Journal of Fish Biology (2005) 66, 315326 doi:10.1111/j.1095-8649.2005.00580.x, available online at http://www.blackwell-synergy.

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Growth of organ systems of Dentex dentex (L) and Psetta maxima (L) during larval development
R. S A L A *, C. A. S A N T A M A R I A
AND

S. C R E S P O *

*Centre de Refere`ncia en Aqu icultura de Catalunya, Departament de Cie`ncia Animal i dels Aliments and Departament de Biologia Animal, de Biologia Vegetal i dEcologia, Facultat de Veterina`ria, Universitat Auto`noma de Barcelona, 08193 Bellaterra, Barcelona, Spain (Received 23 March 2004, Accepted 17 September 2004)
Growth in volume of common dentex Dentex dentex and turbot Psetta maxima during larval development was studied by means of a quantitative histological method. A two-phase pattern of volume increase was recorded for both species, turbot volume being always higher than dentex volume. During the first phase, the increase was small but during the second phase volume rose sharply from 22 days post hatch (dph) and 17 dph onwards in dentex and turbot, respectively. In dentex, the specific growth rate (G) of the whole larva as well as that of all the structures studied (nervous tissue, trunk musculature, digestive tract, liver, pancreas, spleen and thymus) was always higher during the second phase, whereas in turbot, only total volume of the larva, trunk musculature and nervous tissue had a higher G during the same period. The pattern of allometric growth of digestive organs was similar for both species. These organs showed an initial positive allometric growth that later became near-isometric (digestive tract and liver) or negative (pancreas). In dentex, nervous tissue and trunk musculature showed near-isometry throughout the period studied. In turbot, nervous tissue exhibited negative allometry and trunk musculature changed from negative to positive allometry. In both species studied, the highest allometry coefficients were recorded for digestive organs before the larva switched to strict exotrophy. This would indicate the importance of the development of these # 2005 The Fisheries Society of the British Isles organs for survival. Key words: allometry; common dentex; fish larvae; growth; turbot.

INTRODUCTION Marine fish larvae are the smallest free-living and actively feeding vertebrates (Wieser, 1995). Most of their functional systems are incomplete at hatching and, over a relatively short period of time, highly dynamic and complex processes of organ differentiation, morphogenesis and growth take place as they gradually develop to the juvenile stage (van Snik et al., 1997; Koumoundourous et al., 1999; Gisbert et al., 2002) with drastic changes in body shape. Since not all systems grow simultaneously, allometry is a common feature during larval

Author to whom correspondence should be addressed. Tel.: 34 93 581 1897; fax: 34 93 581 1494; email: roser.sala@uab.es

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development (Osse & van den Boogaart, 1995). Allometric growth of morphological characters and organs of young larvae has been related to specific functions at given periods of fish life (Osse, 1990; Fukuhara, 1992; Osse et al., 1997; van Snik et al., 1997; Gisbert, 1999; Osse & van den Boogaart, 1999; Gisbert et al., 2002). Thus, the most essential organs for primary function develop first, followed by those with lower priority for survival (Osse & van den Boogaart, 1995). Information about the growth pattern of larval structures might help in the understanding of critical points throughout early development. Few reports on this topic, however, are available in the literature (Packard & Wainwright, 1974; Bauchot et al., 1979; Oikawa & Itazawa, 1984, 1985; Alami-Durante, 1990; Oikawa et al., 1992). Moreover, most of these reports are incomplete because they are limited to a single organ such as the brain (Packard & Wainwright, 1974; Bauchot et al., 1979) or the gill (Oikawa & Itazawa, 1985). The aim of the present work was to describe the growth of different organs and tissues during larval development in two fast-growing marine species of interest in European aquaculture, common dentex Dentex dentex (L.) (Sparidae) and turbot Psetta maxima (L.) (Pleuronectidae).

