Egg Quality in Fish - What Makes A Good Egg

Reviews in Fish Biology and Fisheries 7, 387416 (1997)
Egg quality in sh: what makes a good egg?

S U Z A N N E B RO O K S , C H A R L E S R . T Y L E R and JO H N P. SU M PT ER
Department of Biology and Biochemistry, Brunel University, Uxbridge, Middlesex UB8 3PH, United
Kingdom
Contents
Abstract
Introduction
The coordinated assembly of a sh egg
What is in an egg?
Hormones and egg quality
Egg size is bigger better?
Age of sh and egg quality
Environmental inuences on egg quality
Diet
Photoperiod and physiochemical properties of the water
Pollutants
Husbandry of captive sh
Genetic inuences on egg quality
Parental genes
Genetic markers for egg quality
Control of gene expression and egg quality
Acknowledgement
References
page 387
388
389
392
395
398
398
399
404
406
406
Abstract
Factors affecting egg quality are determined by the intrinsic properties of the egg itself
and the environment in which the egg is fertilized and subsequently incubated. Egg
quality in sh is very variable. Some of the factors affecting egg quality in sh are
known, but many (probably most) are unknown. Components that do affect egg quality
include the endocrine status of the female during the growth of the oocyte in the ovary,
the diet of the broodsh, the complement of nutrients deposited into the oocyte, and the
physiochemical conditions of the water in which the eggs are subsequently incubated. In
captive broodsh, the husbandry practices to which sh are subjected are probably a
major contributory factor affecting egg quality. Our knowledge of the genetic inuences
on egg quality is very limited indeed. We know that parental genes strongly inuence
both fecundity and egg quality, but almost nothing is known about gene expression
Author to whom correspondence should be addressed (e-mail: Suzanne.Brooks@brunel.ac.uk).

09603166 # 1997 Chapman & Hall
388
Brooks, Tyler and Sumpter
and=or mRNA translation in sh oocytes=embryos. This is surprising because the

products synthesized in ovo and the mechanisms controlling their expression are likely to
play a central role in determining egg quality. The genetic mechanisms underpinning
oocyte and embryo growth and development are a priority for research.
Introduction
Fish populations, both farmed and wild, are dependent upon the production of goodquality eggs. Poor egg quality is one of the major constraints in the expansion of
aquaculture of both marine and many freshwater sh species. In the sh farming industry,
good-quality eggs have been dened as those exhibiting low mortalities at fertilization,
eyeing, hatching and rst feeding (Bromage et al., 1992). Egg survival and hatching
rates, however, while being the ultimate measures of egg quality, tell us nothing about
what factors determine egg quality. Morphological features of larvae have been used as
indicators of gamete quality in some sh species (Kjorsvik, 1994). Other authors have
suggested that the appearance of the zona pellucida, the shape of the egg, its
transparency and distribution of oil globules can be related to quality (Kjorsvik et al.,
1990; Bromage et al., 1994). There is little agreement, however, regarding reliable
methods for `quality' assessment in eggs of marine sh. Hatcheries culturing marine
species often distinguish `good'-quality eggs from `poor'-quality eggs by virtue of the
eggs' ability to oat or sink in sea water, respectively (McEvoy, 1984; Carrillo et al.,
1989; Kjorsvik et al., 1990). However, the positive correlation between buoyancy and
`good' quality does not hold true for a number of marine species for example, in the
Atlantic halibut, Hippoglossus hippoglossus (Pleuronectidae). In this species, the only
reliable indicator of egg quality established so far is based on assessment of cell
symmetry at early stages of cleavage (Bromage et al., 1994).
Developmental biologists would consider that the quality of an egg is determined by
the intrinsic properties of the egg itself, by its genes, and by the maternal mRNA
transcripts and nutrients contained within the yolk, all of which are provided by the
mother. After fertilization, of course, the quality of the egg (or rather the embryo) will
also be determined by the contribution of the paternal genes. Both in aquaculture and in
the wild, the environment in which the eggs are incubated also affects the success of
the egg in producing a viable offspring. The conditions to which fertilized eggs are
exposed, therefore, also often become encompassed in the term ègg quality'.
