J. Appl. Ichthyol.
19 (2003), 239243
 2003 Blackwell Verlag, Berlin
ISSN 01758659
Response of bighead carp Aristichthys nobilis and Asian catsh Clarias
macrocephalus larvae to free-living nematode Panagrellus redivivus
as alternative feed
By C. B. Santiago1, A. C. Gonzal1, M. Ricci2 and S. Harpaz3
1
Southeast Asian Fisheries Development Center (SEAFDEC) Aquaculture Department, Binangonan Freshwater Station,
Binangonan, Rizal, Philippines; 2BioTecnologie B.T. s.r.l., Pantalla di Todi, PG, Italy; 3Ministry of Agriculture and Rural
Development, Agricultural Research Organisation, The Volcani Center Institute of Animal Science, Department of Aquaculture,
Israel
Summary
The use of Panagrellus redivivus as live feed for bighead carp and
Asian catsh larvae was tested. In experiment 1, carp larvae were
given Artemia nauplii (control) or Panagrellus twice daily for
21 days. A third treatment consisted of unfed larvae. The same
three treatments were used in experiment 2 plus another with a
commercial entomopathogenic nematode (EPN). Bighead carp
larvae given Panagrellus in experiment 1 had much lower growth
and survival than those fed Artemia nauplii. This could be due to
low nematode density (530 mL)1 water) during feeding. The
unfed larvae had 100% mortality by days 1113. In experiment 2,
growth and survival of carp larvae given Artemia nauplii
(510 mL)1) and Panagrellus (50 mL)1) did not dier signi-
cantly (P > 0.05). All unfed larvae had died by day 13, while
larvae fed EPN were all dead by day 8. Two experiments on Asian
catsh were likewise conducted. In experiment 1, the catsh
larvae were fed Tubifex (ad libitum), Panagrellus (50100 mL)1
per feeding) orArtemia (5 nauplii mL)1 per feeding) three times
daily for 14 days. In experiment 2, larvae were fed Artemia alone
(10 nauplii mL)1 per feeding), Panagrellus alone (100 mL)1 per
feeding), or their combination with a 38% protein dry diet twice
daily. For both experiments, catsh larvae fed Panagrellus had
signicantly lower growth and survival than those fed Tubifex or
Artemia. The combination of Panagrellus and dry diet created
little improvement in the growth and survival of catsh larvae.
Introduction
Most sh larvae rely mainly on live organisms such as rotifers
Brachionus spp. and brine shrimp (Artemia sp.) nauplii at the
start of exogenous feeding. Both organisms are highly accep-
table to the larvae of bighead carp Aristichthys nobilis
(Richardson) (Santiago and Reyes, 1989; C. Santiago, unpubl.
data). The Asian catsh Clarias macrocephalus (Gunther)
larvae feed well on Artemia nauplii under laboratory condi-
tions (Fermin, 1995). However, the high cost and unavailabil-
ity of the Artemia cysts at times from the local market and, in
the case of Brachionus, stringent requirements in terms of
facilities and skill as well as high production cost are the major
constraints to the use of these live organisms in hatcheries.
Four species of free-living nematodes have been demonstra-
ted to be ingested and easily digested by Danio sp. (Hofsten
et al., 1983). The free-living nematode Panagrellus sp. has been
tested in Danio malabaricus and Poecilia reticulata (Kahan and
Appel, 1975); common carp Cyprinus carpio and silver carp
U.S. Copyright Clearance Centre Code Statement: 01758659/2003/19040239$15.00/0
Received: July 17, 2002
Accepted: December 1, 2002
Hypophthalmichthys molitrix (Kahan et al., 1980, cited in
Hofsten et al., 1983); and grass carp Ctenopharyngodon idella
and the carp Hypophthalmichthys nobilis (Rottmann et al.,
1991). Panagrellus redivivus in particular has also been tested
in larval shrimps Penaeus vannamei (Biedenbach et al., 1989)
and Penaeus indicus (Kumlu and Fletcher, 1997; Kumlu et al.,
1998).The free-living nematode P. redivivus has desirable
characteristics: the female is ovoviviparous and has a high
reproductive rate; generation time is 56 days with up to
83 larvae in a cuticle (Cryan et al., 1963); and its small size
(50 lm diameter; up to 1.5 mm in total length) is suitable for
sh larvae, especially those with a small mouth. The proximate
composition and amino acid prole of P. redivivus are