MATERIAL AND METHODS

Common dentex larvae were obtained from the Estacio dAquicultura, Port dAndraxt, Mallorca, Spain. Broodstock maintenance and reproduction, and larval rearing were performed according to the methodology developed by Pastor et al. (1995, 1997). Larvae were stocked at 199 C, range 20 C in 400 l cylindro-conical tanks at an initial density of 100 larvae l1 in an open circulation system at salinity 37. Cultures were maintained under a natural photoperiod (39 350 N ) and every tank was aerated. Enriched rotifers, Brachionus plicatilis strain Bs (Yufera, 1982), were supplied from 4 days post hatch (dph) to 18 dph at a concentration of 20 rotifers ml1 in greenwater [Nannochloropsis gaditana (25%) and Isochrysis galvana clone T-ISO (75%); 80 000100 000 cells ml1]. Artemia sp. nauplii were administered from 15 to 16 dph and enriched Artemia sp. metanauplii from 17 dph onwards at a concentration of 4 to 7 specimens ml1. Greenwater was composed of 50% N. gaditana and 50% I. galvana (clone T-ISO). Turbot larvae were provided by a commercial hatchery (TinaMenor, S.A., Pesues, Cantabria, Spain). They were stocked at 172 C, range 17 C in 7000 l cylindro-conical tanks at a density of 10 larvae l1 in a flow-through system at salinity 37. The light regime was 16L : 8D and every tank was aerated. Larvae were fed with enriched B. plicatilis from 2 to 11 dph at a density of 5 to 10 rotifers ml1. Artemia sp. (2 to 4 nauplii ml1) was introduced to the rearing tanks from 9 dph. All tanks were equipped with surface cleaner aerators. Samples were taken, every 23 days from 1 dph until the end of experimentation (30 dph for dentex and 32 dph for turbot), and sacrificed with an overdose of tricaine methanosulphonate (MS-222). Common dentex larvae were preserved in buffered formalin. Turbot larvae were fixed for 24 h in Serra liquid (ethanol 6V : formalin 3V : acetic acid 1V) and then dehydrated and preserved in butanol. Standard length (LS) was measured using an ocular micrometer adapted to a light or dissecting microscope and larvae were then processed according to standard histomorphological methods. They were individually embedded in paraffin wax, cut sagittally in serial sections of 10 mm and stained with alcian blue (pH 26), periodic acid Schiff (PAS), Groats haematoxylin and Orange G, sequentially (Gabe, 1968). Five larvae per sampling day were used for organ volume determination by means of a quantitative histological method. Volumes (mm3) were estimated from areas measured in equidistant serial histological sections with an image analysis system (Digital Image System, S.L., Spain) linked to the microscope used to view the sections. In a preliminary study (Sala, 1993), the minimum interval between the equidistant sections was determined
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in order to keep measurement error in volume determination below a value fixed at 56%. This value was obtained by comparing the influence of the number of sections examined on the relative difference (Dr) between the estimated volume of the two eyes of the same animal. This difference takes into account the margin of error in measurements and the asymmetry that may exist between the two eyes. It was calculated by the equation: Dr (%) 100{(V1 V2) [05(V1 V2)]1}, where V1 and V2 are the respective volumes of the two eyes. Each section was measured for 1 dph larvae, every other section was measured for 214 dph larvae, one in three sections for 15 to 17 dph larvae, one in five section for 21 to 25 dph larvae and one in six sections for 26 to 32 dph larvae. At least 11 sections were analysed for each organ or tissue studied. Volume (V) was calculated from V AEC, where A represents the summation of the measured areas, E the thickness of the sections and C the interval between two measured sections. Larval structures studied were: nervous tissue (brain plus spinal cord), trunk musculature, digestive tract (from oesophagus to anus without intestinal lumen), accessory glands (liver and pancreas) and lymphoid organs (spleen and thymus). Histological observations of these organs during larval development are detailed elsewhere (dentex, Santamar a et al., 2004; turbot, Sala, 1993; Padros & Crespo, 1996). The volume of the whole larva (all tissues present on a section minus lumen of the buccopharingeal cavity, digestive tract and swimbladder, and when present, yolk sac, including viteline envelope and oil globule) was also measured. It is well established that histological procedures can modify sample size (Bancroft & Stevens, 1982). Therefore, in order to allow comparisons between species, the effect of histological treatment was previously determined (Sala, 1993; Santamar a, 2002) according to methodology developed by Alami-Durante (1990). As the magnitude of shrinkage was size dependent, a shrinkage coefficient was calculated for each larva. Specific growth rate (G, % day1; Hopkins, 1992) was calculated from G 100(lnxf lnxi) (tf ti)1, where xf was the mean length or mean volume of each sample at time tf, xi was the initial mean length or mean volume at ti. Allometric growth was calculated as a power function y axk (Huxley, 1932; Fuiman, 1983), where y was the volume of an organ system (dependent variable), x was the total volume of the larva (independent variable), a was the intercept and k was the growth coefficient. Isometric growth occurred when k 1. Allometric growth was positive when k was >1 and negative when <1. Linear regressions were performed on log10 transformed data, using total volume as the independent variable. Inflexion points of growth curves were determined by a model of multiple non linear regression (Proc NLIN) using SAS1 (SAS, 1996) based on lineal splines in two or three segments (Seber, 1989). Growth coefficients were compared statistically using the t-test.

