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Effects of different illumination levels on Zooplankton abundance, feeding periodicity, growth and survival of the Asian sea bass, Lates calcarifer (Bloch), fry in illuminated floating nursery cages
Aquaculture ELSEVIER
Aquaculture 157 (1997) 227-237
Effects of different illumination levels on zooplankton abundance, feeding periodicity, growth and survival of the Asian sea bass, Lates calcarifer (Bloch), fry in illuminated floating nursery cages Armando C. Fermin Southeast Asian Fisheries Decelopment
*,
Glendell A. Seronay
Center Aquaculture Department Iloilo, Philippines
(SEAFDEC/
AQDI, Tighauan 5021.
Accepted I I June 1997
Abstract The effects of different illumination levels on zooplankton abundance and feeding periodicity, growth and survival of hatchery-produced Asian sea bass, L.ures calcarifer, fry in illuminated floating net cages were determined in a 35day experiment. Zooplankton abundance (consisting mainly of copepods at 64-78% of total abundance in all cages) was highest in cages illuminated at 180 Ix (mean: 124 individuals I- ‘> and at 300 Ix (mean: 405 individuals I ‘> and peaked at 0400. High prey densities subsequently resulted in increased fish feeding as evidenced by the greatest number of prey (mean: 416-462 individuals fish- ’ > found in their guts between 0400 and 0800. Feeding incidence (range: 84-89%) was generally higher among fish held in illuminated cages than those reared in dark cages (67%). Low feeding of fish held in dark cages eventually led to starvation and mass mortality. The present results indicate that a light intensity of at least 300 Ix attracts the highest number of zooplankton and promotes the best weight specific growth rate (10% day ‘) and survival (40%) in sea bass juveniles reared in illuminated nursery cages. 0 1997 Published by Elsevier Science Ltd. Kexvvvrds: Illuminated cage nursery; Lcltes calcar(fer; Light intensity: Natural zooplankton
* Corresponding author. 0044~84X6/97/$17.00 PII SOO44-8486(97)00
0 1997 Published by Elsevier Science Ltd. All rights reserved. 167-l
228
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157 (19971 227-237
1. Introduction Illumination influences the biology and behavior of many teleosts larvae and juveniles (Holanov and Tash, 1978; Tandler and Helps, 1985; Mills et al., 1986; Duray and Kohno, 1988; Stefansson et al., 1990; Mookerji and Rao, 1993; Gehrke, 1994; Huse, 1994; Barlow et al., 1995). Most planktivorous fish are visual feeders that are limited to feeding in daylight and twilight (Holanov and Tash, 1978). Mills et al. (1986) observed that young yellow perch, Perca jlauescens, fed on large daphnids under low light intensity and shifted to smaller prey as light intensity increased. The growth of European sea bass, Dicentrarchus labrax, larvae was maximal when photoperiod was extended up to 18 h but highest survival was attained at 12-h light (Barahona-Femandes, 1979). Barlow et al. (1995) observed that Asian sea bass, Lutes calcarifer, juveniles have a distinct and constant daytime feeding pattern that ceases totally during darkness. Wild (Davis, 1985; Russel and Garrett, 1985; Patnaik and Jena, 1976) or pond-reared (Barlow et al., 1993) young sea bass are particulate visual feeders that prey selectively on marine zooplankton such as rotifers, copepods and cladocerans. In other studies however, fish larvae have been reared in illuminated nursery cages installed in open waters using light to attract zooplankton as food source (Mamcarz and Szczerbowski, 1984; Szczerbowski and Mamcarz, 1984; Rosch and Eckmann, 1986; Champigneulle and Rojas-Beltran, 1990; Mamcarz and Kozlowski, 1992; Mamcarz, 1995). This nursery technique was recently adopted in the rearing of hatchery-produced Asian sea bass, L. calcarifer, larvae to juvenile stage. Indeed, preliminary experiments indicated that fish grown in cages illuminated for 12 h during the night had significantly better growth and survival than those reared in the unlit control cages and fed chopped fish flesh (Fermin et al., 1996). The presence of light did not only attract sufficient quantities of wild zooplankton that satisfied the food requirements of the fry but also enabled the fish to locate and efficiently prey on these planktonic food. Similar studies in the past have indicated that artificial light during the night significantly increased zooplankton densities in illuminated cages compared with unilluminated areas (Szczerbowski and Mamcarz, 1984; Mamcarz, 1995). The present study was designed to determine the effects of different illumination levels on zooplankton abundance, feeding periodicity, growth and survival of hatchery-produced Asian sea bass, L. calcarifer, fry held in illuminated nursery cages.