comparable with Artemia (see data of Kahan et al., 1980,
presented in Biedenbach et al., 1989). Thus the present study
was conducted to verify or determine the response of rst
feeding bighead carp and Asian catsh larvae given the free-
living nematode P. redivivus as source of nourishment.
Materials and methods
Nematode production
The free-living nematodes were cultured in the laboratory at
2225
C. The culture apparatus consisted of a smaller Petri
dish (9 cm diameter without cover) placed at the middle of a
larger Petri dish (14 cm diameter) with cover. The smaller Petri
dish was half-lled with an oat medium made of sterilized
oatmeal and distilled water. Forty grams (40 g) of nely
ground oatmeal and 100 mL water were mixed and allowed to
stand for about 2 h with occasional thorough mixing. This
amount of prepared medium can be used to partially ll ve
smaller Petri dishes. The oat medium in the dishes was then
inoculated with free-living nematodes (10002000 per dish).
Distilled water was added to the larger Petri dish up to the
level of the oat medium in the smaller dish, and the culture
apparatus was covered. Substantial number of nematodes
started to migrate from the oat medium to the water in the
larger Petri dish in about 10 days. Initially, nematodes were
harvested on day 10 up to day 20 of culture. Water in the
larger Petri dish was replaced after each harvest. The protocol
for nematode production was slightly modied on the
succeeding experiments. The oat medium was made less moist
by mixing 50 g of nely ground oatmeal and 100 mL water.
This allowed migration of nematodes to the collection water at
www.blackwell.de/synergy
240
an earlier time and at higher numbers. Nematodes were
harvested from day 7 up to day 16.
Harvests of nematodes were placed in large conical tubes
and cleaned of the oat medium by washing several times with
ordinary water. During cleaning, the nematodes were allowed
to settle in the cone and the water was siphoned out. The
process was repeated until the water became clear. The clean
nematodes were resuspended in water, counted, and then fed
to the sh larvae. Nematode samples were also freeze-dried for
the proximate and fatty acid analyses performed at the
Centralized Analytical Laboratory of SEAFDEC Aquaculture
Department.
Feeding of bighead carp larvae
Two experiments on bighead carp were conducted in a
completely randomized design. Carp larvae that just started
to feed exogenously (about 3 days post-hatch) were used. In
experiment 1, mean body weight of carp larvae at stocking was
2.3 0.6 mg and total length, 8.98 0.44 mm. The carp
larvae in experiment 2 initially weighed 2.1 1.0 mg, with
total length of 8.57 0.33 mm.
In experiment 1, nine aquaria (40 20 25 cm) lled with
10 L of water were stocked with 25 carp larvae L)1. There
were three treatments with three replicates each: no feeding,
feeding with Artemia nauplii, and feeding with P. redivivus
twice a day (09.00 and 14.00 h). Newly-hatched Artemia
nauplii were given to the larvae initially at 5 mL)1 water in the
aquaria per feeding. This was increased to 10 nauplii mL)1 per
feeding when the larvae were able to consume more. The
bighead carp larvae were given 530 nematodes mL)1 per
feeding. The group of unfed larvae was included to rule out
presence of food organisms in the water supply.
In experiment 2, 12 glass aquaria, each lled with 5 L of
water, were stocked with 25 carp larvae L)1. The feeding
treatments were the same as in experiment 1. In addition, a
commercial entomopathogenic nematode (EPN) was tested on
bighead carp larvae. During each feeding, P. redivivus was
given to the larvae at 50 mL)1 and the EPN at 43 nema-
todes mL)1.
For both experiments, the rearing vessels were cleaned
morning and afternoon by siphoning faeces and other mate-
rials before feeding time. Dead larvae were also counted to
determine daily mortality. Water siphoned out was replaced.
Water temperature was recorded daily. Dissolved oxygen, pH
and total ammonia-nitrogen were monitored weekly before
sampling.
Ten larvae from each aquarium were sampled weekly for
