Nauplii of the Calanoid Copepod, Acartia Sinjiensis As an Initial Food Organism for Larval Red Snapper, Lutjanus Argentimaculatus

〔水産増殖45巻1号31-40 SUISANZOSHOKU (1997-H9)•l

Nauplii of the Calanoid Copepod, Acartia sinjiensis as an Initial Food Organism for Larval Red Snapper, Lutjanus argentimaculatus.

Masanori Doi1) , Atsushi OHNO1), Yasuhiko TAKI1), Tanin SINGHAGRAIWAN2),and Hiroshi KOHNO1)

1)Tokyo University of Fisheries , 4-5-7 Konan, Minato-ku, Tokyo 108, Japan 2)The Eastern Marine Fisheries Development Center , Ban Phe, Muang District, Rayong 21160, Thailand

Abstract Initial feeding traits of larval red snapper Lutjanus argentimaculatus were investigated by supplying nauplii of the calanoid copepod Acartia sinjiensis and rotifers. The gut content of larvae consisted solely of A. sinjiensis nauplii (mean 2.1-7.2 nauplii/larva) on 0-2 days after initial mouth opening (days 0-2). The mean body width of the nauplii ingested was 0.058 mm on day 0, subsequently increasing with larval age. Feeding on rotifers (mean lorica width, 0.117 mm) was observed from day 3 (mean 0.92 rotifers/larva), with the number ingested increasing markedly on days 4 and 5. The mouth width of red snapper larvae on day 0 (0.166-0.188 mm) was larger than the body width of the nauplii and rotifers but smaller than those of other fish species conventionally reared using only rotifers. This small mouth size may have been initially restrictive, allowing only the seizure of early nauplii at the onset of feeding. The larvae grew well from 2.84 mm in mean total length (TL) on day 0 to 3.38 mm TL on day 5, without significant mortality. Nauplii of A. sinjiensis constitute a promising initial food for early red snapper larvae and very likely also for those of other marine fishes with a small mouth size.

initial food organism for groupers and snappers in Introduction Southeast Asia have not been very successful1-4). This

Mass seed production of marine fishes has been suc- is attributable to failures in ensuring the larvae of a cessful for those species of which larvae can feed on smooth transition from endogenous to exogenous feed- the rotifer, Brachionus plicatilis from the onset of feeding. Their mouth size at the onset of feeding may not ing. Among these are the red seabream, Pagrus major be large enough to accept rotifers and the amount of and the flounder, Paralichthys olivaceus in East Asia, endogenous energy resource remaining at this time is the seabass, Lates calcarifer in Southeast Asia, and the small in these species5-7). A search for food organisms turbot, Scophthalmus maximus in Europe. On the other suitable for the larval rearing of such species, con- hand, seed production trials, utilizing rotifers as an sidering factors of body size, nutritional quality and

Received : July 1, 1996 Key words: Acartia sinjiensis, Lutjanus argentimaculatus, Initial feeding, Larval rearing 32 M.Doi et al. (1997)

ease of mass cultivation, has been made by many ing density of the copepodids was 28 individuals/l.

workers, e.g., larval bivalves2,8-10), phytoplankton9,11) After the introduction of the copepodids, the tank

screened small Brachionus rotifers9) and a small Thai- water was found to have been contaminated by the

strain rotifer, Brachionus sp2,12,13) rotifer, Brachionus plicatilis cf. rotundiformis22), due Moderately successful results have been obtained in probably to the initial rotifer-contamination of the the larval rearing of the red snapper, Lutjanus argenti- Nannochloropsis cultures. The study was continued maculatus by supplying unsorted, tank-cultured cope- however, including in its parameters the electivity of pods prior to rotifer feeding14). Because they are the red snapper larvae toward A. sinjiensis and Brachionus main diets of many marine fish larvae in the wild, sp.

copepods have been considered promising candidates Spawning of L.argentimaculatus took place from

for initial larval food15). Among the various coastal 01:00 to 02:00 on May 6.About 8 hours after spawn-

copepod species, those of the calanoid genus Acartia ing, 5,000 fertilized eggs were transferred into each

seem to have great potential as initial dietary orga- rearing tank. The tank water was gently aerated, re-

nisms; they occur world wide16) and can be propagated maining unchanged during the experiment from May 6

in both indoor17) and outdoor18-20) tanks. Successful to May 13. On May 10, 40 •~ 104 rotifer individuals

results have been obtained in the larval rearing of red were added to each tank. During the experiment, the

seabream, Pagrus major using Acartia tsuensis19). water temperature in the tanks at 10:00 ranged from

