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 scienti¢c
symposia, which are completely dedicated to larval
¢sh and shell¢sh 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 2009’’was 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

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Kaushik, Ronaldo Cavalli, Ivar Ronnestad, Elin KjÖrsvik, Jose¤ Zambonino, Giorgos Koumoundouros, Grete
Baeverfjord, Kristin Hamre, Amos Tandler, Gordon
Bell, Bill Koven, Patrick Kestemont, Luis Conceic°aìo,
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 ¢les of most of
the oral and poster presentations can be found at
www.larvi.ugent.be.
Patrick Sorgeloos,
larvi 2009 conference chairman

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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 Universite¤ ^ INRA,Vandoeuvre-le's-Nancy, France
Correspondence: F Teletchea, URAFPA, Nancy-Universite¤ ^ INRA, 2 avenue de la ForeŒt de Haye, F-545000 Vandoeuvre-le's-Nancy,
France. E-mail:

Abstract
Both egg and larvae are di¡erent between freshwater
and marine ¢sh species. Freshwater ¢sh species have
generally larger and fewer eggs than marine species.
Most freshwater ¢sh species have demersal eggs that
develop stuck to various substrata, such as plants or
gravels, while eggs of most marine ¢sh species develop in the water column. These di¡erences have consequences for both the evaluation of the quality and

the incubation of eggs of freshwater ¢sh species compared with marine species. The larvae of many freshwater ¢sh species are larger and more developed at
hatching than their marine counterparts: thus, larval feeding regimes could be di¡erent and cannibalism may emerge sooner in certain freshwater ¢sh
species. The main di¡erences 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 7 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 ¢rst time

630

set to produce half of the ¢sh 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 re£ects not only the vitality of the
aquaculture sector but also global economic growth
and continuing developments in ¢sh processing and
trade (FAO 2009). Yet, such a rapid development has
been questioned on environmental grounds, in particular its dependence on ¢shmeal supplies for aquatic
feeds, which in turn depend on approximately 25% of
the dwindling marine capture ¢shery (Naylor, Goldburg, Primavera, Kautsky, Beveridge, Clay, Folke, Lubchenco, Mooney & Troell 2000; Tacon & Metian
2008) in conjunction with its potential impacts on
biodiversity, chie£y due to the introduction of alien

species (Hall & Mills 2000; Manchester & Bullock
2000; Casal 2006; De Silva, Nguyen, Abery & Amarasinghe 2006; Innal & Erk’akan 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 ¢n¢sh production reached nearly
31 million tonnes, which came primarily from freshwater species (28 million tonnes), followed by diadromous species (2 million tonnes) and marine

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species (1 million tonnes) (); interestingly, 85% of this total came from 15 species
alone (Lazard & LeveŒque 2009). In Europe, ¢n¢sh
production was approximately 1.6 million tonnes in
2007 (). 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 e¡orts 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 £uviatilis),
pikeperch (Sander lucioperca), burbot (Lota lota) and
tench (Tinca tinca), are considered as potential candidates for the diversi¢cation of inland production in
relation to either large or local market demands
(Fontaine 2009).
The ¢sh life cycle is commonly divided into ¢ve
periods: embryo, larvae, juvenile, adult and senescence, despite the ‘decisive’ threshold separating each
period being open to debate (Balon 1984; KovaŁc› &
Copp 1999; Pen›aŁz 2001; Kamler 2002; Urho 2002).
The sustainable production of a new species requires
gathering biological and zootechnical knowledge on
these ¢ve periods (Falk-Petersen 2005; Bilio 2008;
Bobe & Labbe¤ 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 ¢sh species, (ii) to show their di¡erences 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 ¢sh species, particularly those inhabiting European waters (Teletchea,

Early life-stages in freshwater ¢sh F Teletchea & P Fontaine

Fostier, Kamler, Gardeur, Le Bail, Jalabert & Fontaine
2009).

Egg
Freshwater ¢sh species generally have fewer but larger eggs than marine species, a di¡erence that is not
directly attributable to di¡erences in body size between freshwater and marine ¢sh species (Elgar
1990). However, both freshwater and marine species

show a signi¢cant positively skewed distribution of
egg diameters (Kamler 2005; Teletchea, Gardeur,
Kamler & Fontaine 2009). Most freshwater ¢sh 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
(LÖnning, KjÖrsvik & Falk-Petersen 1988), the majority of eggs are pelagic (Ware1975; Houde1994; Hirst &
Lopez-Urrutia 2006; Teletchea, Gardeur et al. 2009).
These di¡erences may have consequences for both
the evaluation of the quality and the incubation of
eggs of freshwater ¢sh species compared with marine
species, as discussed further below.

