Aquaculture research, tập 42, số 5, 2011

Aquaculture Research, 2011, 42, 629 doi:10.1111/j.1365-2109.2011.02874.x Preface This special issue presents a selection of the experience papers presented as posters at larvi 2009, held at Ghent University, Belgium, September 7^10, 2009 The larvi symposia (1991, 1995, 2001, 2005 and 2009) are among the few international scientiÂc symposia, which are completely dedicated to larval Âsh and shellÂsh research larvi 2009 was co-organised by the UGent Aquaculture R&D consortium of Ghent University (Belgium), the Norwegian University of Science and Technology,Trondheim (Norway) and the COST action Larvanet.larvi 2009was organised under the patronage of His Majesty Albert II, King of Belgium and was sponsored in part by the Flemish Interuniversity Council, the Research Council of Norway, the Norwegian University of Science and Technology, the Province of East Flanders and the Flemish Science Foundation We would like to thank the members of the poster selection committee Karin Pittman, Sadasivam r 2011 Blackwell Publishing Ltd Kaushik, Ronaldo Cavalli, Ivar Ronnestad, Elin Kjệrsvik, JoseÔ Zambonino, Giorgos Koumoundouros, Grete Baeverfjord, Kristin Hamre, Amos Tandler, Gordon Bell, Bill Koven, Patrick Kestemont, Luis Conceicaỡo, Kangsen Mai, Manuel Yufera, Atsushi Hagiwara, Yngvar Olsen, Clara Boglione, Dominique Adriaens, Maria Theresa Dinis, Lewis Le Vay, Konrad Dabrowski, Trine Galloway, Peter Bossier, Olav Vadstein and Pavlos Makridis for their thorough work in reviewing all the poster contributions The review papers presented at larvi 2009 are published in Aquaculture (in press) Pdf Âles of most of the oral and poster presentations can be found at www.larvi.ugent.be Patrick Sorgeloos, larvi 2009 conference chairman 629 Aquaculture Research, 2011, 42, 630^654 doi:10.1111/j.1365-2109.2010.02656.x REVIEW ARTICLE Particularities of early life stages in temperate freshwater fish species: comparisons with marine species and implications for aquaculture practices Fabrice Telehea & Pascal Fontaine URAFPA, Nancy UniversiteÔ ^ INRA,Vandoeuvre-le's-Nancy, France Correspondence: F Teletchea, URAFPA, Nancy-UniversiteÔ ^ INRA, avenue de la Foret de Haye, F-545000 Vandoeuvre-le's-Nancy, France E-mail: fabrice.teletchea@lsa-man.uhp-nancy.fr Abstract Both egg and larvae are diĂerent between freshwater and marine Âsh species Freshwater Âsh species have generally larger and fewer eggs than marine species Most freshwater Âsh species have demersal eggs that develop stuck to various substrata, such as plants or gravels, while eggs of most marine Âsh species develop in the water column These diĂerences have consequences for both the evaluation of the quality and the incubation of eggs of freshwater Âsh species compared with marine species The larvae of many freshwater Âsh species are larger and more developed at hatching than their marine counterparts: thus, larval feeding regimes could be diĂerent and cannibalism may emerge sooner in certain freshwater Âsh species The main diĂerences of egg and larvae between freshwater and marine species are highlighted and the possible implications for aquaculture practices are discussed Keywords: domestication, egg, larvae, marine, freshwater Introduction In the past 50 years, aquaculture production has grown at an average annual rate of nearly per cent, starting from a production of o1 million tonnes per year in the early 1950s to 51.7 million tonnes in 2006 (FAO 2009) Considered to be the fastest growing global primary industry, aquaculture is for the Ârst time 630 set to produce half of the Âsh consumed by the human population worldwide, and is expected to maintain an average annual growth rate of 44% over the period 2010^2030 (Bruge're & Ridler 2004; FAO 2009) This reÊects not only the vitality of the aquaculture sector but also global economic growth and continuing developments in Âsh processing and trade (FAO 2009) Yet, such a rapid development has been questioned on environmental grounds, in particular its dependence on Âshmeal supplies for aquatic feeds, which in turn depend on approximately 25% of the dwindling marine capture Âshery (Naylor, Goldburg, Primavera, Kautsky, Beveridge, Clay, Folke, Lubchenco, Mooney & Troell 2000; Tacon & Metian 2008) in conjunction with its potential impacts on biodiversity, chieÊy due to the introduction of alien species (Hall & Mills 2000; Manchester & Bullock 2000; Casal 2006; De Silva, Nguyen, Abery & Amarasinghe 2006; Innal & Erkakan 2006; De Silva, Nguyen, Turchini, Amarasinghe & Abery 2009; Diana 2009) In this relatively young food production industry, mitigating the dependence on alien species while promoting local production of indigenous species, in accordance with regional consumer demand and proximity to consumption areas, is imperative for a sustainable future (Lee 2003; Muir 2005; De Silva et al 2009; Fontaine, Legendre, Vandeputte & Fostier 2009) In 2007, world ÂnÂsh production reached nearly 31 million tonnes, which came primarily from freshwater species (28 million tonnes), followed by diadromous species (2 million tonnes) and marine r 2011 Blackwell Publishing Ltd Aquaculture Research, 2011, 42, 630^654 species (1 million tonnes) (http://www.fao.org); interestingly, 85% of this total came from 15 species alone (Lazard & Leveque 2009) In Europe, ÂnÂsh production was approximately 1.6 million tonnes in 2007 (http://www.fao.org) This total output was dominated by the marine production of three species, these being Atlantic salmon (Salmo salar), European seabass (Dicentrarchus labrax) and gilthead seabream (Sparus aurata) (Lee 2003; Suquet, Divanach, Hussenot, Coves & Fauvel 2009) However, following recent targeted eĂorts to diversify the European marine production, there were also small contributions from other species such as Atlantic cod (Gadus morhua), Atlantic halibut (Hippoglossus hippoglossus), meagre (Argyrosomus regius) and sole species (Solea spp.) (Suquet et al 2009) Concerning inland production, 65% of the total volume was based on alien species, among which the most important were rainbow trout (Oncorhynchus mykiss), silver carp (Hypophthalmichthys molitrix) and common carp (Cyprinus carpio) (Turchini & De Silva 2008) As with the marine sector, a few other species, including Eurasian perch (Perca Êuviatilis), pikeperch (Sander lucioperca), burbot (Lota lota) and tench (Tinca tinca), are considered as potential candidates for the diversiÂcation of inland production in relation to either large or local market demands (Fontaine 2009) The Âsh life cycle is commonly divided into Âve periods: embryo, larvae, juvenile, adult and senescence, despite the decisive threshold separating each period being open to debate (Balon 1984; Kovac & Copp 1999; Penaz 2001; Kamler 2002; Urho 2002) The sustainable production of a new species requires gathering biological and zootechnical knowledge on these Âve periods (Falk-Petersen 2005; Bilio 2008; Bobe & LabbeÔ 2010) This includes, among other considerations, the environmental control of the reproduction of breeders, the incubation of eggs and the subsequent rearing of larvae and juveniles In response to a previous extensive analysis of the literature by Teletchea, Fostier, Le Bail, Jalabert, Gardeur and Fontaine (2007), the three main goals of the present study were (i) to provide an updated review of the knowledge acquired about the early life stages (eggs and larvae) of freshwater temperate Âsh species, (ii) to show their diĂerences with marine species and (iii) to highlight the implications for aquaculture practices This review is part of a wider project aimed at developing a general approach to promote the domestication of new Âsh species, particularly those inhabiting European waters (Teletchea, Early life-stages in freshwater Âsh F Teletchea & P Fontaine Fostier, Kamler, Gardeur, Le Bail, Jalabert & Fontaine 2009) Egg Freshwater Âsh species generally have fewer but larger eggs than marine species, a diĂerence that is not directly attributable to diĂerences in body size between freshwater and marine Âsh species (Elgar 1990) However, both freshwater and marine species show a signiÂcant positively skewed distribution of egg diameters (Kamler 2005; Teletchea, Gardeur, Kamler & Fontaine 2009) Most freshwater Âsh species produce demersal eggs that adhere to various substrata, such as plants or gravels where they develop; while the same is true for some marine species (Lệnning, Kjệrsvik & Falk-Petersen 1988), the majority of eggs are pelagic (Ware1975; Houde1994; Hirst & Lopez-Urrutia 2006; Teletchea, Gardeur et al 2009) These diĂerences may have consequences for both the evaluation of the quality and the incubation of eggs of freshwater Âsh species compared with marine species, as discussed further below Egg quality Egg quality can be deÂned as the ability of the egg to be fertilized and subsequently develop into a normal embryo (Kjệrsvik, Mangor-Jensen & Holmefjord 1990; Bobe & LabbeÔ 2010) Despite extensive research, variable egg quality remains one of the main limiting factors for the successful mass production of Âsh larvae for both freshwater and marine Âsh species (Kjệrsvik et al 1990; Kamler 2005; Bobe & LabbeÔ 2010) Some of the key factors aĂecting egg quality include maternal attributes (age, size, fecundity), broodstock feeding and the environmental conditions (photoperiod, temperature, stress) under which the broodstock are reared and the physico-chemical parameters of the water (temperature, salinity, oxygen, pH) in which the eggs are incubated, but many are still unknown (Dabrowski 1984a; Kjệrsvik et al 1990; Tyler & Sumpter 1996; Brooks,Tyler & Sumpter 1997;Thorsen,Trippel & Lambert 2003; Kamler 2005; Bobe & LabbeÔ 2010) Recent studies focusing on the role of some maternal mRNAs have also provided some hints on the molecular mechanisms involved in the regulation of egg quality in Âsh (reviewed in Bobe & LabbeÔ 2010; Lubzens, Young, Bobe & Cerdaỉ 2010) The identiÂcation of predictive estimators or markers of egg quality would have major