weight and length measurements. Duration of feeding for each
experiment was 21 days. During nal sampling, up to 20 larvae
were measured and the survivors were counted.
Feeding of Asian catsh larvae
Two feeding experiments were performed. In the rst experi-
ment, 12 aquaria lled with 2 L of water were used. Stocking
in the aquaria was 25 catsh larvae L)1. The rst feeding
larvae weighed 4.6 0.9 mg and measured 9.35 0.24 mm
total length at stocking. The larvae were given P. redivivus,
Artemia sp., and Tubifex sp. for 14 days. Feeding was
performed three times a day at 09.00, 13.00 and 15.00 h.
Panagrellus was given to the catsh larvae at 50 mL)1 per
feeding on the rst 9 days and 100 mL)1 per feeding on the
succeeding days. Artemia nauplii were given at 5 mL)1 per
C. B. Santiago et al.
feeding, equivalent to 15 nauplii mL)1 day)1. Tubifex was fed
to the catsh larvae ad libitum. A treatment without feeding
was also included.
In the second experiment, 16 aquaria lled with 3 L of water
were stocked with 50 catsh larvae L)1. Mean body weight
was 3.1 0.9 mg and total length was 8.51 0.31 cm at
stocking. Feeding treatments were Artemia alone (10 nau-
plii mL)1 per feeding), Panagrellus alone (100 mL)1 per
feeding), or their combination with a 38% crude protein
articial diet. In the combination feeding, half the number of
Artemia nauplii or nematodes were used and the articial diet
was given initially at 50% of the sh biomass daily and 30%
on the second week. Feeding was done twice daily at 09.30 and
14.30 h. The aquaria were cleaned daily by siphoning o faeces
and dead larvae or other organic matter found at the bottom.
Dead catsh larvae were counted to determine daily mortality.
The amount of water drawn out was replaced. Fish were
sampled at day 7 and on the nal sampling at day 14. Water
quality was likewise monitored.
Statistical analysis
Data were analysed statistically using the General Linear
Models procedure of the SAS system (SAS Institute Inc.,
1991). When analysis of variance showed dierences in
treatment mean values (P < 0.05), Duncans multiple range
test was performed to determine which of the mean values
diered signicantly from each other.
Results
Experiments on bighead carp larvae
Lower mortality was observed in bighead carp larvae fed
Artemia nauplii than in larvae fed Panagrellus in experiment 1
(Fig. 1a). However, for both treatments, mortality was gradual
and did not increase further after day 16 or 17. High mortality
of unfed sh larvae was observed starting on day 6 and, except
for one tank, all larvae in replicate tanks were dead by day 11
(Fig. 1a). Water quality was similar for all treatments. Water
temperature ranged from 2630
C, with 34
C daily uctu-
ation; dissolved oxygen, 6.97.7 mg L)1; pH, 8.39.3; and
total ammonia-nitrogen, nil.
In experiment 2, mortality of bighead carp larvae fed
Artemia and Panagrellus was gradual, stabilizing by day 15
(Fig. 1b). Moreover, mortality of larvae in these two treat-
ments did not dier signicantly (P > 0.05). The unfed larvae
had high mortality on day 7 and total mortality by day 13. On
the other hand, larvae fed the EPN suered high mortality on
day 2 and total mortality by day 8 (Fig. 1b). Water tempera-
ture in experiment 2 ranged from 2630
C; dissolved oxygen,
7.08.2 mg L)1; pH, 8.18.8; and total ammonia-nitrogen was
nil to 1.43 mg L)1.
The growth of the Artemia-fed carp larvae throughout the
rearing period was much higher than that of Panagrellus-fed
larvae. Final body weight and total length as well as survival
rate were signicantly higher (P < 0.05) for bighead carp fed
Artemia nauplii than those fed Panagrellus (Table 1). In
experiment 2, the Panagrellus-fed larvae had lower body
weight than the larvae fed Artemia nauplii, but the dierence
in growth rate as well as mortality rate between the two groups
of larvae was not as great as in experiment 1. The nal mean
body weight, total length and survival rate did not dier
signicantly between carp larvae fed Artemia nauplii and
Panagrellus (Table 2). The estimates on survival based on
Response of bighead carp and Asian catsh larvae to alternative feed 241

