Aquaculture xxx (2014) xxx–xxx
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Euryhaline rotifer Proales similis as initial live food for rearing fish withsmall mouth
Atsushi Hagiwara a,⁎, Stenly Wullur b, Helen S. Marcial c, Narisato Hirai d, Yosh*taka Sakakura a
a Graduate School of Fisheries Science and Environmental Studies, Nagasaki University, Nagasaki 852-8521, Japanb Faculty of Fisheries and Marine Science, Sam Ratulangi University, Manado 95115, Indonesiac Aquaculture Department, Southeast Asian Fisheries Development Center, Tigbauan, Iloilo 5021, Philippinesd National Research Institute of Aquaculture, Aquaculture Systems Division, Kagoshima 899-7101, Japan
⁎ Corresponding author at: Graduate School of FisherStudies, Nagasaki University, 1-14 Bunkyo, Nagasaki 852819 2830.
E-mail address: [emailprotected] (A. Hagiw
http://dx.doi.org/10.1016/j.aquaculture.2014.03.0340044-8486/© 2014 Elsevier B.V. All rights reserved.
Please cite this article as: Hagiwara, A., et al.(2014), http://dx.doi.org/10.1016/j.aquacult
a b s t r a c t
a r t i c l e i n f o
Article history:Received 17 October 2013Received in revised form 12 March 2014Accepted 17 March 2014Available online xxxx
Keywords:Euryhaline rotiferLarval rearingLive foodSmall-mouth fishProales
The SS-type rotifer Brachionus rotundiformis is a common initial food for rearing fish larvae with a small mouth.However, there are commercially important fish species whose mouth sizes are too small to feed on SS-typerotifers. In 2004, we isolated a small (body length = 82.7 ± 10.9 μm; body width 40.5 ± 6.4 μm), flexible, andiloricate rotifer, Proales similis from an estuary in Okinawa, Japan. Under laboratory conditions (25 °C,2–25 ppt) P. similis produced its first offspring on 2.5 to 2.8 days after hatching, and produced 4.3 to 7.8 offspringwithin 4.0 to 4.7 days life span. Batch cultured P. similis fed Nannochloropsis oculata suspension at 28.8 μgdry weight ml−1 and cultured at 25 °C, 25 ppt filtered seawater, increased exponentially from 25 to 2400 indml−1 after 11 days of culture with an overall intrinsic rate of natural increase (r) of 0.42 day−1. The growthrate of P. similis was not significantly different when fed fresh N. oculata and super fresh Chlorella vulgaris-V12®. Total lipid per wet weight of P. similis fed by N. oculata and C. vulgaris were 2.4 and 2.6%, respectively.The compositions of eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA), and arachidonic acid (ARA) ofP. similis fed N. oculatawere 23.2, 0.0 and 5.3%, respectively, while these were 11.0, 17.5 and 0.5% respectively,when fed C. vulgaris. The use of P. similis to feed small mouth fish including seven-band grouper Epinephelusseptemfasciatus, rusty angelfish Centropyge ferrugata, and humphead wrasse Cheilinus undulatus showed that itis an excellent starter food for these species because of their high selectivity index and improved survival. Inaddition, P. similis was ingested by Japanese eel Anguilla japonica larvae with a complicated digestive system.The use of P. similis as starter feed for small mouth fish larvae is highly recommended.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
In marine fish larvae culture, the rotifers are provided as starter foodduring thefirst days of exogenous feeding, depending on themouth sizeof the larvae (Hagiwara et al., 2001; Lubzens, 1987). Rotifers areexcellent first live food due to their small size (Akazawa et al., 2008;Tanaka et al., 2005), ability to be cultured at high density (Hagiwaraet al., 1997, 2001; Yoshimura et al., 1997) and the capacity to benutritionally manipulated (Hagiwara et al., 2001; Hayashi et al., 2001).Based on lorica size, culturists divided rotifers into L (large;130–340 μm), S (small; 100–1200 μm) and SS (super small; 90–110 μm) type (Hagiwara et al., 1995, 2001). The SS-type is also classifiedas Brachionus rotundiformis (Fontaneto et al., 2007; Kotani et al., 2005;Segers, 1998). Due to its smaller size, B. rotundiformis is commonly
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ara).
