ArticlePDF AvailableLiterature Review

Control of puberty in farmed fish

June 2009
General and Comparative Endocrinology 165(3):483-515

June 2009
165(3):483-515

DOI:10.1016/j.ygcen.2009.05.004

Source
PubMed

Authors:

Geir Lasse Taranger

Institute of Marine Research in Norway

Manuel Carrillo

Spanish National Research Council

Rüdiger Schulz

Utrecht University

Pascal Fontaine

University of Lorraine

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Puberty comprises the transition from an immature juvenile to a mature adult state of the reproductive system, i.e. the individual becomes capable of reproducing sexually for the first time, which implies functional competence of the brain-pituitary-gonad (BPG) axis. Early puberty is a major problem in many farmed fish species due to negative effects on growth performance, flesh composition, external appearance, behaviour, health, welfare and survival, as well as possible genetic impact on wild populations. Late puberty can also be a problem for broodstock management in some species, while some species completely fail to enter puberty under farming conditions. Age and size at puberty varies between and within species and strains, and are modulated by genetic and environmental factors. Puberty onset is controlled by activation of the BPG axis, and a range of internal and external factors are hypothesised to stimulate and/or modulate this activation such as growth, adiposity, feed intake, photoperiod, temperature and social factors. For example, there is a positive correlation between rapid growth and early puberty in fish. Age at puberty can be controlled by selective breeding or control of photoperiod, feeding or temperature. Monosex stocks can exploit sex dimorphic growth patterns and sterility can be achieved by triploidisation. However, all these techniques have limitations under commercial farming conditions. Further knowledge is needed on both basic and applied aspects of puberty control to refine existing methods and to develop new methods that are efficient in terms of production and acceptable in terms of fish welfare and sustainability.

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Control of puberty in farmed ﬁsh

Geir Lasse Taranger

a,*

, Manuel Carrillo

, Rüdiger W. Schulz

a,c

, Pascal Fontaine

, Silvia Zanuy

, Alicia Felip

Finn-Arne Weltzien

, Sylvie Dufour

, Ørjan Karlsen

, Birgitta Norberg

, Eva Andersson

, Tom Hansen

Institute of Marine Research, PO Box 1870 Nordnes, 5817 Bergen, Norway

Spain Instituto de Acuicultura de Torre de la Sal – CSIC, Torre de la Sal S/N, 121595 Ribera de Cabanes, Castellón, Spain

Utrecht University, Science Faculty, Department Biology, Padualaan 8, NL-3584 CH Utrecht, The Netherlands

Unité de Recherche Animal et Fonctionnalités des Produits Animaux, Nancy-Université, INRA, 2 avenue de la Forêt de Haye, B.P. 172, F-54505 Vandoeuvre-lès-Nancy, France

University of Oslo, Department of Molecular Biosciences, 0316 Oslo, Norway

USM 0401, UMR 5178 CNRS/MNHN/UPMC Biologie des Organismes Marins et Ecosystèmes, Département des Milieux et Peuplements Aquatiques,

Muséum National d’Histoire Naturelle, 75005 Paris, France

Institute of Marine Research, 5392 Austevoll, Norway

Institute of Marine Research, 5984 Matredal, Norway

article info

Article history:

Received 8 December 2008

Revised 17 April 2009

Accepted 6 May 2009

Available online 12 May 2009

Keywords:

Puberty control

Fish farming

Brain–pituitary–gonad axis

Environmental conditions

Genetics

Growth

Adiposity

Sterility

Triploids

abstract

Puberty comprises the transition from an immature juvenile to a mature adult state of the reproductive

system, i.e. the individual becomes capable of reproducing sexually for the ﬁrst time, which implies func-

tional competence of the brain–pituitary–gonad (BPG) axis. Early puberty is a major problem in many

farmed ﬁsh species due to negative effects on growth performance, ﬂesh composition, external appear-

ance, behaviour, health, welfare and survival, as well as possible genetic impact on wild populations. Late

puberty can also be a problem for broodstock management in some species, while some species com-

pletely fail to enter puberty under farming conditions. Age and size at puberty varies between and within

species and strains, and are modulated by genetic and environmental factors. Puberty onset is controlled

by activation of the BPG axis, and a range of internal and external factors are hypothesised to stimulate

and/or modulate this activation such as growth, adiposity, feed intake, photoperiod, temperature and

social factors. For example, there is a positive correlation between rapid growth and early puberty in ﬁsh.

Age at puberty can be controlled by selective breeding or control of photoperiod, feeding or temperature.

Monosex stocks can exploit sex dimorphic growth patterns and sterility can be achieved by triploidisa-

tion. However, all these techniques have limitations under commercial farming conditions. Further

knowledge is needed on both basic and applied aspects of puberty control to reﬁne existing methods

and to develop new methods that are efﬁcient in terms of production and acceptable in terms of ﬁsh wel-

fare and sustainability.

1. Introduction

Puberty in ﬁsh is the developmental period during which an

individual becomes capable of reproducing sexually for the ﬁrst

time, and implies a functional competence of the brain–pitui-

tary–gonad (BPG) axis (Schulz and Goos, 1999; Zanuy et al.,

2001; Okuzawa, 2002; Patiño and Sullivan, 2002; Schulz and

Miura, 2002; Weltzien et al., 2004; Jalabert, 2005; Dufour and

Rousseau, 2007). Puberty starts some time after sex differentiation

and is associated with the initiation of germ cell maturation and

full functional differentiation of the germ cell-supporting somatic

cells of the gonads, and culminates in the ﬁrst spermiation and

sperm hydration or ovulation (Okuzawa, 2002).

Early puberty is a major problem in farmed ﬁsh, such as in sal-

monids (McClure et al., 2007), sea basses (Felip et al., 2008a), ﬂatf-

ishes (Weltzien et al., 2003a), cod ﬁshes (Karlsen et al., 2006a),

tilapias (Longalong et al., 1999), sea breams (Gines et al., 2003,

2004) and perches (Shewmon et al., 2007). Puberty adversely af-

fects growth, feed utilisation, health and welfare. Early puberty

can also increase the risk for negative genetic effects of escapees

on wild stocks (Bahri-Sfar et al., 2005; Naylor et al., 2005; Hindar

et al., 2006; Skaala et al., 2006) or after spawning in sea cages

(Jørstad et al., 2008).

Although methods exist to delay puberty in commercial farm-

ing, mainly by selective breeding (Gjedrem, 2000), photoperiod

control (Bromage et al., 2001), monosex stocks (Devlin and Naga-

hama, 2002) and induced triploidy (Benfey, 1999), major limita-

tions still exist in the commercial use of these methods. Breeding

programs usually take multiple generations to signiﬁcantly reduce

the problems with early puberty, they are costly, and they are not

doi:10.1016/j.ygcen.2009.05.004

*Corresponding author. Fax: +47 55 23 85 55.

E-mail address: geirt@imr.no (G.L. Taranger).

General and Comparative Endocrinology 165 (2010) 483–515

Contents lists available at ScienceDirect

General and Comparative Endocrinology

journal homepage: www.elsevier.com/locate/ygcen

always fully efﬁcient in every species (e.g. Kolstad et al., 2006).

Photoperiod protocols to delay puberty have yet to be developed

in some species like Atlantic halibut (Norberg et al., 2001), and

there are unpredictable outcomes of the photoperiod treatments

between different sites and years, e.g. in farming of Atlantic salmon

and Atlantic cod where such techniques are commonly in use

(Hansen et al., 2000; Taranger et al., 2006). This may, in turn, be re-

lated to other factors also impacting on the control of puberty, such

as growth rate, feeding and adiposity/energy homeostasis of the

ﬁsh (Taranger et al., 1999; Oppedal et al., 2003). Production of

monosex stocks are not yet possible in some species (e.g. the

European sea bass; Piferrer et al., 2005), and sterility induced by

triploidisation may compromise ﬁsh welfare and production per-

formance (Benfey, 2001; Felip et al., 2001c; Hulata, 2001).

On the other hand, in some species, a delay, or complete failure

of, rather than a precocious puberty causes problems under farm-

ing conditions, e.g. in European eel (Dufour et al., 2003; van Ginne-

ken et al., 2007), hence preventing reproduction and closure of the

life-cycle in culture. Moreover, in species such as groupers, tunas

or sturgeons it can take many years until puberty starts, increasing

costs and risks since potential broodstock has to be maintained for

prolonged periods of time in farm facilities until maturation. In

such cases, an advancement of puberty to harvest eggs (i.e. for cav-

iar) or for reproduction, will improve the costs-efﬁciency of the ﬁsh

farms. Thus, puberty control implies both techniques to delay/ar-

rest and to advance/induce puberty. This control must be

species-speciﬁc considering the great variety of reproductive pat-

terns among species.

To fully control age and size of onset and completion of puberty

in ﬁsh farming, we need to understand the underlying mechanisms

triggering puberty, as well as the impact of various internal and

external factors that govern and modulate this process. Com-

mencement of puberty in teleosts is linked to genetic factors (Gjer-

de et al., 1994), metabolic signals e.g. related to energy stores

(Campbell et al., 2006; Thorpe, 2007) and environmental inputs

(e.g. Bromage et al., 2001; Drinkwater, 2002).

Although the precise involvement of factors that initiate pub-

erty are generally not well known in ﬁsh, the integrative signals

derived from these internal and external factors stimulate the re-

lease of the hypothalamic neurohormone gonadotropin-releasing

hormone (Gnrh), which stimulates the production and/or release

of pituitary gonadotropins, in turn regulating downstream targets,

such as sex steroid and germ cell production in the gonads (Schulz

and Goos, 1999; Zanuy et al., 2001; Okuzawa, 2002; Patiño and

Sullivan, 2002; Schulz and Miura, 2002; Swanson et al., 2003;

Weltzien et al., 2004; Jalabert, 2005; Yaron and Sivan, 2006; Du-

four and Rousseau, 2007).

Objectives and scope of the paper:

1. Provide deﬁnitions and concepts about puberty in ﬁshes.

2. Review in short our knowledge about puberty related problems

in ﬁsh farming.

3. Provide information about variability in age and size at puberty

of farmed ﬁsh, including differences between sexes (using some

selected species as examples; Atlantic salmon, European sea

bass, Atlantic cod, Atlantic halibut) and the underlying patterns

of gametogenesis prior to and during puberty.

4. Review mechanisms underlying puberty onset and completion

in ﬁshes.

5. Review impact of internal (e.g. genetic, energy homeostasis)

and external (e.g. photoperiod and temperature) factors on

age and size at puberty.

6. Review the status of different techniques (selective breeding,

environmental control, sterility models) to control puberty

(delay/arrest or promote/induce) in ﬁsh farming using some

selected species as examples.

7. Identify gaps in knowledge and perspectives for new

approaches (e.g. new sterility models).

2. Deﬁnitions of puberty

Puberty is the developmental period comprising the transition

from an immature juvenile to a mature adult state of the reproduc-

tive system, i.e. the stage of development during which an individ-

ual becomes capable of reproducing sexually, implying functional

competence of the brain–pituitary–gonad (BPG) axis. Adult verte-

brates produce gametes, the cellular basis of fertility, and have

the somatic and behavioural competence to competitively function

as mating partner and/or parent. These are long-term and demand-

ing tasks in many respects, requiring the integrative regulation of

different life processes, such as extracting energy from the envi-

ronment, regulation of growth and energy metabolism, develop-

ment of secondary sexual characters, reproductive behaviour and

so forth. It is therefore not surprising that the two main functions

of the gonads – to produce fertile gametes and hormones – are

orchestrated by the endocrine system, typically involved in coordi-

nating complex developmental and physiological processes. We

can discern two types of regulatory input in this context. Of pri-

mary relevance is the BPG axis with its feedback systems, regulat-

ing both pubertal development and the maintenance of adult

reproductive capacity. Secondly, other systems such as those regu-

lating growth and energy metabolism, the immune system, or the

brain–pituitary–thyroid axis that is involved in the functional dif-

ferentiation of many cell/tissue types, provide permissive rather

than direct regulatory signals.

The control of puberty and reproduction in general by the BPG

axis offers several evolutionary advantages. For example, the

reproductive system usually is silenced until an individual’s so-

matic development has proceeded sufﬁciently to permit investing

into pubertal development. Through the dependency on sex ste-

roids, the start of germ cell development is integrated with the

development towards reproductive competence in general, and al-

lows for the evolutionary mechanism of sexual selection to have an

impact (Clutton-Brock, 2007; Siller, 2001). Hence, puberty is char-

acterised by the concomitant activation of the two main functions

of the gonad, the production of germ cells and the synthesis of

reproductive hormones, in particular sex steroids, themselves re-

quired for supporting different aspects of germ cell development

in both females (e.g. oestrogens and vitellogenesis) and males

(e.g. androgens and spermatogenesis; Schulz et al., 2009), and

reproductive competence in general.

The ﬁrst successful reproduction or, alternatively, the produc-

tion of the ﬁrst batch of fertile gametes (spermiation and sperm

hydration in males; ovulation in females) can be considered as

end point of puberty (Okuzawa, 2002). The start of puberty, how-

ever, seems more difﬁcult to deﬁne. Genetic models in mammals

show that loss of the androgen receptor (De Gendt et al., 2004),

of the receptor for luteinising hormone (Lhr)(Pakarainen et al.,

2005) of the b-subunit of luteinising hormone (Lh) (Kumar,

2007), of the Gnrh receptor (de Roux et al., 1999), or the loss of a

critical input to the Gnrh-producing neurones via the Kiss/Gpr54

system (de Roux et al., 2003; Seminara et al., 2003), all block entry

into puberty. Loss of follicle stimulating hormone (Fsh) function re-

sulted in follicle development being blocked completely while

spermatogenesis was still possible, although compromised as re-

gards number and motility of the spermatozoa produced (Huhtan-

iemi and Aittomaki, 1998), and with species-speciﬁc differences of

the graveness of the phenotype which can reach infertility in

primates (Themmen and Huhtaniemi, 2000). Recent studies in

channel catﬁsh and zebraﬁsh reported that up-regulation of

pituitary fshband ovarian fshr gene expression started prior to

484 G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515

vitellogenesis, coinciding with the accumulation of cortical alveoli,

and continued through vitellogenesis (Kumar and Trant, 2001;

Kwok et al., 2005; So et al., 2005). Moreover, Campbell et al.

(2006) found evidence suggesting that Fsh signalling is important

during the accumulation of cortical alveoli in oocytes in the early

stages of puberty of coho salmon females.

Taken together, there is convincing evidence that regulatory in-

put from outside the gonads is required to trigger pubertal devel-

opment. Early experiments based on the surgical removal of the

pituitary in ﬁsh, allow drawing a similar conclusion. In particular

rapid proliferation of spermatogonia in males (Billard, 1969; Dob-

son and Dodd, 1977; Khan et al., 1986) and the entry into the lipid

droplet stage of oocyte development (Sundararaj et al., 1972) are

the ﬁrst stages requiring pituitary input in ﬁsh. The requirement

for the gonadotropin-stimulated production of androgens for the

initiation of spermatogenesis is in line with the observation that

11-ketotestosterone (11KT) is able to stimulate rapid spermatogo-

nial proliferation in eel testis tissue fragments in vitro (Miura et al.,

1991), in juvenile African catﬁsh in vivo (Cavaco et al., 1998), and is

in line with concomitantly elevated plasma 11KT levels and sper-

matogonial proliferation in naturally maturing Atlantic salmon

in vivo (Schulz, Andersson, Taranger; unpublished). Moreover, in

male Chinook salmon increases in pituitary Fsh and plasma 11KT

levels were found during the transition from spermatogonia A to

spermatogonia B (Campbell et al., 2003), and recent studies in Jap-

anese eel (Ohta et al., 2007) and African catﬁsh (Garcia-Lopez et al.,

2009) suggested that Fsh can directly stimulate Leydig cells, since

they express the fshr gene.

In coho salmon females, signiﬁcant increases in plasma estra-

diol-17b(E2) and Fsh levels (Campbell et al., 2006) accompany

the entry into the ﬁrst pituitary-dependent stage of ovarian devel-

opment, the lipid droplet stage (Sundararaj et al., 1972). However,

Campbell et al. (2006) also reported that Fsh and E2 levels in-

creased already at the cortical alveoli stage in coho salmon going

into puberty, and Manning et al. (2008) found the ﬁrst endocrine

signs of puberty as an increase in plasma E2 levels in yellowtail

ﬂounder.

We therefore propose to consider the transition to the ﬁrst

wave of rapid spermatogonial proliferation, or to the ﬁrst batch

of oocytes accumulating cortical alveoli, as the start of puberty,

which – in both sexes – may be regulated by Fsh. Recent work indi-

cated that oogonial proliferation and entry into meiosis may also

be sensitive to steroid hormones (Miura et al., 2007), but work in

this direction has just started and the regulatory input in these

early stages has not been investigated yet.

3. Variability in age and size at puberty

3.1. Plasticity in age and size at puberty

There is considerable phenotypic and genotypic variation in

both age and size at puberty in ﬁsh species that is used in farming,

e.g. in Nile tilapia (Duponchelle and Panﬁli, 1998; Longalong et al.,

1999), Atlantic salmon (Saunders et al., 1983; Wild et al., 1994;

Hutchings and Jones, 1998; Taranger et al., 1998), rainbow trout

(Kause et al., 2003; Taylor et al., 2008), Arctic char (Duston et al.,

2003), brook trout (Kennedy et al., 2003), coho salmon (Vollestad

et al., 2004), sea bass (Rodríguez et al., 2001b), sea bream (Matic-

Skoko et al., 2007), turbot (Imsland et al., 1997) Atlantic halibut

(Imsland and Jonassen, 2005), blueﬁn tuna (Fromentin and Powers,

2005), Atlantic cod (Olsen et al., 2005; Karlsen et al., 2006), had-

dock (Davie et al., 2007a), channel catﬁsh (Shephard and Jackson,

2005), Eurasian perch (Migaud et al., 2006) and sole (Mollet

et al., 2007). This variation is found both between and within

strains/populations (Myers et al., 1986; Fleming, 1996; Damsgård

et al., 1999; Jonsson and Jonsson, 2004; L’Abee-Lund et al., 2004;

Grover, 2005; Morita et al., 2005). The Atlantic salmon is one of

the most extensively studied species in this regards, and have been

found to display a remarkable variation in life-history traits such as

age and size at puberty, and including differences between and

within populations as well as between year-classes (Hutchings

and Jones, 1998; Garcia de Leaniz et al., 2007).

Many studies on age and size at puberty are based on examina-

tion of natural populations, or studies of release of offspring of wild

populations into natural environments (e.g. Hutchings and Jones,

1998; Heino and Godo, 2002; Dieckmann and Heino, 2007; Jonsson

and Jonsson, 2007; Dominguez-Petit et al., 2008; Ottersen, 2008),

and it is difﬁcult to establish to which extent the variation in age

and size at puberty is of genotypic or phenotypic origin (Morita

et al., 2005; Kuparinen and Merila, 2007; Marshall and McAdam,

2007). On the other hand, a range of experimental studies have

demonstrated large phenotypic variation in age and size at puberty

(Bromage et al., 2001; Thorpe, 2007), and also a signiﬁcant genetic

variation in age and size at puberty both between and within

strains and families (Gjerde et al., 1994; Wild et al., 1994).

However, the relative importance of phenotypic and genotypic

variation in age and size at maturity has been much debated, and

is complicated by the interaction with growth history/growth

patterns, which may explain why there appears to be no ﬁxed size

or age thresholds for puberty in those species that have been

most closely studied such as salmonids (Morita and Fukuwaka,

2006).

The relation between environmental conditions and changes in

age and size at puberty can be described in terms of reactions

norms (Stearns, 1992). Life history models predicts that age at pub-

erty is delayed when growth conditions become less favourable

(Stearns and Koella, 1986; Stearns, 2000; Hutchings and Fraser,

2008; Piche et al., 2008), while the effects on size at puberty (i.e.

decrease or increase) depends on a range of factors such as mortal-

ity patterns and increase of fecundity and offspring quality with

increasing body size of parents (Fig. 1). In several heavily exploited

ﬁsh populations both age and size at puberty have been reduced

over time (Chen and Mello, 1999; Engelhard and Heino, 2004;

Hutchings, 2005; Olsen et al., 2005), which may reﬂect phenotypic

plasticity response to increased growth rates as the population de-

clines, or genetic changes due to size selective ﬁshing, reducing

both age at size at maturation in long-term exploited stocks (Chen

and Mello, 1999; Heino and Godo, 2002; Engelhard and Heino,

2004; Dieckmann and Heino, 2007). In some paciﬁc salmon popu-

lations, however, growth rate reductions have resulted in delayed

puberty as well as smaller size at puberty, possibly due to concom-

itant changes in mortality patterns (Morita and Fukuwaka, 2007).