Days of feeding Table 2

Growth and survival of bighead carp larvae after 21 days of feeding
a) 0 7 14 21
(experiment 2)
0
10 Body weight1 Total length1 Survival1
20 Treatment (mg) (mm) (%)
30
40 No feeding
No feeding2
50 Artemia Artemia nauplii 46.5 2.3 19.7 0.4 75.0 2.6
60 Panagrellus Panagrellus redivivus 44.2 7.9 18.9 1.2 72.7 10.5
EPN3
70
80 1
Column mean values are not signicantly dierent (P > 0.05). Mean
90 body weight at stocking was 2.1 1.0 mg; total length, 8.57
Mortality (%)

100 0.33 mm.

2
No sh survived by day 13.
3
b) 0 7 14 21 All larvae fed entomopathogenic nematode (EPN) were dead by day 8.
0
10
Days of feeding
20 a) 1 2 3 4 5 6 7 8 9 10 11 12 13 14
30
0
40 No feeding
Artemia
10
50 20
Panagrellus
60 EPN 30
70 40
80 50
90 60
70
100
80
Fig. 1. Cumulative mortality of bighead carp larvae at dierent 90
feeding treatments over a 21-day period in experiment 1 (a) and
Mortality (%)

100
experiment 2 (b) No feeding Artemia Panagrellus Tubifex

b) 1 2 3 4 5 6 7 8 9 10 11 12 13 14
Table 1 0
Growth and survival of bighead carp larvae after 21 days of feeding 10
(experiment 1) 20
30
1 1 1
Feeding Body weight Total length Survival 40
treatment (mg) (mm) (%)
50
2 60
No feeding
70
Artemia nauplii 98.7 10 24.9 0.6 87.8 2.3 Artemia
Panagrellus redivivus 17.0 5 14.5 1.2 71.2 4.9 80
Artemia + AD
90 Panagrellus
1
Column mean values are signicantly dierent (P < 0.05). The mean 100 Panagrellus + AD
body weight of bighead carp larvae at stocking was 2.3 0.6 mg;
total length, 8.98 0.44 mm. Fig. 2. Cumulative mortality rate of Asian catsh larvae at dierent
2 feeding treatments over a 14-day period in experiment 1 (a) and
No sh survived after days 1113.
experiment 2 (b). (AD articial diet)

mortality agreed with the actual counts of larvae at the end of
each feeding trial, as was observed in the feeding trials on
catsh.
Experiments on Asian catsh larvae
In experiment 1, mortality of catsh larvae fed Artemia nauplii
or Tubifex was signicantly lower than that of larvae fed
Panagrellus starting on day 8 (Fig. 2a). On the other hand,
about 60% of the unfed catsh larvae were dead by day 8 and
100% by day 10. For the whole duration of experiment 1, the
DO ranged from 4.06.4 mg L)1, with the aquaria containing
unfed larvae having the highest readings and those of larvae
fed Panagrellus being in the lower range. The lowest total
ammonia-nitrogen (0.610.66 mg L)1) was recorded in Pana-
grellus-fed catsh larvae. Total ammonia-nitrogen was
signicantly high in aquaria containing Tubifex-fed larvae
(0.913.29 mg L)1) and Artemia-fed larvae (1.87
2.05 mg L)1). However, pH in all aquaria was relatively stable
for 2 weeks (7.78.0).
Mortality of catsh larvae in experiment 2 diered signi-
cantly among treatments starting on day 6, with larvae fed
Panagrellus alone or in combination with articial diet having
the highest cumulative mortality up to day 14 (Fig. 2b). A
slight decrease in mortality was observed in larvae given the
combination of articial diet and Artemia nauplii or Pana-
grellus.
The catsh larvae fed Tubifex or Artemia nauplii showed
much higher growth and survival than those given Panagrellus
in experiment 1 (Table 3). Between larvae fed Artemia nauplii
and Tubifex, the Tubifex-fed larvae had signicantly higher
body weight and total length (P < 0.05). However, survival
rates were high in both treatments (Table 3).
In experiment 2, body weight of catsh larvae given
Artemia nauplii alone was signicantly higher than that of
larvae given the combination of Artemia and articial diet.
Growth was signicantly lower in larvae given Panagrellus
alone or in combination with articial diet (Table 4). On the
other hand, survival rates were signicantly higher in larvae
given Artemia nauplii alone or in combination with articial
242 C. B. Santiago et al.