applications r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654 631 Early life-stages in freshwater Âsh F Teletchea & P Fontaine Aquaculture Research, 2011, 42, 630^654 in aquaculture (Bobe & LabbeÔ 2010); however, to date, no such estimators or markers have been found Current methodologies allow non-viable gametes to be identiÂed in select species through the assessment of simple parameters such as buoyancy or appearance (Kjệrsvik et al 1990; Lahnsteiner, Urbanyi, Horvath & Weismann 2001; Thorsen et al 2003; Bobe & LabbeÔ 2010) For example, in marine species with buoyant eggs, such as Atlantic cod, unfertilized eggs sink to the bottom of the tank, while fertilized eggs Êoat (Thorsen et al 2003; Sawanboonchun, Roy, Robertson & Bell 2008) For some freshwater species, such as Eurasian perch or Arctic charr (Salvelinus alpinus), fertilized eggs have a translucent appearance while unfertilized eggs have a whitish appearance or are opaque (Huuskonen, Penttinen & Piironen 2003; Migaud, Wang, Gardeur & Fontaine 2004) Therefore currently, the only biologically relevant ways available to consistently assess egg quality for either freshwater or marine Âsh species are fertilization and hatching rates, survival to speciÂc developmental stages, larval malformations (scoliosis, lordosis), malpigmentation or larval stress tests (Kjệrsvik et al 1990; Dhert, Lavens & Sorgeloos 1992; Abi-Ayad, MeÔlard & Kestemont 1997; Planas & Cunha 1999; Emata, Borlongan & Damaso 2000; Kjệrsvik, Hoehne-Reitan & Reitan 2003; Thorsen et al 2003; Alvarez, Racotta, Arjona & Palacios 2004; Avery, Killen & Hollinger 2009; Bobe & LabbeÔ 2010) Implications for egg incubation The physico-chemical parameters related to the water (temperature, salinity, oxygen, light intensity, pH, xenobiotic) in which eggs are incubated are key factors inÊuencing their quality (Alderdice 1985; Brooks et al 1997; Kamler 2002) Among these diĂerent physico-chemical parameters, water temperature is the most important for both freshwater and marine species, followed by salinity for marine species (Miller, Crowder, Rice & Marschall 1988; Blaxter 1992; Brooks et al 1997; Kamler 2002; Teletchea, Gardeur et al 2009) Indeed, the temperature at which eggs are incubated can aĂect not only their quality but also the tissue diĂerentiation rate, the activity of hatching glands and embryo motility (Elliott, Humpesch & Hurley 1987; Pepin 1991; Brooks et al 1997; Kamler 2002) Over 90% of the variation in the embryo ontogenetic rate is controlled by temperature (Kamler 2002) At the intraspeciÂc level, it is now well established that within a viable temperature 632 range, the time required by fertilized Âsh eggs to incubate decreases with increasing temperature, with all other factors being equal This negative correlation has been found for both marine Âsh species, e.g for Atlantic cod (GeĂen, Fox & Nash 2006) or haddock (Melanogrammus aegleÂnus) (Martell, KieĂer & Trippel 2006) and freshwater Âsh species, such as salmonids (Elliott et al 1987) or cyprinids (Keckeis, Kamler, Bauer-Nemeschkal & Schneeweiss 2001; Kupren, Mamcarz, Kucharczyk, Prusinỡska, KrejszeĂ 2008) At the interspeciÂc level, a negative relationship between incubation time and water temperature was also found for marine Âsh species (Pauly & Pullin 1988; Pepin 1991) and freshwater Âsh species (Teletchea, Gardeur et al 2009) (Table1) Egg diameter also slightly inÊuences the incubation time in both marine and freshwater Âsh species (Pauly & Pullin 1988; Pepin 1991; Bonislawska, Formicki & Winnicki 2000; Teletchea, Gardeur et al 2009) However, equations based on marine species (Pauly & Pullin 1988; Pepin 1991) poorly Ât the dataset of freshwater species (Teletchea, Gardeur et al 2009) primarily because the model greatly underestimates incubation time, especially for the lowest temperatures (seeTeletchea, Gardeur et al 2009) Consequently, the equations obtained from marine species to predict the incubation time based on either water temperature and/or egg diameter cannot be applied to freshwater Âsh species and vice versa (Table 1) More generally, it has been demonstrated that egg diameter alone cannot accurately predict the incubation time This is because Ârstly, it only partly corresponds to the amount of reserves (yolk) and secondly, the caloric values of egg dry matter varies considerably between species (Balon 1986; Lệnning et al.1988;Wiegand 1996; Bonislawska, Formicki, Korzelecka-Orkisz & Winnicki 2001; Kamler 2005; Teletchea & Fontaine 2010) Eggs of teleost Âsh are surrounded with a relatively thick proteinaceous layer, which is called the chorion, egg shell or zona radiata (Lệnning et al 1988; Kunz 2004; Lubzens et al 2010) The zona radiata has both structural and morphological diĂerences depending on the systematic position and ecology of Âsh species (Riehl & Patzner 1998; Kunz 2004) This envelope normally consists of two layers, a zona radiata interna and a zona radiata externa (Riehl & Patzner 1998; Mansour, Lahnsteiner & Patzner 2009) In numerous freshwater Âsh species and particularly cyprinids, the zona radiata externa becomes sticky in contact with water, thus enabling eggs to attach to each other and to aquatic substrata, such as plants or gravels (Riehl & Patzner 1998; Mansour et al 2009; r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654 Aquaculture Research, 2011, 42, 630^654 Early life-stages in freshwater Âsh F Teletchea & P Fontaine Table Relationships between oocyte diameter (+), incubation time (t), water temperature (T) and larval size at hatching (L) for teleost, mostly temperate, Âsh species Variables t and T r2 n Range of + (mm) Range of t (days) Range of T ( 1C) Range of L (mm) t 18.7e t 186.23e 0.197T 0.81 0.87 124 65 1.395.0 3.023.5 0.82 80 0.603.40 0.412 2.829.5 0.85 0.92 124 65 0.443.40 0.756.55 1.395.0 3.023.5 Pepin (1991) Teletchea, Gardeur et al (2009) M M M log10t 7.1010.608 log10 + 4.09 log10 (T126) t 16.1e 0.099T +0.44 Log10t 3.00210.599 log10 + 1.91 log10 (T12) L 1.9611.89 + L 2.89 +0.89 L 2.82 +0.958 0.40 0.62 0.70 100 187 219 0.809.70 0.306.40 1.6017.60 1.2030.00 F L 1.0513.10 + 0.89 65 0.756.55 2.2521.50 Miller et al (1988) Pepin (1991) Chambers and Leggett (1996) Teletchea and Fontaine (2010) Species Equations M F t and T, + M M F ỉ and L 0.1077T References Pepin (1991) Teletchea, Gardeur et al (2009) Pauly and Pullin (1988) F, freshwater; M, marine; n, number of species studied; , values not indicated Teletchea, Fostier et al 2009) In cyprinids, artiÂcial incubation is usually carried out in inverted bottles provided with a continuous water Êow (Carral, Celada, Saez-Royuela, Rodr|Ô guez, Aguilera & Melendre 2006) In these systems, the reduction in egg stickiness is recommended in order to assure the success of the incubation (Gela, Linhart, Flajshans & Rodina 2003; Carral et al 2006) Many methods have been developed for removing the stickiness of Âsh eggs: separating individual eggs mechanically, scouring them physically with abrasives (Âne clay and/or talc suspensions) or treating them chemically with milk, salt, tannic acid or enzymes (Table 2) Gela et al (2003) compared four methods to reduce the egg stickiness in tench: alcalase enzyme, milk powder with talc suspension, Âne clay suspension and talc suspension They found that each procedure was successful, with neither the destruction of egg envelopes nor larval malformations being observed They also found that the alcalase technique increased the hatching rate and required less time than the traditional milk/clay/talc treatments (Gela et al 2003) For certain cyprinid species, e.g barbel (Barbus barbus), the eggs are only slightly sticky and it is not necessary to apply any particular method for removing the stickiness before incubation (Krupka 1988; Krupka & Meszaros 1993) In conclusion, the eggs of freshwater Âsh species are generally diĂerent from those of marine species.Within freshwater species, eggs are very diverse in their diameter, buoyancy, stickiness, incubation time or water temperature requirement (Teletchea, Fostier et al 2009; Teletchea, Gardeur et al 2009; Teletchea & Fontaine 2010) DiĂerent types of incubators have been developed according to the speciÂcity of the eggs of the targeted freshwater Âsh species (Table 3) Larvae Morphological development and larval size at hatching Hatching is usually considered to be the beginning of the larval period, despite some authors considering that the larval period begins either at the moment of the onset of exogenous feeding or after the complete resorption of the yolk sac (for further discussion on this, see Penaz 1983; Balon 1984, 1986; Hensel 1999; Kovac & Copp 1999; Penaz 2001; Kamler 2002, 2008; Urho 2002) Nevertheless, hatching is a major turning point from ecological, physiological and behavioural points of view (Penaz 2001; Kamler 2002) A substantial variability in the stage of morphological development at hatching was found both between and within marine and freshwater Âsh species (Penaz 1983, 2001; Miller et al 1988; Falk-Petersen 2005; Teletchea & Fontaine 2010) For instance, Lệnning et al (1988) found that the larvae from halibut (H hippoglossus) hatch at a very premature stage compared with the larvae from lumpsucker (Cyclopterus lumpus), which hatch at a more advanced stage When comparing 17 taxa of Âsh belonging to the Salmonoi- r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654 633 Early life-stages in freshwater Âsh F Teletchea & P Fontaine Aquaculture Research, 2011, 42, 630^654 Table Main products tested for removing the stickiness of Âsh eggs Species Tannic Milk Clay Talc NaCl Urea acid Kaolin Alcalase Trypsin Protease References Cyprinidae Abramis brama X Chondrostoma X nasus Cyprinus carpio X X X X X X X Penaz and Gajdusek (1979) Halacka and Lusk (1995) X X X X X X X X X X X X X Gobio gobio Tinca tinca X X X X X X X X X X X X X X X Percidae Sander lucioperca Sander vitreus Siluridae Silurus glanis X X X X X X X Woynarovich (1962) Koldras and Mejza (1983) Billard, Cosson, Perchec and Linhart (1995) Linhart, Rodina, Gela, Flajshans