The relationship between growth, body size and age at puberty is

also complicated by frequency dependent ﬁtness of different

reproductive strategies such as mature salmon freshwater parr or

salmon ‘‘jacks” adopting a ‘‘sneaking” spawning strategy compet-

ing with large salmon males returning from seawater that apply

a ‘‘ﬁghting” spawning strategy (Hutchings and Myers, 1994;

Esteve, 2005).

Different relationships between body size and reproductive suc-

cess in males and females are also the predicted reasons for sexu-

ally dimorphic growth, and differences between the sexes in age

and size at puberty. In many species of farmed ﬁsh, male growth

typically levels off at a smaller size and age compared to females

(e.g. sea bass, halibut, etc.), most probably because female fecun-

dity and offspring ‘‘quality”/survival gain more by increasing body

size than in males. However, this is again complicated by fre-

quency dependent alternative mating strategies such as in salmo-

nids where ‘‘sneaking” strategies in freshwater as mature parr can

have an optimal size window (e.g. Aubin-Horth et al., 2006).

In ﬁsh farming, growth conditions and feed availability is nor-

mally improved compared to the situation in natural ecosystems,

G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515 485

and hence both age and size at puberty are often reduced com-

pared to wild ﬁsh from the same strains (Svåsand et al., 1996).

Thus, the phenotypic responses to improved growth conditions

and feed availability, often with associated higher adiposity and

energy stores, are probably the major causes of the early puberty

commonly observed in many farmed ﬁsh species (Fig. 1). This also

poses a challenge to selective breeding programs, because such

phenotypic responses can mask genetic variability in age and size

at maturation, and make it more difﬁcult to select for late maturity.

On the other hand, some species like the European eel do not reach

puberty under farming conditions, most likely due to lack of appro-

priate environmental stimuli and/or lack of appropriate behaviours

such as long term swimming (Dufour et al., 2005; van Ginneken

et al., 2005, 2007; van Ginneken and Maes, 2005; Sébert et al.,

2008a,b; Weltzien et al., 2009).

3.1.1. Atlantic salmon

The Atlantic salmon (Salmon salar) show a stunning variability

in age and size at puberty, both between and within strains, and

also between years and environmental conditions (Hutchings and

Jones, 1998; Garcia de Leaniz et al., 2007; Thorpe, 2007). Similar

variations in life-history strategies are also seen in other salmonids

used in ﬁsh farming such as rainbow/steelhead trout (Kause et al.,

2003; Tipping et al., 2003; Thrower et al., 2004; Thrower and Joyce,

2006; Sharpe et al., 2007) or coho salmon (Vollestad et al., 2004;

Snover et al., 2005, 2006; Wattersi and Bessey, 2008). This large

variability in life-history strategies is believed to be an adaptation

to the local conditions in the native river environments where they

spawn and have their juvenile development, as well as conditions

in the sea including likelihood of marine growth and survival.

Some salmon populations remain in fresh water throughout life,

whereas others have smaller or larger anadromous components,

that migrate to seawater following parr-smolt transformation

(smoltiﬁcation), and live in the marine environment for one or

more years before returning to their native rivers to spawn.

The combinations of different smolt ages and sea age at matu-

rity, with resident parts of the population consisting mainly of

males maturing at a small body size as ‘‘dwarf” males, give rise

to an impressive variety of life-history patterns in terms of age

and size at puberty, both within and between populations. Exper-

imental evidence shows a large phenotypic variability in these life-

history patterns. Within a certain strain or population, variability

in feed availability and water temperature will modulate growth

rate and consequently age and size at puberty (cf. Thorpe, 2007).

However, there are also clear genetic differences both between

and within strains (Garcia de Leaniz et al., 2007) that can be

exploited in selective breeding programs to delay puberty (Gjed-

rem, 2000). The importance of various proximate and ultimate fac-

tors in determining variability in life-history event such as age at

maturity has recently been modelled in salmonids (Mangel and

Satterthwaite, 2008).

In salmon farming, the parr-smolt transformation normally

takes place in one-year old ﬁsh (i.e. at 18 months of age), or even

as underyearling smolts following photo-thermal manipulations

(Berge et al., 1995; Duston and Saunders, 1995). The main problem

with early puberty in farmed salmon is at the ‘‘grilse” stage, i.e.

after 1.5 years in seawater and at a body size typically from 2 to

5 kg. Moreover, some farmed salmon reach puberty as ‘‘jacks” after

only a few months in seawater and at a body size of around 0.5 kg.

Also, male parr that become sexually mature precociously in fresh-

water prior to the parr-smolt transformation (typically at 10–30 g)

can represent a problem, both due to negative interference with

the smoltiﬁcation process, and due to loss of growth (Whalen

and Parrish, 1999).

Atlantic salmon often display sexually dimorphic growth. This

can be a consequence of different age at puberty between sexes,

and may further be affected by a pubertal growth spurt that com-

monly take place in sexually maturing individuals in the marine

phase during the spring prior to spawning. Males normally have

a much higher proportion of parr maturation, and typically also

have a higher proportion of both jacks and grilse compared to fe-

males. Salmon females often can take an intermediary position

and reach puberty after two winters in seawater, whereas some

males delay maturity to 3 years or more in seawater, and grow

very big before reaching puberty.

3.1.2. Atlantic cod

Atlantic cod (Gadus morhua)is distributed in eastern and wes-

tern parts of the Atlantic Ocean, with a polar and temperate distri-

bution. The different stocks inhabit waters with temperatures

Fig. 1. Concept of relation between somatic growth and age and size at puberty in ﬁshes. Arrows represent different growth trajectories and shaded columns represent

potential spawning seasons. The optimal time of spawning within a year for a given species and strain at moderate and high latitudes is often limited by environmental

conditions and food availability for the offspring. Slower growth will normally result in delayed puberty to maintain ﬁtness, and because of the strong seasonality of optimal

spawning time, puberty completion is delayed with one or more years. The effects of slower growth on size at puberty can vary, possibly due to complex trade-offs between

growth, survival to reproduction and offspring survival. The higher growth rates typically seen in ﬁsh farming normally results in puberty occurring both at an earlier age and

at a smaller body size, compared to wild populations.

486 G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515

ranging from -1 to 20 °C, though usually found in waters with tem-

peratures between 1 and 12 °C. The spawning period for most

stocks is between January and April (Brander, 2005). Growth and

age of puberty varies between stocks, and is affected by prey avail-

ability and temperature in their habitat (Drinkwater, 2002). It has

been shown that age at puberty increases by approximately 1 year

when the temperature is decreased by 2 °C(Drinkwater, 2002). The

northeast Arctic cod stock usually spawns at an age between 4 and

8 years (Bergstad et al., 1987; Jørgensen, 1989), while Norwegian

coastal cod recruits to the spawning stock at 3 years and older

(Berg and Albert, 2003). In farming, these strain differences are

more or less lost, as all tested stocks spawn at an age of 2 years un-

der normal growing conditions, reaching a body weight of around

1.5–2 kg at spawning (Godø and Moksness, 1987; Svåsand et al.,

1996; Hansen et al., 2001; Karlsen et al., 2006a; Taranger et al.,

2006). Some males mature even at 1 year of age with a mean

weight of < 300 g, while no females have been observed to mature

at 1 year of age. The reduced age at puberty in farmed cod is prob-

ably due to the favourable food availability, leading to much faster

growth and larger energy stores compared to in wild populations,

most notably seen as a higher liver index in farmed compared to

wild cod (Karlsen et al., 2006a,b). Under farming conditions, a

sex-dependent growth difference has occasionally been observed,

with females being slightly larger than males (Kolstad et al.,

2006; Solberg and Willumsen, 2008).

3.1.3. Atlantic halibut

The Atlantic halibut (Hippoglossus hippoglossus) is distributed in

parts of the Arctic Ocean and in the northern part of the Atlantic

Ocean. Sexually mature animals congregate for spawning in win-

ter, on well-deﬁned deepwater spawning grounds. The spawning

period for Atlantic halibut varies with geographical region, from

December to March in the most northern parts of Norway, with

peak spawning in January/February, while the spawning period

in more southern regions such as the Iceland/Faroes/North Sea area

and the Nova Scotia/Gulf of St Lawrence/Newfoundland banks area

extends into early spring (Haug, 1990).

Atlantic halibut show a distinct, sex speciﬁc growth pattern and

age at sexual maturation, males reaching puberty at a younger age

and smaller size than females (Jakupsstova and Haug, 1988), at

about 80 cm body length in males, compared to 110–120 cm in fe-

males (Methven et al., 1992). The reproductive strategy behind this

dimorphism is a trade-off between body size, age at maturity and

fecundity expressed as number of eggs spawned. The halibut is

periodic spawner that release large numbers of pelagic, transpar-

ent eggs. There is no parental care and survival of offspring is

mainly secured by quantity rather than quality. As a consequence,

females need to attain a large body size to produce a high number

of eggs. Accordingly, females mature at a very large size compared

to male halibut and to other ﬂatﬁshes; wild halibut males typically

mature at a size around 1.7 kg and at 4–5 years of age, while

females mature at around 18 kg and 7–8 years of age (Jakupsstovu

and Haug, 1988). In aquaculture, accelerated growth of juvenile

ﬁsh commonly result in an advancement of age at puberty so that

male halibut mature at 2–3 years and at a similar body size as wild

males (Norberg et al., 2001), while females mature at around 5–

6 years and at a body size of around 8 kg. Farmed female halibut

show signiﬁcantly higher growth at least from one year of age

compared to males (Norberg et al., 1999), and the females gener-

ally reach the desired market size before puberty, making this spe-

cies particularly suited for all-female production.

3.1.4. European sea bass

The European sea bass (Dicentrarchus labrax) is a gonochoristic

perciform ﬁsh in which puberty of females occur at 3 years of

age while in males puberty is attained at 2 years of age (Carrillo

et al., 1995; Saillant et al., 2003). Under intensive culture condi-

tions, sea bass exhibits a high rate of growth and as a consequence

around 20–30% of the male population mature precociously. These

ﬁsh are larger than the non-precocious ones and reproduce in the

ﬁrst year of life, before attaining market size. However, in the sec-

ond annual cycle, precocious males grow up to 18% less in weight

and 5% less in fork length than the non precocious ﬁsh (Felip et al.,

2008a). Moreover, males in general exhibit 20–40% less body

weight at harvest time than females (around 18–22 months of

age), likely induced by their earlier onset of puberty which diverts

energy towards gonadogenesis and breeding behaviour instead of

somatic growth (Carrillo et al., 1995; Saillant et al., 2001a,b). In

addition, under aquaculture conditions there are often a high per-

centage of males, reaching 70–90% of the total population (Carrillo

et al., 1995; Gorshkov et al., 1999). According to these consider-

ations, mono-sex culture (females) has been proposed as a likely

solution to improve production of sea bass in terms of sexual

dimorphism in growth and to alleviate the disadvantage of skewed

proportion rates to males in cultivated populations.

3.2. Patterns of gonadal growth and development prior to and during

puberty

3.2.1. Atlantic salmon

Atlantic salmon females have a group-synchronous oocyte

development, with one leading cohort of oocytes entering into

secondary oocyte growth as marked by the formation of cortical

alveoli and later perinuclear oil drops. Secondary oocyte growth

commences normally at least 1 year before spawning in parallel

with increasing plasma E2 levels (Chadwick et al., 1987; Taranger

et al., 1999; King and Pankhurst, 2003). The leading oocyte cohort

enters true vitellogenesis around winter solstice, approx

10 months prior to spawning, and accumulates yolk during

spring, summer and early autumn in parallel with a massive in-

crease in oocyte diameter and gonad size. After completion of

vitellogenesis and oocyte growth, ﬁnal oocyte maturation re-

sumes approx 1 week before ovulation that normally takes place

between late autumn and early winter depending on strain and

environmental conditions such as water temperature (Heggber-

get, 1988a,b; Taranger and Hansen, 1993). The eggs are ovulated

in a single batch, and can remain in the body cavity for around

one week prior to egg deposition (spawning) and fertilisation.

The gonadosomatic index (GSI) increases from typically <0.3% at

the smolt stage to around 20–25% just prior to ovulation. Recruit-

ment into vitellogenesis appears to take place earlier in the sea-

son in females that mature at a higher age (e.g. comparing

salmon maturing after either 1 or 2 years in seawater), allowing

for larger egg size and/or fecundity in older females. In parallel,

salmon males typically have a GSI of <0.1% at the smolt stage,

which increases rapidly from winter/spring prior to spawning to

a maximum of around 5–10% in the beginning of the spawning

period. The rapid testis growth takes place after the initiation of

rapid spermatogonial (type B) proliferation in parallel with

increasing plasma sex steroid levels in late winter/early spring

depending on strain, age and environmental conditions (Hunt

et al., 1982; Youngson et al., 1988; McLay et al., 1992; Stead

et al., 1999). It appears that onset of puberty marked by the rapid

spermatogonial proliferation and increase in gonad size can com-

mence earlier in the season in older and larger males, in a similar

fashion as in females. The large investments in gametogenesis

and reproductive behaviour in combination with ceased feeding

from the summer months, lead to a marked depletion of lipids,

proteins and astaxanthin (red pigment) from the muscle tissue

in sexually mature salmon (Aksnes et al., 1986). However, both

males and females can survive following spawning and remature

in later seasons.

G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515 487

3.2.2. Atlantic cod

The repeat spawning, group-synchronous Atlantic cod spawns

mainly between January and April depending on the stock and

water temperature, but some stocks spawn during summer and

autumn (Brander, 2005). Females release egg portions every 2 or

3 days, and in captivity they may spawn 17–19 batches during

their spawning period (Kjesbu, 1989). Prior to the ﬁrst spawning

season, the ovary remains immature and contains only small trans-

parent previtellogenic oocytes less than 250

m until about Octo-

ber (Dahle et al., 2003). One month later most females have

commenced formation of cortical alveoli and yolk sequestration.

As vitellogenesis proceeds during late autumn and early winter,

the size of the oocytes increases to above 800

m prior to hydra-

tion (Kjesbu, 1991). The GSI increases from less than 1% in the

beginning of October to about 5% in December. A rapid growth

starts in January until a maximum is reached just prior to spawn-

ing of about 15%. Some females may have much larger GSI. The

proliferation of spermatogonia starts in August, followed by meio-

sis and spermiogenesis from October (Dahle et al., 2003; Almeida

et al., 2008). Free spermatozoa are observed from December on-

wards (Dahle et al., 2003; Almeida et al., 2008). The males are

therefore prepared for spawning at least 1 month prior to females.

The GSI in males increases from below 2% in October, to about 4%

in November and reaching a maximum of about 12% in January.

Cod drains energy from liver and muscle during the spawning per-

iod to supply energy both for the incorporation of yolk during the

development of new batches of eggs (Kjesbu and Kryvi, 1993), and

for reproductive behaviour.

The presence of cortical alveoli and yolk granules observed in

mid-November indicates that these females will spawn the follow-

ing season (Saborido-Rey and Junquera, 1998). It is possible to

distinguish maturing females based on the appearance of circum-

nuclear ring (Woodhead and Woodhead, 1965), which appears in

summer during primary oocyte growth. Spermatogenesis occurs

synchronously within cysts formed by Sertoli cells; different cysts

often develop asynchronously (Dahle et al., 2003; Almeida et al.,

2008). In males there is a gradient in development within the testis

lobes, where undifferentiated spermatogonia are found in the

periphery of the lobes, and the more advanced germ cells closer

to the collecting duct (Almeida et al., 2008).

3.2.3. Atlantic halibut

Female halibut are group-synchronous spawners, releasing

multiple batches of large, pelagic eggs approximately every 72–

80 h over a period of 3–6 weeks (Norberg et al., 1991). The cortical

alveoli stage appears to commence one year before spawning,

while the ﬁrst histological evidence of vitellogenic oocytes was

found ﬁve months before ﬁrst ovulation (Riple, 2000). Plasma lev-

els of E2 and vitellogenin (VTG) increase from August/September,

indicating that the onset of vitellogenesis occurs around 5 months

before spawning (Methven et al., 1992). Concurrent with the in-

crease in plasma VTG and E2, the major vitelline envelope proteins

were also detected (Hyllner et al., 1994). During the spawning per-

iod, plasma VTG and E2 ﬂuctuate, indicating a cyclic synthesis, re-

lease and uptake of VTG into the oocytes before ﬁnal maturation

(Methven et al., 1992). While pituitary gene expression of the

gonadotropins, fsh and lh, appears to be high through all stages

of ovarian development except just prior to ovulation, ovarian

expression of the gonadotropin receptors, fshr and lhr, show a tem-

porally differentiated expression pattern. The fshr is highly ex-

pressed in ovarian follicles during primary growth and

vitellogenesis. During this period, lhr expression is very low, while

it is highly expressed in follicles undergoing ﬁnal maturation

(Kobayashi et al., 2008).

The germinal compartment in Atlantic halibut testis appears to

be organised in branching lobules of the unrestricted spermatogo-

nial type based on the localisation of spermatocysts containing all

germ cell developmental stages throughout the germinal compart-

ment (Weltzien et al., 2002). The reproductive cycle of male Atlan-

tic halibut is characterised by distinct seasonal variations in

absolute and relative testicular size and developmental stage,

and by ﬂuctuations in plasma levels of T and 11KT associated with

different phases of reproductive activity. The growth phase culmi-

nates in the formation of mature spermatozoa (spermiogenesis) at

the initiation of the spawning period in January (Norberg et al.,

2001). During the spawning period, which usually lasts until

March/April, the GSI and plasma androgen levels soon begin to de-

crease, reaching regressed levels by April/May. Thus, spermatogen-

esis in halibut can be divided into three phases (Norberg et al.,

2001; Weltzien et al., 2002, 2004). First, an initial phase with low

levels of circulating T and 11KT, and spermatogonial proliferation

and meiosis marked by the formation of spermatocytes. Second,

a phase with increasing T and 11KT levels, and with haploid germ

cells including spermatozoa present in the testis. Third, a phase

with low T and 11KT levels and a regressing testis with Sertoli cells

displaying signs of phagocytotic activity. In terms of absolute mea-

sures, the GSI in male halibut remains below 0.1% until the appear-

ance of spermatids (Weltzien et al., 2002), and increase to

maximum levels of about 3% at spawning. 11KT normally occurs

in higher quantities than T, generally with levels at least 4-fold

higher during all stages of spermatogenesis (Methven et al.,

1992; Weltzien et al., 2002). Plasma T and 11KT stay below 0.1

and 1.0 ng ml

1

, respectively, in male halibut until the appearance

of spermatids in the testis, whereas maximum levels of 1–2 and 4–

5ngml

1

, respectively, are reached at spawning. Increasing plas-

ma levels of T and 11KT are associated with increasing testicular

mass throughout the reproductive cycle. A slight elevation of

androgen levels is apparent in males one year before ﬁrst matura-

tion, showing that halibut, like several other species, undergo a so-

called dummy-run with increased steroid-production a year before

puberty. It is believed that this gradual increase in androgen levels

is necessary for the onset of puberty (Weltzien et al., 2003a). At the

pituitary level, gene expression of both gonadotropins are apparent

both in juvenile, early maturing, and maturing male halibut

(Weltzien et al., 2003b,c).

3.2.4. European sea bass

Sea bass show a group-synchronous mode of gonadal develop-

ment. In females, successive clutches of germ cells that will mature

and be spawned in a given season are recruited from a population

of vitellogenic oocytes (Alvariño et al., 1992), and a similar situa-

tion is observed in the male. Consequently, different types of ovar-

ian follicles or testicular cysts may appear at certain periods of the

sexual cycle. However, only one type dominates and deﬁnes the

gonadal stage at a given period of the reproductive cycle (Begtashi

et al., 2004; Rodríguez et al., 2001b).