Our knowledge of the processes affecting egg quality in both wild and captive sh is
extremely limited. In the few studies that have been carried out on wild sh, it has
been found that egg quality may show considerable variability from season to season
(Kjorsvik et al., 1990). Egg quality in many farmed sh, particularly marine species, is
the major difculty in their culture (Kjorsvik et al., 1990). For example, in European
sea bass (Dicentrarchus labrax, Percichthyidae) and gilthead seabream (Sparus auratus,
Sparidae), hatching rates are often only 1015% of total eggs spawned (Carrillo et al.,
1989). In Atlantic halibut, a very important commercial species with a considerable
potential for aquaculture, hatching rates are often less than 1% (Norberg et al., 1991;
M. Bruce, pers. comm.). Some of the problems in egg quality in marine species are
probably a function of the difculties in providing optimum culture conditions for egg
incubation. Even for salmonids, however, where the incubation methods for fertilized
eggs are well established, there may be losses of 50% up to hatching (Bromage et al.,
Egg quality in sh
389
1992). In multiple spawning sh, there are also considerable variations in the quality of
eggs produced in different batches over a single spawning season, even when the
batches of eggs are maintained under apparently identical culture conditions (yellowtail
ounder, Pleuronectes ferrugineus, Pleuronectidae Manning and Crim, 1995; Atlantic
cod, Gadus morhua, Gadidae Kjesbu et al., 1996).
A great deal of anecdotal evidence exists concerning what are thought to be the
major determinants of egg quality in sh. There is widespread belief that the nutrient
materials sequestered by the oocyte, and their processing during growth and maturation
of the oocytes, are key factors affecting egg quality (Craik and Harvey, 1984; Kjorsvik
et al., 1990; Bromage et al., 1992). Diet has received the greatest attention with respect
to its effect on egg quality, and recent studies indicate that the major inuences on
quality are exerted by just a few of the many different dietary constituents (Washburn
et al., 1990; Watanabe et al., 1991a,b; Harel et al., 1994). The physiology of the
broodsh and their hormonal status, which in turn affects the incorporation of
compounds, including hormones, into eggs, are also likely to have some inuence on
the quality of the eggs (for example, stressing sh may have deleterious effects;
Campbell et al., 1994). Other important determinants of egg quality, which in captive
sheries may be a function of husbandry, include overripening (the process of ageing of
unfertilized eggs which have been retained in the body cavity after ovulation: Springate
et al., 1984; Kjorsvik et al., 1990) and bacterial colonization of the fertilized eggs
(Barker et al., 1989; Hansen and Olafsen, 1989). Genetic inuences on egg quality and
the possible roles of maternal RNAs have been the focus of studies on oocyte quality in
humans and agricultural animals for some years (Koenig and Stormshak, 1993; Navot et
al., 1994). In sh, however, only very recently have attempts been made to assess and
dene the genetic factors which may underlie and determine egg quality (Lam, 1994;
Nagahama, 1994). This paper reviews the inuences on egg quality of both
environmental and genetic factors and attempts to highlight future research needs.
The coordinated assembly of a sh egg
In teleost sh, an egg is the nal product of oocyte growth and development, a process
that can take a year or more (Tyler and Sumpter, 1996). Once ovulated, sh eggs take up
very little, if any, nutrients: only water, and chemicals in the water, are known to pass
into an ovulated egg (Holliday and Pattie Jones, 1967). Hence, all the contents of an egg,
genetic and nutritive, that will determine its quality, must be incorporated into an egg
when it is an oocyte within the ovary (Fig. 1). This situation is very different to that in
eutherian mammals, where the nutrients contained in an egg simply provide the materials
necessary to initiate embryonic development; once the embryo has implanted into the
uterine wall, all the nutrients needed for development by the embryo are provided by the
mother as and when they are required. The eggs of sh, and other oviparous (egg-laying)
animals, therefore, are considerably larger than in mammals; sh eggs measuring 1 mm
in diameter are more than 23 000 times larger, by volume, than a human egg, and the
eggs of a coelocanth (Latimeria chalumnae, Latimeriidae) are more than a million-fold
larger than a human egg. The developing oocyte autonomously makes most of the
components of the machinery for DNA and protein synthesis, as well as mRNAs needed
immediately after fertilization (Tata, 1986). However, specialized egg constituents such as
yolk proteins and egg coat substances are synthesized in the liver (Ng and Idler, 1983;
390
Fig. 1. A scheme showing the coordinated assembly of a sh egg.