2. Materials and methods The study was conducted at the SEAFDEC Igang Marine Substation, Nueva Valencia, Guimaras Province (Panay Island). Four illumination levels, i.e., 0 (dark), 20, 180 and 300 lx in six replicates were used as experimental treatments. The cages were made of black nylon net of 5-mm mesh measuring 1 X 1 X 1.5 m each and suspended from Styrofoam-floated bamboo rafts. The cages were submerged at l-m water depth. Each treatment group was positioned approximately 3-4 m apart from each other and was enclosed with black plastic sacks placed vertically at 1 m above and below the water surface. Of the six replicates per treatment, four cages were stocked each with 500
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157 (1997) 227-237
229
hatchery-reared sea bass fry (mean total length (TL) = 11.14 mm; wet body weight (BW) = 20.81 mg) while the other two cages were left unstacked and used exclusively for sampling zooplankton. Each cage was illuminated continuously during the normal dark period (1800-0600) with incandescent bulbs installed approximately 0.5 m above the water surface. Average illumination level was computed based on three readings of a portable digital light meter (Minolta, Japan) taken near the water surface inside the cage. Water samples were obtained weekly with a Kemmerer vertical sampler (2. I-1 capacity) starting at 1600 of one day and continuing until 1200 of the following day at 4-h intervals. Water samples were obtained about lo-20 cm below the water surface and near the bottom of each cage. Samples were pooled and then passed through a 150 pm plankton net. The filtered zooplankton were then fixed in 5% (v/v) buffered Formalin solution. Zooplankton were counted and identified to the genus level using a light microscope. During the course of the study, water temperatures ranged from 28 to 32°C salinities varied from 34 to 37%0. Dissolved oxygen levels (3.1-6.8 ppm) were within acceptable limits for fish culture. Fish growth was monitored weekly by measuring the total length and body weight of 5- 10 fish sampled from each cage and fixed in 10% (v/v) buffered Formalin solution. During each sampling, however, ‘shooters’ or cannibals which had a minimum size difference of approximately 33% (Parazo et al., 1991) from the rest of the stocks were removed without replacement in an attempt to minimize cannibalism-induced mortalities (Fermin et al., 1996). The same number of fish sampled weekly for growth was dissected for analysis of ingested food items which were counted and classified using a light microscope whenever possible according to genus. Percentage composition (number of food items of a given food type as a percentage of the total number of food items) of individual prey items and percentage composition by volume based on taxa groupings were determined (Schmitt, 1986). Percent survival was determined by dividing the remaining number of fish in each cage by the total number of fish stocked initially excluding the samples and shooters taken weekly then multiplied by 100. Cages were replaced with clean ones after each sampling. Used cages were brushed thoroughly to remove algae that clogged the mesh and dried under the sun. Die1 mean zooplankton abundance was normalized by log + 1 transformation prior to two-way analysis of variance, while fish data were analyzed by a one-way analysis of variance using the SAS statistical package (SAS Institute Incorporated, 1991). Significant differences among treatment means were compared by Duncan’s multiple range test at 5% probability level.
3. Results 3.1. Zooplankton
abundance
Mean zooplankton abundance in illuminated cages increased with time during the dark part of the die1 sampling period unlike in the unilluminated cages (Fig. 1). Higher zooplankton densities were observed at 0400 in cages illuminated at 180 lx and at 300 lx with mean counts ranging from 124-405 individuals l-‘, respectively (F value = 4.3,
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0 1600
2000
2400
0400
0800
1200
Sampling time (h) Fig. I. Die1 zooplankton abundance in floating net cages illuminated each bar represent standard error of the mean (SEM).
at different
levels. Vertical lines above
df = 95, P < 0.05). Lower zooplankton densities were observed in dark cages that ranged from 26 to 41 individuals 1-l and did not show significant variations at different sampling times (P > 0.05). Prey densities (13-69 individuals 1-l) in all cages during daytime (OSOO- 1600) were generally low. Copepods were most abundant and accounted for 64-78% of the total zooplankton counts obtained from all cages (Table 1). The highest density of 169 individuals 1-l was found in cages illuminated at 300 lx but this did not differ from those at 180 lx with 105 individuals 1~ ’ (P > 0.05). Significantly lower copepod densities of 33 and 36 individuals 1-l were sampled in cages illuminated at 20 and 0 lx, respectively (P < 0.05). Among the copepods (excluding the nauplii), higher densities of cyclopoids occurred (range: 62- 133 individuals 1~ ’ > in 180 and 300 lx-illuminated cages, respectively. 3.2. Feeding periodicity Gut content analysis in fish reared in illuminated cages indicated a generally higher feeding between 0400 and 0800 than at other times of the day (Fig. 2). Mean feeding incidence (range: 84-88%) was similar among fish reared in illuminated cages and were significantly higher than those fish held in dark cages (67%) (P < 0.05, Table 2). The highest total mean number of ingested zooplankton at 462 individuals fish-’ was obtained at 0800 h in fish reared in 300 lx-illuminated cages (F value = 37.33, df = 126, P < 0.05, Fig. 2). Comparatively, fish held in dark cages ingested significantly less zooplankton, although more prey were ingested during daytime (13-26 prey
A.C. Fermin, G.A. Seronag/Ayuaculruree Table 1 Ranges and means Maximal abundance
157 (1997) 227-237
231
of light-attracted zooplankton in floating nursery cages different illumination levels. (average no. I-’ ) were observed at 2000 h in 20 lx and at O400 in 180 lx and 300 lx
Taxon
Illumination,
level (lx)
0 Range Decapods Brachyurans Anomurans/Pagurids
20 Mean
nil nil nil
180
Range
Mean
nil nil nil
nil
0.5-7.8 0.7-48.3 0.3-3.2 9.2-32.7
3 13 1 15
Range
0.5-48.2 nil
300 Mean nil 15
Range
Mean
0.2-46 0.3-1743.5
12 436
6-20.7 4.8-240.3 1.3-10
12 133 4 20
Copep0d.c Calanoids Cyclopoids Harpacticoids Nauplii
0.7-13.6 0.6-107.0 0.2-5.8 2.4-48.3
Fish larvae Polychaetes Balanus (Barnacle Dinoflagellates Pteropods Oikopleurans Tintinnids Nematodes Isopods
nil 0.2-4.3 1.1-42.7 nil I-20.9 nil 0.1-3.4 nil nil
nauplii)
4 14
1 17
1 10 5 2
nil 0.2-1.8 1.7-13.5 nil 0.8-11.3 nil nil nil nil
2.5-38.3 13.7-104 0.8-2.5 8.7-42 nil 0.2-7.0 3.8-31.3 nil 3.7-27.3 nil 0.2-2.2 nil nil
1 5 6
13 62 2 28
3 21 15 1
1.5-34.5 nil 0.8-2.2 0.8-34.7 nil 5.7-14.7 nil nil nil nil
I
20 12
700
600
i
500
2 ._ d Q 3 :: :: % k 2 t
400
300
200
100
0 1600
2000
2400
0400
0800
1200
Sampling time (h)
Fig. 2. Die1 feeding activity of sea bass (L. calcarifer) fry-reared in floating net cages illuminated at different levels. Data are averages of ingested zooplankton fishh’ sampled weekly within a 35-day culture period. Vertical lines above each bar represent SEM.