Egg quality
Egg quality can be de¢ned as the ability of the egg to
be fertilized and subsequently develop into a normal
embryo (KjÖrsvik, Mangor-Jensen & Holmefjord
1990; Bobe & Labbe¤ 2010). Despite extensive research, variable egg quality remains one of the main
limiting factors for the successful mass production of
¢sh larvae for both freshwater and marine ¢sh species (KjÖrsvik et al. 1990; Kamler 2005; Bobe & Labbe¤
2010). Some of the key factors a¡ecting 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; KjÖrsvik et al.
1990; Tyler & Sumpter 1996; Brooks,Tyler & Sumpter
1997;Thorsen,Trippel & Lambert 2003; Kamler 2005;
Bobe & Labbe¤ 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 ¢sh (reviewed in

Bobe & Labbe¤ 2010; Lubzens, Young, Bobe & CerdaØ
2010). The identi¢cation of predictive estimators or
markers of egg quality would have major applications

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Early life-stages in freshwater ¢sh F Teletchea & P Fontaine

Aquaculture Research, 2011, 42, 630^654

in aquaculture (Bobe & Labbe¤ 2010); however, to date,
no such estimators or markers have been found.
Current methodologies allow non-viable gametes to
be identi¢ed in select species through the assessment
of simple parameters such as buoyancy or appearance (KjÖrsvik et al. 1990; Lahnsteiner, Urbanyi, Horvath & Weismann 2001; Thorsen et al. 2003; Bobe &
Labbe¤ 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
£oat (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 ¢sh species are fertilization and
hatching rates, survival to speci¢c developmental
stages, larval malformations (scoliosis, lordosis), malpigmentation or larval stress tests (KjÖrsvik et al.
1990; Dhert, Lavens & Sorgeloos 1992; Abi-Ayad,

Me¤lard & Kestemont 1997; Planas & Cunha 1999;
Emata, Borlongan & Damaso 2000; KjÖrsvik,
Hoehne-Reitan & Reitan 2003; Thorsen et al. 2003;
AŁlvarez, Racotta, Arjona & Palacios 2004; Avery,
Killen & Hollinger 2009; Bobe & Labbe¤ 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 in£uencing their quality (Alderdice 1985;
Brooks et al. 1997; Kamler 2002). Among these di¡erent 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 a¡ect not only their quality but
also the tissue di¡erentiation 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 intraspeci¢c level, it is now
well established that within a viable temperature

632

range, the time required by fertilized ¢sh eggs to incubate decreases with increasing temperature, with
all other factors being equal. This negative correlation has been found for both marine ¢sh species,
e.g. for Atlantic cod (Ge¡en, Fox & Nash 2006) or haddock (Melanogrammus aegle¢nus) (Martell, Kie¡er &
Trippel 2006) and freshwater ¢sh species, such as
salmonids (Elliott et al. 1987) or cyprinids (Keckeis,

Kamler, Bauer-Nemeschkal & Schneeweiss 2001;
Kupren, Mamcarz, Kucharczyk, Prusinìska, Krejsze¡
2008). At the interspeci¢c level, a negative relationship between incubation time and water temperature
was also found for marine ¢sh species (Pauly & Pullin
1988; Pepin 1991) and freshwater ¢sh species (Teletchea, Gardeur et al. 2009) (Table1). Egg diameter also
slightly in£uences the incubation time in both marine and freshwater ¢sh 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 ¢t 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 ¢sh
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 ¢rstly, 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; LÖnning et al.1988;Wiegand 1996; Bonislawska, Formicki, Korzelecka-Orkisz & Winnicki
2001; Kamler 2005; Teletchea & Fontaine 2010).
Eggs of teleost ¢sh are surrounded with a relatively
thick proteinaceous layer, which is called the chorion, egg shell or zona radiata (LÖnning et al. 1988;
Kunz 2004; Lubzens et al. 2010). The zona radiata has
both structural and morphological di¡erences depending on the systematic position and ecology of
¢sh 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 ¢sh 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;

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Early life-stages in freshwater ¢sh F Teletchea & P Fontaine

Table 1 Relationships between oocyte diameter (+), incubation time (t), water temperature (T) and larval size at hatching (L)
for teleost, mostly temperate, ¢sh species

Variables
t and T

r2

n

Range of
+ (mm)

Range of
t (days)

Range of
T ( 1C)

Range of
L (mm)

t 5 18.7e
t 5 186.23e À 0.197T

0.81
0.87

124
65

–
–

–
1.3–95.0

–
3.0–23.5

–
–

0.82

80

0.60–3.40 0.4–12

2.8–29.5

–

0.85
0.92

124
65

0.44–3.40 –
0.75–6.55 1.3–95.0

–
3.0–23.5

–
–

Pepin (1991)
Teletchea, Gardeur
et al. (2009)

M
M
M

log10t 5 7.1010.608
log10 + À 4.09 log10
(T126)
t 5 16.1e À 0.099T +0.44
Log10t 5 3.00210.599

log10 + – 1.91 log10
(T12)
L 5 1.9611.89 +
L 5 2.89 +0.89
L 5 2.82 +0.958

0.40
0.62
0.70

100
187
219

0.80–9.70 –
–
–
0.30–6.40 –

–
–
–

1.60–17.60
–
1.20–30.00

F

L 5 1.0513.10 +

0.89

65

0.75–6.55 –

–

2.25–21.50

Miller et al. (1988)
Pepin (1991)
Chambers and
Leggett (1996)
Teletchea and
Fontaine (2010)

Species Equations
M
F

t and T, + M

M
F

Ø and L

À 0.1077T

References
Pepin (1991)
Teletchea, Gardeur
et al. (2009)
Pauly and Pullin
(1988)

F, freshwater; M, marine; n, number of species studied; À, values not indicated.