and Kocour (2003) Linhart, Rodina, Gela, Kocour and Rodriguez (2003c) Horvath, Miskolczi, Mihalffy, Osz, Szabo and Urbanyi (2007) Mansour et al (2009) Osswald, Carvalho, Claro and Vasconcelos (2009) Palikova and Krejci (2006) Penaz, Wohlgemuth, Hamackova and Kouril (1981) Penaz, Prokes, Kouril and Hamackova (1989) Fernandez San Juan (1995) Linhart, Gela, Flajshans, Duda, Rodina and Novak (2000) Linhart, Rodina et al (2003) Gela et al (2003) Linhart, Gela, Flajshans and Rodina (2003) Carral et al (2006) Kujawa, Kucharczyk and Mamcarz (2010) X Demska-Zakes, Zakes and Roszuk (2005) X X Colesante (1996) Johnston, Wiegand, Leggett, Pronyk, Dyal, Watchorn, Kollar and Casselman (2007) X X X X X X X X Horvath (1980) Legendre, Linhart and Billard (1996) Linhart, Stech, Svarc, Rodina, Audebert, Grecu and Billard (2002) Linhart, Rodina et al (2003) Linhart, Gela, Rodina and Kocour (2004) Product can be either used alone or mix in the same solution dei, Penaz (1983) found that hatching was speciesspeciÂc, occurring between the seventh and the 11th developmental steps (on a developmental scale with 12 steps), and depended mainly on egg size and volume of the yolk Teletchea and Fontaine (2010) demonstrated that the developmental stages at hatching among 65 freshwater temperate Âsh species were not Âxed in ontogeny and were not directly related to either larval size or degree-days for incubation, but were probably species-speciÂc This implies that morphological and physiological development 634 proceeds much further inside the egg shell in some species than in others (Balon 1986; Hensel 1999; Urho 2002) At the intraspeciÂc level, a substantial variability in the developmental stage at hatching was also observed depending on physico-chemical factors, such as temperature and dissolved oxygen levels (Penaz 1983; Blaxter 1992; Urho 2002; Jordaan, Hayhurst & Kling 2006) ConspeciÂc larvae hatching from eggs incubated at higher temperatures are generally shorter in total body length (Blaxter 1992; Jordaan et al 2006) Moreover, within a single egg r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654 Aquaculture Research, 2011, 42, 630^654 Early life-stages in freshwater Âsh F Teletchea & P Fontaine Table Examples of devices used for incubating temperate freshwater Âsh eggs Species Anguillidae Anguilla anguilla Clupeidae Alosa alosa Zoug jar Weiss Tray-type Petri jar incubators dish Others L plastic (Mepal) bowls Pedersen (2004) X X Alosa sapidissima Cobitidae Cobitis taenia Cyprinidae Abramis brama Zydlewski and McCormick (1997) Plastic box Bohlen (1999) Polythene incubators Penaz and Gajdusek (1979) Kucharczyk, Kujawa, Mamcarz, TargonskaDietrich, Wyszomirska, Glogowski and Szabo (2005) Gerasimov and Stolbunov (2007) Glass plates put in containers X X Alburnus alburnus X X X Blicca bjoerkna Carassius auratus Carassius carassius Chondrostoma nasus Cyprinus carpio X X X X X X X Gobio gobio X X Hypophthalmichthys molitrix Leuciscus cephalus X X Rutilus rutilus X X Tinca tinca X X X X Leguen, Veron, Sevellec, Azam, Sabatie, Prunet and Bagliniere (2007) Bardonnet and Jatteau (2008) Wiggins, Bender, Mudrak and Coll (1985) 6.5 L May-Sloan plastic egg incubation jars Upwelling jar X Barbus barbus References Custom-made plastic chambers Vetemaa, Kalda and Tambets (2008) Winnicki and Korzelecka (1997) Krupka (1988) Krupka and Meszaros (1993) Policar, Kozak, Hamackova, Musil and Kouril (2007) Vetemaa et al (2008) Wiegand, Buchanan, Loewen and Hewitt (1988) Juniper twigs in jars Laurila and Holopainen (1990) Kannengieter flasks Penaz (1974) Plastic Chase type flasks Halacka and Lusk (1995) Nylon screens in plastic Keckeis, Bauer-Nemeschkal, Menshutkin, boxes Nemeschkal and Kamler (2000) Woynarovich (1962) Kamler and Malczewski (1982) Penaz, Prokes, Kouril and Hamackova (1983) Brzuska and Bialowas (2002) Horvath et al (2007) Penaz and Prokes (1978) Palikova and Krejci (2006) Burlakov, Dobrynina, Medvedeva and Poluektova (2006) Fiberglass tank Calta (2000) Krejszeff, Kucharczyk, Kupren, Targonska, Mamcarz, Kujawa, Kaszkowski and Ratajski (2008) Fiberglass troughs Jobling, Coey, Whitmore, Kime, Van Look, McAllister, Beresford, Henshaw, Brighty, Tyler and Sumpter (2002) Nzau Matondo, Ovidio, Poncin, Kakesa, Wamuini and Philippart (2007) Glass hatching jars Penaz et al (1981) Penaz et al (1989) Kamler, Szlaminska, Hamackova, Kouril, Vachta, Stibranyiova and Asenjo (1995) Fernandez San Juan (1995) Gela et al (2003) r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654 635 Early life-stages in freshwater Âsh F Teletchea & P Fontaine Aquaculture Research, 2011, 42, 630^654 Table Continued Species Zoug jar Weiss Tray-type Petri jar incubators dish Others References Inverted bottles Linhart, Gela et al (2003) Carral et al (2006) X Esocidae Esox lucius X Flow-through hatchery cones Moronidae Morone saxatilis Ictaluridae Ictalurus punctatus X Percidae Perca flavescens Perca fluviatilis X Sander lucioperca McDonald egg jar Upwelling tank Eldridge, Whipple and Bowers (1982) Macintosh and Duston (2007) Jars McDonald egg jar Legendre et al (1996) Rach, Valentine, Schreier, Gaikowski and Crawford (2004) Wire racks in a 260 L tank Small cups in a beaker Jentoft, Held, Malison and Barry (2002) Twigs placed in Weiss apparatus Flow-through tank 100 L flow-through tank X X X Nests kept in tank X X Sander vitreus 780 mL hatchery jar Downing style jars Plastic jars Salmonidae Coregonus albula X Incubation jar Hatchery jars with continuously upwelling water Glass bell jars Coregonus clupeaformmis Coregonus lavaterus Hucho hucho Oncorhynchus mykiss X X X Salmo salar Salmo trutta Salvelinus alpinus 636 X X X X X X X X X X X X X Bry and Gillet (1980) Vehniaăinen, Haăkkinen and Oikari (2007) Peters, MacKinnon, Van Meer, van den Heuvel and Dixon (2007) Korzelecka, Bonislawska and Winnicki (1998) Jentoft et al (2002) Mandiki, Babiak, Krol, Rasolo and Kestemont (2007) Schlumberger and Proteau (1996) Demska-Zakes et al (2005) Szkudlarek and Zakes (2007) Moodie, Loadman, Wiegand and Mathias (1989) Colesante (1996) Johnston et al (2007) Luczynski and Kirklewska (1984) Dostatni and Luczynski (1991) Drouin, Kidd and Hynes (1986) Harris and Hulsman (1991) Champigneulle and Rojas-Beltran (1990) Glass jars Keinaănen, Tigerstedt, Kalax and Vuorinen (2003) Glass jars Yloănen and Karjalainen (2004) Glass aquaria Witkowski and Kokurewicz (1981) Craik and Harvey (1984) Perkowski and Formicki (1997) Ninness, Don Stevens and Wright (2006) Gibb, Liu and Swanson (2007) Gunnes (1979) Vertical stack incubators Jarrams (1979) Holm 1986 Braănnaăs (1988) Eskelinen (1989) Gorodilov (1996) Johnston and McLay (1997) Vertical stack incubators Jarrams (1979) Hansen (1985) Floating small boxes Olsen and Vollestad (2001) in tank Wallace and Aasjord (1984) Gillet (1991) r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654 Aquaculture Research, 2011, 42, 630^654 Early life-stages in freshwater Âsh F Teletchea & P Fontaine Table Continued Species Zoug jar Weiss Tray-type Petri jar incubators dish Others References X Small jars X Floating plastic cylinders in tank X X Salvelinus fontinalis X X Astro-turfTM USA) Astro-turfTM Lemieux, Le Francáois and Blier (2003) Wedekind and Muăller (2004) Roche-Mayzaud et al (1998) (Dalton, GA, Mirza, Chivers and Godin (2001) X X Salvelinus namaycush Thymallus arcticus Thymallus thymallus X X X Jar Kannengieter jar X X Bernier-Bourgault and Magnan (2002) Bascinar and Okumus (2004) Gunther, Moccia and Bureau (2005) Glass funnel Kaya (1989) Penaz (1975) Humpesch (1985) Carmie, Morelet, Maisse, Jonard and Cuinat (1985) Zaytsev (1986) Honkanen, Kostamo and Kukkonen (2005) Special incubator cage Horvath (1977) Legendre et al (1996) Brzuska and Adamek (1999) Linhart, Rodina, Flajshans, Gela and Kocour (2005) California trays X Siluridae Silurus glanis Guillard, Gillet and Champigneulle (1992) De March (1995) Bebak, Hankins and Summerfelt (2000) Huuskonen et al (2003) X X batch from the same parents that experiences a common environment during its development, hatching is not completely synchronous and, especially at lower temperatures, several days can elapse between the earliest and the latest hatching larvae (GeĂen 2002; Jordaan et al 2006; Laurel, Hurst, Copeman & Davis 2008) Larvae hatching at the beginning of the hatching period are generally shorter, with larger yolk sacs, than individuals hatching later in the hatching period (GeĂen 2002; Jordaan et al 2006; Laurel et al 2008) Like hatching, the onset of exogenous feeding and the full resorption of the yolk sac have enormous physiological, ecological and behavioural signiÂcance and occur over a wide range of developmental stages (Dabrowski 1984a; Blaxter 1992; Urho 2002; Kunz 2004; Falk-Petersen 2005; YuÔfera & Darias 2007) Yet, the stage of morphological development during the transition from endogenous to exogenous feeding is not accompanied by such extensive variability as is observed at hatching This is primarily because all structures and organs related to food intake, digestion and assimilation have to be ready to ensure this transition successfully (Penaz 1983; Miller et al 1988; Cahu & Zambonino-Infante 2001; YuÔfera & Darias 2007) In conclusion, there exists a wide range and continuous spectrum of levels of morphological development attained at the stage of hatching, onset of exogenous feeding and the full absorption of the yolk sac for both marine and freshwater Âsh species (Penaz 2001) Larval size at hatching varies widely both within and between freshwater and marine species (Miller et al.1988; Pepin1991; Chambers & Leggett 1996;Teletchea & Fontaine 2010) At the interspeciÂc level, a signiÂcant positive correlation was found between oocyte diameter and larval size at hatching among marine and freshwater Âsh species (Ware1975; Miller et al 1988; Kjệrsvik et al 1990; Pepin 1991; Chambers & Leggett 1996; Teletchea & Fontaine 2010) However, the three equations based on marine species (Table 1) poorly Ât the dataset of 65 freshwater Âsh species (Teletchea & Fontaine 2010) primarily because