232 Table 2 Percentage in floating
A.C. Fermin, G.A. Serona,v/Aquuculrure
157 11997) 227-237
composition by number of various food items in the stomach of sea bass, L. calcarifer, nursery cages at different illumination levels
Taxon
Illumination 0
level (lx) 20
Brachyurans Anomurans
nil nil
2 8
Copepods Polychaetes Pteropods Rotifers
67 nil 2 nil
89 nil nil nil
Decapods Tintinnids
nil 29 21 51 67
nil ND
Total zooplankton ingested fishFish examined, no. “Mean feeding incidence, %
’
fry-reared
147 110 86
“Mean feeding incidence = (Total number of fish with food in their gut/Total ND = No data.
180
300
3 9 81 nil nil nil 7 ND 126 105 89
3 18 75 nil nil nil 3 ND 356 101 84
number of fish examined)x
100.
fish-‘) than at nighttime (2-4 prey fish-‘). In general, copepods were most commonly ingested by fish in all cages ranging from 21 individuals fish-’ (dark cages) up to 173 individuals fish-’ (300 Ix).
‘h a B z %
35 20 24 20 16 12 a 4 0 0
20 Illumination
180
300
level (lux)
Fig. 3. Changes during 35 days in mean total length (A) and wet body weight (B) of sea bass (L. cnlcar~r) fry-reared in floating net cages illuminated at different levels. Vertical lines above each bar represent SEM.
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157 (1997) 227-237
233
25 -
0’
, 0
I
/
I
I
I
7
14
21
20
35
Rearing period (days)
700
,
600
500 !
-o--
0 IIJX
-m-A-v-
20 Iux 18OlUX 300 Iux
L-!
ij 8
4oo
P 8 d B 9
300 -
200 -
o4
100 -
0
7
14
21
28
35
Rearing period (days)
Fig. 4. Mean specific growth rates (SGR) (‘7~ day-‘) and percent survival of sea bass (L. calcarifrr) fry-reared in floating net cages illuminated at different levels. Vertical lines above each bar represent SEM.
3.3. Fish growth and suruiual Throughout the 35-day culture period, growth of fish reared in 300 lx-illuminated cages was significantly better than those at lower illumination levels (F value = 128.58
234
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157 (1997) 227-237
for length, 52.94 for weight, df = 130, P < 0.05, Fig. 3A and B). At 180 lx, fish grew similarly with those held at 20 lx during the first 14 days of culture but not after 21 days. On the 28th day of culture, growth was even comparable with fish reared in 300 lx-illuminated cages. Experiments in the dark cages were terminated on the 4th week of rearing due to heavy fish mortalities. Weight specific growth rate (10% day- ‘> and percent survival (40%) of fish reared in 300 lx-illuminated cages were significantly higher than those fish held in cages illuminated at 20 or 180 lx (P < 0.05, Fig. 4).
4. Discussion Zooplankton abundance and fish feeding periodicity in sea bass fry-reared in illuminated floating nursery cages were influenced by illumination levels. At the highest illumination levels of 300 lx, zooplankton were most abundant similar with those found at 180 lx-illuminated cages, with maximal densities (up to 653 1-l) occurring between 2000 and 0400. Of the several zooplankton groups identified, copepods were the most abundant in all cages. Copepod adult and nauplii abundance in cages illuminated at 300 lx showed a 5-fold increase over unilluminated areas. The present data were consistent with the study by Fermin et al. (1996) who obtained a 5-6-fold increase in copepod and nauplii abundance in illuminated nursery cages. In a similar study done in a freshwater lake, Szczerbowski and Mamcarz (1984) observed a 1.4-fold increase in the major groups of natural zooplankton such as rotifers, copepods and cladocerans in the presence of artificial light during the night compared to those obtained from unilluminated areas. Mamcarz (1995) also recently reported copepod densities in illuminated cage zones that were 7-8 times higher than those in the unilluminated areas. In contrast, zooplankton abundance in cages illuminated at 20 lx had a slight die1 change while those cages held in the dark did not exhibit significant die1 variations. During daytime from 0800 until 1200, light-attracted zooplankton presumably disperse out in the open area as densities in the illuminated cage groups were observed to significantly decrease. Because copepods occurred in greatest number among zooplankton groups, these microcrustaceans were the most dominant prey in the diet of sea bass fry-reared in illuminated cages. Studies have indicated that rotifers, copepods, and cladocerans are the most preferred food prey of sea bass juveniles (Patnaik and Jena, 1976; Davis, 1985). Under pond nursery conditions 53-85% of sea bass fry IO-14 mm TL fed on copepods (Barlow et al., 1993). Increased zooplankton densities and the presence of light in illuminated cages had a profound effect on fish feeding. Gut content analysis showed significant increases in the number of ingested zooplankton that correspond to the increase in prey densities. Sea bass fry are particulate feeders, feeding continuously during the day but cease during the night (Barlow et al., 1993) and that the presence of light enables them to locate their food (Barlow et al., 1995). Sea bass fry exposed to continuous lighting consumed 40% more food than the fish in the 12L/12D light regime (Barlow et al., 1995). In the age-0 yellow perch, P. jihuescens, low light intensity (< 230 lx) limits the size range of available prey, resulting in the alteration of fish feeding efficiency and growth (Mills et al., 1986). At a light intensity above 230 lx, prey size selection becomes independent of
A.C. Fermin, G.A. Srronay/Aquaculture 157 (1997) 227-237
235
zooplankton abundance and depended mostly on fish size. Huse (1994) observed a maximal feeding percentage of more than 90% in turbot, Sc@zthalmus muximus, at 860 lx compared to the much lesser feeding percentage at 12 lx. The absence of light in dark cages limits the availability of zooplankton prey and both factors cause restriction in fish feeding. Food restriction is evidenced by the lower feeding incidence of sea bass fry held in dark cages compared to those reared in illuminated cages. The rate of feeding at night is affected by the amount of light available as suggested by Forrester et al. (1994). The same workers noted that despite a significant increase of drifting invertebrates during the night, there was no corresponding increase in food consumption after dark by the brook charr (Suluelinus fontinalis). According to Stefansson et al. (1990), continuous or extended daylength increased feeding activity and growth of Atlantic salmon, Salmo salar, while short daylength caused a restricted feeding time that resulted in the inhibition of growth. The feeding and swimming activities of European sea bass larvae stopped during long dark periods (9L/ 15D) as compared to fish reared in constant daylight (24L) (Ronzani-Cerqueira and Chatain, 1991). In the present experiment, unilluminated conditions led to fish starvation and eventually mass mortality. A hypothesis was then defined by Huse (1994) that the preferred illumination level during fish feeding activity is reflective of the vertical positioning strategy of the species. For example, the surface-oriented young turbot S. maximus feed at the highest illumination levels up to 860 lx as opposed to the dusk/dawn-feeding cod, Gadus morhua, larvae which prefer to feed under low light intensities (0. 1- 1.O lx) (Huse, 1994). Because of the limited illumination gradients used, the optimal illumination level for sea bass nursery in sea cages can not be drawn basing on the present results. However, a light intensity of at least 300 lx attracted the highest natural zooplankton abundance consisted mainly of copepods that have sufficiently met the food requirements for promoting growth and survival of seabass fry reared in illuminated nursery cages. Sufficiency of food prey and the presence of light during the normal dark period are important factors in the successful rearing of sea bass fry in illuminated floating sea cages. Artificial illumination enhances visibility of light attracted-zooplankton that may have influenced feeding of fish held in illuminated cages. Sea cages are inexpensive and adaptable to any site which could be of great interest for isolated or small nursery farms (Nehr et al., 1996). The present data further support our previous results which concluded that illuminated nursery cage rearing can be a better alternative to the traditional practice of sea bass fingerling production in pond or in ordinary net cages.