Egg quality in sh
391
Hyllner et al., 1991, 1994; Oppen-Berntsen et al., 1991; Fig. 1). A knowledge of the
mechanisms underlying the processes of oocyte growth and development, and how these
processes are coordinated, is essential for understanding fully the factors affecting egg
quality and fertilization. Oocyte growth and development, and subsequently embryonic
development of the fertilized egg, however, are very complex processes and, despite its
importance, knowledge on the coordinated assembly of the developing egg is far from
complete.
In all teleosts, oocytes appear to undergo the same basic pattern of growth, regardless
of their reproductive strategy. The major developmental events occurring during oocyte
development can be broadly classied into six phases, according to the state of oocyte
growth; they are: oogenesis, primary oocyte growth, cortical alveolus stage,
vitellogenesis, maturation and ovulation (Nagahama, 1983; Selman et al., 1986, 1993;
Bromage and Cumaranatunga, 1988; Tyler, 1991; Tyler and Sumpter, 1996). The genetic
changes and ultrastructural events accompanying oocyte development in teleosts are
described in Nakamura and Nagahama (1993) and Selman et al. (1993). Briey, during
the early stages of oocyte development, DNA replication occurs (leptotene),
homologous chromosomes pair (zygotene) and these pairs shorten and thicken
(pachytene). The chromosomes then unpair into lampbrush congurations (diplotene),
just before the oocyte enters a long period of cytoplasmic growth. The cytoplasmic
growth of the oocyte is characterized by an enormous accumulation of yolk reserves
(vitellogenesis). Meiosis resumes via a hormonal signal, and this leads to oocyte
maturation. During this period, the nucleus, arrested in meiotic prophase, breaks down
and the chromosomes enter rst meiotic metaphase. The oocyte is then released from
the ovary into the body cavity and it becomes an egg ready for fertilization (Nagahama,
1995).
The production of a good-quality egg relies upon the correct progression through
each of these phases, and this coordinated assembly of an oocyte is controlled by an
interplay of endocrine and intra-ovarian factors (both paracrine and autocrine; Tyler and
Sumpter, 1996, Figure 1). The primary signal(s) triggering oocyte growth and
maturation are environmental and these are converted from electrical to chemical
signals in the hypothalamus (Tata, 1986). In sh, gonadotrophin-releasing hormone
(GnRH) is released by the hypothalamus in response to an external stimulus. The
GnRH activates the anterior pituitary to release gonadotrophins (GtH I and GtH II;
probably representing sh FSH and LH, respectively; Prat et al., 1996). GtH I acts on
granulosa and thecal cells, stimulating the synthesis of oestradiol-17 (Suzuki et al.,
1988), which in turn stimulates the production of yolk protein precursors and egg shell
proteins by the liver (Ng and Idler, 1983; Oppen-Berntsen et al., 1994, see below). GtH
I also effects uptake of vitellogenin (VTG) into trout oocytes (Tyler et al., 1991b).
Furthermore, GtH I may play a role in recruitment of primary oocytes into the maturing
pool of vitellogenic oocytes (Prat et al., 1996; our own unpublished observations). GtH
II functions later in oocyte development than GtH I, acting on the follicle cells, to
stimulate the synthesis of progesterones, which control the termination of oocyte growth
and ovulation of the egg (Suzuki et al., 1988). The biosynthetic activity of the
developing oocyte, in contrast to the regulation of the extra-ovarian tissues involved in
the genesis of an egg, is believed to be autonomous and not regulated by hormones or
any external signals (Tata, 1986). Very recently in mammals, the rst oocyte-specic
growth factor has been identied (growth differentiation factor 9; GDF-9) and this
392
growth factor plays a vital role in somatic cell function (Dong et al., 1996). It is likely
that specic growth factors exist for sh oocytes, but as yet none have been identied.