the models greatly underestimate the larval size at hatching, especially for larger eggs (see Teletchea & Fontaine 2010) This conÂrms the notion that marine species generally produce smaller larvae than freshwater Âsh species (Balon 1984) For instance, Houde (1994) measured a 10-fold diĂerence in the r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654 637 InÊuence of diet on Êat oyster reproduction R Gonzalez-Araya et al haptophyte (0.6 million in week 4) For marine bivalves, the reproductive cycle is initially linked to the glycogen storage cycle (Berthelin et al 2000) After an initial period of storage, stocked glycogen is used concomitantly with food as an energetic support of gametogenesis A similar relation between carbohydrate and protein has been already reported (Gabbott & Walker 1971) in the natural environment but the opposite pattern was described when broodstock was fed a mixed diet of T suecica1I galbana under controlled conditions Such contrasting results within the same study (natural/hatchery: Gabbott & Walker 1971) and between these experiments and ours) could be explained by the low feeding concentration used in this previous study (2 cells mL 1), which led to a decrease in the O edulis condition index in the controlled environment In the present work, Êat oysters were fed ad libitum (1 billion cells T-ISO equivalent per day), representing 20^ 24 cells mL 1, which is 10-fold higher than the level used by Gabbott and Walker (1971) In their study, the initial oyster reserves would certainly have played a major role in the allocation of biochemical components between the tissues Lastly, the data in the Gabbott & Walker study were based on wholebody Êesh whereas our results report the composition of speciÂc tissues separately Using a similar approach (speciÂc organ biochemical allocation), Delaporte, Soudant, Lambert et al (2006) reported a similar trend in C gigas, where the protein and glycogen contents were inversely correlated during conditioning, with the maximal protein value recorded during spawning Generally, lipids are issued from carbohydrate catabolism (lipogenesis) However, most of the lipids that accumulated in the gonads during gametogenesis are directly obtained from the diet or by transfer from other tissues (Utting & Millican1997) This is particularly true for PUFA and sterols, which are weakly biosynthesized by bivalves (Chu & Greaves 1991) and thus cannot be obtained from carbohydrate lipogenesis or neosynthesized Hence, tissue-speciÂc fatty acid and sterol variations are well related to food composition, with a possible and variable metabolism buĂering (Soudant, Marty, Moal, Robert, QueÔreÔ, Le Coz & Samain 1996; Palacios, Racotta, KraĂe, Marty, Moal & Samain 2005) The initial fatty acid composition of polar lipids was similar in all tissues analysed, with a preponderance of PUFA ( % 50%) The fatty acid contents of the n-3 family were always greater than those of n-6 family, leading to an n-3/n-6 ratio 41 These results 722 Aquaculture Research, 2011, 42, 710^726 are in accordance with data reported on a natural O edulis population in Spain (Abad, Ruiz, Martinez, Mosquera & Sanchez 1995) In the present work, EPA and DHAwere the major fatty acids detected in all the organs (gonad, digestive gland, muscle and gills) These results agree with fatty acid seasonal variations in O edulis (Helm et al 1991; Abad et al 1995) and Crassostrea virginica (Trider & Castell 1980) When oysters were fed the diatoms C gracilis and S marino|ô , there was a speciÂc accumulation of 20:5(n-3) and when they were fed T-ISO such accretion occurred with 22:6(n-3) These results are partially in agreement with those of Frolov and Pankov (1992), who reported a high correlation (0.65) between the supply of these two particular fatty acids and their concentration in O edulis gonads.Whatever the diet provided and its microalgal fatty acid composition, O edulis gonads accumulated roughly the same amount of 20:5(n-3), varying from 8.5% to 10.7% (Frolov & Pankov 1992) Our study does not fully agree with this result because EPA varied from 5.5% to 17.3% and a relation was shown between the microalgae EPA content and gonad enrichment, with the highest values corresponding to diatoms and the lowest to T-ISO Moreover, 22:6(n-3) varied from 6.5% to 11.2% in Frolov and Pankov (1992) study, with a cumulative eĂect only in the case of a mixed diet while in the present work DHA exhibited a similar low-end value (7%) but a higher content (15%) with T-ISO supply, a microalga known to be particularly rich in this fatty acid In O edulis gonads, a speciÂc enrichment in EPA and DHA occurred (Frolov & Pankov 1992), which seemed to indicate a speciÂc role of these fatty acids in reproduction This pattern must, however, be partially incorrect because the present work shows that such enrichment also occurs in the other organs for the neutral fraction (data not reported), with the exception of the gills for DHA There is accordingly no speciÂc allocation of these two fatty acids to O edulis gonads Except the muscle, all tissues showed the same variations as those observed in the gonad The good and similar relation between the FA supply in the food and its incorporation into the diĂerent oyster tissues emphasized the importance of the food and the active transfer from the digestive gland to other tissues during gametogenesis The absence of a speciÂc imprinting of the gonad compared with other tissues may signify a precocious stage of gametogenesis, with a gonad weakly developed In contrast, the speciÂc composition of muscle, more independent of the food composition, means a strict FA r 2010 Blackwell Publishing Ltd, Aquaculture Research, 42, 710^726 Aquaculture Research, 2011, 42, 710^726 InÊuence of diet on Êat oyster reproduction R Gonzalez-Araya et al regulation of this tissue, and a speciÂc need for DHA to maintain its function Sterols, on the other hand, are known to play an important role in living organisms as structural components of cell membranes, steroid hormones and vitamin D precursors (Soudant et al 2000) After weeks of experimentation, the relative sterol composition of the organs was signiÂcantly inÊuenced by the diet composition In oysters fed diĂerent monospeciÂc diets, the main sterols, characteristic of each microalgae species, were allocated to all tissues except muscle Thus, for oysters fed C gracilis, cholesterol, which represented 51% of total sterols in this microalga, was eciently transferred to the gonad (from 32% on week to 47% on week 6) and other organs Similar enrichment was recorded for campesterol in oysters fed S marino|ô (37% of total sterols in this microalga) Diatoms have been shown to be well assimilated by O edulis and biochemical studies conÂrmed that their main representative fatty acids (EPA) and sterols (cholesterol and campesterol) were eciently transferred to the Êat oyster gonad as well as to most of the other tissues In the present work, T suecica is poorly absorbed when using a physiological assessment This result was conÂrmed by biochemical analysis, where no signiÂcant enrichment in the main fatty acids was found, in any tissue, at the end of the 6-week feeding experiment Thus,16:4(n-3), which is characteristic of this prasinophyte (Volkman, JeĂrey, Nichols, Rogers & Garland 1989; Robert et al 2004), did not show any variation in the gonad in the present work Moreover, while campesterol represented 89% of sterols in T suecica, oysters fed this prasinophyte did not show any diĂerences in allocation of this speciÂc sterol Because such trends also occurred in the other organs, T suecica did not oĂer any beneÂt for O edulis broodstock conditioning or maintenance under controlled conditions The low food value of this alga for the Êat oyster was also indicated by a relative decrease in the mean dry weight and weak fecundity in oysters fed this diet: larval release probably arose from the utilization of original oyster reserves From an ecophysiological point of view, T-ISO ranked in an intermediate position This result was conÂrmed with an additional trial (data not shown) using a refreshed strain of T-ISO (also obtained from the CCAP) Indeed, as absorption eciency was only 20%, doubts can be raised about its eĂective value for broodstock conditioning Biochemical analysis and speciÂcally 22:5(n-6), characteristic of this haptophyte (Volkman et al 1989; Robert et al 2004), clearly showed that this microalga was eciently incorporated into the gonad and the other tissues, including the gills Moreover, brassicasterol, which represented 99% of the total sterols in TISO, was eciently transferred and accumulated in all O edulis organs (from 17% in week to 45% in week 6) Moreover, the highest fecundity was recorded when O edulis was fed T-ISO, although such results should be analysed carefully because the entire Êat oyster spawning season can last up to months (Helm et al 1973, R GonzalesAraya, R Robert, Mingant, Petton unpubl obs.), and a previous study under controlled conditions reported that early larval release and total fecundity were not related (Gonzalez-Araya et al., unpubl obs.) These two approaches therefore yielded conÊicting results on the role of T-ISO in O edulis conditioning Such contradictory results have already been reported with this same microalga when considering C gigas larval development (Rico-villa, Le Coz, Mingant & Robert 2006) Indeed, when fed as a monospeciÂc diet, this microalga is poorly ingested and larval development is accordingly rather low In contrast, associated with the diatom Chaetoceros calcitrans forma pumilum, in diĂerent proportions, microalgae uptake increases markedly, resulting in a higher and more reproducible larval performance (Rico-Villa et al 2006) than that obtained with the diatom alone Such additive eĂects have often been attributed to a better balance in the dietary components (Helm et al 2004), which is true when considering EPA and DHA but that should also be explained by a higher food uptake Because T-ISO was not eciently assimilated