In the present study, early feeding traits of Lutjanus 28.8•Žt to 30.2•Ž (mean 29.3•Ž). argentimaculatus larvae were investigated by supplying Of the two tanks, one was used solely for monitoring them with tank-propagated Acartia sinjiensis nauplii larval survival, all other data being taken from the and rotifers, with the object of examining the avail- other tank. Sampling of food organisms in the tank wa- ability of A. sinjiensis nauplii as an initial food orga- ter was conducted daily at 10:00, by collecting a 5 l nism for tropical marine fish larvae having a small water sample using a water column sampler. Sampling mouth. of red snapper larvae, made by gentle use of a scoop net, was undertaken more than once a day from May 8, Materials and Methods the day of initial mouth opening of the larvae. Larval The study was conducted at the Eastern Marine samples were preserved in 5 % formalin. In each sam- Fisheries Development Center (EMDEC), Rayong ple, 11 to 20 individuals were used for examination of Province, Thailand. Eggs of the red snapper, Lutjanus growth and gut contents, with mouth width measure- argentimaculatus were derived from hormone-induced ments taken from an additional 10 larvae. Larval sur- spawning at EMDEC, the inducement and spawning vival was estimated at 21:00 on May 6, 8, 10 and 12 procedures having been described by Singhagraiwan by the water column method. and Doi14) The body width of A. sinjiensis was obtained by con-

The 2.5m3 circular tanks (2 m in diameter and ca. version from the body length measurement, using the

0.8 m in water depth) were used in the larval rearing length-width relationship determined from 120 indi- experiment. The tanks were filled with sand-filtered viduals in the rearing tank. Likewise, the lorica width sea water (salinity 32 ppt), and supplied with the of rotifers was determined from the length-width re- green algae, Nannochloropsis sp. at a density of 60 •~ lationship established from 100 individuals. The de-

104 cells/ml and a chemical fertilizer (composition: gree of fullness of the gut of red snapper larvae was

78.1% KNO3, 7.8% NaH2PO4, 3.9% Na2SiO3, 2.4% described by the following gut fullness index: 0, food

FeC12 and 7.8 % Nat EDTA) at 91 g/m3 on May 5, absent; 1, food less than 10 % of total gut capacity; 2,

1993. At night of the same day, copepodids of Acartia food 10-50% of total capacity; 3, food 50-80% of total sinjiensis was collected from a 2.5 ha earthen pond at capacity; 4, food 80-100 % of total capacity, the gut

EMDEC using a light trap21), and introduced to the having no empty spaces; 5, gut overfull, determined tanks as brooders for nauplii propagation. The stock- from the smooth, stretched gut surface. The electivity Acartia nauplii, initial food for fish larvae 33

of larvae toward different food organisms was calcu- velopmental stage, without any overlapping of body lated using IVLEV's equation23) for food electivity. lengths between the stages, identification of naupliar In this paper, days are numbered from the time of stages could be determined from body length, in addi- initial mouth opening of the red snapper larvae, which tion to appendage morphology, although slight overlaps occurred on May 8 (=day 0). in body width were seen between more advanced

stages. Results The lorica length and width of the rotifers were

Size and propagation of food organisms 0.150•}0.020 and 0.117•}0.016 mm (mean•}SD, n =100) The organisms occurring in the experimental tanks ,respectively, the relationship being expressed throughout the experimental period comprised mainly as W=0.712L+0.0107(r=0.758) (Fig.l).Rotifer the copepod, Acartia sinjiensis and the rotifer, body width was greater than that of A. sinjiensis of the

Brachionus sp. which together accounted for about 98 % same body length. of the total number of individuals. Other organisms By day 0, adult A. sinjiensis had propagated in the found in the tanks were nauplii of both Oithona sp. and tank. The abundance of nauplii was 347 individuals/l Balanus sp. on day 0 and 486 individuals/l on day 1(Fig.2).The

The mean body length and width of A. sinjiensis nauplii increased as the naupliar stage advanced, from

0.101 •~ 0.051 mm (n=20) at stage 1 (N-1) to

0.248•~0.123 mm (n=20) at N-6 (Fig.l).The

Fig.2.Changes in abundance (individuals/l) of Acartia sinjiensis nauplii (solid circles) and Brachionus sp. (open triangles) in the 2.5 m3 larval rearing tank.