The hormonal regulation of female gonadogenesis has been de-

scribed by Asturiano et al. (2000, 2002) showing that vitellogenic

oocytes can be recruited into maturation in four consecutive

waves, and individual females can produce up to four consecutive

spawns at around bi-weekly intervals during the reproductive per-

iod (mid January–mid March) (Mylonas et al., 2003). During this

period no regression of the gonads was observed until the last

spawning was completed. During the post-spawning period

(May–June) the next generation of the germinal cells starts its

development. Thus, different periods of gonadal activity are very

well established; resting, early, mid and late vitellogenesis and

spermatogenesis, maturation–ovulation, spermiogenesis–spermia-

tion and ﬁnally ovarian and testicular regression.

These patterns of gonadogenesis observed in adult ﬁsh have

also been conﬁrmed in pubertal ﬁsh (Rodríguez et al., 2001b; Begt-

ashi et al., 2004; Carrillo et al., 2009) in parallel with a high in-

488 G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515

crease in plasma sex steroids during spermatogenesis and vitello-

genesis, remaining elevated throughout most of the maturation

period, particularly in females (Rodríguez et al., 2000, 2001a,

2004, 2005; Rocha et al., 2009). The proﬁle of E2 plasma levels ob-

served in pubertal females was similar to the one in adult sea bass

(Prat et al., 1990; Mañanós et al., 1997a,b; Asturiano et al., 2000),

with a single annual peak at late vitellogenesis (December) and

constantly high levels during the whole maturation and ovulation

period. The maintenance of constantly high E2 levels during the

entire maturation and ovulation stage may be required for a pro-

longation of the vitellogenic process, as vitellogenic oocytes are

also present during this stage.

Recently, expression studies on fshr mRNA levels in ﬁsh enter-

ing puberty showed up-regulation of this receptor at early stages

of gonadal development (Rocha et al., 2009). Increased expression

was also observed during the spermiation period in males and the

maturation–ovulation period in females, suggesting that this

receptor may also be involved in the control of these late processes.

Increases in sea bass ovarian lhr mRNA levels were only observed

when post-vitellogenesis began (December). At this stage, fshr

mRNA levels were already at their maximum. During the matura-

tion–ovulation period, expression levels of both receptors re-

mained elevated, returning to their basal levels only after

spawning. The observed high expression level of fshr during matu-

ration could be connected with oocyte growth and is explained by

the reproductive strategy of this species. As mentioned earlier, sea

bass ovary exhibits a group-synchronous type of development and

contains clutches of oocyte populations at various stages of sec-

ondary growth that are successively recruited (Mayer et al.,

1990a; Asturiano et al., 2000). Therefore, the expression of any

gene measured at the ovary level reﬂects the average of the exist-

ing follicles, including that of growing oocytes that would still ex-

press fshr.

11KT is considered to play an important role in stimulating

spermatogenesis in several ﬁsh species (Schulz and Miura, 2002).

In pubertal male sea bass, 11KT levels rise during mid spermato-

genesis, and drop once spermiation begins (Rodríguez et al.,

2000, 2001a, 2004, 2005; Carrillo et al., 2009; Rocha et al., 2009).

Similarly, sea bass plasma Lh levels showed an increase during

spermatogenesis reaching the highest levels during spermiation

which is in agreement with the expression proﬁles of sea bass

lhb(Mateos et al., 2003) and lhr (Rocha et al., 2009). Finally, the

study of the hormonal regulation of the early events of gametogen-

esis in sea bass has revealed the rhythmic nature of the synthesis

and release of hormones. Pubertal sea bass going to maturation

showed daily rhythms of pituitary sbGnrh content negatively cor-

related with daily plasma Lh rhythms, which exhibited nocturnal

peaks (Bayarri et al., 2004). These daily rhythms were drastically

suppressed by exposure to an inhibitory photoperiod (continuous

light), fully arresting maturation (Bayarri et al., 2009).

4. Consequences of puberty

Onset of puberty can have large consequences for important

production parameters in ﬁsh farming such as appetite, growth

rate, feed conversion efﬁciency, ﬂesh quality traits, external

appearance, agonistic behaviours, health, welfare and survival

rates.

4.1. Growth and somatic weight

Puberty results in direction of resources and energy from

somatic growth and maintenance to gonad growth, production of

gametes, and reproductive behaviour. In many species, feed intake

will also be markedly reduced or stop completely prior to and/or

during the spawning period (Kadri et al., 1996). As a consequence,

somatic growth will decrease prior to and during the spawning

period. However, the timing and magnitude of the growth decrease

and/or loss of somatic weight depends on the reproductive effort in

terms of gamete production and reproductive behaviour (Hendry

and Beall, 2004), including the development of secondary sex char-

acteristics as most typically seen in salmonids males (Naesje et al.,

1988; Järvi, 1990). Some species like Atlantic salmon and several of

the Paciﬁc salmon species more or less exhaust their body reserves

completely during spawning migration, gametogenesis and

spawning, and suffer high or total mortality post spawning, at least

on their native spawning grounds in rivers. Other species like the

Atlantic cod, with only subtle secondary sex characteristics (Engen

and Folstad, 1999) will normally survive the spawning season, but

the loss in somatic weight can be more than 30% during a single

spawning season (Karlsen et al., 1995; Fordham and Trippel,

1999). There can be some compensatory growth following comple-

tion of the spawning season, e.g. in Atlantic cod (Pedersen and Jo-

bling, 1989), that will narrow but not remove the difference

between previously mature and immature individuals (Taranger

et al., 2006).

4.2. Pubertal growth spurt

Onset of puberty can also initially have positive effects on appe-

tite and somatic growth. Individuals that enter puberty early are

commonly the larger individuals within a population or a sibling

group (e.g. Skilbrei, 1989). In addition, in the early stages of pub-

erty, somatic growth rates are often observed to be higher than

in immature individuals. This is typically seen in Atlantic salmon,

where maturing individuals often display higher growth rates from

January to June in parallel with increased plasma sex steroid levels

and start/resumption of gametogenesis (Hunt et al., 1982; Young-

son et al., 1988; Skilbrei, 1989; McLay et al., 1992). Thereafter,

feeding ceases in maturing individuals in early summer (Kadri

et al., 1996), and hence somatic weight starts to decrease in paral-

lel with the rapid gonadal growth in summer and autumn when

Atlantic salmon approaches spawning. As a consequence, sexually

maturing salmon are typically much larger than immature siblings

in early summer, in part because the maturing ﬁsh were initially

larger the winter before spawning, but mainly as a consequence

of the puberty induced growth spurt from January to early sum-

mer. It has also been demonstrated that this growth increase fol-

lowing onset of the early stage of pubertal development is

associated with increased appetite and feed intake (Kadri et al.,

1996). Under farming conditions this pubertal growth spurt may

be exploited to maximise growth and feed intake. However, in

the case of Atlantic salmon, harvest should be shortly after the ces-

sation of the growth spurt, as both body weight and ﬂesh quality

will start to become negatively affected at the end of the summer

(Aksnes et al., 1986).

4.3. Feed conversion efﬁciency

Puberty results in reallocation of energy from somatic growth to

gametogenesis and reproductive related behaviours such as migra-

tions and/or agonistic behaviour prior to and during the spawning

period (e.g. Jonsson et al., 1991; Kjesbu et al., 1991; Karlsen et al.,

1995; Hinch and Rand, 1998; Healey et al., 2003; Jonsson and Jons-

son, 2003; Hendry and Beall, 2004). Moreover, the appetite is often

reduced prior to and during large parts of the spawning season

(Kadri et al., 1995, 1996; Tveiten et al., 1996; Fordham and Trippel,

1999; Skj



raasen et al., 2004). As a consequence the feed conver-

sion efﬁciency will be markedly negatively affected (e.g. Stead

et al., 1999). In addition, the weight loss with spawning will result

in longer time to reach harvest size, and thereby larger expendi-

G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515 489

tures to basal metabolism due to longer production time. Hence,

the total amount of feed needed to reach as certain body size will

increase if the ﬁsh is allowed to go through one or more spawning

seasons before harvest, and thereby negatively affect the sustain-

ability of the ﬁsh farming in terms of feed resource use.

4.4. Increased aggression/agonistic behaviour

Sexual maturation can impact on agonistic behaviour as typi-

cally seen in salmonids (Järvi, 1990; Fleming, 1996). Salmon can

adopt different mating strategies and tactics depending on age

and size at maturity (Fleming, 1996; Thorpe, 2007). Salmon males

mature either directly in freshwater as parr (‘‘dwarf males”), after

return from seawater following a few months as ‘‘jacks”, after one

sea winter as ‘‘grilse”, or after 2 or more sea winters as ‘‘hooknose”.

Depending on size, age and competitors they may behave as dom-

inant (ﬁghting) or as subordinate (sneaking) males. Secondary sex

characteristics such as hook on the jaw, bright skin colouration and

other changes in body shape are regarded as display of status (Tch-

ernavin, 1944; Järvi, 1990). The ‘‘hooknose” males usually establish

a size-based hierarchy, where the larger individuals are found clo-

ser to females (Järvi, 1990) and these usually also fertilise more

eggs than the sneakers.

The combined efforts in gametogenesis, development of sec-

ondary sex characteristics and reproduction related behaviours

drain heavily on the energy reserves in salmonids. In Atlantic sal-

mon the cost of reproduction in both sexes have been calculated

to around 59% measured as expended energy reserves (Fleming,

1998), and larger salmon expend more than smaller. There is an in-

tense male–male competition for access to females. While females

usually spend less than a week on the spawning grounds, males

may spend a month (Webb and Hawkins, 1989). In addition, nest-

ing females may have mate choice where they direct their aggres-

sion towards males (Fleming et al., 1997).

A contrasting spawning strategy is seen in the broadcast spaw-

ner Atlantic cod, where females release eggs into the surroundings,

without any parental care. However, in spite of this, cod has a com-

plex mating system where males court females using both display

and sound (Brawn, 1961; Hutchings et al., 1999; Finstad and

Nordeide, 2004; Rowe and Hutchings, 2006). Male cod have a ter-

ritorial behaviour close to and during spawning (Brawn, 1961).

Brawn (1961) observed that one large male occupied half the tank,

and excluded other males by fast aggressive approaches, threat

displays and sound production. Reproductive success increases

with male body length and number of agonistic interactions (Rowe

et al., 2008). Courtship starts with a female approaching a male,

and after a complex behaviour ends with the ventral mount, where

the male and female swims belly to belly and releases eggs and

sperm. The mating pair may be joined by ‘‘satellite males” that

swim amongst the eggs and release sperm in an attempt to fertilise

the eggs in competition with the dominant male (Hutchings et al.,

1999; Rakitin et al., 2001; Bekkevold et al., 2002). In the wild there

is a vertical separation of mature males and females (Morgan and

Trippel, 1996), and there are considerable vertical movements

(Brawn, 1961; Rose, 1993; Hutchings et al., 1999; Lawson and

Rose, 2000), where males assemble lower in the water column

and females sink slowly down to this assembly. Spawning behav-

iour is likely to involve female choice (Hutchings et al., 1999; Rowe

et al., 2007). The most aggressive agonistic male–male behaviour

occurs in the lower parts of the water column, while most court-

ship behaviour appears in the upper part of the water column.

4.5. Increased disease susceptibility, health and welfare problems

Onset of puberty and sexual maturation can have an impact on

the immune system of the ﬁsh (Maule et al., 1996; Suzuki et al.,

1997; Hou et al., 1999; Cuesta et al., 2007), and consequently on

disease susceptibility and the overall health status. This may in

part be due to the immunomodulatory role of hormones such as

sex steroids, cortisol and growth hormone that change in associa-

tion with reproduction (Harris and Bird, 2000; Law et al., 2001;

Yada and Nakanishi, 2002; McQuillan et al., 2003). This problem

can be further aggravated by agonistic behaviours (see above),

resulting in skin damages and in increased risk for secondary infec-

tions and parasite infections (Skarstein et al., 2001). Onset of sex-

ual maturation can also lead to other changes in physiological

homeostasis, e.g. in salmonids where sexual maturation compro-

mise their hypo-osmoregulatory ability (Makino et al., 2007), and

hence can result in dehydration and ultimately mortality if they

are maintained in sea water throughout the reproductive season.

Mortality has also been noted in farmed female cod that are unable

to release their eggs following sexual maturation in sea cages (Ø.

Karlsen, B. Norberg, G.L. Taranger, unpublished results). Thus, early

sexual maturation (i.e. before the ﬁsh reach the desired marketable

size) can also represent a welfare problem in ﬁsh farming due to

compromised health, problems with maintaining homeostasis,

spawning failure and related problems, as well as damages caused

by aggressive behaviour.

4.6. Increased risk of genetic impact on wild stocks

Early puberty can also increase the risk of genetic impact of ﬁsh

farming on wild stocks. In Atlantic salmon farming, it is assumed

that sexually mature individuals will have a much higher likeli-

hood to enter a nearby river and spawn upon escape from the ﬁsh

farm, whereas ﬁsh that are immature at escape will more probably

leave the coast to enter the feeding grounds in the ocean and have

a much lower likelihood to survive until they return to a river to

spawn (Hansen, 2006). This is also seen in sea ranched triploid sal-

mon that show lower return rates to freshwater from the marine

environment than diploid salmon, probably due to the lower inci-

dence of gonadal development seen in triploid salmon (Cotter

et al., 2000). It has also been documented recently, that farmed

Atlantic cod that are naturally spawning in sea cages give rise to

surviving larvae and juveniles in the nearby coastal areas (Jørstad

et al., 2008). This could also represent a risk for unwanted intro-

gression of farmed genotypes into wild ﬁsh populations.

4.7. Atlantic salmon

A range of studies has investigated the impact of puberty on

growth in Atlantic salmon (e.g. Skilbrei, 1989) as discussed above.

The general pattern is initially a growth promoting effect of pub-

erty, typically seen in the winter, spring and early summer before

spawning, and thereafter a decline in body weight during late sum-

mer/autumn when feeding ceases (Kadri et al., 1995, 1996) and en-

ergy is mobilised for rapid gonadal growth, development of

secondary sexual characters, and reproduction-related behaviour

(Aksnes et al., 1986). This has also profound effects on the ﬁllet

composition; initially the higher growth rate in pubertal ﬁsh can

lead to higher lipid stores than in immature ﬁsh, while the ﬁllet

is depleted for lipids, proteins and pigments (astaxhanthin) during

the later stages of maturation. However, the magnitude and sea-

sonal timing of the pubertal growth spurt, the loss of body weight

and the associated changes in ﬁllet composition can vary between

strains with different seasonal timing of spawning, and between

the highly divergent life-histories found in size and age at maturity

in salmonids. The muscle fat content in maturing ﬁsh is higher

than in immature during summer (Aksnes et al., 1986; Kadri

et al., 1996), while in the period September–November the muscle

lipid and protein content of maturing Atlantic salmon decreases. At

spawning the lipid content were found to be about 3% lower, and

490 G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515

protein content about 4% lower (Aksnes et al., 1986). During the

maturation the carotenoids originally deposited in the muscle are

shifted to the gonads and skin, and consequently the muscle loses

its red colour. The ﬂesh quality is not different between mature

and immature salmon until October; thereafter the ﬂavour de-

creased in maturing ﬁsh, and the muscle texture becomes softer

in mature salmon.

4.8. Atlantic cod

There is no, or only a minor sex dependent growth difference

between male and female Atlantic cod prior to maturation. Male

Atlantic cod have only subtle secondary sexual characteristics,

such as increased length of the pelvic ﬁns and larger drumming

muscles (Engen and Folstad, 1999; Skj



raasen et al., 2006), which

probably do not drain excessive energy. Closer to the spawning

season starting in February, the females are usually slightly larger,

mainly due to an enlarged liver compared to the males (Karlsen

et al., 1995; Dahle et al., 2003), and in addition they have larger

maximum GSI and continue gonad growth longer than males. Since

cod reduce/stop feeding due to a loss of appetite approximately

1 month prior to spawning, and during

of the individuals’

spawning season (Fordham and Trippel, 1999; Skj



raasen et al.,

2004), energy used for maintenance, behaviour and gonad devel-

opment is fuelled by stored energy in muscle and liver (Dambergs,

1964; Krivobok and Tokareva, 1973; Black and Love, 1986; Kjesbu

et al., 1991). Spawning therefore results in a major weight loss of

30–35% (Karlsen et al., 1995; Lambert and Dutil, 2000; Dahle

et al., 2003), and the total body weight measured in January is usu-

ally not regained until June (Karlsen et al., 2006b; Taranger et al.,

2006) even though cod show a compensatory growth after spawn-

ing (Pedersen and Jobling, 1989). The actual losses depend on the

diet, considering that the GSI is positively related to the dietary li-

pid content (Karlsen et al., 2006b). The mortality during spawning

varies, but in captivity there seems to be a higher female mortality

during spawning due to problems with irregular spawners in cod.

Females in poor condition do not reduce their investment in repro-

duction, which increases the risk of mortality (Lambert and Dutil,

2000).

During maturation the cod drains energy from the muscle,

which then contains less protein and more water (Kjesbu et al.,

1991; Karlsen et al., 2006b), in particular at the end of the spawn-

ing season. The actual values for dry matter and protein content

again depend on the diet (Karlsen et al., 2006b). Traditional quality

assessment, using a trained sensory panel and texture analyses, did

not reveal any differences between the spawning and the imma-

ture groups in June after the spawning season (Hemre et al., 2004).

4.9. Atlantic halibut

Somatic growth is strongly affected by maturation in Atlantic

halibut (Norberg et al., 2001; Weltzien et al., 2003a). Maturing

males tend to have very low, or even negative growth rates, and

do not recruit new muscle ﬁbres for growth, apparently directing

all surplus energy into testes development and/or reproductive

behaviour (Norberg et al., 2001; Weltzien et al., 2003a; Hagen

et al., 2006). Information on the interplay between growth and

puberty, and how this is regulated is scarce in this species. How-

ever, high Gh plasma levels were demonstrated in mature male

Atlantic halibut during annual cycles compared with mature fe-

males (Einarsdottir et al., 2002). This sex difference could indicate

that the Gh levels are inversely correlated to growth in this species.

Weltzien et al. (2003a) showed that Igf1 levels were correlated to

growth during the period of slow growth in winter/spring in male

Atlantic halibut, but not at other times of year, and there were no

clear differences between immature and mature ﬁsh. In apparent

contrast, Imsland et al. (2008) found a correlation between growth

rates and plasma IGF-1 both in September and in March in juvenile

halibut of both sexes. However, this correlation was stronger in

March than in September, while growth rates were lower. Matura-

tion results in signiﬁcant changes in muscle texture and ﬂesh qual-

ity in male Atlantic halibut (Roth et al., 2007). This was suggested

to be caused by the slower growth of mature males, where no new

muscle ﬁbres are recruited (Hagen et al., 2006).

4.10. European sea bass

Most farmed sea bass populations show skewed sex ratios, with

74% or more males. Many of them (around 20–30%) reach puberty

at one year of age (Carrillo et al., 1995). Although precocious males

are signiﬁcantly larger than the non-precocious ones during their

ﬁrst year of life (Begtashi et al., 2004), they show lower growth

rates than their non-precocious counterparts during their second

year (Felip et al., 2006) resulting in considerable economic losses

to the ﬁsh farmer. A ‘‘critical” size and/or energetic status seem

necessary for the appearance of precocious males, and individuals

below these thresholds remain immature until the next reproduc-

tive season. Most male sea bass reach puberty in the second year of

life by the time when they reach marketable size (400–500 g), and

the growth depressing effect of puberty is more pronounced than

in males maturing in their 1st year of life. Finally, growth cessation

is observed at the end of the third annual cycle when also the fe-

males attain puberty. Thus, the reduction of the growth rate asso-

ciated with puberty becomes progressively more marked with age

in sea bass, partly due to increasing investments into maturation

with age. Moreover, under intensive culture conditions a high pro-

portion of the females can also reach puberty at 2 years of age (pre-

cocious females; Zanuy and Carrillo, unpublished results), which

will affect somatic growth negatively in a similar way as in preco-

ciously mature male ﬁsh.