Acknowledgements We thank the International Foundation for Science and the Asian Fisheries Society for jointly funding this project (IFS/AFS Research Grant No. A/2078-1 awarded to A.C.F.). Thanks are also due to all the staff of the SEAFDEC Igang Marine Substation for their cooperation and support during the course of the experiments and to E. Bolivar and S.B. Balad-on for zooplankton analysis. We are grateful to Mr. L.M.B. Garcia for editing the manuscript in draft form and the two anonymous reviewers for their
236
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157 (1997) 227-237
constructive comments and suggestions. Special thanks are due to Prof. Dr. Andrzej Mamcarz of the Olsztyn University of Agriculture and Technology Department of Fisheries, Olsztyn-Kortowo, Poland who provided us helpful ideas in the conduct of the experiments.
References Barahona-Fernandes, M.H., 1979. Some effects of light intensity and photoperiod on the seabass (Dicentrarchus labrax L.) larvae reared at the Center Oceanologique de Bretagne. Aquaculture 17, 3 11-32 1. Barlow, C.G., Rodgers, L.J., Palmer, P.J., Longhurst, C.J., 1993. Feeding habits of hatchery-reared barramundi Lates calcarifer (Bloch) fry. Aquaculture 109, 131-144. Barlow, C.G., Pearce, M.G., Rodgers, L.J., Clayton, P., 1995. Effects of photoperiod on growth, survival and feeding periodicity of larval and juvenile barramundi Latescalcarifer (Bloch). Aquaculture 138, 159-168. Champigneulle, A., Rojas-Beltran, R., 1990. First attempts to optimize the mass rearing of whitefish (Coregonus lauarefus L.) larvae from Leman and Bourget Lakes (France) in tanks and cages. Aquatic Living Resources 3, 217-228. Davis, T.L.O., 1985. The food of barramundi, Lares calcarifer (Bloch), in coastal and inland waters of Van Diemen Gulf and the Gulf of Carpentaria. Aust. J. Fish Biol. 26, 669-682. Duray, M.N., Kohno, H., 1988. Effects of continuous lighting on growth and survival of first-feeding larval rabbitfish, Siganus guttatus. Aquaculture 109, 31 l-321. Fermin, A.C., Bolivar, M.E.C., Gaitan, A., 1996. Nursery rearing of the Asian sea bass, I.&es calcarifer, fry in illuminated floating net cages with different feeding regimes and stocking densities. Aquatic Living Resources 9, 43-49. Forrester, G.E., Chace, J.G., McCarthy, W., 1994. Die1 and density-related changes in food consumption and prey selection by brook charr in a New Hampshire stream. Environ. Biol. Fishes 39, 301-31 I. Gehrke, P.C., 1994. Influence of light intensity and wavelength on phototactic behavior of larval silver perch, Bidyanus bidyanus, and golden perch, Macquaria ambigua, and the effectiveness of light traps. J. Fish Biol. 44, 741-751. Holanov, S.H., Tash, J.C., 1978. Particulate and filter feeding in threadfin shad, Dorosoma petenense, at different light intensities. J. Fish Biol. 13, 619-625. Huse, I., 1994. Feeding at different illumination levels in the larvae of three marine teleost species: cod, Gudus morhua L.; plaice, Pleuronectes platessa L.; and turbot, Scopthalmus maximus L. Aquacult. Fish. Manage. 25, 687-695. Mamcarz, A., 1995. Changes in zooplankton structure around illuminated cage culture. Aquaculture Res. 26, 515-525. Mamcara A., Kozlowski J., 1992. Rearing peled (Coregonus peled Gmel.) larvae in illuminated cages with supplemental utilization of artificial feed. In: Todd, T.N., Lucynski, M.L. (Eds.), Biology and Management of Coregonid Fishes. Pol. Arch. Hydrobiol. 39, pp. 703-711. Mamcarz, A., Szczerbowski, J.A., 1984. Rearing of coregonid fishes (Coregonidae) in illuminated cages: I. Growth and survival of Coregonus lauaretus L. and Coregonus peled Gmel. Aquaculture 40, 1355145. Mills, E.L., Confer, J.L., Kretchmer, D.W., 1986. Zooplankton selection by young yellow perch: the influence of light, prey density, and predator size. Trans. Am. Fish. Sot. 115, 716-725. Mookerji, N., Rao, T.R., 1993. Patterns of prey selection in rohu (Labeo rohita) and singhi (Heteropneustes fossilis) larvae under light and dark conditions. Aquaculture 118, 85-104. Nehr, O., Blancheton, J.-P., Alliot, E., 1996. Development of an intensive culture system for sea bass (Dicentrarchus labrax) larvae in sea enclosures. Aquaculture 142, 43-58. Parazo, M.M., Avila, E.M., Reyes, D.M. Jr., 1991. Size- and weight-dependent cannibalism in hatchery-bred sea bass (Lutescnlcarifer, Bloch). J. Appl. Ichthyol. 7, 1-7. Patnaik, S., Jena, S., 1976. Some aspects of biology of L.ates calcarifer (Bloch) from Chilka Lake. Indian J. Fish. 23, 65-7 1.
