guideline to choose the suitable algal species

which can maximize the performance of C. cornuta.

Further study should be conducted in detail to examine

the nutritional composition of algal species which needed

by the cladoceran to meet their life requirement. In

addition, further study has to be conducted to assess the

ingestion rate and food selectivity in this cladoceran. Conclusively, this study has reveals the performance

of thiscladoceran species as well as indicate the most

optimal condition for the better production. By knowing

all the requirements to achieve the maximal production,

this species can possibly be reared in man-made

condition as the alternative live food in aquaculture.

Therefore, the continuous supplying of live food for the

fish larvae can give beneficial impact to the aquaculture

industry which then can supports the demand for

aquaculture products from time to time.

ACKNOWLEDGEMENT

Authors would like to thank UniversitiTeknologi Mara

for supporting this project technically and financially.

This project was granted under the Academic Excellent



Fund with project number was 600-

UiTMPs/PJIM&A/ST/DCKP 5/3 (07/2012).

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Hasnun Nita Ismail was born in the quiet

area in Perak, Malaysia on 31 August 1970.

She graduated from Universiti Malaya Kuala

Lumpur for her BSc (Entomology Toxicity) and MSc (Limnology & Aquatic Toxicity) in

1994 and 2004 respectively. She pursued for

her PhD (Zooplankton Ecology) at Flinders University, South Australia and had graduated

in 2010.

Previously, she has been under training as the Research Officer at Institute of Medical Research. Presently, she

attached with Universiti Teknologi MARA (Perak) as a SENIOR

LECTURER and involved in teaching various levels of student from diploma, first degree until post graduates.

Dr Hasnun Nita Ismail has been acting as the Chief-Editor for the

university journal publication and had been appointed as invited reviewer for many national and international journal articles. She has

produced several national and international publications as a book

chapter, academic magazines including journal articles in impact factor journals such as Hydrobiologia, Journal of Plankton Research and

Journal of Experimental Marine Biology and Ecology. Her field of

interests cover the water quality studies and plankton ecology.

Umi Wahidah Ahmad Dini was born in

the

small town of Malaysia, Selangor on 19

January 1992. She just finiished her study at

Universiti Teknologi MARA (Perlis) for her BSc (Zooplankton Biology). She is now

looking forward to pursue for her MSc in the

same field of interest.

Chia Chay Tay was born in the smoothest

state of Malaysia, Johor on 11 November 1978. She graduated from Universiti

Kebangsaan Malaysia for her BSc (Hons) in

marine sciences and MSc. in environmental sciences in 2002 and 2005. respectively.

Subsequently, she obtained PhD in

environmental sciences, technology and engineering from Universiti Malaya in 2012.

Currently, she joined Universiti Teknologi

MARA as a SENIOR LECTURER. She has been working as a lecturer in INTEC for AUSMAT and ADFP program. Besides, she has working

experience in multi-national company in global product development

and customer service. She has published her research in ISI and SCOPUS indexed journals including Water Science Technology and

Korean Journal of Chemical Engineering. Her research interests include

biosorption, environmental management and pollution control. Dr. Tay is a professional member of International Water Association

(IWA). She has been awarded several research grants and medals in

research output exhibitions.



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