5. Internal and external determinants of puberty

5.1. Genetic factors and puberty

A range of studies, in particular in salmonids, have demon-

strated the importance of genetic impact on age at puberty in

ﬁshes (e.g. Nilsson, 1992; Crandell and Gall, 1993; Hankin et al.,

1993; Gjerde et al., 1994; Silverstein and Hershberger, 1995; Long-

along et al., 1999; Su et al., 1999; Martyniuk et al., 2003). As an

example, in farmed Atlantic salmon, large genetic differences were

found both between strains and families with regard to the age of

maturity (e.g. N



vdal, 1983; Gjerde and Gjedrem, 1984; Herbinger

and Newkirk, 1990); the heritability of this trait was estimated to

0.48 by Gjerde (1984), and more recently to 0.15 by Gjedrem

(2000). Strong response to selection for late maturity was also

found in rainbow trout (Kause et al., 2003, 2005; Martinez et al.,

2006; Ritola et al., 2007).

However, several studies have also shown genotype-by-envi-

ronment interactions (GEI) on age at puberty, explaining a

signiﬁcant portion of the observed phenotypic variation (Saun-

ders et al., 1983; Heath et al., 1994; Wild et al., 1994). This

GEI can be described as genetically determined ‘‘reaction norms”

deﬁning how age and size at puberty change in response to

changes in growth and environmental conditions (cf. Dieckmann

and Heino, 2007; Hutchings and Fraser, 2008; Piche et al., 2008).

Thus, in most species and strains, the inherited trait is not a

ﬁxed age and/or size at puberty, but an adaptive response that

is believed to maximise reproductive success and ﬁtness as

growth and mortality patterns change in natural populations

(Stearns, 1992).

G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515 491

Moreover, genetic factors may have an indirect effect on age at

maturity through other heritable traits, such as growth rate, size-

at-age and energy stores. A range of studies, e.g. in salmonids, have

demonstrated large genetic variation in muscle fat content (Gjerde

and Schaeffer, 1989; Rye and Gjerde, 1996) and growth (Gjerde

et al., 1994; Friars et al., 1995). Thus, genetic background may have

indirect effect on age-at-puberty through its inﬂuence on these

parameters. On the other hand, there are Atlantic salmon families

that display high growth and late age at maturity (Gjerde et al.,

1994), allowing for simultaneous selection of fast growing and late

puberty (Gjedrem, 2000). Moreover in experimental studies with

wild Atlantic salmon populations, strains with high age and size

at puberty also display higher growth during the ﬁrst year in sea-

water compared to strains with earlier maturity (Jonsson and Jons-

son, 2007), suggesting that genetic factors for high growth rate and

early puberty are not necessarily positively correlated.

5.2. Correlation between feeding, growth, energy allocation, adiposity

and puberty

As in all vertebrates, puberty in ﬁsh occurs when individuals

have reached a certain combination of age and size, and most likely

also, have accumulated sufﬁcient energy reserves (generally in the

form of body fat) to meet the nutritional and energetic require-

ments of maturation. This is supported by evidence indicating a

strong relationship between body growth rates and age of puberty

in salmonids (e.g. McCormick and Naiman, 1984; Skilbrei, 1989;

Rowe and Thorpe, 1990a,b; Thorpe et al., 1990; Silverstein and

Shimma, 1994; Friedland and Haas, 1996; Friedland et al., 1996;

Kadri et al., 1996; Duston and Saunders, 1999; Thorpe, 2004,

2007). In this context, it has been suggested that the onset of pub-

erty in ﬁsh is linked to absolute levels or rates of accumulation of

lipid stores (Rowe et al., 1991; Silverstein et al., 1997, 1998;

Shearer and Swanson, 2000; Shearer et al., 2006). However, this

relationship between growth/adiposity and onset of puberty is of-

ten complicated due to large plasticity in life-history strategies

both within and between populations (Hutchings and Jones,

1998), and is further inﬂuenced by environmental signals (Tarang-

er et al., 1999).

High growth rate and/or lipid storage under farming conditions

often results in earlier onset of puberty than their wild counter-

parts as discussed above (cf. Thorpe, 2007). The interactions be-

tween the brain and peripheral signals which regulate appetite,

growth, adiposity, and how they affect onset of puberty, have been

studied extensively in mammals including the role of leptin (e.g.

Zieba et al., 2005). By contrast, information of this type is very lim-

ited for ﬁsh. Adiposity appears to exert a negative feedback on

appetite in ﬁsh (Shearer et al., 1997a,b; Silverstein et al., 1999;

Johansen et al., 2001, 2002; Jobling et al., 2002). Based on this,

and similar results in mammals, a lipostatic model was hypothe-

sised for ﬁsh (Johansen et al., 2002), suggesting that adipose tissue

participates in the regulation of feed intake through negative feed-

back signals to the brain. However, the mechanisms for such neg-

ative feedback are not yet known in ﬁsh, nor the precise impact of

energy homeostasis and related endocrine signalling on puberty

(see below for discussion of potential roles of leptin and ghrelin).

5.3. Impact of environmental factors

In ﬁsh species with marked seasonality of breeding activity, the

reproductive cycle is controlled and synchronised by annual envi-

ronmental variations in relation to local climatic and feed availabil-

ity conditions. A range of environmental factors such as

photoperiod, water temperature, rainfall, food availability, water

quality and water level have been shown to synchronise the repro-

ductive cycle with the seasonal cycle (reviews; Sumpter, 1990;

Bromage et al., 2001). However, in temperate regions, photoperiod

and/or temperature variations are the main cues controlling the

ﬁsh reproductive cycle. Such environmental cues and factors can

be classiﬁed as proximate and ultimate factors. Proximate factors

provide seasonal cues for reproduction whereas ultimate factors

determine the optimal reproductive timing (often a combination

of temperature conditions and optimal prey/feed availability for

the offspring).

As an example, in the Atlantic salmon, winter water tempera-

ture can be considered as an ultimate factor determining the tim-

ing of spawning. This is again related to the timing of egg and larval

development in the river, since number of day-degrees from fertil-

isation to hatching and ﬁrst feeding appears to be fairly constant

across salmon populations, and hence the timing of gravel emer-

gence and ﬁrst feed intake that should take place at the optimal

time in the spring which depends on when appropriate prey are

available. The salmon then use photoperiod as a proximate cue

to enable initiation and completion of sexual maturation and

spawning at the appropriate time in the autumn/early winter. Dif-

ferent river populations of salmon show an adaption in spawning

time associated with winter temperature with earlier spawning

in winter-cold rivers enabling sufﬁcient numbers of day-degrees

for optimal hatching- and emergence-time next spring (Heggber-

get, 1988a,b). Thus, spawning time appears to be an inherited trait

adapted to the average winter temperature conditions and/or opti-

mal timing of emergence and ﬁrst feeding of the offspring.

However, water temperature may also act as a proximate factor,

probably ﬁne-tuning timing of spawning between years, as high

water temperature can arrest or delay ovulation and spermiation

in Atlantic salmon (Taranger and Hansen, 1993; Taranger et al.,

2003; King and Pankhurst, 2004; Vikingstad et al., 2008), whereas

cold water can advance and/or allow spawning (Taranger and Han-

sen, 1993; Taranger et al., 2003; King et al., 2007; Vikingstad et al.,

2008). A similar situation has been observed in the sea bass, a win-

ter spawning marine ﬁsh (Carrillo et al., 1993a,b, 1995).

5.3.1. Photoperiod

Photoperiod is regarded as a key environmental factor for initi-

ation and completion of puberty in ﬁsh species living at moderate

to high latitudes, ensuring the appropriate seasonal timing of

reproduction according to favourable conditions for the offspring

(Bromage et al., 2001). In salmonids, a decreasing proportion of ﬁsh

were able to initiate or complete puberty within a given year when

the seasonal timing of spawning was progressively advanced by

photoperiod manipulations (e.g. Taranger et al., 1998; Bromage

et al., 2001; Duston et al., 2003; Taylor et al., 2008). Based on a

range of studies, it was suggested that photoperiod treatment act

via entrainment of circannual endogenous rhythms controlling a

‘‘gating” mechanisms or a ‘‘critical time window” during which

puberty is allowed to commence or continue depending on the

physiological state of the animal (e.g. body size, adiposity and/or

stage of gonadal development) or being postponed to the next

reproductive season if the animal failed to exceed genetically

determined developmental thresholds (Fig. 2;McCormick and Nai-

man, 1984; Thorpe, 1986, 2004, 2007; Duston and Bromage, 1987,

1988, 1991; Duston and Saunders, 1999; Randall and Bromage,

1998; Taranger et al., 1999; Bromage et al., 2001; Oppedal et al.,

2006).

The role of different constant and changing photoperiods on

entrainment of the seasonal timing of reproduction has also been

extensively studied in salmonids and some perciforms, in particu-

lar in rainbow trout and sea bass, suggesting that the direction of

change in photoperiod is more important than the absolute day-

length, and that exposure to long days at a speciﬁc time period

of the year in an otherwise short day regime is very effective in

entraining the reproductive cycle (e.g. Bromage and Duston,

492 G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515

1986; Duston and Bromage, 1987, 1988; Carrillo et al., 1993a,b,

1995; Randall and Bromage, 1998; Randall et al., 1988, 1998).

Moreover, the role of the pineal and melatonin in transducing

the photic information on the seasonal entrainment of physiologi-

cal processes such as reproduction and smoltiﬁcation has been

extensively studied in salmonids (Randall et al., 1995; Porter

et al., 1996; Mazurais et al., 1999). While advancing photoperiods

can reduce the proportion of salmonids entering into puberty in a

given year, e.g. by a change from short to long days in winter or

early spring (Randall et al., 1988; Taranger et al., 1998), prolonged

exposure to long days or continuous light, or exposure to long days

or continuous light after summer solstice can have the opposite ef-

fect by increasing the proportion of ﬁsh recruiting into puberty

(Duncan et al., 1999; Oppedal et al., 2006) (see Fig. 2).

It has been demonstrated that continuous light (24L:0D or LL)

or long day treatments can inhibit or delay onset of puberty in sev-

eral ﬁsh species (Fig. 2). In European sea bass, constant long days of

short duration (i.e. 1–2 months) applied in a regime with other-

wise constant short days can advance spawning time if applied be-

fore summer solstice, whereas constant long days applied after

summer solstice delay spawning, providing solid evidence that

reproduction can be entrained by the photoperiod in this species

(Carrillo et al., 1993a,b, 1995). Moreover, LL treatments applied

over the entire reproductive cycle (12 months), during the pre-

gametogenesis (4 months), or during the gametogenesis

(6 months) were all effective in reducing the number of early

maturing males in sea bass (Begtashi et al., 2004; Felip et al.,

2008a). Similar effects were observed in grey mullet (O’Donovan-

Lockard et al., 1990), Atlantic cod (Hansen et al., 2001; Davie

et al., 2003, 2007b; Karlsen et al., 2006a), Eurasian perch (Migaud

et al., 2006) and haddock (Davie et al., 2007a). However, in the

Atlantic cod, the inhibitory effect of LL depends on the timing of

its initial application (Hansen et al., 2001; Davie et al., 2003). Inter-

estingly, in grey mullet, both continuous light and continuous

darkness inhibits gonad development (O’Donovan-Lockard et al.,

1990).

Recently, it was also demonstrated that application of constant

long days can inhibit the onset of the reproductive cycle in Eur-

asian perch. Eurasian perch maintained at a constant and long pho-

toperiod (17L:7D) from the juvenile stage (2 g) did not respond to a

water temperature decrease, while both males and females

showed normal gonad development under a similar temperature

decrease when combined with a one, four or eight hour photope-

riod decrease (Abdulfatah et al., 2007). Such inhibitory effects of

constant and long photoperiods has also been observed in yellow

perch (Perca ﬂavescens) under a 14L:10D photoperiod (Shewmon

et al., 2007). These results are in line with previous studies that

suggested that a photoperiod decrease is necessary for induction

of the reproductive cycle in other perciform species (Zanuy et al.,

1986, 1995; Mañanós et al., 1997a,b; Wang et al., 2006). By con-

trast, Migaud et al. (2003, 2004) observed only a partial inhibition

of reproduction in female Eurasian perch when a constant photo-

period (16L:8D) was applied from mid-July. However, the ﬁsh were

introduced into tanks mid-June and were subjected to a natural

photoperiod during the corresponding one month long acclimati-

sation phase. Therefore over this time period, the ﬁsh received a

one hour photoperiod decrease which may have been sufﬁcient

to trigger reproductive development.

The observed inhibitory effects of constant photoperiods may

also depend on the photophase duration (e.g. O’Donovan-Lockard

et al., 1990). Total inhibition of reproduction was observed under a

constant long photoperiod (17L:7D), while only a partial inhibition

was observed when a shorter constant photoperiod (12L:12D) was

applied (Migaud et al., 2002, 2004). On the other hand, in sea bass

there is evidence that the direction of change of the photoperiod

(i.e. from long to short) is more important than the absolute values

of the photoperiod decrease in determining the onset of gonadal

recrudescence (Carrillo et al., 1993a,b, 1995).

Moreover, in three species of mid-spring/early summer spaw-

ners, barbel (Barbus barbus), tench (Tinca tinca) and chub (Leuciscus

cephalus), Poncin et al. (1987) showed that a photoperiod decrease

inhibited pubertal development, suggesting some species speciﬁc

responses to photoperiod changes. Also a recent study on Eurasian

perch demonstrated that a 3-h photoperiod increase from 13L:11D

to 16L:8D applied two weeks before the application of an efﬁcient

inductive program inhibited onset of the reproductive cycle (Fon-

taine et al., 2006). These results indicate that the photoperiod his-

tory before the application of a certain photo-thermal inductive

program is a major factor in the induction of the pubertal

development.

5.3.2. Temperature

Water temperature plays an important role in teleost ﬁsh be-

cause it can modulate all physiological processes and endocrine

regulations. Temperature can potentially affect puberty by modu-

lating the rate of gametogenesis, or allow or inhibit gametogenesis

to proceed beyond certain stages and/or being completed, e.g. as

indicated in European sea bass (Prat et al., 1999; Zanuy et al.,

1986; Mañanós et al., 1997a). Moreover, water temperature can

also affect onset of puberty indirectly by its effects on somatic

growth and energy storing as discussed above.

Although temperature appears to play a minor role in the prox-

imate control of the reproductive cycle of salmonids (e.g. Bromage

et al., 2001; Davies and Bromage, 2002), it is often considered as

key-factor in cyprinids (Peter and Yu, 1997). Also in percids and

Fig. 2. Concept of photoperiodic effects on the timing of puberty in salmonids. The

dotted curve represents a yearly ambient photoperiod cycle at high latitudes, and

arrows represent artiﬁcial changes in photoperiod that can affect timing of puberty.

Long photoperiods or continuous light early in the season are believed to phase

advance circannual rhythms that control the seasonal timing of onset and

completion of puberty, whereas short photoperiods early in the season delay such

rhythms (Bromage et al., 2001). Long photoperiods or continuous light from

midsummer onwards also delay such rhythms, whereas short photoperiods from

around spring/early summer advances such rhythms. Advancing photoperiod

signals can either accelerate the seasonal timing of gonadal growth and spawning

or – alternatively - result in puberty being delayed to the next spawning season. The

outcome of the advancing signals on puberty, i.e. either advancing the seasonal

timing of puberty completion - or a complete delay until the next year – can depend

on the exact timing of the long photoperiod signal in the season as well as the

physiological readiness of the individual to proceed to pubertal completion. This

physiological readiness, in turn, can depend on factors such as body size, growth

rate, adiposity and stage of development of the brain–pituitary–gonad axis.

Delaying photoperiod signals will normally have the opposite effect; the timing

of spawning in the season is delayed and more individuals can reach the

physiological thresholds to complete puberty in a given year. Hence, advancing

photoperiod tends to reduce the proportion of ﬁsh reaching puberty in a given year

whereas delaying photoperiods increase this proportion. These principles appears

also to apply to other ﬁsh species at moderate to high latitudes such as European

sea bass, Gilthead sea bream, Atlantic cod and Atlantic halibut. However, in some

species like Atlantic cod, continuous light or long photoperiod from mid-summer

and onwards can inhibit the onset of puberty by one or more years.

G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515 493

moronids, a decrease of temperature was found to induce the

reproductive cycle (Dabrowski et al., 1996; Prat et al., 1999; Mi-

gaud et al., 2002; Clark et al., 2005). However, this positive re-

sponse of temperature could depend on the constant photoperiod

applied in these studies, as suggested by contradictory results ob-

tained in Eurasian perch (Migaud et al., 2002; Abdulfatah et al.,

2007). On the other hand, in Eurasian and yellow perch, almost

all data suggest that gonadal recrudescence occurs only when tem-

perature decreases after, or at the same time as the decrease of

photoperiod, and in Eurasian perch the amplitude of the initial

temperature decrease was found to play an important role for

the induction of reproductive development (Dabrowski et al.,

1996; Ciereszko et al., 1997; Migaud et al., 2002, 2004; Shewmon

et al., 2007; Wang et al., 2006).

Moreover, a series of studies demonstrate that maturation and/

or ovulation can be inhibited when temperature exceed a certain

threshold; i.e. P6°C for Atlantic halibut (Brown et al., 2006);

P8°C for Arctic charr (Gillet, 1991); P10 °C for Paciﬁc herring

(Hay, 1986); P12 °C for Atlantic salmon (Taranger and Hansen,

1993); P15 °C for white sturgeon and rainbow trout (Pankhurst

et al., 1996; Webb et al., 1999); P17 °C for sea bass (Zanuy et al.,

1986) and P28 °C for grass carp (Glasser et al., 2004). All of these

results suggest that temperature can act as a permissive factor,

particularly during the ﬁnal stages of gonadal maturation and at

spawning.

5.3.3. Other factors (salinity, raining period, swimming exercise, social

factors...)

Other types of control of reproduction (environmental or not) in

ﬁsh obviously exist, but they have been far less studied. The case of

the eels, Anguilla spp. is particular since these species have a very

long life cycle from 8 to 20 years (van Ginneken and Maes, 2005).

They reproduce only once after a long migration and the control

of reproduction in these species is far from clear, although a period

of prolonged swimming might be a physiological stimulus neces-

sary for the onset of puberty in the European eel (Palstra et al.,

2007; Sébert et al., 2007; van Ginneken et al., 2007). Moreover,

other factors like salinity (Saunders et al., 1994), water level/rain-

ing periods (Duarte et al., 2007) or social communication, e.g. by

pheromones (Burnard et al., 2008), may also be of importance for

puberty onset and/or completion in some ﬁsh species. As an exam-

ple it has been shown that sexually mature European eels stimu-

late gonadal development in neighbouring males, which may be

due to chemical communication (Huertas et al., 2006a,b, 2007).

6. Neuroendocrine control of puberty

6.1. Activation of BPG axis during puberty

Reproductive competence is acquired during puberty. Hallmark

events include enhanced gonadotropin secretion, and complete go-

nadal maturation and functioning (Ojeda et al., 2006). Prior to the

full activation of the pituitary and gonads, a series of developmen-

tal and neuroendocrine events paves the way to full activation of

the Gnrh system. This neuroendocrine system is dynamically inte-

grating central, peripheral, and environmental information, which

then reaches the pituitary via Gnrh neurons (Ojeda and Skinner,

2005; Ojeda et al., 2006).

The onset of puberty in vertebrates is marked by a (re-) activa-

tion of hypophysiotropic Gnrh neurons that stimulate pituitary

gonadotropin release, triggering pubertal development of the go-

nads. Until recently, it has not been known what controls the acti-

vation of Gnrh neurons. However, pharmacological and clinical

data obtained in mammals, strongly suggest that kisspeptins, the

peptide products of the kiss-1 gene, and their receptor (Gpr54) con-

stitute an essential gatekeeper of Gnrh functions, allowing the

integration of central and peripheral inputs (Tena-Sempere,

2006; Roa et al., 2008).