RESULTS
COMMON DENTEX LARVAL GROWTH

The mean S.D LS of common dentex larvae during the experiment are shown in Table I. They increased from 311 009 mm on 1 dph to 846 073 mm on 30 dph, with G at 35% day1. When total larval volume was considered, the increase recorded over the same period became more marked (100, Table I). Mean S.D. volume rose from 0121 0009 mm3 (1 dph) to 12143 1978 mm3 (30 dph), two phases being clearly distinguishable. The first phase, from 1 to 22 dph was characterized by a small increase, and, in the second phase, the volume increased sharply. This two-phase pattern was also recorded for all organ systems studied, G from 22 to 30 dph being higher than that obtained from 1 to 21 dph (Table II).
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TABLE I. Mean S.D. standard length and volume of different organ systems of common dentex larvae (n 5 per sampling day) during the experiment

dph 0021 0001 0028 0002 0028 0006 0024 0003 0038 0004 0045 0005 0067 0011 0107 0039 0155 0031 0640 0017 1326 0074 0002 0002 0004 00003 0007 00016 0009 00031 0018 00011 0024 00041 0033 00051 0038 00118 0049 00229 0230 00231 0564 01194 00003 00001 00007 00002 00018 00003 00030 00012 00065 00015 00094 00016 00117 00044 00195 00084 00172 00080 01090 00166 02799 00851

LS (mm) 000062 000006 000158 000046 000149 000054 000314 000039 000408 000035 000624 000076 000543 000174 000789 000555 003443 000678 006696 001966

Total volume (mm3) Liver (mm3) Pancreas (mm3)

Trunk musculature (mm3)

Nervous tissue (mm3)

Digestive tract (mm3)

Spleen (mm3) 000004 000001 000004 000001 000011 000002 000016 000003 000021 000006 000036 000012 000056 000014 000314 000055 000524 000093

Thymus (mm3)
R. SALA ET AL.

1 3 5 7 9 12 15 17 22 26 30

311 009 0121 0009 334 010 0165 0017 337 011 0192 0031 346 009 0194 0022 365 014 0280 0023 405 020 0338 0032 430 028 0439 0105 443 031 0658 0213 524 070 0964 0257 692 049 4485 0296 846 073 12143 1978

0019 0002 0031 0003 0035 0007 0031 005 0050 0005 0063 0009 0094 0012 0121 0046 0186 0086 1080 0096 3299 0654

000006 000002 000009 000004 000062 000013 000288 000049

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TABLE II. Specific growth rate of the volume of different organ systems of common dentex and turbot larvae (n 5 per sampling day) Common dentex G (% day1) Turbot G (% day1)

Phase 1 Phase 2 Phase 12 Phase 1 Phase 2 Phase 12 122 dph 2230 dph 130 dph 117 dph 1732 dph 132 dph Total volume Nervous tissue Trunk musculature Digestive tract Liver Pancreas Spleen Thymus
1

97 101 106 149 194 1251 1682 664

282 238 319 272 310 238 249 389

146 158 166 169 203 149 198 312

155 128 159 237 2321 2181 2953

221 161 279 208 215 174 287 3464

187 144 217 223 223 195 290 346

3, 25, 37 and 417 days post hatch (dph).