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Ronzani-Cerqueira, V., Chatain, B., 1991. Photoperiodic effects on the growth and feeding rhythm of European sea bass. In: Lavens, P., Sorgeloos, P., Jaspers, E., Ollevier, F. (Eds.), Fish and Crustacean Larviculture Symposium. European Aquaculture Sot., Spec. Pub]. 15, Gent, Belgium, pp. 304-306. Rosch, R., Eckmann, R., 1986. Survival and growth of prefed Gregonus lawretus L. held in illuminated net cages. Aquaculture 52, 245-252. Russel, D.J.. Garrett, R.N., 1985. Early life history of barramundi, Lutescalcarfer (Bloch), in northeastern Queensland. Amt. J. Mar. Freshwater Res. 36, 191-201. SAS Institute Incorporated, 1991. SAS Systems for Linear Models, 3rd edn. Guy, NC, 329 pp. Schmitt, P.D., 1986. Feeding by larvae of Hyxmtherina tropiculis (Pisces: Atherinidae) and its relation to prey availability on One Tree Lagoon, Great Barrier Reef, Australia. Environ. Biol. Fishes 16, 79-94. Stefansson, S.O., Nortvedt, R., Hansen, T.J., Taranger, G.L., 1990. First feeding of Atlantic salmon, Saltno salar L., under different photoperiods and light intensities. Aquacult. Fish. Manage. 21, 435-441. Szczerbowski, J.A., Mamcara, A., 1984. Rearing of coregonid fishes (Corigonidae) in illuminated lake cages: II. Environmental conditions during fish rearing. Aquaculture 40, 147-161. Tandler, A., Helps, S., 1985. The effects of photoperiod and water exchange rate on growth and survival of gilthead sea bream (Sparus auruta, Linneus; Sparidael from hatching to metamorphosis in mass rearing systems. Aquaculture 48, 7 l-82.
Aquaculture 157 (1997) 227-237
Effects of different illumination levels on zooplankton abundance, feeding periodicity, growth and survival of the Asian sea bass, Lates calcarifer (Bloch), fry in illuminated floating nursery cages Armando C. Fermin Southeast Asian Fisheries Decelopment
*,
Glendell A. Seronay
Center Aquaculture Department Iloilo, Philippines
(SEAFDEC/
AQDI, Tighauan 5021.
Accepted I I June 1997
Abstract The effects of different illumination levels on zooplankton abundance and feeding periodicity, growth and survival of hatchery-produced Asian sea bass, L.ures calcarifer, fry in illuminated floating net cages were determined in a 35day experiment. Zooplankton abundance (consisting mainly of copepods at 64-78% of total abundance in all cages) was highest in cages illuminated at 180 Ix (mean: 124 individuals I- ‘> and at 300 Ix (mean: 405 individuals I ‘> and peaked at 0400. High prey densities subsequently resulted in increased fish feeding as evidenced by the greatest number of prey (mean: 416-462 individuals fish- ’ > found in their guts between 0400 and 0800. Feeding incidence (range: 84-89%) was generally higher among fish held in illuminated cages than those reared in dark cages (67%). Low feeding of fish held in dark cages eventually led to starvation and mass mortality. The present results indicate that a light intensity of at least 300 Ix attracts the highest number of zooplankton and promotes the best weight specific growth rate (10% day ‘) and survival (40%) in sea bass juveniles reared in illuminated nursery cages. 0 1997 Published by Elsevier Science Ltd. Kexvvvrds: Illuminated cage nursery; Lcltes calcar(fer; Light intensity: Natural zooplankton
* Corresponding author. 0044~84X6/97/$17.00 PII SOO44-8486(97)00
0 1997 Published by Elsevier Science Ltd. All rights reserved. 167-l
228
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1. Introduction Illumination influences the biology and behavior of many teleosts larvae and juveniles (Holanov and Tash, 1978; Tandler and Helps, 1985; Mills et al., 1986; Duray and Kohno, 1988; Stefansson et al., 1990; Mookerji and Rao, 1993; Gehrke, 1994; Huse, 1994; Barlow et al., 1995). Most planktivorous fish are visual feeders that are limited to feeding in daylight and twilight (Holanov and Tash, 1978). Mills et al. (1986) observed that young yellow perch, Perca jlauescens, fed on large daphnids under low light intensity and shifted to smaller prey as light intensity increased. The growth of European sea bass, Dicentrarchus labrax, larvae was maximal when photoperiod was extended up to 18 h but highest survival was attained at 12-h light (Barahona-Femandes, 1979). Barlow et al. (1995) observed that Asian sea bass, Lutes calcarifer, juveniles have a distinct and constant daytime feeding pattern that ceases totally during darkness. Wild (Davis, 1985; Russel and Garrett, 1985; Patnaik and Jena, 1976) or pond-reared (Barlow et al., 1993) young sea bass are particulate visual feeders that prey selectively on marine zooplankton such as rotifers, copepods and cladocerans. In other studies however, fish larvae have been reared in illuminated nursery cages installed in open waters using light to attract zooplankton as food source (Mamcarz and Szczerbowski, 1984; Szczerbowski and Mamcarz, 1984; Rosch and Eckmann, 1986; Champigneulle and Rojas-Beltran, 1990; Mamcarz and Kozlowski, 1992; Mamcarz, 1995). This nursery technique was recently adopted in the rearing of hatchery-produced Asian sea bass, L. calcarifer, larvae to juvenile stage. Indeed, preliminary experiments indicated that fish grown in cages illuminated for 12 h during the night had significantly better growth and survival than those reared in the unlit control cages and fed chopped fish flesh (Fermin et al., 1996). The presence of light did not only attract sufficient quantities of wild zooplankton that satisfied the food requirements of the fry but also enabled the fish to locate and efficiently prey on these planktonic food. Similar studies in the past have indicated that artificial light during the night significantly increased zooplankton densities in illuminated cages compared with unilluminated areas (Szczerbowski and Mamcarz, 1984; Mamcarz, 1995). The present study was designed to determine the effects of different illumination levels on zooplankton abundance, feeding periodicity, growth and survival of hatchery-produced Asian sea bass, L. calcarifer, fry held in illuminated nursery cages.