Teletchea, Fostier et al. 2009). In cyprinids, arti¢cial
incubation is usually carried out in inverted bottles
provided with a continuous water £ow (Carral, Celada, SaŁez-Royuela, Rodr|¤ 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 ¢sh eggs: separating individual eggs mechanically, scouring
them physically with abrasives (¢ne 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, ¢ne 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 ¢sh species are

generally di¡erent 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). Di¡erent types of incubators have been
developed according to the speci¢city of the eggs of the
targeted freshwater ¢sh 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 Pen›aŁz 1983; Balon 1984, 1986; Hensel 1999;
KovaŁc› & Copp 1999; Pen›aŁz 2001; Kamler 2002, 2008;
Urho 2002). Nevertheless, hatching is a major turning point from ecological, physiological and behavioural points of view (Pen›aŁz 2001; Kamler 2002). A
substantial variability in the stage of morphological
development at hatching was found both between
and within marine and freshwater ¢sh species (Pen›aŁz 1983, 2001; Miller et al. 1988; Falk-Petersen 2005;
Teletchea & Fontaine 2010). For instance, LÖnning
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 ¢sh belonging to the Salmonoi-

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Early life-stages in freshwater ¢sh F Teletchea & P Fontaine

Aquaculture Research, 2011, 42, 630^654

Table 2 Main products tested for removing the stickiness of ¢sh 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

Penˇa´z 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)
Penˇa´z, Wohlgemuth, Hamackova and Kouril
(1981)
Penˇa´z, Prokes, Kouril and Hamackova (1989)
Ferna´ndez 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, Pen›aŁz (1983) found that hatching was speciesspeci¢c, 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 ¢sh species
were not ¢xed in ontogeny and were not directly related to either larval size or degree-days for incubation, but were probably species-speci¢c. 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 intraspeci¢c 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 (Pen›aŁz 1983; Blaxter 1992; Urho 2002; Jordaan,
Hayhurst & Kling 2006). Conspeci¢c 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

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Early life-stages in freshwater ¢sh F Teletchea & P Fontaine

Table 3 Examples of devices used for incubating temperate freshwater ¢sh eggs

Species
Anguillidae
Anguilla anguilla
Clupeidae
Alosa alosa

Zoug
jar

Weiss Tray-type Petri
jar
incubators dish

Others

4 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

Penˇa´z 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, Ve´ron, 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
Penˇa´z (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)
Penˇa´z, Prokes, Kouril and Hamackova (1983)
Brzuska and Bialowas (2002)
Horvath et al. (2007)
Penˇa´z 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
Penˇa´z et al. (1981)
Penˇa´z et al. (1989)
Kamler, Szlaminska, Hamackova, Kouril, Vachta,
Stibranyiova and Asenjo (1995)
Ferna´ndez San Juan (1995)
Gela et al. (2003)

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635


Early life-stages in freshwater ¢sh F Teletchea & P Fontaine

Aquaculture Research, 2011, 42, 630^654

Table 3 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)
Vehnia¨inen, Ha¨kkinen 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
Keina¨nen, Tigerstedt, Kalax and Vuorinen (2003)
Glass jars
Ylo¨nen 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
Bra¨nna¨s (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)

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Aquaculture Research, 2011, 42, 630^654

Early life-stages in freshwater ¢sh F Teletchea & P Fontaine

Table 3 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 Franc¸ois and Blier (2003)
Wedekind and Mu¨ller (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)
Penˇa´z (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 (Ge¡en 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 (Ge¡en 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 signi¢cance and occur over a wide range of developmental
stages (Dabrowski 1984a; Blaxter 1992; Urho 2002;

Kunz 2004; Falk-Petersen 2005; Yu¤fera & 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 (Pen›aŁz 1983; Miller et al.
1988; Cahu & Zambonino-Infante 2001; Yu¤fera &

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 ¢sh species
(Pen›aŁz 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 interspeci¢c level, a
signi¢cant positive correlation was found between
oocyte diameter and larval size at hatching among
marine and freshwater ¢sh species (Ware1975; Miller
et al. 1988; KjÖrsvik et al. 1990; Pepin 1991; Chambers
& Leggett 1996; Teletchea & Fontaine 2010). However,
the three equations based on marine species (Table 1)
poorly ¢t the dataset of 65 freshwater ¢sh species
(Teletchea & Fontaine 2010) primarily because the
models greatly underestimate the larval size at hatching, especially for larger eggs (see Teletchea & Fontaine 2010). This con¢rms the notion that marine
species generally produce smaller larvae than freshwater ¢sh species do (Balon 1984). For instance,
Houde (1994) measured a 10-fold di¡erence in the