by O edulis, it should be rejected from an ecophysiological point of view However, its high DHA content (15%) and its ecient DHA transfer from microalgae to Êat oyster tissues, including the gonad, make T-ISO dicult to replace Another microalga, rich in DHA and exhibiting higher absorption eciency, needs to be found Rhodomonas salina is a potential species whose performances will be examined in a forthcoming paper Conclusion Chaetoceros gracilis and S marinoi are both ecient for O edulis conditioning because of their physiological responses and ecient transfer of EPA and characteristic sterols In contrast, T suecica holds no interest for O edulis conditioning due to its low ingestion and absorption as well as the poor transfer of dietary components r 2010 Blackwell Publishing Ltd, Aquaculture Research, 42, 710^726 723 InÊuence of diet on Êat oyster reproduction R Gonzalez-Araya et al ConÊicting results were found for T-ISO, showing relatively low ingestion and absorption values contrasting with ecient transfer and allocation of DHA and brassicasterol A mixed diet is therefore recommended for O edulis conditioning to oĂer a dietary balance Chaetoceros gracilis (or S marino|ô )1T-ISO is proposed but a substitute for T-ISO should also be sought Acknowledgments This work could not have been completed without the technical support of the team at the Argenton Ifremer station ^ C Mingant, L Lebrun and P Le Souchu ^ plus the help of a project student L David, all of whom we wish to thank We are also grateful to the Universidad de Los Lagos (MECESUP-ULA 03/02), which contributed to the funding of a PhD grant for the Ârst author This work was carried out during the SETTLE project and was partially funded by FP7/ 2007-2013 under agreement no 222043 References Abad M., Ruiz C., Martinez D., Mosquera G & Sanchez J.L (1995) Seasonal variation of lipids classes and fatty acids in Êat oysters, Ostrea edulis from San Cibran (Galicia, Spain) Comparative Biochemistry and Physiology 110 C, 109^118 Albentosa M., Fernandez-Reiriz M.J., Labarta U & 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Svend Steenfeldt, Ivar Lund & Erik Hglund Section for Aquaculture,The North Sea Research Centre,Technical University of Denmark, DTU-Aqua, Hirtshals, Denmark Correspondence: S Steenfeldt, Section for Aquaculture,The North Sea Research Centre,Technical University of Denmark, DTU-Aqua, PO Box 101, DK-9850 Hirtshals, Denmark E-mail: sjs@aqua.dtu.dk Abstract Larval size heterogeneity is known to induce cannibalism, and procedures to avoid larval size diĂerences are consequently implemented already during egg incubation and hatching.We investigated the relation between larval development variability, size heterogeneity and cannibalism in pikeperch Larvae were sorted into Âve groups according to the time of hatching during a 65-h period The larvae with diĂerent times of hatch were then reared separately or together during an 18-day period Late hatched larvae were longer (P 0.003) and had less yolk remaining (Po0.001) than early hatched individuals at the time of hatching However, on 11 days post fertilization, the late-hatching larvae tended to have larger yolk reserves than earlier hatched individuals (P 0.07) Furthermore, the next day, a lower proportion in the late fraction had switched to exogenous feeding (P 0.024) That larvae with a late hatching time developed slower suggests a positive relationship between the hatching time and the embryonic developmental rate However, diĂerences in the length and available yolk reserves at hatching between larval fractions with diĂerent hatching times suggest that hatching is not strictly associated with a speciÂc developmental stage, and that factors other than the development rate of the embryo are involved in the timing of hatching Keywords: Pikeperch, Sander lucioperca, hatching time, Ârst feeding, size heterogeneity, cannibalism Introduction Pikeperch (Sander lucioperca) is a promising candidate for intensive aquaculture due to its high potential r 2010 Blackwell Publishing Ltd growth rate, density tolerance and high temperature preference (Hokanson 1977; Wang, Xu & Kestemont 2009) However, pikeperch is highly piscivorous and the cannibalistic behaviour of pikeperch is a challenge to successful intensive rearing of this Âsh (Kestemont, Xueliang, Hamza, Maboudou & Toko 2007) Cannibalism is often categorized as type I and type II In type I cannibalism, the prey is only partly ingested, whereas in type II, the whole prey is swallowed (Kestemont, Jourdan, Houbart, MeÔlard, Paspatis, Fontaine, Cuvier, Kentouri & Baras 2003) The intensity of cannibalism is generally determined by the ratio between predator gape size and prey size (Smith & Reay1991) A high predator to prey gape size ratio is usually required in type II cannibalism (CuĂ 1980; Hecht & Applebaum 1988; Van Damme, Applebaum & Hecht 1989; Otterễ & Folkvord 1993; Baras, Maxi, Ndeao, & MeÔlard, 2000) Size heterogeneity between predator and prey within a batch can be caused by multiple factors including parental, abiotic as well as biotic factors (Geffen 2002) One of the underlying factors for inducing size heterogeneity within a batch may be individual diĂerences in larval development; larvae reaching time to Ârst feeding early may later grow faster than the remaining larvae in the batch This has been demonstrated in salmonids, where fry developmental rate has been related to future growth and survival (Metcalfe & Thorpe,1992; Sundstrm, Lohmus & Devlin 2005) Furthermore, during the egg and yolk sack stages, the development is mostly dependent on internal resources and individual metabolism (Kamler 2008) Individual diĂerences in oxygen consumption in larvae end eggs (Bang, Grệnkjìr & Malte 2004; Regnier, Bolliet, Labonne & Gaudin 2010) suggest 727 EĂects of hatching time in pikeperch S Steenfeldt et al Aquaculture Research, 2011, 42, 727^732 variability in the developmental rates However, to our knowledge, it is not known whether this variability in the developmental rate is coupled to size heterogeneity and cannibalism in pikeperch The present study was aimed to investigate the relation between larval development variability, size heterogeneity and cannibalism in pikeperch Materials and methods Stripping, egg incubation and hatching time Nineteen wild mature pikeperch breeders were obtained from Mossệ, Skanderborg, Denmark Egg ovulation was induced by the injection of luteinizing hormone-releasing hormone (LHRH) at a concentration of 20 mg kg female Temperature in the broodstock facility was maintained at 15 1C Two days post injection, at 06:30 hours on 30 April, ripe eggs were stripped from a 2.5 kg female and subsequently fertilized with semen from two mature males To avoid sticking of eggs after stripping, alcalase from Novo Nordisk, Denmark was added at a concentration of 0.5 mL L for Five hundred and Âfty millilitres of eggs were incubated in two L McDonald-type upwelling units and these were left undisturbed until hatching The temperature in the incubators was increased 1C day from 15 1C to 18 1C and identical temperatures were maintained in the incubation system and the larval rearing system Hatching began on May, i.e days post fertilization (DPF) Newly hatched larvae were sampled after leaving the incubators in the following time intervals, registered as hours post fertilization: 200^208 (very early), 216^225 (early), 225^232 (mid) and 259^265 (late) Larval rearing The very early larvae were not reared due to the number of tanks available in the experimental system and the relatively low number of larvae sampled at this time The early, mid and late fractions were transferred to and reared separately or together in a12-tank recirculation system in triplicate, each larval tank holding 150 L and stocked with 2500 larvae.The tanks holding larvae reared together (mixed) were stocked with 833 early plus, 833 mid plus and 833 late-hatched larvae The larvae were fed AF Artemia, size 430 mm INVE aquaculture nv, Dendermonde, Belgium from10 to13 DPF, followed by EG Artemia (INVE) enriched with 0.6 g L DHA Selco emulsion (INVE) for 24 h from 14 to 29 DPH 728 Artemia were harvested once a day in the morning and kept aerated in a refrigerator until use Each tank received Artemia corresponding to Artemia mL three times daily At each feeding, the Artemia were poured into a 1L beaker hanging beside each tank The Êow from the beaker to the larval tank was controlled by a peristaltic pump connected to an IKS Aquastar microprocessor (IKS ComputerSysteme GmbH, Karlsbad, Germany) One feeding cycle was set to h The photo period was 24 h of dim light provided by light bulbs above the tanks The light intensity at the water surface was 50 lux The experiment lasted till 29 DPF Larval sampling Samples of larvae were collected from all groups at the time of hatching and on 11, 12, 13, 14, 19 and 29 DPF The sampling time was between 10:00 and 11:00 hours, i.e h after they were fed in the morning Larval standard lengths were measured by photographing four samples of 10 larvae using a digital DFC 320 Leica camera connected to a dissecting microscope (MZ6), both from Leica Microsystems, Heerbruug, Switzerland, and using Leica Application SystemVersion 3.5 for image analysis Oil globule diameter and yolk sac volume were measured and gut content was estimated from the pictures Yolk sac volume (V) was estimated using the equation V p(6 l h2) 1, where l and h are the length (mm) and the height (mm) of the yolk sac respectively (Bagarinao 1986) Fraction of larvae with gut content was quantiÂed as the fraction of larvae (% of sampled larvae) with visible gut contents Coecients of variation (CVlength) were calculated as: CVlength SDlength (mean length) Mortality and cannibalism Larval mortality throughout the experiment was monitored by counting dead larvae siphoned from the bottom of each rearing tank on a daily basis Type II cannibalism was calculated based on the number of larvae stocked initially, the sum of dead larvae siphoned and live larvae present in the