2. Materials and methods The study was conducted at the SEAFDEC Igang Marine Substation, Nueva Valencia, Guimaras Province (Panay Island). Four illumination levels, i.e., 0 (dark), 20, 180 and 300 lx in six replicates were used as experimental treatments. The cages were made of black nylon net of 5-mm mesh measuring 1 X 1 X 1.5 m each and suspended from Styrofoam-floated bamboo rafts. The cages were submerged at l-m water depth. Each treatment group was positioned approximately 3-4 m apart from each other and was enclosed with black plastic sacks placed vertically at 1 m above and below the water surface. Of the six replicates per treatment, four cages were stocked each with 500
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229
hatchery-reared sea bass fry (mean total length (TL) = 11.14 mm; wet body weight (BW) = 20.81 mg) while the other two cages were left unstacked and used exclusively for sampling zooplankton. Each cage was illuminated continuously during the normal dark period (1800-0600) with incandescent bulbs installed approximately 0.5 m above the water surface. Average illumination level was computed based on three readings of a portable digital light meter (Minolta, Japan) taken near the water surface inside the cage. Water samples were obtained weekly with a Kemmerer vertical sampler (2. I-1 capacity) starting at 1600 of one day and continuing until 1200 of the following day at 4-h intervals. Water samples were obtained about lo-20 cm below the water surface and near the bottom of each cage. Samples were pooled and then passed through a 150 pm plankton net. The filtered zooplankton were then fixed in 5% (v/v) buffered Formalin solution. Zooplankton were counted and identified to the genus level using a light microscope. During the course of the study, water temperatures ranged from 28 to 32°C salinities varied from 34 to 37%0. Dissolved oxygen levels (3.1-6.8 ppm) were within acceptable limits for fish culture. Fish growth was monitored weekly by measuring the total length and body weight of 5- 10 fish sampled from each cage and fixed in 10% (v/v) buffered Formalin solution. During each sampling, however, ‘shooters’ or cannibals which had a minimum size difference of approximately 33% (Parazo et al., 1991) from the rest of the stocks were removed without replacement in an attempt to minimize cannibalism-induced mortalities (Fermin et al., 1996). The same number of fish sampled weekly for growth was dissected for analysis of ingested food items which were counted and classified using a light microscope whenever possible according to genus. Percentage composition (number of food items of a given food type as a percentage of the total number of food items) of individual prey items and percentage composition by volume based on taxa groupings were determined (Schmitt, 1986). Percent survival was determined by dividing the remaining number of fish in each cage by the total number of fish stocked initially excluding the samples and shooters taken weekly then multiplied by 100. Cages were replaced with clean ones after each sampling. Used cages were brushed thoroughly to remove algae that clogged the mesh and dried under the sun. Die1 mean zooplankton abundance was normalized by log + 1 transformation prior to two-way analysis of variance, while fish data were analyzed by a one-way analysis of variance using the SAS statistical package (SAS Institute Incorporated, 1991). Significant differences among treatment means were compared by Duncan’s multiple range test at 5% probability level.
3. Results 3.1. Zooplankton
abundance
Mean zooplankton abundance in illuminated cages increased with time during the dark part of the die1 sampling period unlike in the unilluminated cages (Fig. 1). Higher zooplankton densities were observed at 0400 in cages illuminated at 180 lx and at 300 lx with mean counts ranging from 124-405 individuals l-‘, respectively (F value = 4.3,
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0 1600
2000
2400
0400
0800
1200
Sampling time (h) Fig. I. Die1 zooplankton abundance in floating net cages illuminated each bar represent standard error of the mean (SEM).
at different
levels. Vertical lines above
df = 95, P < 0.05). Lower zooplankton densities were observed in dark cages that ranged from 26 to 41 individuals 1-l and did not show significant variations at different sampling times (P > 0.05). Prey densities (13-69 individuals 1-l) in all cages during daytime (OSOO- 1600) were generally low. Copepods were most abundant and accounted for 64-78% of the total zooplankton counts obtained from all cages (Table 1). The highest density of 169 individuals 1-l was found in cages illuminated at 300 lx but this did not differ from those at 180 lx with 105 individuals 1~ ’ (P > 0.05). Significantly lower copepod densities of 33 and 36 individuals 1-l were sampled in cages illuminated at 20 and 0 lx, respectively (P < 0.05). Among the copepods (excluding the nauplii), higher densities of cyclopoids occurred (range: 62- 133 individuals 1~ ’ > in 180 and 300 lx-illuminated cages, respectively. 3.2. Feeding periodicity Gut content analysis in fish reared in illuminated cages indicated a generally higher feeding between 0400 and 0800 than at other times of the day (Fig. 2). Mean feeding incidence (range: 84-88%) was similar among fish reared in illuminated cages and were significantly higher than those fish held in dark cages (67%) (P < 0.05, Table 2). The highest total mean number of ingested zooplankton at 462 individuals fish-’ was obtained at 0800 h in fish reared in 300 lx-illuminated cages (F value = 37.33, df = 126, P < 0.05, Fig. 2). Comparatively, fish held in dark cages ingested significantly less zooplankton, although more prey were ingested during daytime (13-26 prey
A.C. Fermin, G.A. Seronag/Ayuaculruree Table 1 Ranges and means Maximal abundance
157 (1997) 227-237
231
of light-attracted zooplankton in floating nursery cages different illumination levels. (average no. I-’ ) were observed at 2000 h in 20 lx and at O400 in 180 lx and 300 lx
Taxon
Illumination,
level (lx)
0 Range Decapods Brachyurans Anomurans/Pagurids
20 Mean
nil nil nil
180
Range
Mean
nil nil nil
nil
0.5-7.8 0.7-48.3 0.3-3.2 9.2-32.7
3 13 1 15
Range
0.5-48.2 nil
300 Mean nil 15
Range
Mean
0.2-46 0.3-1743.5
12 436
6-20.7 4.8-240.3 1.3-10
12 133 4 20
Copep0d.c Calanoids Cyclopoids Harpacticoids Nauplii
0.7-13.6 0.6-107.0 0.2-5.8 2.4-48.3
Fish larvae Polychaetes Balanus (Barnacle Dinoflagellates Pteropods Oikopleurans Tintinnids Nematodes Isopods
nil 0.2-4.3 1.1-42.7 nil I-20.9 nil 0.1-3.4 nil nil
nauplii)
4 14
1 17
1 10 5 2
nil 0.2-1.8 1.7-13.5 nil 0.8-11.3 nil nil nil nil
2.5-38.3 13.7-104 0.8-2.5 8.7-42 nil 0.2-7.0 3.8-31.3 nil 3.7-27.3 nil 0.2-2.2 nil nil
1 5 6
13 62 2 28
3 21 15 1
1.5-34.5 nil 0.8-2.2 0.8-34.7 nil 5.7-14.7 nil nil nil nil
I
20 12
700
600
i
500
2 ._ d Q 3 :: :: % k 2 t
400
300
200
100
0 1600
2000
2400
0400
0800
1200
Sampling time (h)
Fig. 2. Die1 feeding activity of sea bass (L. calcarifer) fry-reared in floating net cages illuminated at different levels. Data are averages of ingested zooplankton fishh’ sampled weekly within a 35-day culture period. Vertical lines above each bar represent SEM.