What is in an egg?
An egg needs all the necessary information to direct the development of a functional,
free-swimming embryo and all the `building blocks' to form the embryo; so, it needs all
the amino acids, lipids and carbohydrates that make up an embryo, together with calcium
(for bones), vitamins and metals for enzyme and other metabolic actions, and many other
things (Fig. 2). These specialized materials are derived from a number of maternal
sources and must be incorporated during the growth of the oocyte in the ovary. If an egg
does not contain a particular compound, or contains an inappropriate amount of a
compound, it will not be able to sustain development of a viable embryo. Hence to
understand egg quality, one needs to be able to understand what gets into oocytes, how it
gets there, and the role of the various constituents.
In vertebrates' eggs, a large variety of macromolecules stored in the mature egg are
synthesized within the developing oocyte itself (Tata, 1986; Fig. 2). Many of these
macromolecules constitute the machinery for post-fertilization cell division and protein
synthesis, i.e. ribosomes, DNA and RNA polymerases, histone proteins, transcription
and translation factors, etc. In Xenopus the embryo does not transcribe its ribosomal
genes until the late gastrula stage is reached (when the embryo has reached almost
10 000 cells; Tata, 1986), illustrating the need for large stores of maternal ribosomes in
oviparous eggs. A similar situation is likely to occur in sh. Another group of
macromolecules synthesized in situ during oogenesis are messenger RNAs, including
those coding for cytoskeletal and membrane proteins (Tata, 1986). In amphibians
(review: Wallace and Selman, 1990), it appears that most of the RNA in full-grown
oocytes is already present by the end of the primary growth phase (Anderson and
Smith, 1978). In sh, although there is little information available on RNA synthetic
activity, a period of intense RNA synthesis occurs during the initial stages of primary
oocyte growth (Wallace and Selman, 1990). There is some evidence in oviparous
animals to suggest that mRNA transcripts may pass from the maternal circulation into
the developing oocyte and thus inuence oocyte growth and development, and
subsequently, the development of the embryo (Amanai et al., 1994; Hales et al., 1994).
Endogenous production of proteins has been shown to occur in Xenopus oocytes, but
most of these proteins appear to undergo turnover. Most, if not all, of these proteins are
involved in general cell function (Wallace and Hollinger, 1979). Again, little is known
about endogenous production of proteins in sh oocytes=eggs.
Vitellogenesis is the principal event responsible for the enormous growth of oocytes
in many teleosts, and this is when most nutritive products are taken up and stored for
future use by the developing embryo. In salmonid sh, for example, vitellogenesis may
account for over 90% of the nal volume of an oocyte (Tyler, 1991; Tyler et al.,
1991a). In most sh studied, the `building blocks' for the subsequent embryo, including
the amino acids, energy (from phosphate bonds), lipid and calcium, are derived from
the plasma during vitellogenesis, most of them originating from the uptake of a large
complex molecule, called vitellogenin (VTG; Tyler, 1991; Specker and Sullivan, 1994).
VTG is synthesized by the liver in response to circulating oestradiol-17 from the ovary
(Ng and Idler, 1983) and selectively sequestered by receptor-mediated endocytosis
Egg quality in sh
393
Fig. 2. Uptake of materials into a developing oocyte and their subsequent mobilization for use in forming the developing embryo.
394
(Chan et al., 1991; Le Menn and Nunez-Rodriguez, 1991; Tyler and Lancaster, 1993).