, Euryhaline rotifer Proales simure.2014.03.034
used as starter food for fish species with a small mouth gape. However,feeding mix stages of B. rotundiformis is infective or unsuitable for thelarvae of several marine fishes with even a smaller mouth, includingsome species of groupers (Glamuzina et al., 1998, 2000; Kohno et al.,1997; Okumura, 1997), angelfishes (Olivotto et al., 2006) and wrasse(Sugama et al., 2004). The larvae of angelfishes of the family Poma-chantidae for example is reported to have a gape size of approximately160 μm (Leu et al., 2009; Olivotto et al., 2006), while the larvae ofNapoleon wrasse Cheilinus undulatus have a mouth size of 133 μm(Slamet and Hutapea, 2004). These two commercially valuable fishspecies require even smaller live food in the range of 40–80 μm at theinitial feeding stages (Olivotto et al., 2006; Slamet and Hutapea, 2004).Despite much success achieved in the maturation and spawning ofrusty angelfish and Napoleon wrasse, larval rearing has achieved littlesuccess due to the lack of starter food suitable for their larvae. If thesuitable size of prey is assumed from 20 to 70% of the mouth size(Cunha and Planas, 1999; Yúfera and Darias, 2007), the larvae of rustyangelfish may require starter food with a size from 32 to 112 μm,while the larvae of Napoleon wrasse may require 26 to 93 μm fooditems.
ilis as initial live food for rearing fish with small mouth, Aquaculture
mailto:[emailprotected]
25 µm
Totallength
Bodylength
Body width
Fig. 1. The Proales similis isolated in Ishigaki Island, Okinawa, Japan.
Table 1Total highly unsaturated fatty acid (HUFA) of P. similis fed N. oculata and super fresh.
HUFA P. similis fed P. similis fed B. rotundiformis fed
N. oculata Super fresh C. vulgaris® Super fresh C. vulgaris®
C20: 4n-6 5.3 0.5 0.8C20: 5n-3 23.2 11.0 6.1C22: 6n-3 0 17.5 6.6DHA/EPA 0 1.59 1.08
2 A. Hagiwara et al. / Aquaculture xxx (2014) xxx–xxx
Aside from a small mouth gape, some fish species have a complicat-ed digestive system that requires a smooth and easily digested fooditem. An example is the Japanese eel Anguilla japonica. Although eellarvae have a large mouth size at initial feeding their oesophagus isnarrow and without mucus cells (Yoshimatsu and Matsuda, 2008;Yoshimatsu et al., 2008), thus could not ingest rotifers with lorica orcopepods with exoskeleton. At present, the larvae culture of Japaneseeel uses a slurry diet made of dried shark egg, particularly the egg ofspiny dogfish Squalus acanthias (Kagawa et al., 2005; Tanaka et al.,2001, 2003). However, the use of shark egg raised concerns because ofserious depletion of shark population, and the species presently isconsidered as endangered (Baum et al., 2003). Finding an alternativedietary source for eel larvae is necessary for its sustainable aquaculture.
In July 2004, we isolated a rotifer species from an estuary in Okina-wa, Japan, and tentatively identified it as Proales similis. The identitywas confirmed by Professor Russel Shiel of Albury, NSW, Australia.P. similis belongs to classMonogonta, family Proalidae and genus Proales(De Smet, 1996; Koste and Shiel, 1990). It was firstly reported byDe Beauchamp in 1907 (De Smet, 1996), and later on, reported tobe found in a wide range of water bodies, from freshwater (Manuelet al., 1992; Ricci and Balsamo, 2000; Turner, 1996), estuarine andbrackishwater (De Smet, 1996) to hypersaline water (De Smet, 1996;Moscatello and Belmonte, 2004; Walsh et al., 2008). Its body is softand flexible without lorica (iloricate) unlike other rotifer species (DeSmet, 1996). Among the species in genus Proales, only Proales sordid(Jennings and Lynch, 1928a, 1928b) and Proales decipiens (Noyes,1922) have been successfully cultured. Recognizing the demand offish larvae on small, smooth and flexible starter food and the potentialof P. similis to meet this demand, we conducted a series of experimentsin order to determine the life history, mass production, and nutritionalvalue of P. similis. After establishing its culture, we tested its suitabilityas starter food for various fish species under laboratory conditions. Forthe first time, we successfully mass cultured P. similis at high densityin the laboratory (Wullur, 2009). Our feeding experiments also provedthat P. similis is a suitable first food for fish species with a very smallmouth and a complicated digestive system.