232 Table 2 Percentage in floating
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157 11997) 227-237
composition by number of various food items in the stomach of sea bass, L. calcarifer, nursery cages at different illumination levels
Taxon
Illumination 0
level (lx) 20
Brachyurans Anomurans
nil nil
2 8
Copepods Polychaetes Pteropods Rotifers
67 nil 2 nil
89 nil nil nil
Decapods Tintinnids
nil 29 21 51 67
nil ND
Total zooplankton ingested fishFish examined, no. “Mean feeding incidence, %
’
fry-reared
147 110 86
“Mean feeding incidence = (Total number of fish with food in their gut/Total ND = No data.
180
300
3 9 81 nil nil nil 7 ND 126 105 89
3 18 75 nil nil nil 3 ND 356 101 84
number of fish examined)x
100.
fish-‘) than at nighttime (2-4 prey fish-‘). In general, copepods were most commonly ingested by fish in all cages ranging from 21 individuals fish-’ (dark cages) up to 173 individuals fish-’ (300 Ix).
‘h a B z %
35 20 24 20 16 12 a 4 0 0
20 Illumination
180
300
level (lux)
Fig. 3. Changes during 35 days in mean total length (A) and wet body weight (B) of sea bass (L. cnlcar~r) fry-reared in floating net cages illuminated at different levels. Vertical lines above each bar represent SEM.
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157 (1997) 227-237
233
25 -
0’
, 0
I
/
I
I
I
7
14
21
20
35
Rearing period (days)
700
,
600
500 !
-o--
0 IIJX
-m-A-v-
20 Iux 18OlUX 300 Iux
L-!
ij 8
4oo
P 8 d B 9
300 -
200 -
o4
100 -
0
7
14
21
28
35
Rearing period (days)
Fig. 4. Mean specific growth rates (SGR) (‘7~ day-‘) and percent survival of sea bass (L. calcarifrr) fry-reared in floating net cages illuminated at different levels. Vertical lines above each bar represent SEM.
3.3. Fish growth and suruiual Throughout the 35-day culture period, growth of fish reared in 300 lx-illuminated cages was significantly better than those at lower illumination levels (F value = 128.58
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157 (1997) 227-237
for length, 52.94 for weight, df = 130, P < 0.05, Fig. 3A and B). At 180 lx, fish grew similarly with those held at 20 lx during the first 14 days of culture but not after 21 days. On the 28th day of culture, growth was even comparable with fish reared in 300 lx-illuminated cages. Experiments in the dark cages were terminated on the 4th week of rearing due to heavy fish mortalities. Weight specific growth rate (10% day- ‘> and percent survival (40%) of fish reared in 300 lx-illuminated cages were significantly higher than those fish held in cages illuminated at 20 or 180 lx (P < 0.05, Fig. 4).