During the first month of life, an increase in the relative volume (expressed as percentage of the total volume of the larva) of all structures except nervous tissue, was also recorded (Table III). Nervous tissue, together with musculature, accounted for almost 30% of common dentex volume at 1 dph. The relative volume of nervous tissue, which represented 17% of total volume of the larva on 1 dph, decreased to 11% on 30 dph. In contrast, musculature increased nearly 30% in the same time period. The relative volume of the digestive tract and liver increased considerably, but only a slight increase was obtained for the pancreas. Allometry coefficients (k) of organs and tissues are shown in Table IV. Throughout the period studied, allometric growth of both nervous tissue and musculature was near-isometric (k 095 for nervous tissue; k 11 for musculature). The coefficients of digestive organs were initially highly positive (k > 2) and became negative (pancreas) or near-isometric (digestive tract and liver) at 9 dph. The relative growth of the spleen was strongly positive before inflexion (k1) (k1 > 16) changing by 22 dph to negative allometry post inflexion (k2) (k2 051). The thymus, with a positive allometric growth (k > 13), did not undergo any important growth changes during the experimental period.
TURBOT LARVAL GROWTH

The LS of larvae changed from 308 033 mm on 1 dph to 1458 107 mm on 32 dph (Table V), showing a G of 5% day1. When total larval volume was considered, the increase recorded over the same period became more marked (326). Mean volume rose from 0258 0009 mm3 on 1 dph to 84005 9990 mm3 on 32 dph. A small increase of all structures studied was observed from 1 to 17 dph, followed by an abrupt increase from then on (Table V). The G of total larval volume, trunk musculature and nervous tissue from 18 to 32 dph was higher than that obtained from 1 to 17 dph (Table II). In contrast, G of the digestive organs decreased slightly during the second growth phase.
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TABLE III. Relative volume (% of the total body volume) of different organ systems of common dentex and turbot larvae (n 5 per sampling day) Common dentex Relative volume (% total body volume) 1 dph Nervous tissue Trunk musculature Digestive tract Liver Pancreas Spleen Thymus
1

Turbot Relative volume (% total body volume) 1 dph 125 112 21 121 041 0013 0014 32 dph 33 322 66 33 05 007 007

30 dph 112 271 46 23 05 004 0024

172 155 18 03 041 0022 0014

3, 25, 37 and 417 days post hatch (dph).

On 1 dph, nervous tissue and trunk musculature represented 125 and 112% of total volume of the larva, respectively. Relative volume of nervous tissue showed a marked decrease for the whole period studied, representing only 3% of body volume on 32 dph. In contrast, musculature rose, accounting for c. 30%

TABLE IV. Allometry coefficients (k) of different organ systems for common dentex and turbot during the first month after hatching (n 5 per sampling day)
Common dentex
1

Turbot
1

Inflexion points k r2 099**** 099**** 099**** 099**** 099****

Inflexion points

Organs/Tissues

r2

mm3 LS (mm) dph 36 36 36

mm3 LS (mm) dph 126 054 289 050 398 46 42 57 05 60 78 11 7 17 7 17 21

Nervous tissue k 095 099**** Trunk musculature k 110 099**** Digestive tract Liver Pancreas

k1 255 099**** 027 k2 099 k1 389 098**** 029 k2 098 k1 253 097**** 028 k2 081 k1 162 097**** 199 k2 051 k 131 096****

Spleen Thymus

52

k 081 k1 085 k2 126 9 k1 275 k2 097 9 k1 149 k2 098 9 k1 238 k2 125 k3 076 22 k1 186 k2 097 k 157

098**** 1138 098****

dph, day post hatch; LS, standard length; 1total volume, LS and age of larvae when the inflexion point occurred; k1, allometry coefficient before inflexion point; k2, allometry coefficient after inflexion point; ****P < 00001.