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637


Early life-stages in freshwater ¢sh F Teletchea & P Fontaine

Aquaculture Research, 2011, 42, 630^654

mean weight at hatching between marine (37.6 mg;
n 5 77) and freshwater (359.7 mg; n 5 20) larvae.
No larva can feed before it is functionally capable
(i.e., its mouth and digestive system must have developed), but it must feed before reaching irreversible
starvation or a ‘point of no return’ (Miller et al. 1988).
Miller et al. (1988) and Pepin (1991) found that larger
larvae at hatching are generally more resistant to
starvation because they have more energy reserves
than small larvae, but more importantly, they have a
greater £exibility (window of opportunity) in ¢rst
feeding times. The period between the mouth opening and the ‘point of no return’ is species-speci¢c and
also depends on water temperature, ranging approximately from 3 days in temperate waters to 20 days in
cold waters (Yu¤fera & Darias 2007). In conclusion,
the larvae of many freshwater ¢sh species are larger
and more developed than their marine counterparts;
thus, feeding regimes could be di¡erent and cannibalism may emerge sooner in certain freshwater ¢sh
species, as is discussed further below.

Implications for the larviculture of
freshwater ¢sh species
The transition from yolk sac larvae to actively feeding
larvae is considered to be the most critical event during the early life of larval ¢sh (Roche-Mayzaud, Mayzaud & Audet 1998; Yu¤fera & Darias 2007). To achieve

this transition successfully, all structures and organs
related with food uptake, digestion and assimilation
have to be ready in time and the appropriate food
has to be available by the time the yolk is depleted
(Yu¤fera & Darias 2007). The two main limitations at
the beginning of exogenous feeding of larvae are
mouth gape, restricting the particle size (a prey/gape
ratio of 25^50% seems to be the most appropriate),
and larval length, which restricts swimming activity
and therefore hunting success (Dabrowski 1984a;
Miller et al.1988; Planas & Cunha 1999;Yu¤fera & Darias 2007). In order to avoid mass mortalities due to
starvation, an appropriate diet must be provided to
the larvae when they ¢rst begin feeding. Two main
kinds of diet are available for ¢sh larvae: live prey
and compound or formulated diet.
For marine ¢sh species, the feeding regimes of larvae begin with live prey, usually rotifers (Brachionus
spp.) and brine shrimp (Artemia spp.) nauplii for the
early life stages; then larvae are weaned to formulated feeds (Rainuzzo, Reitan & Olsen 1997; Planas &
Cunha 1999; Langdon 2003; Lee 2003; Conceic°aìo,

638

Aragaìo, Richard, Engrola, Gavaia, Mira & Dias 2010;
Conceic°aìo,Yu¤fera, Makridis, Morais & Dinis 2010). In
the past 25 years, e¡orts have been made to develop
new formulated diets in order to partially or totally
replace live feeds for rearing the early larval stages of
several marine species (Planas & Cunha 1999; Shields
2001; Langdon 2003; Lee 2003; Conceic°aìo, Aragaìo
et al. 2010; Conceic°aìo,Yu¤fera et al. 2010). This substitution of live prey is crucial for reducing production

costs and for sustaining the production of high- and
constant-quality juveniles (Cahu & Zambonino-Infante 2001). Several factors must be considered when
developing formulated diets, including homogeneous
composition, digestibility, nutritional value, palatability, water stability and an optimum size to ensure that
larvae can detect and ingest them (Rainuzzo et al.
1997; Planas & Cunha 1999; Cahu & Zambonino-Infante 2001; Lee 2003; Cahu, Gisbert,Villeneuve, Morais, Hamza, Wold, Zambonino-Infante 2009).
Currently, formulated diets are still not adequate
when used exclusively to rear marine ¢sh larvae
(Langdon 2003; Lee 2003; Conceic°aìo, Aragaìo et al.
2010; Conceic°aìo, Yu¤fera et al. 2010). The poor performance of formulated diets is related partly to the inadequate incorporation of nutrients into the
diets in conjunction with poor ingestion, digestion
and/or assimilation (Planas & Cunha 1999; Cahu &
Zambonino-Infante 2001; Langdon 2003; Lee 2003).
However, results are markedly improved when
formulated diets are co-fed with live prey (Planas &
Cunha 1999; Langdon 2003). Co-feeding not only stimulates the ingestion of food particles but also promotes digestion and assimilation of formulated diets
by ¢sh larvae (Lee 2003). Any failure or limitation in
the nutrients and energy uptake during the feeding
onset period a¡ects the correct development of organs and structures and the subsequent growth and
survival of the larvae (Yu¤fera & Darias 2007; Shan,
Huang, Cao & Wu 2008; Conceic°aìo, Aragaìo et al.
2010; Conceic°aìo, Yu¤fera et al. 2010). Environmental
factors such as water temperature, salinity, light intensity and microalgae (green water) can all in£uence
the feeding of larvae (Dabrowski 1984a; Planas &
Cunha 1999; Dou, Masuda, Tanaka & Tsukamoto
2005). For instance, light is of primary importance in
marine larviculture, as most marine ¢sh larvae are visual feeders (Planas & Cunha 1999; Cahu & Zambonino-Infante 2001; Yu¤fera & Darias 2007). Temperature
is generally considered to be a major factor in determining the advent of endogenous feeding of ¢sh larvae because of its direct e¡ects on their oxygen
consumption, yolk exhaustion rate, feeding activity