4. Discussion Zooplankton abundance and fish feeding periodicity in sea bass fry-reared in illuminated floating nursery cages were influenced by illumination levels. At the highest illumination levels of 300 lx, zooplankton were most abundant similar with those found at 180 lx-illuminated cages, with maximal densities (up to 653 1-l) occurring between 2000 and 0400. Of the several zooplankton groups identified, copepods were the most abundant in all cages. Copepod adult and nauplii abundance in cages illuminated at 300 lx showed a 5-fold increase over unilluminated areas. The present data were consistent with the study by Fermin et al. (1996) who obtained a 5-6-fold increase in copepod and nauplii abundance in illuminated nursery cages. In a similar study done in a freshwater lake, Szczerbowski and Mamcarz (1984) observed a 1.4-fold increase in the major groups of natural zooplankton such as rotifers, copepods and cladocerans in the presence of artificial light during the night compared to those obtained from unilluminated areas. Mamcarz (1995) also recently reported copepod densities in illuminated cage zones that were 7-8 times higher than those in the unilluminated areas. In contrast, zooplankton abundance in cages illuminated at 20 lx had a slight die1 change while those cages held in the dark did not exhibit significant die1 variations. During daytime from 0800 until 1200, light-attracted zooplankton presumably disperse out in the open area as densities in the illuminated cage groups were observed to significantly decrease. Because copepods occurred in greatest number among zooplankton groups, these microcrustaceans were the most dominant prey in the diet of sea bass fry-reared in illuminated cages. Studies have indicated that rotifers, copepods, and cladocerans are the most preferred food prey of sea bass juveniles (Patnaik and Jena, 1976; Davis, 1985). Under pond nursery conditions 53-85% of sea bass fry IO-14 mm TL fed on copepods (Barlow et al., 1993). Increased zooplankton densities and the presence of light in illuminated cages had a profound effect on fish feeding. Gut content analysis showed significant increases in the number of ingested zooplankton that correspond to the increase in prey densities. Sea bass fry are particulate feeders, feeding continuously during the day but cease during the night (Barlow et al., 1993) and that the presence of light enables them to locate their food (Barlow et al., 1995). Sea bass fry exposed to continuous lighting consumed 40% more food than the fish in the 12L/12D light regime (Barlow et al., 1995). In the age-0 yellow perch, P. jihuescens, low light intensity (< 230 lx) limits the size range of available prey, resulting in the alteration of fish feeding efficiency and growth (Mills et al., 1986). At a light intensity above 230 lx, prey size selection becomes independent of
A.C. Fermin, G.A. Srronay/Aquaculture 157 (1997) 227-237
235
zooplankton abundance and depended mostly on fish size. Huse (1994) observed a maximal feeding percentage of more than 90% in turbot, Sc@zthalmus muximus, at 860 lx compared to the much lesser feeding percentage at 12 lx. The absence of light in dark cages limits the availability of zooplankton prey and both factors cause restriction in fish feeding. Food restriction is evidenced by the lower feeding incidence of sea bass fry held in dark cages compared to those reared in illuminated cages. The rate of feeding at night is affected by the amount of light available as suggested by Forrester et al. (1994). The same workers noted that despite a significant increase of drifting invertebrates during the night, there was no corresponding increase in food consumption after dark by the brook charr (Suluelinus fontinalis). According to Stefansson et al. (1990), continuous or extended daylength increased feeding activity and growth of Atlantic salmon, Salmo salar, while short daylength caused a restricted feeding time that resulted in the inhibition of growth. The feeding and swimming activities of European sea bass larvae stopped during long dark periods (9L/ 15D) as compared to fish reared in constant daylight (24L) (Ronzani-Cerqueira and Chatain, 1991). In the present experiment, unilluminated conditions led to fish starvation and eventually mass mortality. A hypothesis was then defined by Huse (1994) that the preferred illumination level during fish feeding activity is reflective of the vertical positioning strategy of the species. For example, the surface-oriented young turbot S. maximus feed at the highest illumination levels up to 860 lx as opposed to the dusk/dawn-feeding cod, Gadus morhua, larvae which prefer to feed under low light intensities (0. 1- 1.O lx) (Huse, 1994). Because of the limited illumination gradients used, the optimal illumination level for sea bass nursery in sea cages can not be drawn basing on the present results. However, a light intensity of at least 300 lx attracted the highest natural zooplankton abundance consisted mainly of copepods that have sufficiently met the food requirements for promoting growth and survival of seabass fry reared in illuminated nursery cages. Sufficiency of food prey and the presence of light during the normal dark period are important factors in the successful rearing of sea bass fry in illuminated floating sea cages. Artificial illumination enhances visibility of light attracted-zooplankton that may have influenced feeding of fish held in illuminated cages. Sea cages are inexpensive and adaptable to any site which could be of great interest for isolated or small nursery farms (Nehr et al., 1996). The present data further support our previous results which concluded that illuminated nursery cage rearing can be a better alternative to the traditional practice of sea bass fingerling production in pond or in ordinary net cages.
Acknowledgements We thank the International Foundation for Science and the Asian Fisheries Society for jointly funding this project (IFS/AFS Research Grant No. A/2078-1 awarded to A.C.F.). Thanks are also due to all the staff of the SEAFDEC Igang Marine Substation for their cooperation and support during the course of the experiments and to E. Bolivar and S.B. Balad-on for zooplankton analysis. We are grateful to Mr. L.M.B. Garcia for editing the manuscript in draft form and the two anonymous reviewers for their
236
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157 (1997) 227-237
constructive comments and suggestions. Special thanks are due to Prof. Dr. Andrzej Mamcarz of the Olsztyn University of Agriculture and Technology Department of Fisheries, Olsztyn-Kortowo, Poland who provided us helpful ideas in the conduct of the experiments.
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Ronzani-Cerqueira, V., Chatain, B., 1991. Photoperiodic effects on the growth and feeding rhythm of European sea bass. In: Lavens, P., Sorgeloos, P., Jaspers, E., Ollevier, F. (Eds.), Fish and Crustacean Larviculture Symposium. European Aquaculture Sot., Spec. Pub]. 15, Gent, Belgium, pp. 304-306. Rosch, R., Eckmann, R., 1986. Survival and growth of prefed Gregonus lawretus L. held in illuminated net cages. Aquaculture 52, 245-252. Russel, D.J.. Garrett, R.N., 1985. Early life history of barramundi, Lutescalcarfer (Bloch), in northeastern Queensland. Amt. J. Mar. Freshwater Res. 36, 191-201. SAS Institute Incorporated, 1991. SAS Systems for Linear Models, 3rd edn. Guy, NC, 329 pp. Schmitt, P.D., 1986. Feeding by larvae of Hyxmtherina tropiculis (Pisces: Atherinidae) and its relation to prey availability on One Tree Lagoon, Great Barrier Reef, Australia. Environ. Biol. Fishes 16, 79-94. Stefansson, S.O., Nortvedt, R., Hansen, T.J., Taranger, G.L., 1990. First feeding of Atlantic salmon, Saltno salar L., under different photoperiods and light intensities. Aquacult. Fish. Manage. 21, 435-441. Szczerbowski, J.A., Mamcara, A., 1984. Rearing of coregonid fishes (Corigonidae) in illuminated lake cages: II. Environmental conditions during fish rearing. Aquaculture 40, 147-161. Tandler, A., Helps, S., 1985. The effects of photoperiod and water exchange rate on growth and survival of gilthead sea bream (Sparus auruta, Linneus; Sparidael from hatching to metamorphosis in mass rearing systems. Aquaculture 48, 7 l-82.