Multigene families for VTG have been shown to exist in a number of oviparous
vertebrates (Wang et al., 1983; Wahli and Ryf, 1985). To date, only one VTG mRNA
has been isolated from any sh (Chen, 1983; LaFleur et al., 1995). There are reports,
however, in the zebra sh (Brachydanio rerio, Cyprinidae; Selman et al., 1993) and in
the blue tiliapia (Tilapia aurea, Oreochromis aureus, Cichlidae; Ding et al., 1989) that
more than one type of VTG molecule may exist. These `different' forms of VTG may
arise from different genes, or differential splicing of the mRNA transcript. Alternatively,
they may arise as a result of different post-translation modications of the same VTG
molecule. The functional signicance to the subsequent egg of these different forms of
VTG is not known. An array of other plasma lipoproteins distinct from VTG are
present in the circulation during vitellogenesis (Babin, 1987), but most studies indicate
that they are not sequestered in signicant amounts by the growing oocyte (Tyler and
Sumpter, 1996).
The major yolk proteins in sh oocytes are lipoproteins, called lipovitellins, and
phosphoproteins, which include phosvitins and phosvettes (reviews: Wallace, 1985;
Specker and Sullivan, 1994). The number, types and forms of yolk proteins isolated
may differ between different species of teleosts, but all seem to be derived from VTG
(Specker and Sullivan, 1994). Materials present in an oocyte which are required for the
developing embryo must be positioned correctly within the oocyte and protected from
turnover and degradation until they are required. Yolk proteins are stored either in a
crystalline platelet form (zebra sh, Selman et al., 1993), or, as is more common, in
uid-lled yolk spheres or globules (Wallace and Selman, 1981). Lipids, in addition to
those derived from VTG, may be deposited from the circulation into the developing
oocyte and in turn provide a nutrient source for the subsequent embryo. A
comprehensive review on the composition, accumulation and utilization of yolk lipids
in teleosts has recently been published (Wiegand, 1996a) and so the topic is not
discussed here.
Although yolk proteins and lipids constitute the bulk of material in sh eggs, there
are other molecules that must be derived from sources outside of the oocyte, such as
vitamins and metals that, although present in far lower quantities, are equally necessary
for producing a viable egg and, subsequently, a viable offspring (Fig. 2). For example,
some vitamins and metals are required for enzyme activities, including hatching (Brown
and Lynam, 1981). Binding proteins and induction factors for embryonic development
also cross the oocyte membrane to support the development of the subsequent embryo
(Uchiyama et al., 1994). Embryogenesis is inuenced by a variety of hormones and
growth factors, and by RNAs deposited into the yolk which encode for hormones
growth factors and receptors. Vitamins, metals, binding proteins and hormones may
enter the oocyte adventitiously in the uid phase during receptor-mediated uptake of
VTG, others attach to VTG, or alternatively, they may enter quite specically, bound to
distinct, specic receptors. In Xenopus, VTG has been shown to function as a carrier
protein for maternal factors involved in early development; activin, a candidate for
mesodermal induction factor (Smith et al., 1990) and follistatin, an activin-binding
protein (Nakamura et al., 1990), preferentially bind to VTG in the plasma and both of
these proteins localize in yolk platelets (Uchiyama et al., 1994). In the chicken, both
vitamin A and thyroid hormones (triiodothyronine and thyroxine) are transported into
oocytes, attached to a transport protein called transthyretin, which has its own specic
Egg quality in sh
395
receptor (Vieira et al., 1995). In sh, thyroid hormones attach to VTG in the blood and
in turn are transported into the oocyte in this way (Babin, 1992; Cyr and Eales, 1992).
Overall, however, very little is known in sh about the transport systems and the
regulatory systems effecting uptake of hormones, vitamins and metals into the growing
oocyte, despite the fact that they are likely to play key roles in determining egg quality.
Enzymes are present in the oocyte which catalyse a series of metabolic processes
vital for the production of a viable offspring (Fig. 2). They include enzymes like the
cathepsins that degrade VTG into yolk proteins for storage in the oocyte and, postfertilization, which mediate the degradation of the stored yolk proteins into free amino
acids for use by the developing embryo (Sire et al., 1994). Very little is known about
the content of enzymes in sh oocyte=eggs, even though these enzymes will play a
central role in modifying free amino acids, fatty acids, etc. prior to their incorporation
into newly synthesized proteins and lipids in the developing embryo.