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Aquaculture Research, 2011, 42, 630^654

and food conversion e⁄ciency (Pepin 1991; Blaxter
1992; Kamler 2002; Dou et al. 2005). In intensive rearing tanks in European hatcheries, the formation of an
oily ¢lm on the water surface impedes the access of
larvae to the surface and thus inhibits air intake by
physostomous larvae, particularly seabass and seabream, which could lead to both skeletal deformities
and poor growth and resistance (Planas & Cunha
1999). Excessive turbulence can also inhibit in£ation
of the swimbladder (Planas & Cunha 1999).
For some freshwater ¢sh species, such as pike (Esox
lucius), coregonids (Coregonus spp.) and salmonids, it
is believed that larvae can be fed formulated diets as
early as mouth opening (Dabrowski 1984a; Cahu &
Zambonino-Infante 2001); see also Table 4. Yet, for
other species, and particularly cyprinids, the larval
ability to utilize formulated diets from the ¢rst feeding is low (Dabrowski 1984a; Wolnicki 2005; Kamler
& Wolnicki 2006). Thus, feeding regimes need to begin with live prey for at least 5 days, and sometimes
not less than 8^12 days are required before larvae
can be weaned to formulated feeds (Dabrowski
1984a; Wolnicki 2005). For instance, satisfactory
growth performance and/or survival were not
achieved when exclusively formulated diets were fed
to larval asp (Aspius aspius), gudgeon (Gobio gobio),
chub (Leuciscus cephalus), dace (Leuciscus leuciscus)
or tench (Wolnicki 2005; Wolnicki, Sikorska &
Kaminìski 2009). In fact, only a few cyprinids demonstrate relatively fast growth and high survival rates

when fed formulated diets exclusively from the very
beginning of exogenous feeding, these include barbel
(B. barbus), gold¢sh (Carassius auratus), nase (Chondrostoma nasus), roach (Rutilus rutilus) and vimba
(Vimba vimba) (Wolnicki 2005; Wolnicki et al. 2009).
Morphological (particularly mouth size) and functional di¡erences between ¢sh species and during
ontogenesis may, to some extent, explain the nutritional constraints in the acceptance and assimilation
of a formulated diet (Dabrowski1984a). To our knowledge, no extensive review on the nutritional requirements of freshwater larvae has been performed
which matches the works on marine ¢sh species (Planas & Cunha1999; Cahu & Zambonino-Infante 2001;
Langdon 2003; Cahu et al. 2009; Conceic°aìo, Aragaìo
et al. 2010; Conceic°aìo, Yu¤fera et al. 2010). However, it
is clear that problems due to sub-nutrition or other
environmental parameters observed in marine ¢sh
species (such as low growth and high mortalities, as
well as malformations) are also often encountered in
the larviculture of freshwater species such as rudd
Scardinius erythrophthalmus (Wolnicki et al. 2009),

Early life-stages in freshwater ¢sh F Teletchea & P Fontaine

Eurasian perch (Tamazouzt, Leray, Esca¡re & Terver
1998; Tamazouzt, Chatain & Fontaine 2000) or
pikeperch (Schlumberger, Proteau & Albiges 1993;
Hamza, Mhetli, Khemis, Cahu & Kestemont 2008).
Therefore, a better understanding of the speci¢c nutritional requirements of larvae of freshwater ¢sh
species is needed.
Cannibalism is the act of killing and consuming
the whole, or a major part, of a conspeci¢c individual
(Smith & Reay 1991). Cannibalistic behaviour is reported in a large number of both marine and freshwater ¢sh species occupying di¡erent habitats and
pursuing di¡erent life-history strategies, but it is particularly common in piscivorous and parental caregiving species (Smith & Reay 1991; Hecht & Pienaar
1993). Piscivores often have a large gape and wellformed teeth, allowing them to consume relatively