density then decreased gradually to 11 individuals/l

Fig.1.Relationships between body length and width on day 5. Of the different developmental stages occurr- of Acartia sinjiensis nauplii (solid circles) and ing in the tank, nauplii at N-2 were most abundant on lorica length and width of Brachionussp. (open day 0, accounting for 47 % of the total number of nau- circles, n =100) used in the study. Solid circles plii, followed by N-3 (16 %) and N-1 (14 %). The and bars indicate stage specific means and abundance of copepodids was 73 individuals/l on day ranges of the nauplii (n=20 for each stage, 2, thereafter remaining steady at 25-39 individuals/l N-1-N-6). Some of the points for Brachionus sp. represent multiple measurements. till day 5. The abundance of rotifers increased from 69 stage-specific means fitted well to the regression W= individuals/l on day 0 to 114 individuals/l on day 2 0.510L+0.0007 (r=0.993). Because the linear in- (Fig.2). Following the additional supply of rotifers crease in body size was closely correlated with de- on day 2 (after the monitoring of rotifer abundance 34 M.Doi et al. (1997)

Fig.3.Changes in total length (A) and mouth width (B) of larval Lutjanus argentimaculatus reared in the 2.5 m3 tank. Means and ranges are shown.

for the day), the abundance increased to 557 increase in width during days 1 and 2, after which it

individuals/l on day 4, but subsequently declined to increased linearly, reaching 0.300•}0.041 mm (n=10)

189 individuals/i on day 5. on day 4.

Survival and growth of red snapper larvae Feeding of larvae The hatching and survival rates from hatching (day The feeding incidence rate (percentage of larvae -2) to the onset of feeding (day 0) were low (about 40 % and 50 %, respectively), with about 1, 000 larvae being estimated as surviving until day 0 in each tank. However, the number of larvae per tank was calculated as 800-1, 200 on days 2 and 4, indicating high survival rates, nearly 100 %, after the onset of feeding.

At 08 :00 on day 0, larvae measured 2.84•}0.06 mm

TL (mean•}SD, n=20; Fig. 3A), growing to 2.90•}

0.01 mm TL (n=11) by 17:00 on the same day. Lar- val length almost did not increase during days 1 (2.90

•} 0.01 mm TL, n=20, at 07:00) and 2 (2.95•}0.01 mm TL, n=11, at 10 : 00), but subsequently acceler- ated, attaining 3.38•}0.09 mm TL (n=12) on day 5.

By 03:00 on day 0, the mouth had opened in about

50 % of the larvae. The mouth width, measured at

08:00 on the same day, was 0.166•}0.010 mm (mean Fig. 4. Feeding incidence (% of larvae with food in •} SD, n =10; Fig. 3B), increasing to 0.188•}0.008 mm gut; solid circles) and mean index of gut fullness (n=10) at 14:00 on the same day and 0.224•}0.017 (see, text; open circles) in larval Lutjanus argen- mm (n=10) at 07:00 on day 1. Mouth opening did not timaculatus. Acartia nauplii, initial food for fish larvae 35 with food in the gut) was 0 % (n = 20) at 08 :00 on increased to 7.2 on day 2 (n ii), subsequently de- day 0 (5 hours after mouth opening in about 50 % of creasing gradually to 1.7 on day 5 (n=12). larvae). The rate then increased abruptly to 87.5 % (n Rotifers were first observed in the larval gut on day =16) by 11:00 and 90.9% (n=11) by 17:00 on the same day (Fig. 4). The feeding incidence rate was 100 % at 10:00 on day 1 and thereafter (n=11-20). The mean gut fullness index was 2.50 (n=16) at 11:00 and 2.95 (n=11) at 17:00 on day 0, and 2.81 (n=20) at 07:00 and 3.75 (n=12) at 10:00 on day 1 (Fig.4). The index maintained a level greater than 3.3 in all observations made at 10 : 00 on days 2-5 (n= 11-12). Throughout the experimental period, the gut contents comprised almost entirely of A. sinjiensis nauplii and rotifers. Occasional other items found were eggs of the above two species. Copepodids of A. sinjiensis were not found in the gut contents until the end of the experiment (day 5). At 11:00 and 17:00 on day 0, the gut contents of Fig. 5. Average numbers (individuals/larva) of Acar- larvae consisted solely of A. sinjiensis nauplii (mean tia sinjiensis nauplii (solid circles) and 2.1 (n=16) and 3.4 (n=11) individuals/larva, Brachionus sp. (open triangles) observed in gut respectively) (Fig. 5). The number of nauplii per gut of larval Lutjanus argentimaculatus.