During ovarian growth, the oocyte becomes surrounded by an acellular envelope called
the vitelline envelope (Brummett et al., 1982). The proteins forming the vitelline envelope,
which are produced by the liver in response to oestrogen (Oppen-Berntsen et al., 1992a,b,
1994), play important functions during fertilization and embryo development; when
hardened after fertilization (Yamagami, 1992), the vitelline envelope protects the
developing embryo against mechanical damage, desiccation and rapid chemical changes
in the environment, and it also exerts bactericidal and fungicidal activity (Kudo, 1992).
Hormones and egg quality
Hormones play a role in larval development and thus may affect egg quality. Hormones
could be supplied to the egg before fertilization, in which case they must enter by
maternal transfer, or they could be synthesized in situ at any time after fertilization
(Fig. 3). Studies looking at the ontogeny of the endocrine system (Leatherland and
Barrett, 1993; Naito et al., 1993; Tanaka et al., 1995) have so far indicated that sh
larvae are physiologically immature, with little or no capacity to produce certain
enzymes, growth factors and hormones, until at or around the end of yolk resorption.
Thus, sh larvae appear to be dependent on exogenous sources (mother and=or live food)
for the supply of these regulatory factors, rather than their in situ synthesis in the
egg=larvae (Lam, 1994). Indeed, hormones have been shown to pass into sh oocytes
from the maternal circulation (Greenblatt et al., 1989). This store of maternal hormones
may full the regulatory needs of sh larvae for growth, development, osmoregulation,
stress responses and other physiological functions prior to the functional development of
their own endocrine glands (Lam, 1994). Our knowledge on the hormonal content of
eggs prior to fertilization, however, is limited to a very few hormones, including the
thyroid hormones, thyroxine (Tagawa and Hirano, 1991) and triiodothyronine (Tagawa
and Hirano, 1987), cortisol (De Jesus et al., 1991: Hwang et al., 1992; ContrerasSanchez et al., 1995; Brooks et al., 1995) and several sex steroids (Rothbard et al., 1987;
Feist et al., 1990). A very limited number of studies (to date) have attempted to
manipulate the hormonal content of eggs and assess the subsequent effects (Brown et al.,
1988, 1989; Tagawa and Hirano, 1991; Ayson and Lam, 1993; Brooks et al., 1995) and
these are discussed below.
Thyroid hormones of maternal origin are deposited in egg yolk, and they may have
signicant effects on sh embryo development (Lam, 1994). Triiodothyronine is
396
Fig. 3. Environmental and genetic factors that affect egg quality. Factors in light blue (pollutants, fungi, bacteria) are always detrimental to egg
quality.
Egg quality in sh
397
maintained in eggs in chum salmon (Oncorhynchus keta, Salmonidae) until hatching,

and thereafter the amount in the egg gradually decreases, until completion of yolk
absorption (Tagawa and Hirano, 1987), whereas the amount of thyroxine remains more
or less constant throughout early development (Tagawa and Hirano, 1991). The onset of
endogenous thyroid hormone production usually occurs at or around the end of yolk sac
resorption. There is conicting evidence linking the thyroid hormones and egg quality.
Boosting thyroid hormone levels in sh eggs can enhance subsequent larval growth
(striped sea bass, Morone saxatilis, Centrarchidae Brown et al., 1988, 1989).
However a study by Tagawa and Hirano (1991), where eggs were made thyroid
hormone-decient by treating female medaka (Oryzias latipes, Oryziidae), with thiourea
which caused a reduction in egg hormone levels to a tenth of egg levels from females
maintained under normal conditions showed that there were no differences in
hatchability, time of hatching or survival under starvation compared to eggs from
control sh. Furthermore, there were no apparent differences between the two groups of
eggs after hatching, in the body weight, body length, condition factor and survival rate
of the subsequent offspring (Tagawa and Hirano, 1991).