2. Life history, culture, and nutritional value of Proales similis
The P. similis (Fig. 1) that we explored was collected using a45 μm mesh plankton net from an estuary in Ishigaki Island, Okinawa,Japan on July 2004. The water temperature and salinity during the col-lection were 27 °C and 2 ppt, respectively. A clonal culture of P. similiswas subsequently acclimatized to higher salinity under laboratoryconditions, fed Nannochloropsis oculata. The total length, body length,and body width of P. similis ranged from 50 to 150 μm (mean ± SD;109 ± 15 μm), 40 to 110 μm (mean ± SD; 83 ± 11 μm), and 10 to50 μm (mean ± SD; 40 ± 6 μm), respectively. Its body length is 38%smaller than the lorica length of B. rotundiformis (which ranged from70 to 170 μm), and its body width is 60% narrower than the loricawidth of B. rotundiformis which ranged from 50 to 150 μm (Wulluret al., 2009).
Temperature and salinity are two important factors that influencethe population growth of rotifers. The life history parameters ofP. similis under a wide range of temperature and salinity measureswere undertaken. Temperature showed a strong influence on thepopulation growth of P. similis under the batch culture method(Wullur et al., 2009). The maximum density (1400 ind ml−1) wasobtained at 30 to 35 °C. This indicates its usefulness in feeding sub-tropical and tropical fish species. Results also showed that P. similis is aeuryhaline species because it can propagate in a wide range of salinity(2–25 ppt), although it can reproduce faster at 2 ppt (Wullur et al.,2009). This salinity corresponds to the salinity to where P. similis wassampled. However, Brain and Koste (1993) found P. similis in hyper-saline water (48–98 ppt). The capability of P. similis to tolerate a widerange of salinity is similar to that of the euryhaline rotifer Brachionus
Please cite this article as: Hagiwara, A., et al., Euryhaline rotifer Proales sim(2014), http://dx.doi.org/10.1016/j.aquaculture.2014.03.034
plicatilis sp. complex, which is reported to thrive from 1 to 60 ppt(Hoff and Snell, 1987).
We also conducted a series of life table experiments of individualcultured P. similis, in order to determine its lifespan, generation time,reproductive period, and fecundity under different temperatures (15,20, 25, 30 and 35 °C) and salinities (2, 15, and 25 ppt; Wullur et al.,2009). During the experiment, the animals were fed with 2.5 × 106
N. oculata and were kept in darkness. The animals were inspecteddaily until they die. Life span ranged from 4.0 to 4.7 days, generationtime from 2.4 to 2.8 days, reproductive period from 2.9 to 3.4 days,and fecundity 4.3 to 7.8 (Wullur et al., 2009). Based from the aboveresults, we also conducted a mass culture (2-l) experiment in order todetermine the population growth rate of P. similis in a bigger scale.The experiment was conducted at 25 °C, 25 ppt and fed withN. oculata at 28.8 μg dry weight ml−1. Results showed that P. similisgrew from 25 ind ml−1 on day 0 to 2400 ind ml−1 on day 11, with alag growth from day 1 to day 4, an exponential growth from day 5 today 8, and a stationary phase from day 9 onwards. The mean r-valuewe obtained from 3 runs was 0.42 day−1 (Wullur et al., 2009).
ilis as initial live food for rearing fish with small mouth, Aquaculture
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P. similis could be nutritionally enriched by feeding N. oculata andSuper Fresh Chlorella® (Wullur et al., 2011). The highly unsaturatedfatty acid (HUFA) of P. similis is comparable to that of B. rotundiformiswhen cultured, fed or treated with the same microalgae at the sameconcentration (Table 1). The DHA of the P. similis fed with Super FreshChlorella® was 2.6 times higher than that of B. rotundiformis fed withthe same food. The ratios of DHA/EPA in P. similis and B. rotundiformisfed Super Fresh Chlorella were 1.59 and 1.08, respectively. These levelsof DHAs, EPAs and of the DHA/EPA ratio were in the range of the sug-gested levels for marine fish larvae (Sargent et al., 1999; Tucker, 1998).