Recently, the cloning of gpr54 and kiss-1 sequences, and the ana-

tomical distribution of kiss-1 mRNA expressing neurones in the

brain have been identiﬁed in several teleosts (Carrillo et al., 2009;

Elizur, 2008; Felip et al., 2008b,c; Kah et al., 2008; Mechaly et al.,

2008; Nocillado and Elizur, 2008). These studies support the notion

that the Kiss-1/Gpr54 system is well-conserved in vertebrate evolu-

tion, not only in adults but also during pubertal development, as

suggested by changes in kiss gene expression during puberty in fat-

head minnow males and females (Filby et al., 2008). Moreover, kiss

mRNA expressing neurons in the preoptic area and the mediobasal

hypothalamus were sensitive to steroid treatment in medaka (Kan-

da et al., 2008). It has also been proved in sea bass that two kiss-1-

like genes exist in this species. Both genes show a marked expres-

sion in the brain and gonadal tissues of pubertal sea bass. Func-

tional activity of the two kiss-1-like genes has been examined

in vivo and the results show that both Kisspeptins stimulated Lh

and Fsh secretion, although Kiss2 induces a stronger response than

Kiss1 (Felip et al., 2008b). Likewise, two gpr54 (kiss1r) genes have

been characterised in sea bass, and their tissue expression analysis

revealed that both are mainly expressed in brain, pituitary and tes-

tis (Carrillo et al., 2009). Although more information on the physio-

logical effects of Kiss1/Kiss2 in ﬁsh, notably on Gnrh neurons and

gonadotropin release is needed, it is expected that future studies

will point to a high conservation of the Kiss/Gpr54 system between

ﬁsh and mammals (Nocillado and Elizur, 2008), possibly represent-

ing an integration of various internal (e.g. sex steroid feedback and

nutritional homeostasis signalling) and external factors (e.g. photo-

period) on puberty onset in ﬁshes (Fig. 3).

The Gnrh system has been extensively investigated during pub-

erty in sea bass. Rodríguez et al. (2000b) reported high to moderate

levels of Gnrh1 and Gnrh3 in the pituitary at the onset of puberty.

Later, three different gnrh cDNAs were characterised in the brain of

sea bass: gnrh1 (sbgnrh), gnrh2 (cgnrh-II), and gnrh3 (sgnrh)(Gon-

zález-Martínez et al., 2001, 2002a,b, 2004a,b), of which Gnrh1

and 3 are considered as the main hypophysiotropic isoforms. In

addition, ﬁve gnrh receptors have been cloned and characterised

in sea bass, all of them being functional and all showing highest

binding afﬁnity for Gnrh2. However, only one of these receptors

(dlGnrhr-II.1a), which is strongly expressed by the pituitary Lh

cells and also by some Fsh cells, showed afﬁnity for Gnrh1 and

Gnrh3 (Kah et al., 2007). Interestingly, it was previously demon-

strated that the expression of this receptor increases as the sea

bass enters puberty (González-Martínez et al., 2004a). Recently,

Molés et al. (2007) showed that pituitary dlgnrhr-II.1a gene expres-

sion increased in parallel with the brain gnrh1 mRNA levels during

sex differentiation and the anticipated puberty period. Collectively,

these data suggest that Gnrh1 and dlGnrhr-II.1a are most relevant

for the onset of puberty in sea bass.

Long-term Gnrha release delivery systems also induce long-

term release of Lh in male sea bass (Mañanós et al., 2002). Pretreat-

ment of immature adult sea bass with T and E2 followed by injec-

tions of Gnrha stimulated lhband gp

subunit mRNA, but not fshb

gene expression (Mateos et al., 2002). However, a peak of pituitary

fshbgene expression was observed during sex differentiation,

simultaneously with the aforementioned peak in brain (Molés

et al., 2007). Taken together, this opens the possibility that activa-

tion of the brain Gnrh system triggers both, sex differentiation and

the onset of puberty in sea bass, possibly via Fsh, while increased

expression of lhbsubunit may be more prominent at later stages

of development.

In addition to the stimulatory control by Gnrh, anatomical and

physiological investigations have shown that gonadotropes can be

subjected to an inhibitory control by dopamine. Pioneer works by

494 G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515

Richard E. Peter and co-workers identiﬁed dopamine as the main

inhibitor of ovulation and spermiation in goldﬁsh (Peter et al.,

1978; Chang and Peter, 1983; Kah et al., 1987). Following the initial

discovery in goldﬁsh, the inhibitory role of dopamine was con-

ﬁrmed in various adult teleosts, including other cyprinids (Lin

et al., 1988), silurids (de Leeuw et al., 1986), salmonids (Saligaut

et al., 1999), and some percomorphs (Yaron et al., 2003; Aizen

et al., 2005). Dopamine inhibits both basal and Gnrh-stimulated

Lh expression and release in these species, for instance through

down-regulation of Gnrh receptor levels (receptor binding activity,

de Leeuw et al., 1989; receptor mRNA expression (Levavi-Sivan

et al., 2004), and intracellular signalling pathways of gonadotropes

following binding of Gnrh (reviews; Peter et al., 1986; Yaron et al.,

2003).

While the role of dopamine in the regulation of ovulation and

spermiation has been established in adults in a certain number

of teleost species, there is no evidence for a similar inhibitory role

at the beginning of puberty in most teleosts. Indeed, the observa-

tion in many species that E2 increases the inhibitory tone during

vitellogenesis, suggests that dopamine inhibition is an adult-spe-

ciﬁc control of the last steps of gametogenesis. Accordingly, results

obtained in juvenile striped bass, indicate that dopamine is not in-

volved in the control of puberty in this species, since the dopamine

antagonist pimozide did not affect the changes in pituitary or plas-

ma Lh levels induced by T and/or Gnrha (Holland et al., 1998a,b).

Similar results were obtained in another percomorph ﬁsh, where

Gnrha alone induced precocious puberty, and no further effect

was observed using a dopamine antagonist (Kumakura et al.,

2003). In rainbow trout precocious puberty could be induced using

a combination of Gnrha and steroids (Crim and Evans, 1983); a

dopamine antagonist was not required. On the other hand, dopa-

mine might play an inhibitory role in the control of puberty in

the spadeﬁsh, where Marcano et al. (1995) found a decrease in

dopaminergic metabolism in hypothalamus at the initiation of

puberty, although a causal link has not been established yet.

Functional evidence for a role of dopamine in the inhibitory

control of puberty was ﬁrst provided in the European eel, a species

with a unique life cycle including a long-lasting juvenile stage dur-

ing the continental period. Dopamine plays a key role in the inhib-

itory control of eel puberty onset: In female (prepubertal) silver

eel, only a triple treatment with Gnrha, pimozide and steroid (T

or E2) is able to trigger an increase in Lh synthesis and release,

and subsequent vitellogenin production (Dufour et al., 1988; Vidal

et al., 2004). Preventing silver eel from completing their down-

stream migration towards the ocean will keep them in pubertal ar-

rest. This shows that one or several environmental cues

encountered during the migration route are necessary to release

the dopaminergic lock on puberty. Recent studies demonstrated

that melatonin regulates the activity of the eel dopaminergic sys-

tem, revealing a new pathway for the integration of environmental

effects on the gonadotropic axis (Sébert et al., 2008b). For details

on the nature of dopamine inhibition on eel puberty, including

physiology, anatomy, and regulation by internal and environmen-

tal factors (see recent works by Dufour et al., 2003, 2005; Vidal

et al., 2004; Pasqualini et al., 2004, 2009; Weltzien et al.,

2005a,b, 2006; Aroua et al., 2007; Sébert et al., 2007, 2008a,b).

Comparative studies in eel and striped bass, using similar

experimental conditions, highlighted the speciﬁc strength of the

dopaminergic inhibition of puberty in eel, as compared to its

apparent lack of involvement in the striped bass (Holland et al.,

1998b; Vidal et al., 2004). Recently, Aizen et al. (2005) provided

evidence that dopamine inhibition may be involved in the early

Fig. 3. Schematic representation of selected, regulatory pathways in the brain–pituitary–gonad axis during puberty in teleost ﬁsh. It is hypothesised that peripheral signals

related to somatic growth and/or energy storage are integrated in the brain with external (biotic and abiotic) signals, as well as with endocrine feedback from the gonads to

activate Gnrh neurons. Gnrh, in turn, triggers production and/or release of gonadotropins (Fsh and Lh) in the pituitary via activation of Gnrhrs). Other pituitary hormones such

as growth hormone (Gh) can also modulate gonadal development and activity during puberty onset and completion. Fsh and Lh stimulate germ cell development via

activation of the Fshr and Lhr, in part by stimulating the production of sex steroids in gonadal somatic cells and by releasing gonadal paracrine growth factors that control

germ cell growth, development and survival. Gonadal sex steroids and growth factors exert positive and negative feedback effects on the brain and/or pituitary level to

modulate Fsh and Lh production and secretion. Leptin, ghrelin and Igf1 are candidate factors that may be involved in mediating information on somatic growth and energy

storage to the brain, but these endocrine factors may also have direct effects on the gonads. The Kiss/Gpr54 system may have a role in the brain in mediating such growth/

energy related signals, gonadal feedback and external cues into regulatory input for the activation of the Gnrh neurons, thereby activating the pituitary gonadotropes during

puberty.

G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515 495

stages of vitellogenesis in grey mullet, indicating that puberty can

be under dopaminergic control in various teleost species.

Regarding gonadotropin participation, the relative importance

of Fsh or Lh has been studied in a range of teleost species during

initiation and completion of puberty, most notably by studying

gene expression of fshband lhbsubunits in the pituitary (Sohn

et al., 1998a,b, 1999, 2001; Gomez et al., 1999; Hassin et al.,

1999, 2000; Jackson et al., 1999; Melamed et al., 2000; Kajimura

et al., 2001a,b; Yaron et al., 2001, 2003; Mateos et al., 2002,

2003; Ishii et al., 2003; Onuma et al., 2003; Weltzien et al.,

2003b,c; Kumar and Trant, 2004; Meiri et al., 2004; Schmitz

et al., 2005; Choi et al., 2005).

Among the teleosts, homologous immunoassays for both Fsh

and Lh have until recently only been developed for salmonids such

as chum salmon (Suzuki et al., 1988), coho salmon (Swanson et al.,

1991) and rainbow trout (Fsh and Lh; Govoroun et al., 1998, Fsh;

Santos et al., 2001), while ontogeny and quantiﬁcation of Fsh in

non-salmonids have relied on the expression levels of gth subunit

genes in the pituitary. Lh immunoassays have been developed for

tilapia (Bogomolnaya et al., 1989), European eel (Dufour et al.,

1983), hybrid striped bass (Mañanós et al., 1997b), red sea bream

(Tanaka et al., 1993), silver carp (Kobayashi et al., 1985), goldﬁsh

(Kah et al., 1989), African catﬁsh (Koide et al., 1992) and European

sea bass (Mateos et al., 2006). Recently, homologous ELISAs were

developed for both Fsh and Lh in tilapia using recombinant gonad-

otropins (Aizen et al., 2007).

Taken together, the expression data of gonadotropin subunits

and plasma gonadotropin studies suggest that Fsh is mainly in-

volved in gametogenesis in both sexes, whereas Lh is mainly in-

volved in ﬁnal maturation and ovulation and spermiation and

sperm hydration. However, the relative importance of Fsh and Lh

in gametogenesis and spawning can differ between species, e.g.

Lh levels may be elevated also at stages before spawning in perci-

forms (Swanson et al., 2003; Yaron et al., 2003; Yaron and Sivan,

2006). On the other hand, studies focusing on puberty onset sug-

gest that Fsh signalling is more important in the early stages of

puberty, most notably associated with rapid spermatogonial prolif-

eration in males and secondary oocyte growth including vitello-

genesis and zonagenesis in females (e.g. Hassin et al., 1999;

Campbell et al., 2006; Manning et al., 2008; Felip et al., 2008a;

Molés et al., 2007, 2008, see also the discussion on gonadotropin

receptor expression sites).

The two gonadotropin receptors, Fshr and Lhr have been char-

acterised in several teleost groups including Salmoniformes (Oba

et al., 1999a,b; Maugars and Schmitz, 2006; Andersson et al.,

2010), Gadiformes (Mittelholzer et al., 2009), Cypriniformes (Basu

and Bhattacharya, 2002; Laan et al., 2002; Kwok et al., 2005), Silur-

iformes (Bogerd et al., 2001; Kumar et al., 2001a,b; Vischer and Bo-

gerd, 2003)Pleuronectiformes (Kobayashi and Andersen, 2008;

Kobayashi et al., 2008), Anguilliformes (Jeng et al., 2007; Kazeto

et al., 2008), and Perciformes (Oba et al., 2001; Wong et al., 2004;

Rocha et al., 2007, 2009). The hormone binding speciﬁcity of the

gonadotropin receptors studied in zebraﬁsh (Kwok et al., 2005;

So et al., 2005), channel catﬁsh (Kumar and Trant, 2001), Japanese

eel (Kazeto et al., 2008), and African catﬁsh (Bogerd et al., 2001;

Vischer et al., 2003), have indicated that Fshrs show a preference

for Fsh but also respond to high (e.g. ovulatory) concentrations of

Lh, while Lhrs speciﬁcally respond to Lh. Recently, pharmacological

studies showed also that the Atlantic salmon follow this pattern

(Andersson et al., 2010), which is in agreement with earlier ligand

binding data from coho salmon gonad tissue (Yan et al., 1992;

Miwa et al., 1994). However, in amago salmon (Oba et al.,

1999a,b), rainbow trout (Sambroni et al., 2007) and Atlantic hali-

but (Kobayashi et al., 2008), receptor activation studies suggested

that the Lhr, but not the Fshr responded to both gonadotropins,

indicating some species differences.

The fshr and lhr show different expression proﬁles during the

seasonal reproductive cycle and pubertal development in amago

salmon (Oba et al., 2000) and channel catﬁsh (Kumar and Trant,

2001). In the gonads of channel catﬁsh, both fshr and lhr transcripts

are expressed in a stable fashion, except for an increase of lhr dur-

ing spawning, and of fshr during a 2- to 3-month long post-spawn-

ing period. In amago salmon and tilapia, the fshr is highly

expressed early in the reproductive cycle, whereas the lhr reaches

its maximum expression level around spawning (Hirai et al., 2000;

Oba et al., 2000). Studies in Nile tilapia, zebraﬁsh and Atlantic cod

indicate that fshr expression is associated predominantly with

vitellogenesis, while the lhr is mainly up-regulated during ﬁnal oo-

cyte maturation and ovulation (Hirai et al., 2002; Kwok et al., 2005;

Mittelholzer et al., 2009). Also, Luckenbach et al. (2008) found that

ovarian fshr expression increased signiﬁcantly already at the corti-

cal alveoli stage in female coho salmon. Furthermore, in Japanese

eel, ovarian fshr mRNA level was signiﬁcantly higher than that of

lhr in immature previtellogenic female eels (Jeng et al., 2007).

These data suggest that Fsh signalling is most important during

pubertal onset. This notion is further strengthened by the observa-

tions in male ﬁsh that Fsh and 11KT plasma levels increases in

association with rapid spermatogonial proliferation (Campbell

et al., 2003; Molés et al., 2007, 2008), and that in Japanese eel (Ohta

et al., 2007) and African catﬁsh (Garcia-Lopez et al., 2009), Fsh is a

potent stimulator of androgen production, mediated by Fshr

expression by Leydig cells.

6.1.1. Pubertal activation of steroidogenesis in gonads

In most species, precocious puberty is a problem that is partic-

ularly prominent in males. Moreover, in males the causal relation-

ship between Fsh-stimulated androgen production and the shift

from the slow proliferation of A type spermatogonia to the rapid

proliferation of B type spermatogonia has been demonstrated.

The following section will therefore focus on the pubertal activa-

tion of steroidogenesis in gonads only in males.

11KT is the major androgen produced in the testicles of teleost

ﬁsh, it stimulates the Sertoli cells to produce growth factors and

promotes spermatogonial proliferation leading to meiosis and later

stages of spermatogenesis (Miura et al., 1991). It has also been sug-

gested that the 11KT may have a positive feedback on sbgnrh

expression levels in the brain of some teleosts (Okuzawa, 2002).

In sea bass, various lines of evidence show that 11KT is likely to

trigger the onset of puberty (Rodríguez et al., 2005). In prepubertal

males, 11KT induced spermatogenesis and exogenous 11KT (not T)

administered to LL (continuous light) exposed ﬁsh rescued active

spermiogenesis and induced increases of pituitary lhbgene expres-

sion and pituitary and plasma Lh levels (Carrillo et al., 2007).

The juvenile testis of a number of ﬁsh species is characterised

by a rather high production of androgens per weight unit (Schulz

and Blüm, 1990; Consten et al., 2001): speciﬁc androgen release

(i.e. release per weight unit) decreases with the start of pubertal

testis growth, to increase again when approaching adulthood. We

assume that immature testes show a high speciﬁc androgen re-

lease because Leydig cell density is relatively high before but be-

comes ‘‘diluted” after germ cell numbers increase following the

start of spermatogenesis. This phenomenon has been studied in

African catﬁsh. In this species, the Lhr shows a constitutive activity,

but still is clearly sensitive to Lh (Vischer and Bogerd, 2003). Leydig

cells in the juvenile catﬁsh testis already show all ultrastructural

signs of fully active steroidogenic cells (Cavaco et al., 1999). Inter-

estingly, Leydig cells produce a biologically inactive androgen, 11b-

hydroxyandrostenedione (OHA), which is released into the blood

and converted to 11KT in the liver (Mayer et al., 1990a,b,c; Cavaco

et al., 1997), the main androgen in adult male ﬁsh (Borg, 1994). At

the start of puberty, two things happen concomitantly. Rapid testis

growth starts reﬂecting mainly an increase in germ cell number,

496 G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515

thereby reducing the OHA release per mg of tissue (Schulz et al.,

1996). However, also Leydig cells proliferate during rapid testis

growth (Schulz et al., 2005), which may explain the increase in to-

tal testicular androgen output and increasing plasma androgen lev-

els that typically accompany puberty (Schulz et al., 1994). Another

level of regulation is exerted via androgen-mediated inhibition of

the steroidogenic capacity of the testis (Cavaco et al., 1999), reduc-

ing the number of mitochondria and the cell surface in Leydig cells

along with a reduced capacity to produce androgens via an impair-

ment of the 17–20 lyase activity. Both T and 11KT exert these ef-

fects in juveniles, while during pubertal maturation, the

inhibitory effects of 11KT, but not T, fade out (Schulz et al.,

2008), which might be a mechanism to allow increased production

of 11KT, the main androgen, without compromising Leydig cell

function. The molecular basis for this observation remains to be

elucidated.

Also in rainbow trout (Schulz and Blüm, 1990), speciﬁc andro-

gen release was highest in juveniles. While initially the two main

11-oxygenated androgens released, 11KT and 11b-hydroxytestos-

terone (OHT), were produced in similar amounts (with

11KT > OHT), OHT was exceeding the release of 11KT when maxi-

mum GSI levels were present during full spermatogenesis. This re-

verted back to 11KT being the main androgen released in spawning

animals, before the post-spawning associated reduction in andro-

gen release started. This suggests that testicular expression of the

enzyme responsible for the conversion of OHT ?11KT, 11b-

hydroxysteroiddehydrogenase, would increase speciﬁcally when

approaching the spawning season. Indeed, Kusakabe et al. (2003)

described an increase in the expression of this enzyme when the

GSI levels started to decrease from maximum levels towards the

spawning season. On the ultrastructural level, trout Leydig cells

were present before the start of spermatogenesis but full func-

tional maturity developed slowly and was attained in mature

males (Loir et al., 1995). Enzyme histochemical approaches also

suggested a gradual development of Leydig cell functionality (van

den Hurk et al., 1978). The main changes in testicular expression

of genes associated with steroidogenesis as well as expression of

gonadotropin receptors were recorded when the ﬁrst spermatozoa

were observed in the testis (Kusakabe et al., 2006), suggesting that

the initial steps of puberty, i.e. the switch to rapid spermatogonial

proliferation may depend on changes in the plasma levels of

gonadotropins.

Consten et al. (2001) showed that immature carp testes pro-

duced mainly 11-ketandrostenedione (OA), which switched to

11KT during puberty. This suggested that 17b-hydroxysteroid

dehydrogenase activity might be limiting 11KT production in the

immature testis. In another cyprinid species, the zebraﬁsh, the

adult testis produces relatively high amounts of OA as well, and

it has been suggested that expression of a testicular 17b-hydroxy-

steroid dehydrogenase isoform may increase during zebraﬁsh pub-

erty (de Waal et al., 2008). This enzyme activity is also present in

blood cells of several species (Schulz, 1986; Mayer et al.,

1990a,b,c) but depends, of course, on the provision of substrate,

probably from the testis.