large prey, which advances the onset of cannibalism
(Smith & Reay 1991). Non-piscivorous species can
also exhibit sibling (intracohort) cannibalism in larviculture, such as common carp (Table 5). From a
functional viewpoint, ¢sh can start cannibalizing as
soon as the structures required for suction feeding
are developed. This can take place as early as the start
of exogenous feeding in certain species, although
most ¢sh species start exerting cannibalism much later (Baras & Jobling 2002). Owing to the fact that the
larvae of many freshwater ¢sh species are larger and
more developed at hatching than that of their marine
counterparts, cannibalism may emerge sooner
(Baras & Jobling 2002). For instance, pike, pikeperch
and Eurasian perch are three freshwater piscivorous
¢sh species in which cannibalism occurs quite early
in the development (Table 5). On the contrary, even
though seabass is a piscivorous species, cannibalism
is not observed in young stages (Cahu & ZamboninoInfante 2001). There are two types of cannibalism:
partial ingestion of prey, mainly tail ¢rst (type I), and
complete cannibalism, with a head-¢rst ingestion of
prey (type II) (Baras & Jobling 2002; Kestemont, Jourdan, Houbart, Me¤lard, Paspatis, Fontaine, Cuvier,
Kentouri & Baras 2003). Type I precedes type II cannibalism, because the caudal peduncle of a ¢sh
is generally much smaller than the gape of a ¢sh of
similar size. Type I cannibalism does not require the
predator to prey size ratio to be large (Hecht & Pienaar 1993; Folkvord 1997; Baras & Jobling 2002). The
switch to type II cannibalism occurs as size heterogeneity develops, i.e., when some ¢sh have gained su⁄ciently from type I cannibalism to have a large size
advantage over others (Baras & Jobling 2002). In theory, intracohort type II cannibalism can persist as

r 2011 Blackwell Publishing Ltd, Aquaculture Research, 42, 630^654

639

640

Carassius carassius

Blicca bjoerkna
Carassius auratus

Barbus barbus

Aspius aspius

Alburnus alburnus
Aristichthys nobilis

Cyprinidae
Abramis brama

Centrarchidae
Micropterus salmoides
Cobitidae
Cobitis taenia

1

1

1
1

1
1

1
1
1
1

1

1
1

1
1

1

1
1
1
1
1

1

Clupeidae
Alosa alosa

Alosa sapidissima

Artemia

Species

1

Rotifer

1

1
2

1
1
1
1

2

1

2

1

Zooplankton

X

X

X
X

X

X
X

X

Co-feeding

Table 4 Examples of ¢rst-feeding regimes used for freshwater ¢sh species

2
1

2

1

2

1
1

1

3

1
1

1

Dry feed

(1) Tubificids
(1) Tubificids

(1) Nematodes
(1) Nematodes

Others

Penˇa´z and Gajdusek (1979)
Mooij (1989)
Kucharczyk, Luczynski, Kujawa, Kaminski, Ulikowski
and Brzuzan (1998)
Gerasimov and Stolbunov (2007)
Keckeis and Schiemer (1992)
Dabrowski and Bardega (1984)
Dabrowski (1984b)
Rottmann, Shireman and Lincoln (1991)
Santiago, Gonzal, Ricci and Harpaz (2003)
Ostaszewska (2002)
Kujawa, Mamcarz and Kucharczyk (2007)

Krupka (1988)
Krupka and Meszaros (1993)
Wolnicki and Gorny (1995a)
Calta (1998)
Policar et al. (2007)
Mooij (1989)
Battle (1940)
Kaiser, Endemann and Paulet (2003)
Coutinho, Rema, Otero, Pereira and Fabregas (2006)
Laurila and Holopainen (1990)

Bohlen (1999)
Bohlen and Ritterbusch (2000)

Roncarati, Vicenzi, Melotti and Dees (2005)

Leguen et al. (2007)
Bardonnet and Jatteau (2008)
Wiggins et al. (1985)
Limburg and Ross (1995)
Johnson and Dropkin (1995)
Zydlewski and McCormick (1997)
Leach and Houde (1999)

References

Early life-stages in freshwater ¢sh F Teletchea & P Fontaine
Aquaculture Research, 2011, 42, 630^654

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Esocidae
Esox lucius

Vimba vimba

Tinca tinca

Rutilus rutilus

Leuciscus idus

Leucapius delineatus
Leuciscus cephalus

Cyprinus carpio

Ctenopharyngodon idella

Chondrostoma toxostoma

Chondrostoma nasus

1

1
1

1
1
1

1
2
1
1
1
1
1
1
1

1

1

1

1

1
1
1
1

1

1

1
1
1

1
1

1

2

3
1

1

1

1
1

1
1

X

X

X

X
X
X

X
X

X

X

1
2

1

2
1
1

2
2
1
1

2

1

1
1
1
1
1
2

1
1
2
1
1
1
1
(1) Nematodes

Giles, Wright and Nord (1986)
Kucharczyk, Mamcarz, Kujawa and Skrzypczak (1997)
Wolska-Neja and Neja (2006)

Pinder and Gozlan (2004)
Penˇa´z (1968)
Calta (2000)
Harzevili, De Charleroy, Auwerx, Vught and Van Slycken (2003)
Wolnicki and Gorny (1995b)
Harzevili, Vught, Auwerx and De Charleroy (2004)
Hamackova, Lepicova, Prokes, Lepic, Kozak, Policar and Stanny (2007)
Keckeis and Schiemer (1992)
Nzau Matondo et al. (2007)
Paull, Lange, Henshaw and Tyler (2008)