3. The suitability of P. similis as initial food for:
3.1. Seven-band grouper Epinephelus septemfasciatus
The mouth of the seven-band grouper E. septemfasciatus opens at3 day after hatching (DAH), and themouth size at thefirst day of feeding(4 DAH) is 180 ± 20 μm (Wullur et al., 2011). On 4 DAH, the larvaeshowed a higher selectivity on P. similis than B. rotundiformis, with aselectivity index of 0.7 and 0.3, respectively. The preference becameneutral on 5 DAH, and the larvae switched their preference to largerprey (B. rotundiformis) on 6 DAH and thereafter. Therefore, a combina-tion of P. similis and B. rotundiformis is recommended in larval rearingof grouper, E. septemfasciatus (Wullur et al., 2011). The consistent bettergrowth and survival of grouper larvae fed with the combination of tworotifer species indicated that they effectively utilized P. similisduring thefirst few days of feeding, in addition to B. rotundiformis as an energyresource for growth and survival. Feeding P. similis to other grouperspecies with similar characteristics to E. septemfasciatus is thereforerecommended.
3.2. Rusty angelfish Centropyge ferrugata
Angelfishes (family Pomacanthidae) are among the top ten familiesin international trade of marine aquarium species (Baensch andTamaru, 2009). Within family Pomacanthidae, the genus Centropyge isamong the most popular, highly prized and heavily traded (Baenschand Tamaru, 2009; Olivotto et al., 2006). Despite much success incaptive maturation and spawning of angelfishes have been achievedin the last three decades (Arai, 1994; Leu et al., 2009; Olivotto et al.,2006; Suzuki et al., 1979), massive mortality related to poor initial
I
2
4
3 4 5Days after hatching
Num
ber
of f
ood
in g
ut (
ind.
-1)
Fig. 2.Number of zooplankton in the gut of C. ferrugata larvae. I,first run; II, second run. Proales snauplii ( ).
Please cite this article as: Hagiwara, A., et al., Euryhaline rotifer Proales sim(2014), http://dx.doi.org/10.1016/j.aquaculture.2014.03.034
feeding of the larvae still remains a bottleneck for successful captiveproduction of this species (Leu et al., 2009; Olivotto et al., 2006).
Wullur (2009) conducted two feeding trials on angelfish C. ferrugatato determine the acceptability of P. similis as well as other zooplankton,including Keratella sp. cf. sinensis, Paracyclopina nana, and SS-typerotifer B. rotundiformis. Larvae were stocked in a 2.5 l natural seawater(32 ppt) at 25 °C. All test zooplankton were supplied to the larvae at20 ind ml−1 starting from 3 DAH. Results showed that the feedingincidence (measured by the quantity of zooplankton found in the gutof the larvae) of the larvae fed P. similis was higher than those fedwith other zooplankton species (Fig. 2). Furthermore, survival on day6 was higher in the larvae fed P. similis (18.5 to 38.0%) than those inother treatments (1 to 11.5%; Fig. 3). Results of this study proved thatP. similis is a good candidate as first food for angelfishes.
3.3. Humphead wrasse Cheilinus undulates
The total length of humphead wrasse C. undulatus after 6 h ofhatching was approximately 2.4 mm; then the mouth opens and theeye pigmentation was observed at 2 DAH (Hirai et al., 2013). Themouth diameter and mouth width were 154 μm and 133 μm,respectively. Due to their small mouth gape, we conducted a pre-liminary experiment exploring the use of particulate diets such aspowdered milk and boiled chicken yolk which are small and containhigh protein (Hirai et al., 2012). C. undulatus larvae ingest P. similis,boiled chicken egg yolk and powdered milk on 2 DAH, and increasedingestion of P. similis was observed on 3 DAH. On both days,C. undulatus did not ingest B. rotundiformis. However, on 7 DAH, thenumber of B. rotundiformis in the gut of C. undulatus was greater thanthe number of P. similis. During this experiment, we produced 537juveniles at 50 DAH (survival rate = 10.7%), indicating the successof C. undulatus seed production with the use of P. similis as initial food(Hirai et al., 2013).
3.4. Japanese eel Anguilla japonica
The mouth size of the Japanese eel A. japonica larvae is large (521 ±28 μm), but they have difficulty ingesting large and solid food itemsbecause their esophagus is characteristically narrow and devoid ofmucus cells (Yoshimatsu et al., 2008). The lack of mucus cells in theesophagus may limit the larvae to ingest only soft, small, and smooth
II
Num
ber
of f
ood
in g
ut (
ind.