Taken together, it appears that puberty-associated testis

growth, including a certain proliferation also of Leydig cells as well

as their functional differentiation (e.g. increase in expression of

key-enzymes), form the basis for the increased testicular androgen

production, and hence increasing circulating androgen levels that

accompany male puberty. Depending on the species, the regulatory

input triggering these changes is either Fsh alone (e.g. salmonids,

eel, sea bass), or Fsh and Lh (e.g. Nile tilapia; see previous section

on gonadotropins and their receptors). Steroid-mediated inhibitory

effects may prevent Leydig cell hyperactivity at initial stages of

puberty, while the selective loss of 11KT-mediated inhibition

may allow the speciﬁc increase of the production of this androgen.

6.1.2. Gonadal feedback to brain and pituitary

Castrating juvenile African catﬁsh did not change the amount of

the hypophysiotropic (catﬁsh) GnrhI while treatment with T or E2,

but not with 11KT, did increase GnrhI content in the pituitary (Du-

bois et al., 2001, 2002). Also the number of GnrhI producing neuro-

nes increased under T treatment, prematurely reaching, but not

surpassing, adult levels (Dubois et al., 2001). This suggests that

(i) a predetermined but partially dormant number of GnrhI neuro-

nes exists before puberty and can be awakened by T treatment in

terms of GnrhI synthesis, and that (ii) the status quo levels of GnrhI

do not depend on the presence of the juvenile gonads. However, in-

creased pituitary GnrhI levels can also, at least in part, be explained

by an accumulation of GnrhI, possibly reﬂecting a steroid-medi-

ated inhibition of GnrhI release. In this context, it is interesting

to note that the amount of Lh in the pituitary decreases within

2 weeks after castration of 10-week-old catﬁsh and can be rescued

by treatment with T (and E2 but not 11KT) (Cavaco, 2005). This

shows that removal of aromatiseable androgens were responsible

for the decrease in Lh. Since also in castrated ﬁsh the Lh amount

increased above start control levels to a certain degree, a gonad-

independent pathway stimulating Lh synthesis might exist, possi-

bly involving a Gnrh-mediated effect. However, plasma Lh levels

had not increased 2 weeks after castration in juvenile catﬁsh while

T treatment did reduce plasma Lh levels (Cavaco et al., 2001a), sug-

gesting that the juvenile gonad does not produce sufﬁcient

amounts of steroids to exert a negative feedback on Lh release.

In gonad-intact, immature Atlantic salmon male parr, the re-

sponse to T treatment depended on the dose, low doses being stim-

ulatory, high doses being inhibitory to gonad growth and plasma

sex steroid levels (Berglund et al., 1995). However, these long-term

experiments were not designed to investigate short-term effects

on the initiation of puberty. Using gonad-intact juvenile male Afri-

can catﬁsh, 11KT treatment stimulated gonad growth and sper-

matogenesis, probably via a direct stimulatory action on the

testis. Interestingly, however, co-treatment with 11KT and T abol-

ished the stimulatory effect of 11KT on spermatogenesis (Cavaco

et al., 2001b). It appears that gonadal steroids are required on

the one hand to promote the functional development of the Gnrh

neurones and the build-up of pituitary Lh stores, while they sup-

press testicular steroidogenesis or 11KT-stimulated spermatogene-

sis. Under these circumstances, a signal from outside of the

pituitary–gonad feedback system on the Gnrh/gonadotroph may

have to break the deadlock. Future studies will have to show if

the Kiss1-producing neurones play this role and activate the repro-

ductive system in prepubertal ﬁsh, as has been shown for the ini-

tiation of puberty in mammals, and as has been suggested for

fathead minnow (Filby et al., 2008) and zebraﬁsh (Biran et al.,

2008). In this case, expression of Kiss and/or of its cognate receptor

Gpr54 are possible targets of the steroid feedback that would then

be conveyed to the Gnrh neurones, and eventually to the pituitary,

as has been reported for some mammalian species (Ojeda et al.,

2006, 2008).

After unilateral ovaryectomy of rainbow trout (Tyler et al.,

1997), a drop of plasma E2 but a rise of plasma Fsh levels was re-

corded, which was associated with recruiting an additional batch

of follicles into maturation. It would be interesting to examine if

this recruitment activated oocytes before or after they entered

the lipid vesicle stage, the hypothesis being that the ﬁrst pitui-

tary-dependent stage (i.e. lipid vesicle stage) would have been

the one induced by the rising Fsh levels.

6.2. Growth and adiposity related endocrine factors

The relationship between body weight and fertility that inte-

grates body weight and food intake as puberty initiating factors

has been known for decades in mammals. However, only recently,

G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515 497

peripheral signals and neuroendocrine networks that integrate en-

ergy balance and reproduction are being identiﬁed (Fernandez-Fer-

nandez et al., 2006).

Cloning of mammalian leptin in 1994 was a major breakthrough

to understand the mechanisms underlying reproduction and

metabolism. Leptin secreted by white adipose tissue, is considered

as a satiety factor in the regulation of body weight in mammals.

Leptin has also a role in the control of reproduction by its action

in the hypothalamus involving Gnrh release, which in turn, regu-

lates pulsatile Lh secretion, suggesting that leptin may play a per-

missive role in the onset of puberty in mammals (Tena-Sempere

and Barreiro, 2002). In teleost ﬁsh, leptin characterisation is very

recent, i.e. in puffer ﬁsh (Kurokawa et al., 2005; Yacobovitz et al.,

2008) and in rainbow trout (Murashita et al., 2008). Physiological

evidences for involvement of leptin in the regulation of the repro-

ductive function in teleosts came from observations that mamma-

lian leptin stimulated the release of luteinizing hormone (Peyon

et al., 2001) and somatolactin (Peyon et al., 2003) in sea bass,

and that high concentration of human leptin stimulated in vitro re-

lease of pituitary Fsh and Lh in female rainbow trout (Weil et al.,

2003). In the ayu (Nagasaka et al., 2006) a clear correlation be-

tween Ir-Leptin values, rising levels of E2 and an increase of prolac-

tin secretion at maturity was found. The recent availability of

recombinant leptin (Kurokawa et al., 2005; Yacobovitz et al.,

2008; Murashita et al., 2008) in some teleost species will help to

enlighten the likely participation of this hormone in the control

of puberty in ﬁsh.

Ghrelin, a hormone secreted by the stomach as signal of energy

insufﬁciency, has been proposed as functional antagonist of the ef-

fects of leptin on energy balance in ﬁshes (Kaiya et al., 2003a,b,c),

and the role of ghrelin in non-mammalian vertebrates has recently

been reviewed by Kaiya et al. (2008). Ghrelin links food intake and

the Gh-Igf1 system by stimulating Gh-secretion (Kaiya et al.,

2003a,b,c,2008). Ghrelin has been identiﬁed in several teleosts

including goldﬁsh (Unniappan et al., 2002), eel (Kaiya et al.,

2003b), Mozambique tilapia (Kaiya et al., 2003c), Nile tilapia (Par-

har et al., 2003), rainbow trout (Kaiya et al., 2003a), channel catﬁsh

(Kaiya et al., 2005), sea bream (Yeung et al., 2006), European sea

bass (Terova et al., 2008) and zebraﬁsh cf. (Olsson et al., 2008).

Moreover, Ghrelin receptor (Ghsr) has been found in two teleost

species; black sea bream (Chan and Cheng, 2004; Chan et al.,

2004) and a pufferﬁsh (Palyha et al., 2000). Ghrelin was found to

stimulate food intake in goldﬁsh (Unniappan et al., 2002, 2004;

Unniappan and Peter, 2005; Matsuda et al., 2006a,b), Mozambique

tilapia (Riley et al., 2005) and rainbow trout (Shepherd et al., 2007).

By contrast, Jonsson et al. (2007) found no effect of trout ghrelin on

food intake in 2-year-old rainbow trout. Ghrelin may also have di-

rect effects on the reproductive axis as ghrelin was found to stim-

ulate Lh release and lhbmRNA expression in pituitary cells in

goldﬁsh (Unniappan and Peter, 2004), indicating direct actions of

ghrelin on goldﬁsh gonadotrophs. This suggests that ghrelin may

have an important role in regulating appetite and growth, and

potentially affecting puberty onset in ﬁsh, either by direct effects

on the reproductive axis – or indirectly via controlling appetite

and/or energy storage.

There is also evidence for a role of the growth hormone/insulin

like growth factor 1 (Gh-Igf1) system in control of gonadal growth

and development in ﬁsh, either by direct action of Gh or Igf1 on the

gonads, or indirectly by effects on the gonadotropes (cf. Le Gac

et al., 1993; Björnsson et al., 1994, 2002; Björnsson, 1997; Jalabert

et al., 2000). Gh receptor has been identiﬁed in gonads of several

teleosts (e.g. Gomez et al., 1999; Kajimura et al., 2004), and Gh

has been shown to stimulate or modulate gonadal steroid produc-

tion (Young et al., 1983; Singh et al., 1988; van der Kraak et al.,

1990; Le Gac et al., 1992; Singh and Thomas, 1993). Igf1r is ex-

pressed in gonads, and there is locally produced Igf1 (Gray et al.,

1990; Sakamoto and Hirano, 1991; Yao et al., 1991; Gutiérrez

et al., 1993; Gomez et al., 1999; Gioacchini et al., 2005). Igf1 and

Igf2 has been shown to increase during oocyte maturation in rain-

bow trout (Bobe et al., 2003, 2004), and the Igf binding proteins in

oocytes are modulated by stimulation of 17,20bP and gonadotro-

pins (Kamangar et al., 2006).

Igf1 has direct effect in the gonads (e.g. Le Gac et al., 1993; Kag-

awa et al., 1994; Weber and Sullivan, 2000; Weber et al., 2007).

Moreover, plasma Igf1 levels can modulate hypothalamic Gnrh re-

lease and subsequent pituitary gonadotropin secretion (Huang

et al., 1999; Baker et al., 2000; Schmitz, 2003), providing a possible

link between the growth and reproductive axes. Recently, Furu-

kuma et al. (2008) showed that Igf1 stimulated gonadotropin sub-

unit expression in a dose-dependent manner in primary pituitary

cells early in gametogenesis in masu salmon males, but not in

the later stages. In females, Igf1 also stimulated release of Fsh

and Lh early in gametogenesis, but did not stimulate gonadotropin

subunit expression at any stage. These results suggest that Igf1 di-

rectly stimulates synthesis and/or release of Gth early in gameto-

genesis in masu salmon, possibly acting as a metabolic signal

that triggers the onset of puberty, but apparently with some gen-

der speciﬁc effects.

The pituitary hormone somatolactin (Sl) may also affect repro-

ductive function in ﬁsh. Sl levels were found to increase in parallel

with ﬁnal gonadal growth in salmonids (Rand-Weaver et al., 1992;

Rand-Weaver and Swanson, 1993), and were higher in mature

rainbow trout and chinook salmon than in immature individuals

(Rand-Weaver and Swanson, 1993; Rand-Weaver et al., 1995).

Moreover, sl mRNA expression was enhanced by sexual maturation

in chum salmon (Taniyama et al., 1999), and both sl

and slbtran-

scripts were found to increase in pituitaries before and during

spawning in Atlantic salmon females and the SL receptor was

highly expressed in the ovaries (Benedet et al., 2008). Also, the

somatolactotrophs were found to be activated in sexually maturing

and spawning sockeye, chum and Chinook salmon (Olivereau and

Rand-Weaver, 1994a,b). By contrast, Kakizawa et al. (1995), found

no correlation between plasma Sl and ﬁnal gonadal maturation. Sl

has been suggested to act during early oogenesis (Campbell et al.,

2006), gonadal maturation (Rand-Weaver et al., 1992) and gonadal

steroid biosynthesis (Planas et al., 1992). It has also been proposed

to act as a facilitator of oocyte maturation through its regulation of

lipid metabolism (Fukada et al., 2005; Fukamachi et al., 2005).

However, the exact functions of Sl in reproduction are still not

known in ﬁshes (cf. Benedet et al., 2008).

7. Techniques for puberty control in ﬁsh farming

7.1. Selective breeding

Selective breeding programs can be effective in delaying age at

maturity in farmed ﬁsh and thereby also increase body size at pub-

erty (Gjedrem, 2000). Selecting strains with genetically high age

and size at puberty has been, successfully applied in Atlantic sal-

mon farming, and these traits have been further improved after

several generations of selective breeding based on family selection,

individual selection or combinations of these two approaches

(Gjerde, 1984, 1986; Gjøen and Bentsen, 1997; Gjedrem, 2000).

However, improvements of feed, feeding protocols and other hus-

bandry conditions in ﬁsh farming results in rapid improvement of

growth performance that to some extent can counteract the results

of the breeding programs on age at puberty, due to the strong phe-

notypic link between growth rate and early puberty.

There is considerable genetic variation in age at maturity or

puberty in farmed ﬁsh species. In Atlantic salmon (Salmo salar)

heritability (h

) estimates range from 0.15 to 0.48 (Gjerde, 1984;

498 G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515

Wild et al., 1994; Gjerde et al., 1994; Gjedrem, 2000), while in rain-

bow trout (Oncorhynchus mykiss) the estimates range from 0.12 to

0.35 (Gjerde and Schaeffer, 1989; Crandell and Gall, 1993; Kause

et al., 2003), and in Atlantic cod (Gadus morhua)h

was estimated

to 0.21 (Kolstad et al., 2006). However, there are also reports on ge-

netic correlations between growth (i.e. body weight at age) and

early puberty in Atlantic salmon (Gjerde, 1984; Wild et al., 1994;

Gjerde et al., 1994) and Atlantic cod (Kolstad et al., 2006). Such ge-

netic correlations must be taken into consideration in selective

breeding programs to avoid simultaneous selection of rapid so-

matic growth and early puberty.

In spite of the large potential to delay puberty in farmed ﬁsh by

selective breeding, this technique has only been adopted in the

breeding programmes for a limited number of farmed ﬁsh species

so far. The status of selective breeding in farmed ﬁsh and shellﬁsh

species in Europe has recently been reviewed in the project Aqua-

breeding (http://www.aquabreeding.eu). Currently there are more

than 30 different selective breeding programmes ﬁsh species in

Europe. These programs include mainly rainbow trout, Atlantic sal-

mon, Common carp, brown trout, turbot, Gilthead sea bream and

European sea bass. However, only a few of these programmes,

mainly for salmonids, have included age at maturity as one of

the selection criteria so far.

7.2. Feeding control

A clear link between feeding and age at puberty is seen in sev-

eral experimental studies, in particular in salmonids (Thorpe et al.,

1990; Silverstein et al., 1997, 1998; Duston and Saunders, 1999;

Shearer and Swanson, 2000; Shearer et al., 2006). Restricted feed-

ing reduces growth rate, can reduce energy stores and adiposity

(Shearer et al., 1997a, 2006), and can delay age at puberty, and

therefore it has been suggested that lipid stores, or rate of lipid

deposition, are important factors in determining age at ﬁrst matu-

rity in salmonids (Rowe and Thorpe, 1990b; Rowe et al., 1991; Her-

binger and Friars, 1992; Berglund, 1995; Hopkins and Unwin,

1997; Duston and Saunders, 1999; Shearer and Swanson, 2000;

Shearer et al., 2006). Cod depend upon reserves of protein and lipid

for gonad maturation (Dambergs, 1964; Kjesbu et al., 1991; Kjesbu

and Holm, 1994), and it has been postulated that the age at which

sexual maturity is initiated in gadoids may be dependent upon li-

pid reserves (Eliassen and Vahl, 1982). Periodic starvation during

the autumn before puberty (Karlsen et al., 1995), or restricted feed-

ing (starved every second week) from January a year prior to pub-

erty (Kjesbu and Holm, 1994) did not reduce relative fecundity nor

age at puberty. Increasing the energy expenditure by exercising

Atlantic cod 7 months prior to spawning did not inﬂuence age at

puberty (Karlsen et al., 2006). Studies indicate that this approach

is only/mostly effective when applied on ﬁsh with limited energy

reserves and or small body size (Silverstein et al., 1998; Shearer

et al., 2006), and the apparent lack of any response of restricted

feeding on age of puberty in cod could be due to the farmed cod

having much larger livers (energy stores) than their wild counter-

parts, and therefore is less sensitive to dietary manipulations un-

less these are extreme. In addition, growth control by restricted

feeding during the ﬁrst year of life may be more efﬁcient in terms

of puberty control (Herbinger and Friars, 1992; Silverstein et al.,

1998; Shearer et al., 2006).

Feed ration may also affect reproductive investments (Bagenal,

1969; Luquet and Watanabe, 1986; Kjesbu et al., 1991), and simi-

larly may feed composition, such as lowering the dietary lipid con-

tent, result in lower gonadosomatic index in Atlantic cod (Karlsen

et al., 2006b). The feed composition may also have an effect on age

at puberty, as the dietary content of energy and/or protein affects

growth and energy stores (Einen and Roem, 1997; Karlsen et al.,

2006b). However, prolonged periods of restricted feeding have also

severe negative effects on growth and condition (Karlsen et al.,

1995), and can negatively affect ﬁsh health (Damsgård et al.,

2004) and lead to higher incidence of agonistic behaviours (Mag-

nusson, 1962; Symons, 1968) and resulting damages, e.g. as a con-

sequence of ﬁn biting (Turnbull et al., 1998; Hatlen et al., 2006;

Noble et al., 2007, 2008). In addition, reduced growth normally re-

sults in longer production time to harvestable size, hence having

negative effects on the economy and sustainability of ﬁsh farming.

However, it has been hypothesised, and partially shown, that re-

stricted feeding in shorter time periods that are believed to be crit-

ical ‘decision’ periods can delay age at puberty, with minor effects

on the overall growth rate due to compensatory growth during full

feeding subsequent to the feed deprivation period (Thorpe et al.,

1990). The above mentioned negative factors limits the applicabil-

ity of overall restricted feeding as a way to reduced incidence of

early puberty in farmed ﬁsh, and may thus not be suitable for prac-

tical aquaculture purposes, whereas shorter and repeated periods

of restricted feeding may have some application in puberty control

in farmed ﬁsh.

7.3. Photoperiod control

Photoperiod control of the reproductive process has been suc-

cessfully applied to broodstock to alter the phase of the annual sex-

ual cycles and hence the spawning time in a range of ﬁsh species

(e.g. Carrillo et al., 1993a,b; Bromage et al., 2001). The process of

puberty could be considered as a particular (the ﬁrst) case of the

cyclic reproductive events in the lifespan of the ﬁsh. Consequently

it was expected that environmental manipulation altering spawn-

ing time in adults may also be effective in altering the onset of pub-

erty in juvenile ﬁsh, such as seen in rainbow trout (Duston and

Bromage, 1988; Bromage et al., 2001).

A range of studies demonstrate that photoperiod manipulation

can be an effective tool to delay or advance puberty in farmed ﬁsh,

e.g. Atlantic salmon (Oppedal et al., 2006), rainbow trout (Taylor

et al., 2008), Chinook salmon (Unwin et al., 2005), pink salmon

(Beacham and Murray, 1993; Beacham et al., 1994), Arctic charr

(Duston et al., 2003), brook trout (Holcombe et al., 2000), Atlantic

cod (Hansen et al., 2001), haddock (Davie et al., 2007a), channel

catﬁsh (Kelly and Kohler, 1996), striped trumpeter (Morehead

et al., 2000), yellowtail (Mushiake et al., 1994, 1998; Hamada

and Mushiake, 2006), European sea bass (Begtashi et al., 2004;

Rodríguez et al., 2005), striped bass (Clark et al., 2005), black sea

bass (Howell et al., 2003), Gilthead sea bream (Kissil et al., 2001;

Gines et al., 2003, 2004), Atlantic halibut (Norberg et al., 2001), tur-

bot (Imsland et al., 2003; Imsland and Jonassen, 2003), Senegalen-

sis sole (Garcia-Lopez et al., 2006), Eurasian perch (Migaud et al.,

2003, 2006), yellow perch (Ciereszko et al., 1997; Shewmon

et al., 2007) and Nile tilapia (Biswas et al., 2005; Rad et al., 2006).