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TABLE V. Mean S.D. standard length and volume of different organ systems of turbot larvae (n 5 per sampling day) during the experiment

dph 0032 0002 0043 0007 0060 0012 0077 0012 0252 0039 0758 0113 1258 0244 2806 0261 00042 00010 00086 00016 00145 00085 01093 00299 04089 01144 06915 02851 27523 03107 00014 00005 00040 00012 00068 00015 00299 00079 00957 00177 01556 00251 04099 00434 0005 00005 0012 00014 0045 00106 0073 00167 0241 00463 0836 01750 1507 03224 5526 03728

LS (mm)

Total volume (mm3) Liver (mm3) Pancreas (mm3)

Trunk musculature (mm3)

Nervous tissue (mm3)

Digestive tract (mm3)

Spleen (mm3) 000004 000002 000009 000005 000080 00033 000880 000317 001708 000959 005920 002119

Thymus (mm3) 000030 000004 000188 000067 000579 000270 005468 000913

1 3 7 11 17 21 26 32

308 033 0258 0009 0029 0001 351 010 0353 0016 0049 0007 417 027 0606 0108 0072 0016 457 046 1018 0225 0098 0017 569 067 3085 0698 0369 0073 782 059 11570 2580 2238 0637 966 082 21744 7040 4640 1989 1458 107 84055 9990 27072 3054

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dph, days post hatch.

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of body volume. A considerable increase was also observed for the digestive tract and liver. Allometric growth of nervous tissue was negative (k 081) (Table IV). In contrast, trunk musculature showed an inflexion point at 11 dph, when negative allometry (k1 085) became positive (k2 126). In all digestive organs studied, a highly positive allometry (k > 2) in early larvae became negative (pancreas) or near-isometric (digestive tract and liver). A first inflexion point was recorded on 7 dph for the digestive tract and pancreas, and a second inflexion point was obtained c. 17 dph in the liver and pancreas. The spleen showed strong positive allometry (k1 > 16) changing by 21 dph to near-isometry (k2 097). The thymus, with a positive allometric growth (k > 13), did not undergo any important growth changes during the experimental period.