tanks on 29 DPF It was not attempted to distinguish between type cannibalism and other types of mortalities, i.e starvation, bacterial infections, etc Consequently, the term type I mortality is used instead of type I cannibalism r 2010 Blackwell Publishing Ltd, Aquaculture Research, 42, 727^732 Aquaculture Research, 2011, 42, 727^732 EĂects of hatching time in pikeperch S Steenfeldt et al Statistics Statistics were based on a nested-ANOVA design in STATISTICA ver 9.0 (Statsoft, Tulsa, OK, USA): measurements of individual Âsh nested in tanks nested in treatments If a nested-ANOVA design was not applicable, e.g when estimates were based on pooled samples of larvae, a one-way ANOVA was used When signiÂcant diĂerences were found between treatments (Po0.05), Tukeys post hoc tests were used to screen for signiÂcant diĂerences between pairs of treatments Error bars are presented as standard error of means if nothing else is stated Results Figure Yolk sac volume (mm3) at the time of hatching for very early, early, mid and late hatched larvae Error bars represents standard error of means DiĂerent letters denote a signiÂcant diĂerence (Po0.05) Newly hatched larvae When comparing larval total lengths at the time of hatching, a signiÂcant diĂerence between larval lengths at hatching was observed (P 0.003) This resulted in signiÂcantly shorter larvae in the very early group compared with the group with the latest hatching (Fig 1; Po0.01) Yolk sac volume was signiÂcantly aĂected by the time of hatching (Fig 2; Po0.001) The very early larvae had a signiÂcantly larger yolk sac volume than later hatched larvae (Po0.05) The late hatched larvae had a signiÂcantly smaller yolk sac volume than the early and mid hatched larvae (Po0.001) Larval growth and feeding At DPF 11 and 12 yolk sac volumes were not signiÂcantly diĂerent (Fig 3; P 0.07 and P 0.11 respectively) On both days, though, late hatched larvae tended to have higher yolk sac volumes Figure Larval total length (mm) at the time of hatching for very early, early, mid and late hatched larvae Error bars represents standard error of means DiĂerent letters denote a signiÂcant diĂerence (Po0.05) Figure Yolk sac volume (mm3) for, early, mid and late hatched larvae plus mixed larvae on 11 and 12 days post fertilization Error bars represent standard error of means Oil globule diameter at the time of hatching (P 0.42) or at 11, 12, 13 or 14 DPF (P 0.11) was not aĂected by the time of hatching It reduced in size from 12 to 13 and 13 to 14 DPF respectively (Po0.01) All larvae had empty guts at day 11 DPF despite the presence of Artemia in all larval rearing tanks At 12 DPF, 28% of all larvae in the experiment had ingested live feed and this increased to 56% at 13 DPF and to 69% at 14 DPF (Fig 4).When including early, mid and late hatched larvae, the stomach contents did not differ signiÂcantly between the hatching groups (P40.09) There seemed to be a tendency, though, that late hatched larvae began feeding later than early hatched larvae This was supported by a pairwise comparison of only the early and the late hatched larvae on12 DPF The analysis revealed a signiÂcantly higher proportion of early hatched larvae with stomach content than late hatched individuals (P 0.024) r 2010 Blackwell Publishing Ltd, Aquaculture Research, 42, 727^732 729 EĂects of hatching time in pikeperch S Steenfeldt et al Aquaculture Research, 2011, 42, 727^732 Figure Fraction of larvae with stomach content on 11, 12, 13 and 14 days post fertilization for early, mid and late hatched larvae plus mixed larvae Error bars represent standard deviations between replicates Figure Larval total length (mm) for early, mid and late hatched larvae plus mixed larvae Error bars represent standard error of means Throughout larval rearing from 11 to 29 DPF, larval lengths did not diĂer considerably (Fig.5) Only at 13 DPF a signiÂcant diĂerence between larval lengths between groups was observed (Fig 5; P 0.02) but the remaining samples revealed no effects of hatching time on larval growth (P40.061) The CVlength on DPH 29 were 0.10 ặ 0.01 (early); 0.10 ặ 0.02 (mid); 0.13 ặ 0.01 (late) and 0.11 ặ 0.01 (mixed) and they were not signiÂcantly diĂerent (P 0.91) Mortality and cannibalism Mortality throughout the experimental period was not constant Initially, approximately 20 dead larvae were siphoned from each tank daily, increasing to a maximum of 30^120 larvae per tank at16 DPF Extraordinarily high mortalities were registered in three tanks on 16 DPF, two of them holding early hatched larvae Mortality thereafter declined and all tanks maintained a low mortality around 20 DPF before it gradually increased towards the end of the experiment (Fig 6) Total mortality throughout the experimental period was between 59% and 68% Mortalities due to type II cannibalism were between 41% and 53% and mortalities due to type I mortality were between 15% and 20% There was no signiÂcant diĂerence between any of the types of mortality as a consequence of treatment (P40.13) Pooled type II cannibalism was signiÂcantly higher than pooled type I mortality (Fig.7; Po0.001) 730 Figure Mortality registered as the number of dead larvae siphoned from experimental tanks throughout the experiment for early, mid and late hatched larvae plus mixed larvae Error bars represent standard deviations between replicates Discussion Pikeperch with a late hatching time had a longer body length and less yolk at hatching compared with larvae that hatched earlier Two days after hatching, late hatched larvae tended to have more yolk remaining than larvae that hatched early, suggesting a slower yolk consumption and development in the late hatching larvae A slower development in late hatching larvae was also reÊected in a lower proportion of larvae that had initiated exogenous feeding days after hatching However, these diĂerences in development were not related to Ârst feeding, growth or mortality Early released herring larvae were smaller than later naturally ones at the time of hatching Larval length was not diĂerent though when comparing r 2010 Blackwell Publishing Ltd, Aquaculture Research, 42, 727^732 Aquaculture Research, 2011, 42, 727^732 Figure Total mortality, type II cannibalism and type I mortality (deÂned as mortality causing larvae to die and sink to the bottom of larval rearing tanks) for early, mid and late hatched larvae plus mixed larvae Mortalities are in% of initially stocked larvae Error bars represent standard deviations between replicates hatched individuals of the same age (DPF), suggesting no advantage of early hatching (GeĂen 2002) In ocean pout Macrozoarces americanus early hatched individuals were also smaller at hatching than later hatched ones Their ability though to feed exogenously before late hatched individuals were released caused the early hatched individuals to grow considerably larger than later hatched siblings, thereby gaining a competitive advantage to these (Methven & Brown 1990) We observed diĂerences in length and available yolk at hatching between larval fractions with diĂerent hatching times This is in agreement with other studies suggesting that hatching is not strictly associated with a speciÂc developmental stage, and that other factors such as the development rate of the embryo are also involved in the timing of hatching (Kocan, Hose, Brown & Baker 1996; Jordaan, Hayhurst & Kling 2006) However, that the late hatched larvae had less yolk at hatching, but on the other hand, showed a tendency to have more yolk 11 DPF and a lower proportion of larvae that had initiated exogenous feeding at day 12 DPF, in the present study, suggests a slower development in these individuals The results are based on a single batch of eggs, though, and would be strengthened by checking with future comparable experiments Further studies of the relation between hatching and developmental ratio are needed to investigate whether this diĂerence in the developmental ratio between larvae with an early or a late hatching time is also expressed post hatching EĂects of hatching time in pikeperch S Steenfeldt et al In salmon, it seems not to be the hatching time, but rather the time when larvae reach Ârst feeding that correlates with other traits expressed later in life, such as postlarval growth (Farrell, Bennett & Devlin 1997; Stevens, Sutterlin & Cook 1998; Cook, McNiven, Sutterlin 2000) In the present study, we observed a lower proportion of larvae that had initiated exogenous feeding at 12 DPF in the late fraction; however, this was not related to post Ârst feeding growth and size heterogeneity This is in agreement with studies performed in perch (Perca Êuviatilis) and sea bass, demonstrating that later hatching larvae are less competitive in terms of growth and survival than earlier hatched individuals (Kestemont et al 2003) However, the initial size heterogeneity seems not to be the key to cannibalism (Kestemont et al 2003) In the present study, the mortality was relatively high The general mortality pattern Êuctuated with a local peak on 16 DPF This likely coincides with the depletion of the energy reserves of nonfeeding larvae The extraordinarily high mortality in three of the experimental tanks may be explained by this, in combination with other unidentiÂed stressors Type II cannibalism was the main cause of mortality Mortality, i.e type II cannibalism or type I mortality was not aĂected by the time of hatching, nor was it diĂerent in the tanks holding a mixture of larvae with diĂerent hatching times Conclusion We report diĂerences in the developmental ratio in larvae with early or late time to hatch Late hatching individuals developed slower However, when sorting Âsh with respect to the hatching time, with the method presented in this paper, we could not detect any relation between hatching and size heterogeneity or cannibalism post Ârst feeding Acknowledgements The authors wish to thank the Financial Instrument for Fisheries Guidance programme and the Danish Ministry of Fisheries, under the administration of the Directorate for Food and Agribusiness