Fig. 6. Frequency distribution (individuals/larva) of body width of Acartia sinjiensis nauplii (open areas) and Brachionus sp. (shaded areas) ingested by larval Lutjanus argentimaculatus. 36 M. Doi et al. (1997)

Table 1. Ivlev's food electivity index toward Acartia sinjiensis nauplii and Brachionus sp. in Lutjanus argentimaculatus larvae

1 Numbers in parentheses indicate number of larval specimens examined . 2 N ot available.

3 (mean 0.92 individuals/larva, n=12) (Fig. 5). 0.73 and 0.87 on days 4 and 5, respectively, Subsequently, the number of rotifers ingested in- The mean lorica width of rotifers ingested was creased exponentially, reaching 3.75 (n=12) and 0.112 mm (range 0.10-0.15 mm, n=11) on day 3 8.92 individuals/larva (n=12) on days 4 and 5, and 0.116 mm (range 0.09-0.15 mm, n = 152) on respectively. days 4 and 5 (Fig. 6). Although there were no statis- The body size of A. sinjiensis nauplii in the larval tical differences between the mean lorica width in- gut increased with larval growth (Fig. 6). The mean gested on days 3-5 (ANOVA, p > 0.05), the mode body width was 0.058 mm (range 0.05-0.08 mm, n- changed from 0.10 mm on day 3 to 0.12 mm on days 4 70) on day 0, thereafter increasing to 0.064 mm and 5 (Fig. 6). The mode of lorica width on days 4 and (range 0.05-0.09 mm, n=79) on day 1, 0.065 mm 5, 0.12 mm, was equivalent to the mode for rotifers in (range 0.05-0.09 mm, n=79) on day 2, 0.074 mm the tank water, indicating that the larvae on day 3 (range 0.05-0.10 mm, n=75) on day 3, 0.068 mm tended to feed on relatively small sized rotifers. (range 0.05-0.10 mm, n=44) on day 4 and 0.065 The food electivity index for rotifers was -1.0 (no mm (range 0.05-0.08 mm, n=19) on day 5, respec- feeding) on days 0-2, -0.63 on day 3, -0.25 on day 4 tively. Based on the linear relationship between body and 0.15 on day 5 (Table 1). Although the index had size and naupliar stage and the size distribution pat- gradual positive increase, it was much lower than that terns shown in Fig. 1, the stage of the nauplii in the for A, sinjiensis nauplii, indicating that the larvae fed gut was considered to be mostly N-1 on day 0, N-2 on selectively on the latter, rather than on rotifers, days 1 and 2, N-2 to N-4 on day 3, and N-2 to N-3 on throughout the experimental period. days 4 and 5. Discussion Changes in the food electivity index indicated that the above advances in the size and stage of nauplii Preference of food organisms ingested were due to changes in larval preference The increases in size of the food organisms (Acartia toward larger and hence more advanced nauplii (Table sinjiensis nauplii and rotifers) ingested by the red 1). On day 0, the index was highest for N-l, 0.59 at snapper larvae (Fig. 6) and in mouth width of the lat- 11:00 and 0.55 at 17:00. The index for N-1 became ter (Fig. 3B) strongly suggested that the size of food negative on day 1, being -0.12 at 07:00 and -0.23 at organisms in relation to mouth size was the primary 10:00, and remained so on days 3-5, from -0.36 to factor in the selection of food organisms by the larvae, -0 .79. In contrast, electivity to N-2 shifted from as in the seabream, Archosargus rhomboidalis24), turbot, essentially neutral on day 0 (-0.02 at 11:00 and 0.01 Scophthalmus muximus25), gilt-head seabream, Sparus at 17:00), to positive, 0.41-0.45 on days 1-3 and aurata26) and many other marine fish larvae15,27) Acartia nauplii, initial food for fish larvae 37