-1)
1
2
3 4 5 6Days after hatching
imilis (□), Brachionus rotundiformis (■), Keratella sp. cf. sinensis ( ) and Paracyclopina nana
ilis as initial live food for rearing fish with small mouth, Aquaculture
40
35
30
25
20
Surv
ival
rat
e (%
)
15
10
5
0P. similis B. rot Keratella sp P. nana
Fig. 3. Survival of C. ferrugata larvae in the first ( ) and second run ( ).
4 A. Hagiwara et al. / Aquaculture xxx (2014) xxx–xxx
food materials. At present, the primary food of A. japonica larvae incaptivity is a slurry diet, made of shark egg powder (Kagawa et al.,2005; Tanaka et al., 2001, 2003). However, the use of this food is notsustainable because of serious depletion of shark population (Baumet al., 2003).
We conducted a series of experiments to determine if A. japonicalarvae could survive when fed P. similis, both as living and non-livingdiet. A slurry diet made of shark egg powder was fed to the controlgroup. P. similis paste was made by concentrating the rotifer culture atan exponential growth stage and the concentrated rotifers were storedin a refrigerator (4 °C) until use, while live P. similis diet was takendirectly from the culture tanks during feeding time. Feeding started on7 DAH and terminated on 13 DAH where survival rate and total lengthof survivors were determined. Results showed that survival wassignificantly higher in the slurry diet fed group (62.8%) than those fednon-living P. similis (37.2%) and living P. similis (0.8%). The resultsindicated that A. japonica larvae ingest only non-living diet (Wullur,2009). In successive experiments, in addition to P. similis, we testedthe acceptability of other minute zooplankton species including,Synchaeta sp. cf. cecilia, B. rotundiformis, Keratella sp. cf. sinensis,B. angularis and nauplii of copepod Paracyclopina nana as initial foodfor A. japonica. Mass cultured zooplanktons were harvested, con-centrated, and paste as described above, and fed to A. japonica. Feedingincidence (percentage of larvae with food in the gut) of the larvae fedslurry diet (control) was 26.7 to 100.0%, and P. similis paste was 20.0to 46.7% (Wullur et al., 2013). The feeding incidence of larvae fedP. similis was significantly higher than those of other zooplanktons (0to 6.7%). The ingested slurry diet (20.3 to 68.9%) and P. similis (1.8 to37.2%) appeared in larval foregut and mid-hindgut, while the ingestedB. rotundiformis, Keratella sp., and B. angularis remained in the foregut.Although the feeding incidence of group fed P. similis paste was lowerthan the slurry diet, the use of P. similis paste is a good potential asfood for eel larvae because the uneaten slurry diet needs to be flushedout of the rearing tank every after feeding time to avoid deteriorationof the culture water.
4. Conclusion
P. similis is so far among the smallest rotifer species successfullymasscultured in the laboratory and successfully used in the larval rearing ofmarine fish with a very small mouth gape. Since it is iloricate, it is alsobetter ingested and digested by fish larvae with a complicated digestivesystem. Its culture is the same as the widely used Brachionus species(B. plicatilis and B. rotundiformis) with the use of either N. oculata orC. vulgaris. P. similis is euryhaline and eurythermic; thus, it can be usedfor freshwater and marine species as well as in subtropical and tropicalfish species. Based on the above feeding experiments, P. similis proved to
Please cite this article as: Hagiwara, A., et al., Euryhaline rotifer Proales sim(2014), http://dx.doi.org/10.1016/j.aquaculture.2014.03.034
be an excellent first food for fish larvae with a very small mouth gapesuch as groupers, wrasse, and angelfishes, and with a complicateddigestive system such as Japanese eel. Although small live foodorganisms such as ciliates, bivalve larvae, sea urchin eggs, oystertrocophores, and copepods, were accepted by fish larvae with a smallmouth, these live feed are either low in nutritional value or difficultto culture or obtain at high density. The use of euryhaline rotifer,P. similis is highly recommended for testing to other fish larvae withsimilar characteristics as the above tested fish species.
Acknowledgment
This research was supported by the JSPS Kakenhi (Grant-in-Aid forScientific Research B), Grant Number 24380108 to A.H.
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