for funding the work References Bagarinao T (1986) Yolk resorption, onset of feeding and survival potential of larvae of three tropical marine Âsh r 2010 Blackwell Publishing Ltd, Aquaculture Research, 42, 727^732 731 EĂects of hatching time in pikeperch S Steenfeldt et al Aquaculture Research, 2011, 42, 727^732 species reared in the hatchery Marine Biology 91, 449^ 459 Bang A., Grệnkjìr P & Malte H (2004) Individual variation in the rate of oxygen consumption by zebraÂsh embryos Journal of Fish Biology 64, 1285^1296 Baras E., Maxi M.Y.J., Ndeao M & MeÔlard C (2000) Sibling cannibalism in dorada under experimental conditions II EĂect of initial size heterogeneity, diet and light regime on early cannibalism Journal of Fish Biology 57,1021^1036 Cook J.T., McNiven M.A & Sutterlin A.M (2000) Metabolic rate of pre-smolt growth-enhanced transgenic Atlantic salmon (Salmo salar) Aquaculture 188, 33^45 CuĂ W.R (1980) Behavioral aspects of cannibalism in larval walleye, Stizostedion vitreum Canadian Journal of Zoology 58, 1504^1507 Farrell A.P., Bennett W & Devlin R.H (1997) Growth-enhanced transgenic salmon can be inferior swimmers CanadianJournal of Zoology 75, 335^337 GeĂen A.J (2002) Length of herring larvae in relation to age and time of hatching Journal of Âsh biology 60, 479^485 Hecht T & Applebaum S (1988) Observations on intraspeciÂc aggression and coeval sibling cannibalism by larval and juvenile Clarias gariepinus (Clariidae: Pisces) under controlled conditions Journal of Zoology 214, 21^44 Hokanson K.E.F (1977) Temperature requirements of some percids and adaptations to the seasonal temperature cycle Journal of the Fisheries Research Board of Canada 34, 1524^1550 Jordaan A., Hayhurst S.E & Kling L.J (2006) The inÊuence of temperature on the stage at hatch of laboratory reared Gadus morhua and implications for comparisons of length and morphology Journal of Fish Biology 68,7^24 Kamler E (2008) Resource allocation in yolk-feeding Âsh Reviews in Fish Biology and Fisheries 18, 143^200 Kestemont P., Jourdan S., Houbart M., MeÔlard C., Paspatis M., Fontaine P., Cuvier A., Kentouri M & Baras E (2003) Size heterogeneity, cannibalism and competition in cultured predatory Âsh larvae: biotic and abiotic inÊuences Aquaculture 227, 333^356 Kestemont P., Xueliang X., Hamza N., Maboudou J & Toko I.I (2007) EĂects of weaning age and diet on pikeperch larviculture Aquaculture 264, 197^204 732 Kocan R.M., Hose J.E., Brown E.D & Baker T.T (1996) PaciÂc herring (Clupea pallasi) embryo sensitivity to Prudhoe Bay petroleum hydrocarbons: laboratory evaluation and in situ exposure at oiled and unoiled sites in Prince William Sound Canadian Journal of Fisheries and Aquatic Sciences 53, 2366^2375 Metcalfe N.B & Thorpe J.E (1992) Early predictions of lifehistory events: the link between Ârst feeding date, dominance and seaward migration in Atlantic salmon, Salmo salar L Journal of Fish Biology 41B, 93^99 Methven D.A & Brown J.A (1991) Time of hatching aĂects development, size, yolk volume, and mortality of newly hatched Marcrozoarces americanus (Pisces:Zoarcidae) Canadian Journal of Zoology 69, 2161^2167 Otterễ H & Folkvord A (1993) Allometric growth in juvenile cod (Gadhus morhua) and possible eĂects on cannibalism Journal of Âsh biology 43, 643^645 Regnier T., Bolliet V., Lavonne J & Gaudin P (2010) Assessing maternal eĂects on metabolic rate dynamics along early development in brown trout (salmo trutta): an individualbased approach Journal of Comparative Physiology B 180, 25^31 Smith C & Reay P (1991) Cannibalism in teleost Âsh Reviews in Fish Biology and Fisheries 1, 41^64 Stevens E.D., Sutterlin A & Cook T (1998) Respiratory metabolism and swimming performance in growth hormone transgenic Atlantic salmon Canadian Journal of Fisheries and Aquatic Sciences 55, 2028^2035 Sundstrm L.F., Lohmus M & Devlin R.H (2005) Selection on increased intrinsic growth rates in coho salmon (Oncorhynchus kisutch) Evolution 59, 1560^1569 Van Damme P., Applebaum S & Hecht T (1989) Sibling cannibalism in Koi carp, Cyprinus carpio L., larvae and juveniles reared under controlled conditions Journal of Fish Biology 34, 855^863 Wang N., Xu X & Kestemont P (2009) EĂect of temperature and feeding frequency on growth performances, feed eciency and body composition of pikeperch juvenilis (Sander lucioperca) Aquaculture 289,70^73 r 2010 Blackwell Publishing Ltd, Aquaculture Research, 42, 727^732 Aquaculture Research, 2011, 42, 733^736 doi:10.1111/j.1365-2109.2010.02709.x SHORT COMMUNICATION Effect of feeding regimes on growth and survival of Clarias gariepinus larvae: replacement of Artemia by a commercial feed Michaeôl Vandecan, Amara Diallo & Charles MeÔlard Aquaculture Research and Education Center (CEFRA), University of Lie'ge,Tihange, Belgium Correspondence: C MeÔlard, Aquaculture Research and Education Center (CEFRA), University of Lie'ge, Chemin de la Justice 10, B-4500 Tihange, Belgium E-mail: c.melard@ulg.ac.be The African catÂsh, Clarias gariepinus (Burchell 1822) is one of the most important species currently being farmed Clarias gariepinus is a native species of tropical and subtropical fresh waters It has been widely farmed in heated waters outside its natural range (Hecht & Appelbaum 1987), mainly in intensive culture in recirculating systems The rapid growth even at high density, ability to breathe air and to withstand poor water quality and low food requirement make C gariepinus an excellent Âsh for aquaculture In recirculating systems, larval rearing is the bottleneck in C gariepinus production (Verreth 1994), although great progress has been made on the development of larval diets (Hecht, Ollermann & Verheust 1996) Larvae of African catÂsh are generally weaned with natural food organisms that seem to be a prerequisite for the early larval rearing, and Artemia is often described as a reference diet in larval nutrition studies Using natural food is costly, time consuming and not always available for the Âsh breeder Production of live food also needs adapted structures Recently, an alternative to Artemia live food was developed for the marine hatchery market This new generation of starter feed is described as more digestible, metabolizable and with better formulation s (Gemma micro , Skretting, commercial prospectus) The objective of the present investigation was to assess the possibility to replace partially or totally live food (Artemia nauplii) by a commercial artiÂcial food Larvae of C gariepinus were obtained by artiÂcial reproduction with captive breeders reared in the Aquaculture Research and Education Centre of the r 2010 Blackwell Publishing Ltd University of Lie'ge Larvae were reared in 50-L aquaria in a recirculating system at 28.0 ặ 0.1 1C, pH 7.6 ặ 0.2, with constant aeration (O2 55 ặ 0.8 ppm) and renewal rate (0.5 L 1) Concentrations of total ammonia and nitrites were 0.68 ặ 0.26 and 0.22 ặ 0.26 mg L The experiment was conducted in two phases: during the Ârst 13 days post Ârst feeding (feeding begin 48 h post hatching), larvae were fed with or without A nauplii and with diĂerent feed (six feeding regimes in duplicate, Table 1) at 500 Âsh/50-L aquaria Two s commercial larval feed were used: Gemma micro Skretting (particles size 150^300 mm), a marine lars val feed or Lucky Star (particles size 150^300 mm), a freshwater larval feed Compositions are presented in Table Fish were fed ad libitum six times a day from 09:00 to 17:00 hours When necessary, excess feed was removed from the aquaria at the end of the day In the second phase, from D13 to D32, larvae weaned with the diĂerent regimes were reared at 200 Âsh/50-L aquaria and fed with the same feed s (Lucky Star , particles size 300^500 mm) to evaluate the eĂect of Ârst feeding regimes on growth and survival after the weaning period At the end of each phase, biomass was measured and 50 Âsh were individually weighed SpeciÂc growth rate SGR, food conversion ratio FCR and survival rate were calculated according to the formula: SGR 5100 (lnW2 lnW1) (t2 t1) whereW2 and W1 are mean body weight (g) at day t2 and t1, FCR 5C (Ânal biomass initial biomass) where C is total food 733 Aquaculture Research, 2011, 42, 733736 Feeding regimes C gariepinus larvae M Vandecan et al Table Feeding regimes for Clarias gariepinus larvae from D1 to D32 post Ârst feeding Feeding days 10 11 12 13 s Regime Regime Regime Artemia Artemia Artemia Regime Artemia Regime Regime Lucky Star s Gemma micro 13 ! 32 s Co-feeding Artemia Lucky Star s Co-feeding Artemia Gemma micro s Co-feeding Lucky Star Artemia s Lucky Star s Co-feeding Gemma micro Artemia s Gemma micro Lucky Star s Lucky Star s Lucky Star s Lucky Star s s Lucky Star s Lucky Star distributed during the experimental period and survival Rate Ânal number/initial number Statistical analysis (one way analysis of variance) of growth parameters (Ânal weight between duplicate and among treatments) was performed using STATISTICA software SigniÂcant ANOVAs were followed by an LSD multiple comparison test to identify diĂerences among treatments Mortality data were compared with the Chi-square (w2) test Level of signiÂcance was accepted at Po0.05 In the Ârst phase of the experiment (D1 to D13), growth (Ânal body weight: 66 ặ mg) and survival (92 ặ 4%) of larvae fed with theGemma onlyregime were signiÂcantly higher (Po0.05) than with the other regimes All mixed regimes (Artemias1artiÂcial feeding) showed better growth and survival with s Gemma thanLucky Star (Table 3) In the second phase (follow-up from D14 to D32 after weaning period, same feed for all groups), no growth diĂerence was observed in term of SGR (37.5 ặ 0.6% day 1), or for the FCR (0.7 ặ 0.1) between groups (Table 4) Body weight at D32 was higher for Âsh fed previously with regimes including Gemma: 993 ặ 55 mg vs 820 ặ 82 mg for other regimes Survival of larvae fed previously with regimes including Gemma was higher than the other regimes (83 ặ 4% vs 71 ặ 7%) (Figs1, 2) No external Table Composition of the larval feed Ingredient composition (%) Gemma micro Fish Meal Squid meal Phospholipids