However, the effectiveness of photoperiod protocols differs

among species and appears also to be modulated by other factors

such as age, feeding, body size and adiposity of the ﬁsh (Taranger

et al., 1999; Oppedal et al., 2006; Taylor et al., 2008). Moreover, full

photoperiod control can be difﬁcult to achieve in outdoor rearing

systems such as sea cages (Oppedal et al., 1997; Porter et al.,

1999; Taranger et al., 2006), and improved lighting technologies

and approaches are needed to implement such techniques at lower

cost and with more predictable outcomes in commercial farming

situations.

7.3.1. Atlantic salmon

A range of studies demonstrated the effects of photoperiod on

age at puberty in Atlantic salmon (Hansen et al., 1992; Kråkenes

et al., 1991; Duston and Saunders, 1992; Oppedal et al., 1997,

1999, 2003, 2006; Porter et al., 1999; Taranger et al., 1995, 1998,

1999; Endal et al., 2000; Peterson and Harmon, 2005; Schulz

G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515 499

et al., 2006). Continuous light (LL) treatment from mid winter on-

wards has proved to be a simple way to reduce the incidence of

early puberty in salmon in sea cages (e.g. Taranger et al., 1995; Por-

ter et al., 1999). This has been successfully applied in commercial

scale cages (Taranger et al., 1995), and is routinely used on salmon

farms to combat problems with early maturation (Hansen et al.,

2000). Photoperiod treatment can also be applied to induce preco-

cious maturation in salmon (King et al., 2003). Moreover, LL treat-

ment has also been found to delay age at puberty when applied to

underyearling postsmolts in sea cages (Oppedal et al., 2003) or sea-

water tanks (Duncan et al., 1999). However, the LL treatment was

found to increase the incidence of early puberty when applied from

the time of seawater transfer in the autumn to next summer by

Oppedal et al. (2003), and also when applied after the summer sol-

stice in sea water tanks (Duncan et al., 1999). The effect of the LL

treatment on puberty also varies between studies and depends

amongst others on the timing of the LL treatment in winter

(Taranger et al., 1998), and most likely on other factors such as

body size, adiposity and/or stage of gonadal development (Tarang-

er et al., 1999). In some cases, the LL treatment can even give the

opposite result, with an increase of the incidence of early puberty

(Kråkenes et al., 1991; Endal et al., 2000).

7.3.2. Atlantic cod

LL treatment was found to arrest or delay pubertal development

when applied to cod in indoor tanks from around mid-summer on-

wards (Hansen et al., 2001; Davie et al., 2003, 2007b; Norberg

et al., 2004; Karlsen et al., 2006a). The effect on puberty depended

on the timing of the exposure to the LL treatment (Hansen et al.,

2001; Davie et al., 2007b; Almeida et al., 2009). LL treatment in-

doors appears to arrest oocyte development in the cortical alveoli

stage (i.e. previtellogenesis) in female cod (Hansen et al., 2001),

whereas the effects on testis development were more variable with

some individuals showing full spermatogenesis but with a low tes-

tis weight compared to controls under ambient light (Almeida

et al., 2009). Interestingly, when cod were transferred back from

LL to natural light in mid-winter, puberty resumed and spawning

occurred within a few months (Hansen et al., 2001; Almeida

et al., 2009). However, LL treatment was less effective when ap-

plied in commercial sea cages (Taranger et al., 2006; Trippel

et al., 2008), and appeared to depend on the intensity of the artiﬁ-

cial light (Dahle et al., 2000; Trippel et al., 2008). The difference in

effectiveness was attributed to the strong ambient light in the

cages relative to the artiﬁcial LL light that was superimposed on

the ambient light cycle (Taranger et al., 2006). Recent studies on

cod in outdoor tank subjected to LL of different intensities in super-

imposed on the ambient light cycle show that that higher intensi-

ties of the LL treatment were more efﬁcient in delaying puberty,

possibly by being more effective in overruling the strong ambient

light signal (Kristoffersen, Karlsen, Norberg, Taranger, unpublished

results).

7.3.3. Atlantic halibut

Attempts to control maturation by photoperiod manipulation

have yielded varying results in Atlantic halibut, and appear to de-

pend on the timing of manipulation, as regards both to time of year

and initial age of the ﬁsh (Norberg et al., 2001; Imsland and Jonas-

sen, 2005; Imsland et al., 2006). Juvenile halibut exposed to LL dis-

played higher growth and lower incidence of maturation than ﬁsh

held at simulated natural photoperiod or on a short day regime

(Imsland and Jonassen, 2003, 2005). On the other hand, LL applied

15 or 5 months prior to maturation accelerated growth, but also

advanced maturation by 3 months, while a period of LL from 15

to 5months prior to maturation, followed by natural photoperiod

reduced incidence of maturation and promoted growth (Norberg

et al., 2001). Moreover, exposure to LL for 2 years prior to ﬁrst mat-

uration reduced the incidence of male maturation and promoted

growth, while shorter LL exposure either advanced maturation,

or was inefﬁcient (Imsland et al., 2008).

7.3.4. European sea bass

The ﬁrst detailed study on the effect of modiﬁed photoperiod

cycles to delay the ﬁrst maturity in sea bass (Rodríguez et al.,

2001b) investigated the long-term (starting with 4-month-old

sea bass and during three consecutive years) effects of a constant

long photoperiod (15L:9D) on pre-pubertal male sea bass. Gonadal

maturation was signiﬁcantly delayed compared to ﬁsh exposed to

simulated natural photoperiods. Recently (Carrillo, Begtashi, Rodri-

guez, Marin, Zanuy, unpublished results), conﬁrmed the delaying

effects of long photoperiods on the onset of puberty in out-door

ﬂoating cage culture system. The ﬁrst evidence for the LL effects

on gonadal maturation in sea bass was obtained by Begtashi

et al. (2004). These authors reported that juvenile ﬁsh exposed to

LL throughout a year showed a drastic reduction in the rates of

male entering early puberty (0–3% in LL treated ﬁsh versus 22%

in ambient controls). Recently it has also been shown that shorter

LL treatments, lasting 4 or 6 months during pre-gametogenesis and

gametogenesis, respectively (Felip et al., 2008a) resulted in similar

low rates of precocity as when maintained under LL all the year

round. These studies paved the way for screening the period Au-

gust–November with LL windows of short duration (2 months) to

ﬁnd a the most sensitive period to block gametogenesis in sea bass

(Carrillo et al., 2008).

7.4. Induced sterility

7.4.1. Triploidy

Sterile ﬁsh can be an effective means to combat problems asso-

ciated with early puberty, both to avoid negative effects on produc-

tion performance, health and welfare, as well as to prevent any

negative genetic impacts of ﬁsh farming on wild populations. Trip-

loidy is relatively easily achieved in many ﬁsh species, either by

pressure or temperature shocks on the eggs just after fertilisation.

Triploid ﬁsh are normally fully sterile, but the males can develop

large gonads and display secondary sexual characters. By contrast,

triploid females will normally only develop small gonads and avoid

development of secondary sexual characters. Hence, it is com-

monly beneﬁcial to combine triploid sterile ﬁsh with all-female

stocks.

All-female production can be achieved in many ﬁsh species by

either hormone or enzyme inhibitor treatments in early life, nor-

mally applied to the generation prior to the on-growing ﬁsh. The

mechanisms of sex differentiation, impact of environmental factors

on sex differentiation and effects of sex steroids and enzyme inhib-

itors on sex reversal and ultimately the production of monosex

stocks has been reviewed several times (e.g. Piferrer, 2001; Devlin

and Nagahama, 2002; Gomelsky, 2003; Shelton, 2006), and is not

detailed further in the current paper.

7.4.2. Methods for triploidy induction – success and survival

Production of triploids is still recognised as the most practical,

economic, and effective method for large scale production of sterile

ﬁsh. The induction of triploidy throughout chromosome set manip-

ulation has been applied on many cultured ﬁsh species, especially

freshwater, including mainly salmonids, cyprinids, cichlids and

ictalurids. Several studies have applied these manipulations also

to about a dozen marine species, including sparids, moronids and

ﬂatﬁshes (Ihssen et al., 1990; Pandian and Koteeswaran, 1998;

Benfey, 1999; Felip et al., 2001a; Hulata, 2001; Tiwary et al.,

2004; Maxime, 2008).

Triploidy is induced by forcing retention of the second polar

body by applying temperature (hot or cold), hydrostatic pressure,

500 G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515

anaesthetics or chemical shocks, shortly after a normal fertilisa-

tion. Of these methods, temperature and hydrostatic pressure

shocks are in practical use. Temperature and hydrostatic pressure

shock treatments are inexpensive to apply and can be successfully

adapted for mass production on ﬁshfarms. Cold shock in general

has been most successful in warm water ﬁshes (Felip et al.,

2001a) with good examples from sea bass (Felip et al., 1997) and

turbot (Piferrer et al., 2000). Heat shock has been 100% effective

in producing triploids in tilapia (Varadaraj and Pandian, 1990),

rainbow trout (Solar et al., 1984) and gilthead sea bream (Gorshkov

et al., 1998). Hydrostatic pressure shock has been successfully used

to produce triploids in several species, e.g. zebraﬁsh (Streisinger

et al., 1981), rainbow trout (Lou and Purdom, 1984), Atlantic sal-

mon (Benfey and Sutterlin, 1984), common carp (Linhart et al.,

1991), Nile tilapia (Hussain et al., 1991), yellow perch (Malison

et al., 1993), coho salmon (Piferrer et al., 1994), yellowtail ﬂounder

(Manning and Crim, 2000) and Atlantic cod (Trippel et al., 2008).

Generally, pressure shocks seemed to be less harmful and give

higher survival than cold shocks (Peruzzi and Chatain, 2000) and

heat shocks (Carrillo et al., 1993a,b; Teskeredz

ˇic

´et al., 1993; Haf-

fray et al., 2007).

7.4.3. Survival

After the initial mortality associated with the handling and

shock treatments in the triploidisation protocols, the difference

in survival between triploids and diploids are less pronounced. In

Atlantic salmon, freshwater mortality is reported to be higher in

triploids in both experimental and commercial studies (McGeachy

et al., 1995; O’Flynn et al., 1998; Benfey, 2001; Cotter et al., 2002).

However, mortality rates are often within commercially acceptable

levels, with the highest mortality during embryonic and larval

development prior to ﬁrst-feeding (Johnson et al., 2004). Higher

mortality in triploids has also been found in sea bass up to

3 months of age (Peruzzi et al., 2004) and rainbow trout (Quillet

et al., 1987). However, examples with no difference in survival be-

tween triploids and diploids were reported in Thai silver barb

(Koedprang and Na-Nakorn, 2000), and higher survival were found

in triploid turbot compared with diploid controls (Cal et al., 2006).

7.4.4. Growth

Quillet et al. (1988) reviewed the growth of diploids and trip-

loids from 19 publications and Pandian and Koteeswaran (1998)

added 13 papers to a total of 32 papers in a later review. The trip-

loid/diploid (T/D) ratio for weight varied from 0.38 to 1.43 in the

pre-maturation phase, but triploids grow generally slower than

diploids. However, in the post-maturation phase the triploids took

advantage of their sterility and in almost all species the triploids

grew 10–30% faster than diploid controls. Moreover, triploids from

herbivorous species (Cyprinidae and Cichlidae) appear to be less

negatively affected than carnivorous species during the pre-matu-

ration phase, and more positively affected during the post-matura-

tion phase. There is also a general tendency that triploids grow

faster when reared alone than when they are reared in commune

with diploids. This is possibly because the triploids are less aggres-

sive and have a lower ability to compete for food (Maxime, 2008).

In one of the few studies to show enhanced growth of triploid

salmon under commercial conditions it was evident that there

were signiﬁcant family/year class differences observed between

ploidies advocating the need for selection to obtain the best per-

formers (O’Flynn et al., 1997). Numerous studies now recommend

the need for selection programs for successful triploid production

in salmonids, particularly since triploids often show greater vari-

ability in performance both within and between families (Bonnet

et al., 1999; Friars et al., 2001; Cotter et al., 2002; Oppedal et al.,

2003). Signiﬁcantly enhanced growth of triploid Atlantic salmon

under continuous light (LL) relative to diploids has been observed

(Oppedal et al., 2003), suggesting that some environmental condi-

tions are particularly beneﬁcial for triploids, and that poorer

growth reported in some triploid stocks may be due to unfavour-

able husbandry regimes.

7.4.5. Morphology and deformities

Several morphological differences and deformities has been re-

ported in triploid non-salmonids like tilapia (Varadaraj and Pan-

dian, 1990), pejerrey (Strüssmann et al., 1993), carp (Gomelsky

et al., 1992), tench (Flajshans et al., 1993), bighead carp and grass

carp (Tave, 1993) and catﬁsh (Varkonyi et al., 1998).In salmonid

farming the occurrence of speciﬁc morphological abnormalities

in triploids has signiﬁcantly hindered the adoption of this technol-

ogy. The most commonly described deformity in triploid salmon is

the ‘‘lower jaw deformity syndrome” (Sutterlin et al., 1987; Jungal-

walla, 1991; Benfey, 2001; Sadler et al., 2001). Other deformities

include shortened gill covers, reduced numbers of primary gill ﬁl-

aments and eye cataracts. Prevalence and occurrence of speciﬁc

abnormalities differs between rearing environments, stocks and

strains. Furthermore, deformities are not always observed, and

occurrence of deformities may not necessary be the result of trip-

loid induction methods as such, as similar levels of deformity have

been found in diploids (Sutterlin et al., 1987; Kacem et al., 2004).

7.4.6. Immunology and disease resistance

The reported differences between diploid and triploid immu-

nology and disease resistance are generally small. Yamamoto and

Iida (1994) found similar complement activity in triploid and dip-

loid rainbow trout, and Langston et al. (2001) found a small delay

in the complement activity and hypoferraemic response in Atlantic

salmon. Budino et al. (2006) found no differences in total respira-

tory burst activity and phagocytosis between triploid and diploid

turbot because the lower blood cell number of the triploids was

compensated by a larger size and a higher activity per cell. The dif-

ferential cell count, serum complement and lysozyme or bacterici-

dal activities was similar in both types of ﬁsh, indicating that the

activities of the humoral components of the innate immune system

tested are similar in diploid and triploid ﬁsh. Also, Small and Ben-

fey (1987) found a higher cellular phagocytic activity in triploid

salmon, but this was balanced by a lower number of leucocytes

(Yamamoto and Iida, 1994; Benfey, 1999). Also challenge tests

did not uncover differences in disease resistance between diploids

and triploids. Yamamoto and Iida (1995b) found no differences in

susceptibility of diploid and triploid rainbow trout for Infectious

Haematopoietic Necrosis (IHN) virus, furunculosis and vibriosis,

and Dorson et al. (1991) found no difference in the susceptibility

of diploid and triploid rainbow trout, arctic charr, brook trout

and lake trout for Infectious Pancreatic Necrosis virus, Viral haem-

orrhagic septicemia virus type 1 and 3 and IHN virus. Moreover,

Yamamoto and Iida (1995a) found a similar response to vaccina-

tion in diploid and triploid rainbow trout.

7.4.7. Sensitivity of triploids to sub-optimal environmental conditions

Triploid ﬁsh have been reported to be more sensitive to envi-

ronmental changes than diploid ﬁsh. However, triploid brook

trout, rainbow trout and Atlantic salmon have been shown to

have the same response to acute stress (handling and crowding)

as diploid ﬁsh (Biron and Benfey, 1994; Benfey and Biron,

2000). Primary and secondary stress responses do not differ, sug-

gesting that mortalities reported under commercial conditions

cannot be attributed to differences in their physiological response

to stress in relation to husbandry or management practices

(Sadler et al., 2000a; Leggatt et al., 2006). However, it is plausible

that intolerances to environmental extremes may explain the

higher mortalities at times of increased physiological stress in

triploid ﬁsh.

G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515 501

Triploid red blood cells exhibit increased mean corpuscular vol-

ume (MCV), which decreases the surface-to-volume ratio and may

have marked effect on triploid physiology, as the total area avail-

able for oxygen assimilation and other diffusion processes will be

reduced. In triploid ﬁsh, this may result in a reduced aerobic capac-

ity. However, this has not been deﬁnitively demonstrated in any

species (Benfey and Sutterlin, 1984; Yamamoto and Iida, 1994;

Cal et al., 2005; Peruzzi et al., 2005). Ventilation rate is higher in

triploid than diploid Atlantic salmon (Benfey, 1999), but not in

brook trout (Stillwell and Benfey, 1996), again suggesting that trip-

loid state is not necessarily associated with reduced aerobic capac-

ity. It would thus appear that farm mortalities of triploids in

response to stress are not due to failure in respiratory homeostasis

(Sadler et al., 2000a,b). Such problems may therefore relate to

other sub-optimal rearing conditions which need to be clearly

identiﬁed.

Increased mortality in triploid trout has been reported when the

temperature is at its highest in the summer (Ojolick et al., 1995;

Altimiras et al., 2002). Stillwell and Benfey (1996) demonstrated

that triploid brook trout had lower metabolic rate (i.e. oxygen

requirement) than diploids, a possible compensation for a reduc-

tion in the efﬁciency of gas exchange. However, the metabolic rate

did not differ between ploidy in brown trout at thermal optima,

but at higher temperatures the metabolic scope was reduced, thus

lowering the energy available for the animal to grow, digest food,

support locomotion, etc., and may be a factor explaining the in-

crease in mortality often seen in triploid trout at higher tempera-

tures. In triploid brown trout evidence was lacking to support

reduced maximal heart capacity between ploidies, although maxi-

mal performance may be limited at higher temperatures poten-

tially contributing to an increased mortality (Mercier et al., 2002).

7.4.8. Triploidy in European sea bass

In European sea bass induced triploidy disrupts gametogenesis

resulting in functional sterility with more pronounced effects in fe-

males than in males. Speciﬁcally it was found that triploidy

blocked the initial phases of meiosis in females and the late phases

of meiosis in males, resulting in the absence of, or a reduction in

gonadal development, respectively. Speciﬁcally, in females, trip-

loidy blocked meiosis during the zygotene stage, preventing the

pairing of homologous chromosomes. In contrast, in males, trip-

loidy blocked meiosis during the transformation of secondary sper-

matocytes into spermatids, thus preventing spermiogenesis (Felip

et al., 2001b). The induction of triploidy in sea bass conferred func-

tional sterility in both males and females, thus proving a good

model to describe the effects of triploidy on the gonadal develop-

ment in the two sexes.

The reviews of Zanuy et al. (2001) and Felip et al. (2001a) sum-

marise the methodologies used to obtain triploid sea bass and the

yields obtained after its application. Among those cold shock has

proven to be the most reliable and simple procedure ready to be

used in large-scale production of triploid sea bass. Felip et al.

(1997) found the optimal conditions for induction of triploidy in

sea bass to be 10 min of 0 °C cold shock administered 5 min after

fertilisation. The resulting yield of triploids of this procedure was

around 80%. Later on Peruzzi and Chatain (2000) induced 100%

triploidy in sea bass using very similar conditions. During their

3–4 ﬁrst years of life, triploid sea bass grew in a similar fashion

as diploids in fork length but slower than diploids in body weight,

even when the diploids reached full sexual maturity. On the other

hand, older triploids (from 5 to 7 year old ﬁsh) showed gender re-

lated dimorphic growth with triploid females attaining the largest

body size (Felip, Zanuy, Carrillo, unpublished results).

The presence of jaw, operculum and vertebral column deformi-

ties was also observed in triploid sea bass, but have been attributed

to handling during artiﬁcial fertilisation, inbreeding or chromo-

somal aberrations (Felip et al., 2001a). This suggests that develop-

ment and the external morphology of triploid ﬁsh is essentially

similar to that of diploids. However, more studies are needed to

more fully ascertain the usefulness of triploid sea bass under inten-

sive culture conditions.

7.4.9. Other methods for sterility

Recently, functional studies have identiﬁed genes involved in

regulating the migratory behaviour of primordial germ cells (PGCs)

during embryogenesis in ﬁsh (Doitsidou et al., 2002; Slanchev

et al., 2005). When suppressing the function of these genes that en-

code a cytokine attracting PGCs to the genital ridge or the receptor

for this cytokine on the migrating PGCs, the migratory direction of

PGCs becomes random, so that most PGCs ‘‘miss” the genital ridge

and become apoptotic.