Nevertheless, the red snapper larvae showed a strong been able to seize early nauplii, but not advanced ones preference toward advanced A. sinjiensis nauplii (N-4 or rotifers, at the onset of feeding. Although the mouth and N-5) rather than rotifers on days 3 and 4 (Table width of the larvae was larger than the width of the 1), although their body sizes were nearly equal (Fig. nauplii and rotifers, the gape of the former seemed to 1). Factors involved in such electivity are considered have not been large enough for capturing advanced to include locomotory patterns of the prey28,29), body nauplii and rotifers, a situation similar to that sug- color and external morphology. Clarification however gested for early grouper larvae31,32) In fact, the mouth necessitates further detailed observations. width of the red snapper larvae at the onset of feeding In the present study, the larvae had started to feed observed in this study (0.166-0.188 mm) was small on rotifers from day 3, at a time when the density of compared with other species for which larval rearing available A. sinjiensis nauplii had declined, but that of is conducted using only rotifers (e. g., 0.224 mm in rotifers had increased (due to the additional supply). seabass, Lates calcarifer33); 0.258 mm in milkfish, Cha- In case when the density of nauplii had been main- nos chanos34)), even considering the possible effect of tained at a higher level, the larvae might have fed them formalin-preservation on the mouth size measurement. on more often, if not solely, on and after day 3. Although the present rearing experiment was on a small and preliminary scale, the findings demonstrated Availability of Acartia for initial larval feeding that the early larvae of red snapper, and most prob- In our four previous attempts to rear red snapper ably those of other species with a relatively small larvae using rotifers, high mortalities occurred during mouth size at the time of initial mouth opening, such as the first few days, not only before but also after the grouper, Epinephelus fuscoguttatus (0.193 mm5)) and onset of larval feeding, resulting in the nearly complete rabbitf ish, Siganus guttatus (0.168 mm35)), can be extinction of the larvae by around day 3 (= 5 days reared successfully if early stage nauplii of A. sinjien- after hatching). Bonlipatanonl) also reported high mor- sis or other Acartia species are provided for the first talities occurring in red snapper larvae fed with few days prior to rotifer feeding. rotifers, the rate of larvae with rotifers in the gut Acknowledgments being 0-66.7% on day 1. All larvae died by day 13 in nine of his 28 rearing experiment replicates. We wish to thank Dr. G. Hardy, Thames, New On the other hand, in the present study in which red Zealand, for his critical review of the manuscript. This snapper larvae were provided with both A. sinjiensis study was supported partly by the Japan International and rotifers, the larvae showed high survivorship after Cooperation Agency. the commencement of feeding, preying solely upon A. References sinjiensis nauplii during the first three days, shifting gradually from smaller, earlier nauplii to larger, more 1) Bonlipatanon, P. (1988): Study of red snapper advanced ones. The larvae started feeding at the latest (Lutjanus argentimaculatus Forsskð¡l) spawning in some eight hours after their initial mouth opening. All captivity, in •gReport of Thailand and Japan Joint individuals examined had significant numbers of nau- Coastal Aquaculture Research Project, No. 3•h, plii in the gut on and after day 1 (Figs. 4 and 5), National Institute of Coastal Aquaculture, Thai- although the density of nauplii in the rearing tank land, and Japan International Cooperation Agency,

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ゴマフエダイ仔魚、の初期餌料としての Acartia sinjiensisノープリウスの有効性

土居正典1)・大野淳1)・多紀保彦1)・

Tanin Singhagraiwan2)・河野博1)

(1)東京水産大学・2)タイ国東部海洋漁業開発センター)

海産コペポーダAcartia sinjiensis8のノープリウスとワムシが同時に存在する環境下でゴマフエダイ仔魚の初期摂餌状況を観察した。仔魚の開口日およびその後2日間(day 0-2)の消化管内容はすべてA .sinjiensisのノープリウス(平均2.1-7.2個体/尾)であった。摂餌されたノープリウスの平均体幅はday 0で0.058mmであり,以後仔魚の成長とともに増大した。ワムシ(平均被甲長0.117mm)に対する摂餌はday 3より観察され(平均0.92個体/尾),day 4およびday 5において摂餌量は急増した。開口日におけるゴマフエダイ仔魚の口幅(0.166-0.188mm)は,ノープリウスやワムシの体幅より大きいとは言え,従来よりワムシのみで飼育されている他の海産魚の口幅より小さい。このことが初期摂餌の制限要因となり,結果的に摂餌開始時の餌生物が若齢ノープリウスに限定されたものと思われる。仔魚は開口日の平均全長2.84mmからday 5の3.38mmに成長し,この間のへい死率は低かった。A.sinjiensisのノープリウスはゴマフエダイおよび本種と同様の小さい口径をもつ他の海産仔魚飼育における有効な初期餌料となり得る。