Wolnicki and Korwin-Kossakowski (1993)
Kamler et al. (1995)
Ferna´ndez San Juan (1995)
Wolnicki, Kaminski and Myszkowski (2003)
Carral et al. (2006)
Celada, Carral, Rodriguez, Saez-Royuela, Aguilera, Melendre
and Martin (2007)
Ostaszewska, Dabrowski, Hliwa and Kwasek (2008)
Hamackova, Prokes, Kozak, Penˇa´z, Stanny, Policar and Barus (2009)

Wolnicki and Myszkowski (1998)
Spurny, Fiala and Mares (2004)
Ostaszewska, Boruta and Olejniczak (2005)
Sysa, Ostaszewska and Olejniczak (2006)
Gozlan, Copp and Tourenq (1999)
Dabrowski (1984b)
Opuszynski, Shireman, Aldridge and Rottmann (1985)
Rottmann et al. (1991)
Woynarovich (1962)
Szlaminska (1982)
Charlon and Bergot (1984)
Dabrowski (1984b)
Van Damme, Appelbaum and Hecht (1989)
Kamler, Szlaminska, Przybyl, Barska and Jakubas (1990)
Carvalho, Escaffre, Oliva Teles and Bergot (1997)
Ito, Sano, Kurita, Yuasa and Iida (2007)

Aquaculture Research, 2011, 42, 630^654
Early life-stages in freshwater ¢sh F Teletchea & P Fontaine

641


642

Coregonus clupeaformis

Salmonidae
Coregonus albula

1
1

1

1

Sander lucioperca

Sander vitreus

1
1
1

Perca fluviatilis

1
1
1

1

1
2
2

Artemia

2
1
1

Percidae
Perca flavescens

Moronidae
Morone saxatilis

Ictaluridae
Ictalurus punctatus

Hypophthalmichthys molitrix

Gadidae
Lota lota

Species

Table 4 Continued

1

1

1
1
1

1
1

1
1
1

1
1

1

Zooplankton

1
1

1
1

Rotifer

X

X

X

X

X

X

Co-feeding

1
1

1

2

1

3
1
2
1
2
2

1

1
1
1

1
1

Dry feed

Others

Jezierska, Korwinn-Kossakowski and Jowko (1979)
Luczynski, Majkowski, Bardega and Dabrowski (1986)
Dostatni and Luczynski (1991)
Taylor and Freeberg (1984)
Drouin et al. (1986)
Zitzow and Millard (1988)

Tamazouzt et al. (1998)
Tamazouzt et al. (2000)
Mandiki et al. (2007)
Ostaszewska (2005)
Szkudlarek and Zakes (2007)
Li and Mathias (1982)
Krise and Meade (1986)

Brown, Dabrowski and Garling (1996)
Fulford, Rice, Miller, Binkowski, Dettmers and Belonger (2006)

Kestemont, Me´lard, Fiogbe´, Valnonou and Masson (1996)
Me´lard, Baras, Mary and Kestemont (1996)

Braid and Shell (1981)
Eldridge et al. (1982)
Martin-Robichaud and Peterson (1998)
Macintosh and Duston (2007)

Hecht (1996)
El-Saidy, Dabrowski and Bai (2000)
Sink and Lochman (2008)

Wolnicki, Kaminski and Myszkowski (2002)
Harzevili, De Charleroy, Auwerx, Vught, Van Slycken, Dhert and Sorgeloos (2003)
Harzevili, Dooremont, Vught, Auwerx, Quataert and De Charleroy (2004)
Dabrowski (1984b)
Radenko and Alimov (1991)

References

Early life-stages in freshwater ¢sh F Teletchea & P Fontaine
Aquaculture Research, 2011, 42, 630^654

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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
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(1) Nematodes

Wolnicki, Przybyl and Starzonek (1998)
Krzemieniewski, Teodorowicz, Debowski and Pesta (2004)
Kozaric, Kuzir, Petrinec, Gjurcevic and Bozic (2008)

Harris and Hulsman (1991)
Flu¨chter (1980)
Ro¨sch and Appelbaum (1985)
Luczynski et al. (1986)
Champigneulle (1988)
Segner, Ro¨sch, Schmidt, von Poeppinghausen (1988)
Champigneulle and Rojas-Beltran (1990)
Schlechtriem, Ricci, Focken and Becker (2004)
Ylo¨nen and Karjalainen (2004)
Witkowski and Kokurewicz (1981)
Escaffre and Bergot (1985)
Barrows, Gaylord, Stone and Smith (2007)
Geurden, Aramendi, Zambonino-Infante and Panserat (2007)
Lizardo-Daudt and Kennedy (2008)
Bazyar Lakeh, Ahmadi, Safi, Ytrestøyl and Bjerkeng (2010)
Gunnes (1979)
Jarrams (1979)
Holm (1986)
Eskelinen (1989)
Jarrams (1979)
Hansen (1985)
Wallace and Aasjord (1984)
Guillard et al. (1992)

De March (1995)
Lemieux et al. (2003)
Roche-Mayzaud et al. (1998)
Gunn and Noakes (1987)
Gunther et al. (2005)
Penˇa´z (1975)
Carmie and Jonard (1988)
Honkanen et al. (2005)

1, type of food given ¢rst; 2, type of food given second after few days. Co-feeding (if present: X) 5 period during which both live preys (Rotifer, Artemia or plankton) and dry feed are given to larvae. This cofeeding could occur just after the larvae start feeding or after a period of time when only one of the two types of food is given to larvae.