DISCUSSION The increase in LS of turbot was higher than that of common dentex for the whole period studied. When volume was considered, differences between the species became more marked, with volume always being higher for turbot than for common dentex. On 1 dph, total volume of turbot doubled that of common dentex and, on 30 dph, turbot volume was seven times higher than common dentex volume. It is well established that temperature has an important influence on fish metabolism, affecting growth and development (Blaxter, 1988; Jobling, 1994). Larval culture of both turbot and common dentex was carried out at water temperatures close to optimal temperatures for larval growth and survival (Glamuzina et al., 1989; Minkoff & Broadhurst, 1994). So, the higher growth obtained for turbot might be related to factors other than temperature (e.g. genetics and species-specific metabolism). Despite differences in larval volume found between common dentex and turbot, a similar two-phase pattern of volume increase was recorded. During the first phase larvae exhibited a small volume increase but during the second phase, volume rose sharply. According to Osse et al. (1997), this remarkable increase in larval volume would suggest that at least the systems for obtaining energy and building materials are adequately developed at the beginning of this fast-growth phase. Histological and histochemical studies carried out in common dentex (Santamar a et al., 2004) and turbot (Cousin & Baudin Laurencin, 1985; Padros et al., 1991; Segner et al., 1994, 1995) have shown that differentiation of digestive organs takes place during endotrophic and endo-exotrophic stages. It is also interesting to point out that the drastic increase in volume of all structures studied, coincided with the differentiation and subsequent proliferation of gastric glands: at 22 dph in common dentex (Santamar a et al., 2004) and 1720 dph in turbot (Cousin & Baudin Laurencin, 1985; Sala, 1993; Segner et al., 1994). The abrupt change in larval volume also coincided, in both species, with the timing of finfold differentiation into unpaired fins (Sala, 1993; Santamar a, 2002). This would suggest, as previously pointed out by Gisbert (1999) and Gisbert et al. (2002), an enhancement of swimming capabilities which would enable larvae to disperse actively over a wide area and improve prey capture efficiencies. Thus, from a practical point of
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view, not only quality, but also quantity and adequate size of the prey supplied to larvae should be guaranteed at this stage. In both species nervous tissue and trunk musculature represented the major proportion of larval volume on 1 dph. The relative volume of nervous tissue decreased throughout development, specially in turbot. Similar results were described in larval (Alami-Durante, 1990), juvenile and adult (Oikawa & Itazawa, 1984; Goolish & Adelman, 1988; Yapo, 1990) common carp Cyprinus carpio L. as well as in Mozambique tilapia Oreochromis mossambicus (Peters) during post-natal development (Yapo, 1990). The important decrease obtained in turbot nervous tissue might reflect the negative allometric growth (k 081) exhibited by this species. A negative allometry for the brain against body mass in common carp (from 007 to 1900 g body mass) and porgy Pagrus major (Temminck & Schlegel) (from 00033 to 1200 g body mass), was also obtained by Oikawa & Itazawa (1984) and Oikawa et al. (1992), respectively. These authors, however, described an isometric growth during the very early stages of the life history of these species, similar to that observed for common dentex (k 095). The negative allometry of the brain throughout life is a feature of fishes because their growth slows down but never terminates (Ridet & Bauchot, 1990; Kotrschal et al., 1998), and seems to be related to the rapid development of sensitive and nervous structures prior to hatching (Osse & van den Boogaart, 1999). In contrast, relative volume of trunk musculature did not decrease during larval development accounting in both species for 30% of total tissues by 30 dph. Allometric growth showed different patterns between species. Common dentex musculature showed a near-isometric growth, similar to that described in common carp (Alami-Durante, 1990) and porgy (Oikawa et al., 1992). On the contrary, turbot exhibited a biphasic allometric growth with the inflexion point at c. 11 dph, when negative allometry became positive. This increase in musculature growth seemed to be associated with the development of epiaxial and hypaxial musculature (Sala, 1993), resulting in a considerable change in body shape (from elongate larvae to more robust specimens) in later stages of development. Both absolute and relative volumes of the digestive tract were higher in turbot than in common dentex. According to Lilja (1981, 1983, 1997), the growth of an animal would be restricted by the capacity of the animal to ingest food. Thus the higher growth in volume of turbot larva might be related to the higher volume of its digestive organs, permitting a higher food ingestion capacity. The digestive organs of both species were characterized by a fast relative growth in early development, exhibiting the highest allometry coefficients of all organ systems studied. These coefficients slowed down and became near-isometric (digestive tract and liver) or negative (pancreas). It is interesting that the inflexion points in common dentex and those observed in turbot by 7 dph coincided with the change of endotrophy into exclusively exotrophy (Sala, 1993; Santamar a et al., 2004.), Thus, the high allometry coefficient recorded before the exhaustion of endogenous reserves would indicate the priority of the development of these organs for survival. Once the larva switched to purely exotrophy, the growth rate of digestive tract and liver paralleled that of the whole larva, showing allometric coefficients similar to those observed in common carp (Alami-Durante, 1990; Oikawa et al., 1992).
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Thanks to P. Puig for the statistical advice and to the staff of Unite dElevage Larvaire, Station dHydrobiologie, Unite mixte INRA-IFREMER de Nutrition des Poissons, Saint-Pee-sur-Nivelle, France, for their technical support in the quantitative histological methodology. This study was supported by grants from the Spanish Government ` (ACU-006) and the Centre de Referencia de Recerca i Desenvolupament en Aquicultura (Generalitat de Catalunya).

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