Table 3 two studies could not be compared because of lack of

Body weight, total length and survival of catsh larvae after 14 days of information. On the basis of the length measurements after
feeding in experiment 1
3 weeks, the bighead carp larvae given Artemia in the present
Body weight1 Total length1 Survival1 study were longer than the larvae that were also fed Artemia in
Treatment (mg) (mm) (%) the other study (Rottmann et al., 1991). The nal weight
measurements of the bighead carp larvae in the two studies
No feeding2 could not be directly compared. Wet weight of individual sh
Artemia nauplii 110.4 10.1b 24.5 0.9b 87.9 5.2a
Panagrellus redivivus 13.3 1.5c 12.4 0.3c 35.3 16.6b was measured and the mean weights are hereby reported, while
Tubifex sp. 157.1 23.0a 26.1 0.7a 88.9 4.8a the nal weight of the bighead carp larvae in the other study
was reported as the dry weight of 50 individuals (Rottmann
1
Column mean values followed by a common superscript are not et al., 1991). On a dry-matter basis, however, the dry weight of
signicantly dierent (P > 0.05). Initial body weight 4.6 0.9 mg;
total length 9.35 0.24 mm.
the bighead carp fed Artemia or P. redivivus in the present
2
All catsh larvae were dead by day 10. study was higher than that reported by Rottmann et al. (1991).
Although stocking rates were close (28 larvae L)1 vs 25 L)1),
survival rates of bighead carp studied by Rottmann et al.
diet than in larvae given Panagrellus (Table 4). Use of the (1991) were higher than currently obtained. This could be
combination diet slightly increased the nal survival of attributed to the method of estimating number of larvae at
catsh larvae. stocking and determining survival rates and, more import-
antly, to the innovative aeration and water ltration designed
to maintain good water quality in larger tanks without water
Composition of the free-living nematodes produced ush (Rottmann et al., 1991).
The P. redivivus used in the present study had a relatively Nematode density appeared to be an important factor that
lower protein content but higher lipid content than those inuenced carp growth and survival. This was shown by the
reported for the same species of nematodes grown in improved performance of the larvae given higher density of
dierent media (Table 5). Of the two groups of essential nematodes in experiment 2. On the other hand, the EPN
fatty acids, the total n-6 fatty acid content was much higher appeared unsuitable for bighead carp larvae probably due to
than the total n-3 fatty acids (Table 6). The relatively high the clay formulation that carried the nematodes and which was
level of unidentied fatty acids could be due to lack of some dicult to separate.
standard fatty acids. The Asian catsh larvae performed poorly with the free-
living nematodes as live feed. The larvae ingested some
nematodes but appeared emaciated even if nematodes were
Discussion abundant in the water, especially in experiment 1. Catsh
The present results demonstrate the acceptability of larvae normally feed at the bottom and remain in clusters
P. redivivus to bighead carp larvae. This nding agrees with when satiated. Panagrellus-fed catsh larvae stayed longer at
an earlier report on the positive response of bighead carp the water column and were dispersed as if in search of food.
Hypophthalmichthys nobilis larvae to Panagrellus sp. The present results also conrm an earlier nding on the
(Rottmann et al., 1991). The bighead carp Aristichthys nobilis excellent performance of catsh larvae fed Tubifex
larvae in the present study, however, appear to be dierent (A. Evangelista, pers. comm.).
from the bighead carp H. nobilis studied by Rottmann et al. Unlike bighead carp larvae which had high performance
(1991). At the outset, it was presumed that there was an when fed a combination of zooplankton (Brachionus or
uncertainty in the identity of species because bighead carp is Artemia) and articial diet (Santiago and Reyes, 1989;
closely related to silver carp Hypophthalmichthys molitrix and C. Santiago, unpubl. data), the catsh larvae in the present
the two are sometimes dicult to distinguish. Moreover, the study did not show improvement in growth and survival when
size of the rst feeding larvae (about 72 h post-hatch) in the fed a combination of Panagrellus and articial diet. Previous

Table 4
Body weight1 Total length1 Survival1 Body weight, total length and survival
Treatment (mg) (mm) (%) of catsh larvae after 14 days of
feeding in experiment 2
Artemia nauplii 35.7 8.3a 17.4 1.2a 68.2 8.9a
Artemia nauplii + articial diet 22.8 6.5b 14.8 1.4b 78.3 5.0a
Panagrellus redivivus 7.6 2.8c 10.7 0.7d 30.2 7.2b
Panagrellus redivivus + articial diet 8.8 3.3c 11.5 1.2c 37.7 5.4 b
1
Column mean values followed by a common superscript are not signicantly dierent (P > 0.05).
Initial body weight 3.1 0.9 mg; total length 8.51 0.31 mm.

Table 5
Composition of Panagrellus redivivus (% dry matter) produced for the present study compared with those produced in other culture media

Carbohydrates/
Media Crude protein Lipids/crude fat nitrogen-free extract Reference

Oatmeal 38.8 23.7 28.9 Present study

Oatmeal + yogurt 52 13 15.4 Kahan and Appel, 1975
Cornmeal + unbleached white wheat our 48.3 17.3 31.3 Biedenbach et al., 1989
Response of bighead carp and Asian catsh larvae to alternative feed 243

Table 6 National Sun Yat-Sen University, Kaohsiung, Taiwan on

Fatty acid composition (% of total fatty acids) of the free-living 2530 November 2001.
nematode Panagrellus redivivus used in the feeding of bighead carp
larvae compared with reported values

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This study is part of the collaborative, EU-funded INCO-DC
Project with Contract No. ERB IC18 CT98-0333. We thank Authors address: C. B. Santiago, Southeast Asian Fisheries
Development Center (SEAFDEC) Aquaculture
Ms Ofelia Reyes for the fatty acid analysis. Part of this study Department, Binangonan Freshwater Station,
was presented during the 6th Asian Fisheries Forum held in Binangonan, Rizal 1940, Philippines.
E-mail: csantiago@aqd.seafdec.org.ph