An even more effective manner of generating animals with

germ cell-free gonads is to interfere with the expression of the

dead end (dnd) gene, since PGC migration is blocked at very early

stages (within 12 h after fertilisation) of embryogenesis, leading

to the loss of all PGCs by apoptosis (Weidinger et al., 2003). The ap-

proach to interfere with the expression of the dnd gene has been

transferred successfully to other ﬁsh species (Saito et al., 2008).

Moreover, techniques have been developed allowing the transient

(i.e. non-transgenic) labelling of PGCs with ﬂuorescent proteins

that is applicable to different species (Yoshizaki et al., 2005) and

that is an excellent tool to control the efﬁciency of dnd knock-

down. Clearly, however, these approaches are not suitable for gen-

erating a large number of individuals. The mutagenesis-induced

loss of function of the ziwi gene (Houwing et al., 2007) leads to a

similar phenotype of the gonads, which stay small due to the com-

plete loss of all germ cells up until day 12–14 after fertilisation.

Interestingly, as in the case of dnd knock down, all zebraﬁsh with-

out germ cells develop as phenotypic males, so that the default

state of sex differentiation for the somatic compartment of the go-

nad in the absence of germ cells seems to be male. These animals

apparently go through normal puberty and show typical male

reproductive behaviour, so that the production of sex steroids does

not seem to be affected. Despite the experimental state of these

techniques, it can be anticipated that technical developments

may allow the use of this knowledge for applied purposes in the fu-

ture in a manner compatible with regulations and consumer

interests.

8. Gaps in knowledge and research directions

Early puberty represents a major problem in farming of many

ﬁsh species due to negative effects on growth, feed utilisation,

health and welfare, and potential genetic effects on wild stocks

after escape or release of fertilised eggs into natural ecosystems.

In some species, late puberty leads to increased cost with brood-

stock management, while in other species a complete block of pub-

erty under farming conditions prevents reproduction and closure

of the life cycle.

There is still limited knowledge on the neuroendocrine mecha-

nisms that control onset and/or completion of puberty in ﬁshes

and other vertebrates. These mechanisms are sensitive to external

factors, such as environmental and husbandry conditions. For

example, there is a strong link between feeding level/somatic

growth and early puberty, but the underlying physiological mech-

anisms are still to be elucidated. More knowledge is needed on

both fundamental and applied aspects for a full and targeted con-

trol of puberty. This will also allow developing cost-effective meth-

ods for delaying or advancing/inducing puberty that are acceptable

in terms of ﬁsh welfare, environmental impact, and consumer

interests.

502 G.L. Taranger et al. / General and Comparative Endocrinology 165 (2010) 483–515

Selective breeding has a large potential for delaying age and size

at puberty in ﬁshes, but genotype-environment interactions need

further investigations to improve breeding programs operating un-

der changing environmental and husbandry conditions. Moreover,

breeding programs could beneﬁt from the identiﬁcation of genetic

markers for age at puberty to assist selection, and by a deeper

understanding of the interplay between genetic and environmental

factors in controlling puberty.

Photoperiod control has been successfully applied to both delay

and advance puberty in farmed ﬁsh. However, such protocols do

not always work when applied in commercial rearing systems.

Moreover, photoperiod effects can depend on interactions with

other factors such as genetic background, growth and adiposity.

Although photoperiod effects have been extensively investigated

in ﬁshes, the mechanistic basis for photoperiod-mediated changes

in the activity of the neuroendocrine systems regulating puberty

still awaits elucidation, the interactions with other factors are

poorly studied; this also applies to the secure application with a

more predictable outcome of these techniques under commercial

rearing conditions.

Induced sterility, e.g. by triploidy, can eliminate the risk of a

genetic impact of farmed ﬁsh on wild stocks, and can also miti-

gate or prevent many or all of the negative impacts of early pub-

erty on farmed ﬁsh. Triploidy induction is possible in several

species and there is information on the performance of triploid

ﬁsh in ﬁsh farming. However, despite clear beneﬁts, this tech-

nique is not yet applied commercially in many species, due to

production and welfare related problems under certain environ-

mental conditions. Hence, more knowledge is needed on the

physiology, health and welfare of triploid ﬁsh, in the light of envi-

ronmental conditions required to secure optimal production per-

formance and welfare. Such knowledge will also allow the design

of breeding programs in order to select for more robust triploid

ﬁsh.

Triploidy is often combined with all-female production to get

the beneﬁcial effects of sterilization on production performance

and health of the ﬁsh; after all, despite sterility (i.e. no production

of fertile sperm), the maturation of the somatic component of the

testis does occur, including the increased sex steroid levels and

their pleiotropic effects. However, the techniques to produce all-fe-

male populations are not yet available in all farmed ﬁsh species,

and more knowledge is needed on sex determination and sex dif-

ferentiation to provide more secure methods for mono sex

production.

Finally, efforts should be directed towards the development of

new sterility models, including techniques to induce germ cell free

gonads (e.g. dead-end knock down approach) that could result in

both a robust and sterile ﬁsh, and would avoid the complications

associated with the use of mono-sex techniques.

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Pascal Fontaine · Sylvie Dufour · Rüdiger Schulz · Eva Andersson · Tom Hansen

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Unravelling spermatogenesis in spotted wolffish: Insights from the ultrastructure of juvenile male testes to the cryopreservation of broodstock sperm

Article

Full-text available

Jun 2024
AQUACULTURE

This study aimed to deepen our understanding of the reproductive biology of male spotted wolffish (Anarhichas minor) using two different experimental approaches involving juvenile and mature broodstock fish. The first approach consisted of a detailed histological examination of the testes to identify the onset of gonadal maturation and characterize the spermatogenic stages in two- and three-year-old juvenile specimens. Light microscopy analysis revealed clear differences between the age groups. Two-year-old fish displayed well-defined interstitial tissue, Sertoli cells, and cysts housing spermatogonia stem cells in which meiosis had not yet begun. In contrast, three-year-old fish exhibited cysts containing spermatocytes, spermatids, and abundant spermatozoa, indicating the initiation of the spermatogenic cycle, albeit with asynchronous puberty. Histochemical staining revealed a significant presence of smooth myoid cells in the interstitial tissue of sexually mature fish. In contrast, electron microscopy further revealed synaptonemal complexes, indicating the onset of meiosis and centriolar structures that gave rise to flagella. The second approach focused on optimizing semen freezing and cryopreservation procedures in mature broodstock individuals over the age of 10 years. Seven freezing extenders (KT, TS-2, OP, MT, MH, HBSS, or SR), with seawater (SW) as a control, were assessed along with two cryoprotectants dimethylsulfoxide (DMSO) or methanol to evaluate their impact on pre- and post-thaw semen quality. Results showed that the MT and HBSS extenders were superior in total sperm kinetics at 1:3 dilution and that DMSO showed optimal results in sperm motility and velocity variants. Moreover, the MT and HBSS groups demonstrated consistent sperm viability after cryopreservation, with values similar to fresh samples. Based on the viability results of the SYBR-green-14/PI assay comparing fresh and cryopreserved sperm using MT and HBSS, the MT extender emerged as the most effective freezing medium for cryopreservation of spotted wolffish broodstock sperm. In conclusion, this study provides a comprehensive understanding of the reproductive dynamics of male spotted wolffish, offering valuable insights for both scientific research and aquaculture management.

Implicaciones de la alimentación continua sobre la demanda de oxígeno en un pez agástrico con intestino corto (Teleostei: Atherinopsidae)Implicaciones de la alimentación continua sobre la demanda de oxígeno en un pez agástrico con intestino corto (Teleostei: Atherinopsidae)

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Jun 2024

Continuous illumination and increased feeding periods have enhanced growth in commercial fish species. However, oxygen consumption under these conditions has yet to be previously assessed in agastric short-intestine fish. This study evaluated Chirostoma estor (Atherinopsidae) oxygen consumption under three specific feeding and light regimes: resting-unfed, routine-fed, and continuous light/feeding. Fish in the continuous light/feeding condition presented oxygen consumption levels 60 and 20% higher than resting-unfed and routine-fed fish, respectively. The latter implies that constant high oxygen supply levels are required to satisfy the demand for C. estor raised under these high growth rate conditions. The present study shows the relevance of determining oxygen consumption levels during continuous illumination and extended feeding periods to consider optimal oxygen levels required to achieve better performance indicators, such as the growth and welfare of atherinopsids and species with similar digestive configurations.

Characterization of a novel fast-growing zebrafish: a new approach to growth hormone transgenesis

Article

Full-text available

Apr 2024

The manipulation of the somatotropic axis, governing growth, has been a focus of numerous transgenic approaches aimed at developing fast-growing fish for research, medicine and aquaculture purposes. However, the excessively high growth hormone (GH) levels in these transgenic fish often result in deformities that impact both fish health and consumer acceptance. In an effort to mitigate these issues and synchronize exogenous GH expression with reproductive processes, we employed a novel transgenic construct driven by a tilapia luteinizing hormone (LH) promoter. This approach was anticipated to induce more localized and lower exogenous GH secretion. In this study, we characterized the growth and reproduction of these transgenic LHp-GH zebrafish using hormonal and physiological parameters. Our findings reveal that LHp-GH fish exhibited accelerated growth in both length and weight, along with a lower feed conversion ratio, indicating more efficient feed utilization, all while maintaining unchanged body proportions. These fish demonstrated higher expression levels of LH and GH in the pituitary and elevated IGF-1 levels in the liver compared to wild-type fish. An examination of reproductive function in LHp-GH fish unveiled lower pituitary LH and FSH contents, smaller follicle diameter in female gonads, and reduced relative fecundity. However, in transgenic males, neither the distribution of spermatogenesis stages nor sperm concentrations differed significantly between the fish lines. These results suggest that coupling exogenous GH expression with endogenous LH expression in females directs resource investment toward somatic growth at the expense of reproductive processes. Consequently, we conclude that incorporating GH under the LH promoter represents a suitable construct for the genetic engineering of commercial fish species, providing accelerated growth while preserving body proportions.

Combining genome-wide association study and transcriptome analysis to identify molecular markers and genetic basis of population-asynchronous ovarian development in Coilia nasus

Article

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Jan 2023

Coilia nasus, a migratory fish species found in the middle and lower reaches of the Yangtze River and along offshore areas of China, possesses considerable aquacultural and economic potential. However, the species faces challenges due to significant variation in the gonadal development rate among females, resulting in inconsistent ovarian maturation times at the population level, an extended reproductive period, and limitations on fish growth rate due to ovarian prematurity. In the present study, we combined genome-wide association study (GWAS) and comparative transcriptome analysis to investigate the potential single nucleotide polymorphisms (SNPs) and candidate genes associated with population-asynchronous ovarian development in C. nasus. Genotyping of the female population based on whole-genome resequencing yielded 2 120 695 high-quality SNPs, 39 of which were suggestively associated with ovarian development. Of note, a significant SNP peak on LG21 containing 30 suggestively associated SNPs was identified, with cpne5a determined as the causal gene of the peak. Therefore, single-marker and haplotype association analyses were performed on cpne5a, revealing four genetic markers ( P<0.05) and seven haplotypes (r 2>0.9) significantly associated with the phenotype. Comparative transcriptome analysis of precociously and normally maturing individuals screened out 29 and 426 overlapping differentially expressed genes in the brain and ovary, respectively, between individuals of different body sizes. Integrating the GWAS and transcriptome analysis results, this study identified genes and pathways related to hypothalamic-pituitary-gonadal axis hormone secretion, extracellular matrix, angiogenesis, and gap junctions involved in population-asynchronous ovarian development. The insights gained from this study provide a basis for a deeper understanding of the molecular mechanisms underlying ovarian development in fish and may facilitate the genetic breeding of C. nasus strains exhibiting population-synchronous ovarian development in the future.

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Full-text available

Apr 2024
AQUACULT INT

Farming of red tilapia is one promising direction in aquaculture. The objective of this study was to investigate the impact of long-day photoperiod on the growth performance, reproductive parameters, maturity, sex ratio, β-carotene content, and skin coloration of red tilapia. Early life larvae were allocated into three treatment groups in triplicates: T1 = control group (12L:12D), T2 = long-day group (18L:6D), and T3 = continuous illumination group (24L:0D) for 90 days. By the end of the experiment, gonadosomatic index (GSI), relative fecundity, steroid hormones, maturity stages, sex ratio, and ovarian and testicular histology were examined; also, growth performance, survival rate, skin color, and total β-carotene content were measured. The results indicated that GSI% and serum testosterone (T) in T3 group significantly increased with greater amount of spermatozoa of male fish. Also, growth parameters and HSI% in female fish displayed significantly increased for T3 group. Females in group T2 showed significant elevation in GSI%, relative fecundity, and estradiol (E2) with higher number of mature stage. Continuous light group (T3) showed shifted male sex ratio, while female percentage was higher in T2 group. The total β-carotene content of T3 group showed significant elevation with less number of black spots. This study demonstrated that continuous light manipulation during red tilapia early life could stimulate the growth and enhance coloration by reducing black spots that significantly affects economic profitability. Long-day application was effective in female reproductive performance and maturity. This study also served as an important reference for red tilapia aquaculture.

Broodstock Management and Nutrition

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Mar 2024

Gene co-expression patterns in Atlantic salmon adipose tissue provide a molecular link among seasonal changes, energy balance and age at maturity

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Mar 2024
MOL ECOL

Sexual maturation in many fishes requires a major physiological change that involves a rapid transition between energy storage and usage. In Atlantic salmon, this transition for the initiation of maturation is tightly controlled by seasonality and requires a high-energy status. Lipid metabolism is at the heart of this transition since lipids are the main energy storing molecules. The balance between lipogenesis (lipid accumulation) and lipolysis (lipid use) determines energy status transitions. A genomic region containing a transcription co-factor of the Hippo pathway, vgll3, is the main determinant of maturation timing in Atlantic salmon. Interestingly, vgll3 acts as an inhibitor of adipogenesis in mice and its genotypes are potentially associated with seasonal heterochrony in lipid storage and usage in juvenile Atlantic salmon. Here, we explored changes in expression of more than 300 genes directly involved in the processes of adipogenesis, lipogenesis and lipolysis, as well as the Hippo pathway in the adipose tissue of immature and mature Atlantic salmon with distinct vgll3 genotypes. We found molecular evidence consistent with a scenario in which immature males with different vgll3 genotypes exhibit contrasting seasonal dynamics in their lipid profiles. We also identified components of the Hippo signalling pathway as potential major drivers of vgll3 genotype-specific differences in adipose tissue gene expression. This study demonstrates the importance of adipose gene expression patterns for directly linking environmental changes with energy balance and age at maturity through genetic factors bridging lipid metabolism, seasonality and sexual maturation.

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Jun 2024
AQUACULTURE

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Jun 2024

Zebrafish (Danio rerio) as a Model Organism in Reproductive Research

Chapter

Jan 2024

Wei Ge

THE EVOLUTION OF PHENOTYPIC PLASTICITY IN LIFE-HISTORY TRAITS: PREDICTIONS OF REACTION NORMS FOR AGE AND SIZE AT MATURITY

Article

Full-text available

Sep 1986
EVOLUTION

We used life-history theory to predict reaction norms for age and size at maturation. We assumed that fecundity increases with size and that juvenile mortality rates of offspring decrease as ages-at-maturity of parents increase, then calculated the reaction norm by varying growth rate and calculating an optimal age at maturity for each growth rate. The reaction norm for maturation should take one of at least four shapes that depend on specific relations between changes in growth rates and changes in adult mortality rates, juvenile mortality rates, or both. Most organisms should mature neither at a fixed size nor at a fixed age, but along an age-size trajectory. The model makes possible a clear distinction between the genetic and phenotypic components of variation. The evolved response to selection is reflected in the shape and position of the reaction norm. The phenotypic response of a single organism to rapid or slow growth is defined by the location of its maturation event as a point on the reaction norm. A quantitative test with data from 19 populations and species of fish showed that predictions were in good agreement with observations (r = 0.93, P < 0.0001). The predictions of the model also agreed qualitatively with observed phenotypic variation in age and size at maturity in humans, platyfish, fruit flies, and red deer. This preliminary success suggests that experiments designed to test the predictions directly will be worthwhile.

Chromosomal and morphological abnormalities caused by oocyte ageing in Silurus glanis

Article

Full-text available

Mar 1998

The effects of aging oocytes for 6 hours before fertilization in the European catfish Silurus glanis are compared with the same experiment under normal conditions (stripping and fertilization immediately after ovulation). Fertilization rate and hatching rate are lower in the aged groups, while the percentages of malformed larvae and chromosomal abnormalities are significantly higher. Several kinds of abnormalities are described in detail.

Pattern and variability in the breeding system of Atlantic salmon ( Salmo salar ), with comparisons to other salmonids

Article

Jan 1998
CAN J FISH AQUAT SCI

Ian Fleming

The breeding system of Atlantic salmon (Salmo salar) is shaped both by natural selection for offspring production and by sexual selection for access to mating opportunities. These evolutionary forces operate with differing intensities in the two sexes to shape their breeding behaviour and tactics. Female breeding success is largely dependent on egg production, access to breeding territories, and nest quality and survival. By contrast, male breeding success is largely determined by access to ovipositing females. As such, the breeding system of Atlantic salmon is similar to that of other members of the subfamily Salmoninae. However, early male maturity, a common pattern within the Salmoninae, reaches its greatest expression in both terms of frequency and magnitude of the mature male size difference in Atlantic salmon. Despite generalities, spawning populations of Atlantic salmon are not static, as they exhibit spatial and temporal variability in demography (e.g., spawner density, sex ratio, age at maturity, and body size). Events, both natural and anthropogenic (e.g., exploitation, habitat alteration, and climatic changes), affect this variability and ultimately shape the breeding system.

Early maturity in amago salmon (Oncorhynchus masu ishikawai): An association with energy storage

Article

Jan 1997
CAN J FISH AQUAT SCI

Two groups of amago salmon (Oncorhynchus masu ishikawai) with large differences in incidence of early maturity were reared in similar environments and periodically sampled beginning 1 week after exogenous feeding commenced in January and ending in June when maturing individuals could be distinguished. Mean weight of fish in the two groups did not differ beyond the first month of feeding; however, the early-maturing group had significantly greater variation in weight, significantly higher triacylglycerol content in the first sample taken, and maintained higher triacylglycerol content throughout the experiment. Thus, we describe fat storage differences in early-maturing salmon and in salmon that do not mature early, at a far younger age than has been reported previously. In addition, glycogen content and the activities of several enzymes involved in energy storage were examined. Seasonal trends in energy storage show an overall reduction in fat storage in both groups and some differences in glycogen storage dynamics between the groups in late spring. Our results support a previous hypothesis that a size or energy storage threshold must be surpassed for maturation to occur and furthermore suggest that the decision to mature could be made at a very early stage of development.

Evidence for Binding and Action of Growth Hormone in Trout Testis

Article

May 1992

Growth hormone (GH) binding to testis tissue and GH action on trout testicular cells were studied in vitro. Labeled salmon GH (sGH) was able to bind to a trout testis membrane preparation. Binding sites showed high affinity (Ka = 1–2 × 109M-1 ) and low capacity (11 fmol/g fresh tissue) for 125I-sGH. Salmon GH and bovine GH, but not salmon gonadotropin, could compete with 125I-sGH for site occupancy. The binding characteristics were similar to those of trout liver GH receptors that we previously described. Salmon GH (0.1 and 1 µg/rn1) and bovine GH (10 µg/ml) could modulate steroidogenesis in cultured testicular cells: 17α-hydroxy, 20β-dihydroprogesterone (17α20β0HP) accumulation in culture medium was stimulated by GH addition, and this effect increased with duration of culture and/or stimulation; 11-ketotestosterone accumulation tended to be inhibited in the presence of GH at the beginning of culture. These effects were dependent on GH concentration and were observed both in the absence and presence of gonadotropin. The amplitude of the sGH effect varied between experiments, probably according to the physiological state of the cells used. In vivo, GH and 17α20βOHP plasma levels increased at the beginning of spermiation (sperm production) and decreased at the end of spermiation. This relationship suggests that, at the end of the reproductive cycle, high GH levels are associated with the production of 17α20βOHP, a progestin necessary for efficient spawning in this species. We conclude that GH may play a role in testicular physiology, at least at certain stages of spermatogenesis.

Interactions of catecholamines and GnRH in regulation of gonadotropin secretion in teleost fish

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