Siluridae
Silurus glanis

Thymallus thymallus

Salvelinus fontinalis
Salvelinus namaycush

Salvelinus alpinus

Salmo trutta

Salmo salar

Hucho hucho
Oncorhynchus mykiss

Coregonus lavaterus

Aquaculture Research, 2011, 42, 630^654
Early life-stages in freshwater ¢sh F Teletchea & P Fontaine

643


Early life-stages in freshwater ¢sh F Teletchea & P Fontaine

Aquaculture Research, 2011, 42, 630^654

Table 5 List of the freshwater temperate species where
cannibalism has been found at the larval stages
Species
Cyprinidae
Cyprinus carpio
Cenrarchidae
Micropterus
salmoides
Esocidae
Esox lucius

Moronidae
Morone saxatilis
Percidae
Perca fluviatilis

Sander lucioperca

Sander vitreus

Siluridae
Silurus glanis

References

Charlon and Bergot (1984)
Van Damme et al. (1989)
Roncarati et al. (2005)

Bry and Gillet (1980)
Giles et al. (1986)
Bry, Basset, Rognon and Bonamy (1992)
Kucharczyk et al. (1997)
Braid and Shell (1981)
Kestemont et al. (1996)
Me´lard et al. (1996)
Mandiki et al. (2007)
Schlumberger et al. (1993)
Hilge and Steffens (1996)
Szkudlarek and Zakes (2007)
Li and Mathias (1982)
Krise and Meade (1986)
Moodie et al. (1989)
Colesante (1996)
Summerfelt (1996)

Conclusions

Wolnicki et al. (1998)
Kozlowski and Poczyczynski (1999)

long as siblings small enough to be consumed by
the cannibal are available (Baras & Jobling 2002).
Cannibalism is thus facilitated by size heterogeneity,
but it also a¡ects size heterogeneity, as the smallest
¢sh are consumed by the largest ones, and it can be
viewed as both a cause and a consequence of size heterogeneity (Hecht & Pienaar 1993; Baras & Jobling
2002; Kestemont et al. 2003). Even though cannibalism is genetically determined (Hecht & Pienaar1993),
many environmental biotic and abiotic factors appear to a¡ect the extent of the rate of cannibalism;
these include food availability, population density, refuges, water clarity, light intensity, feeding frequency
and the frequency at which alternative prey is presented (Smith & Reay 1991; Hecht & Pienaar 1993;
Baras & Jobling 2002). In larviculture, cannibalism
can cause signi¢cant losses, particularly when the
size variation in the population is su⁄ciently large,
because of high stocking densities, lack of alternative
live food and absence of refuges from predation
(Smith & Reay 1991; Folkvord 1997; Baras & Jobling
2002). The complete elimination of cannibalism in
larviculture is probably impossible (Baras & Jobling

644

2002); however, it is possible to mitigate cannibalism,
notably by frequent grading to reduce size variability
(Smith & Reay 1991). The value of mitigating cannibalism in larviculture in both freshwater and marine
species is a matter of cost-e¡ectiveness, which depends on labour costs and the productivity of rearing
systems (Baras & Jobling 2002).
The progeny of most species must disperse after
hatching (species with pelagic eggs start earlier) and
others after a short inactive period (Urho 2002). The

way in which larvae of di¡erent species disperse seems
to depend on their morphology and development stage
at hatching (Urho 2002). In freshwater ¢sh species,
some remain nearly motionless during the entire period of yolk resorption, such as pike or bream (Abramis
brama), while others, such as burbot or pikeperch, disperse immediately after hatching (Teletchea, Fostier
et al. 2009;Teletchea & Fontaine 2010).

Both egg and larvae di¡er in many respects between
marine and freshwater ¢sh species. These di¡erences
have consequences for aquaculture practices, particularly for the evaluation of the quality of the egg,
the incubation of adhesive eggs, the ¢rst feeding of
larvae and the onset of cannibalism. Further experiments are required to improve the current methods
for removing the adhesiveness of eggs of freshwater
¢sh species, particularly for some cyprinids. In addition, studies that focus on the speci¢c nutritional requirements of larvae of freshwater ¢sh species,
including the in£uence of dietary phospholipids
(Cahu et al. 2009) and the importance of live prey
and formulated diets in larviculture (Shields 2001;
Conceic°aìo, Aragaìo et al. 2010; Conceic°aìo,Yu¤fera et al.
2010), are needed in order to improve growth and reduce both mortalities and deformities.

Acknowledgment
We thank Andrew Davie and two anonymous reviewers who helped to improve the manuscript.

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