Lecithin Wheat gluten Cereals Yeast Vitamins Mineral premix Starch Fish oils Betain Analytical content (%) Protein content Fat content Fiber Ash Moisture Phosphorus Copper Vit A (IU kg 1) Vit D3 (IU/kg 1) Vit E (IU/kg 1) Total n-3 HUFA DHA EPA 71 s Lucky Star s 45 20 412 12 10 5 4 2.5 o5 55 15 13.5 40 000 2800 400 13.3 4.3 7.1 56 1.4 13 10 Not given Table Growth parameters of clarias larvae during the 13-day feeding experiment with diĂerent regimes Initial weight (mg) Final weight (mg) SGR (% day 1) Survival (%) A131L A131G A61L Ar61G L G 3 3 3 21 ặ 0a 22.3 ặ 0.0 69 ặ 2a 52 ặ 4b 29.9 ặ 0.6 75 ặ 6a 22 ặ 6a 22.5 ặ 2.3 64 ặ 4a 37 ặ 0b 27.1 ặ 0.0 75 ặ 7a 16 ặ 1a 19.8 ặ 0.8 72 ặ 8a 66 ặ 3c 31.9 ặ 0.3 92 ặ 4b Means indicated with a diĂerent letter are signiÂcantly diĂerent (Po0.05) s s A, Artemia (during or 13 days); L, Lucky Star ; G, Gemma micro ; SGR, speciÂc growth rate 734 r 2010 Blackwell Publishing Ltd, Aquaculture Research, 42, 733^736 Aquaculture Research, 2011, 42, 733^736 Feeding regimes C gariepinus larvae M Vandecan et al Table Growth parameters of clarias juveniles previously fed with diĂerent feeding schemes from days 14 to 32 A131L Body weight J14 (mg) Body weight J32 (mg) SGR (% day 1) FCR Survival (%) 21 750 36.6 0.7 70 ặ ặ ặ ặ ặ A131G 0a 50a 0.4 0.0 2a 52 930 37.6 0.6 85 ặ ặ ặ ặ ặ A61L 4b 70b 0.5 0.2 1b 22 800 37.0 0.7 79 ặ ặ ặ ặ ặ A61G 6a 80a 0.5 0.1 7b 37 1030 38.3 0.6 78 ặ ặ ặ ặ ặ L 0b 20b 0.1 0.0 2b G 16 910 37.5 0.7 65 ặ ặ ặ ặ ặ 1a 330a 2.1 0.0 18a 66 1020 38.1 0.6 86 ặ ặ ặ ặ ặ 3c 10b 0.1 0.0 1b Means indicated with a diĂerent letter are signiÂcantly diĂerent (Po0.05) s s A, Artemia (during or 13 days); L, Lucky Star ; G, Gemma micro ; SGR, speciÂc growth rate; FCR, food conversion ratio 100 1200 b' Mean weight D13 (mg) 80 a' 70 1000 c a' 60 b' a' b' 800 b 600 50 b 40 30 400 a a Mean weight D32 (mg) 90 a 20 200 10 0 A13+L A13+G A6+L A6+G L G Figure Body weight of clarias after 13 days (feeding regimes experiment) and 32 days (follow-up of growth after wean0 s s ing period) experiment A Artemia (during or 13 days); L, Lucky Star ; G, Gemma micro a,a , b,b , cMeans indicated with a diĂerent letter are signiÂcantly diĂerent (Po0.05) 90 Survival D13 (%) b' a 80 70 100 b b' a a b' a' b' a 90 80 a' a 70 60 60 50 50 40 40 30 30 20 20 10 10 Survival D32 (%) 100 0 A13+L A13+G A6+L A6+G L G Figure Survival of Clarias gariepinus after13 days (feeding regimes experiment) and 32 days (follow-up of growth after 0 s s weaning period) experiment A Artemia (during or 13 days L, Lucky Star ; G, Gemma micro a,a , b,b Means indicated with a diĂerent letter are signiÂcantly diĂerent (Po0.05) evidence of nutritional deÂciencies was present after feeding with the same diet for 18 days No cannibalism was observed in our experiment In our experiment, the growth and survival of the larvae of C gariepinus are in accordance with previous results (Hogendoorn 1980; Verreth & Den r 2010 Blackwell Publishing Ltd, Aquaculture Research, 42, 733^736 735 Aquaculture Research, 2011, 42, 733736 Feeding regimes C gariepinus larvae M Vandecan et al Bieman 1987; Appelbaum & Van Damme 1988; Verreth & Van Tongeren 1989; Appelbaum & Kamler 2000) Previous studies showed that total replacement of live food by commercial feed led to very bad growth and survival performances (Verreth & Van Tongeren 1989; Curnow, King, Bosmans & Kolkovski 2006) Authors assumed that the digestive system was not yet suciently developed before 4^5 days to enable good growth and survival However, Appelbaum and Van Damme (1988) tested an experimental dry food with good growth performances (body weight: 141mg after 15-days feeding), feed utilization and survival (78%) Our experiment using s Gemma micro showed similar performances in term of growth (66 mg after 13-days feeding, 300 mg after 18 days), but a better survival (92% after 13 days) Thanks to the development of high-quality larval feed, we demonstrated the possibility to totally replace live food by an artiÂcial feed Feeding only with the high quality feed without Artemia during weaning period showed best results in terms of growth and survival Higher energy content of this artiÂcial feed combined with a good supply in micro-nutriments (amino acids, phospholipids, vitamins, carotenoids) probably explains this result References Appelbaum S & Kamler E (2000) Survival, growth, metabolism and behaviour of Clarias gariepinus (Burchell 1822) early stages under diĂerent light conditions Aquacultural Engineering 22, 269^287 Appelbaum S & Van Damme P (1988) The feasibility of using exclusively artiÂcial dry feed for the rearing of Israeli Clarias gariepinus (Burchell, 1822) larvae and fry Journal of Applied Ichthyology 4,105^110 Curnow J., King J., Bosmans J & Kolkovski S (2006) The effect of reduced Artemia and rotifer use facilitated by a new microdiet in the rearing of barramundi Lates calcarifer (BLOCH) larvae Aquaculture 257, 204^213 Hecht T & Appelbaum S (1987) Notes on the growth of Israeli sharptooth catÂsh (Clarias gariepinus) during the primary nursing phase Aquaculture 63, 195^204 Hecht T., Ollermann L & Verheust L (1996) Perspectives on clariid catÂshes culture in Africa Aquatic Living Resources 9, 197^206 Hogendoorn H (1980) Controlled propagation of the African catÂsh, Clarias lazera (C & V.): III Feeding and growth of fry Aquaculture 21, 233^241 Verreth J & Den Bieman H (1987) Quantitative feed requirements of African catÂsh (Clarias gariepinus Burchell) larvae fed with decapsulated cysts of Artemia I The eĂect of temperature and feeding level Aquaculture 63, 251^267 Verreth J & van Tongeren M (1989) Weaning time in Clarias gariepinus larvae Aquaculture 83, 81^88 Verreth J (1994) Nutrition and related ontogenetic aspects in larvae of the African catÂsh Clarias gariepinus DSc thesis, Wageningen Agricultural University,Wageningen, 205pp Acknowledgments This study was supported by Electrabel-Suez and the Walloon government (APE project N1 NM 02451) 736 Keywords: C gariepinus, larvae, feeding r 2010 Blackwell Publishing Ltd, Aquaculture Research, 42, 733^736 [...]... Zydlewski and McCormick (1997) Leach and Houde (1999) References Early life-stages in freshwater Âsh F Teletchea & P Fontaine Aquaculture Research, 2011, 42, 630^654 r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654 r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654 Esocidae Esox lucius Vimba vimba Tinca tinca Rutilus rutilus Leuciscus idus Leucapius delineatus Leuciscus cephalus... (2004) Dabrowski (1984b) Radenko and Alimov (1991) References Early life-stages in freshwater Âsh F Teletchea & P Fontaine Aquaculture Research, 2011, 42, 630^654 r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654 r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654 1 1 1 1 1 1 1 1 1 1 1 1 1 1 X X 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 (1) Nematodes Wolnicki,... Kestemont P (1997) EĂects of n-3 fatty acids in Eurasian perch broodstock diet on egg fatty acid composition and larvae stress resistance Aquaculture International 5,1 61^168 r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654 Aquaculture Research, 2011, 42, 630^654 Alderdice D.F (1985) A pragmatic view of early life history studies of Âsh Transactions of the American Fisheries Society 114,... in marine Âsh larvae Aquaculture 200, 161^180 Cahu C.L., Gisbert E.,Villeneuve L.A.N., Morais S., Hamza N., Wold P.-A & Zambonino-Infante J.L (2009) InÊuence of r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654 645 Early life-stages in freshwater Âsh F Teletchea & P Fontaine Aquaculture Research, 2011, 42, 630^654 dietary phospholipids on early ontogenesis of Âsh Aquaculture Research... (2007) Success of nursing ide (Leuciscus idus, L.) fry related to the period of feeding with live food Aquaculture International 15, 255^265 r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654 647 Early life-stages in freshwater Âsh F Teletchea & P Fontaine Aquaculture Research, 2011, 42, 630^654 Hamackova J., Prokes M., Kozak P., Penaz M., Stanny L.A., Policar T & Barus V (2009) Growth... (2007) EĂect of stoking density on survival and growth performances of pikeperch, Sander lucioperca (L.), larvae under controlled conditions Aquaculture International 15, 67^81 r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654 Aquaculture Research, 2011, 42, 630^654 Szlaminska M (1982) Preliminary studies on proteolytic activity in carp (Cyprinus carpio L.) larvae intestines Acta Ichthyologica... Êuviatilis L larvae and juveniles under controlled conditions Aquaculture 268, 149^155 Mansour N., Lahnsteiner F & Patzner R (2009) Physiological and biochemical investigations on egg stickiness in common carp Animal Reproduction Science 114, 256^268 r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654 Aquaculture Research, 2011, 42, 630^654 Martell D.J., KieĂer J.D & Trippel E.A (2006) EĂects... measurement was repeated Âve times If the coecient of variation within these repetitions exceeded 0.4%, the measurements were repeated r 2011 The Authors Journal Compilation r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 655^663 Aquaculture Research, 2011, 42, 655^663 InÊuence of dietary phospholipid on Caspian brown trout A A Kenari et al Table 1 Composition and proximate analyses of the... of Caspian brown trout alevin varied between 2.87 and 3.19 g and were signiÂcantly (Po0.05) higher in treatments fed the PtCho 4 and r 2011 The Authors Journal Compilation r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 655^663 Aquaculture Research, 2011, 42, 655^663 InÊuence of dietary phospholipid on Caspian brown trout A A Kenari et al Table 3 Growth, survival and body lipid content of... in choline provision In the present study, the growth rates were probably not signiÂcantly in- r 2011 The Authors Journal Compilation r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 655^663 659 InÊuence of dietary phospholipid on Caspian brown trout A A Kenari et al Aquaculture Research, 2011, 42, 655^663 120 a 80 60 a b 40 20 0 Lipase specific activity Umg-1 protein Initial 1800 1600 1400