Cortisol is readily accumulated in growing sh oocytes and signicant amounts occur
in fertilized eggs, embryos and larvae (De Jesus et al., 1991; Hwang et al., 1992;
Contreras-Sanchez et al., 1995). The cortisol content of eggs, however, appears to
decline rapidly between fertilization and hatching. Studies on the rainbow trout
(Oncorhynchus mykiss, Salmonidae) indicate that at ovulation, as much as 90% of the
cortisol contained within the egg may be eliminated during `water hardening' (Brooks
et al., 1995). Exposure of adult and juvenile sh to high concentrations of cortisol has
deleterious effects (Carragher et al., 1989; Contreras-Sanchez et al., 1995); however, it
is not known what the signicance of cortisol in eggs is, nor whether it affects egg
quality. Studies on sh larvae indicate that cortisol may enhance the stimulatory action
of thyroid hormones (de Jesus et al., 1990), promote larval survival (in sea bass,
Sampathkumar et al., 1993) and (in Mozambique tilapia, Tilapia mossambica,
Cichlidae), stimulate larval growth (Lam, 1994).
Several sex steroids have been reported to be present in fertilized eggs of tilapia
(Rothbard et al., 1987) as well as in eggs of salmonids (Feist et al., 1990). The
functional signicance of these hormones is unclear. If maternal transfer of testosterone
to the oocytes is enhanced, it leads to increased polyamine synthesis, and therefore,
increased protein synthesis during embryonic development (Srivastava and Brown,
1993). The egg content of sex steroids shows a rapid decline from fertilization to
hatching (Feist et al., 1990), in a similar manner to that for cortisol, described above
(Brooks et al., 1995). In birds, yolks of eggs may contain signicant amounts of
oestradiol-17, concentrations comparable to those in the maternal circulation (AdkinsRegan et al., 1995). Such maternal transport of a sex steroid to the egg yolk constitutes
a potentially signicant source of maternal inuence over embryonic development and
adult phenotype in oviparous species.
In mammals, tonically elevated levels of serum luteinizing hormone (LH) have been
suggested to affect oocyte quality and the development potential of the early embryo
(Regan et al., 1990). Studies on humans have also demonstrated a decrease in oocyte
quality following ovarian stimulation with clomiphene citrate and human menopausal
gonadotrophin (Fluker et al., 1993). Attempts to control the ovarian cycle with
hormones in sh have met with mixed success. Induction of ovulation and spawning in
398
sea bream (S. auratus) with human chorionic gonadotrophin (hCG) resulted in eggs of
poor quality (Gordin and Zohar, 1978). However, administration of GnRHa via
controlled-release delivery systems, which stimulated long-term elevations of plasma
GtH II, have been successfully used to induce ovulation of captive white bass (Morone
chrysops, Percichthyidae; Mylonas et al., 1996) and striped bass (Morone saxatilis;
Hodson and Sullivan, 1993; Woods and Sullivan, 1993) without apparent detrimental
affects on survival to hatching. Indeed, there have been numerous studies on articial
induction of spawning and its effects on egg quality in commercially important species.
However, because of the very different hormone dosing regimes, the timing of the
hormone injections=implantations and the subsequent variability in the egg quality
(survival to hatching), interpreting the data is very difcult.
Egg size is bigger better?
In aquaculture, historically there has been the perception that, in terms of quality, bigger
eggs are better. Egg size may vary both within a species and between populations of the
same species (within the limits set by their genes: Beacham, 1982; Beacham and Murray,
1985, 1987; West and Mason, 1987). Variations in egg weight between populations of coho
salmon (Oncorhynchus kisutch, Salmonidae), for instance, of comparable weights and age,
may be up to 70%. Ecological explanations for differences in egg size of sh in different
populations include temporal and spatial changes in food particle size and in food
availability to larvae, and predation. Age at maturity may also affect egg size in sh (Sargent
et al., 1987), with a larger body size often resulting in the production of larger eggs
(Bagenal, 1969; L'Abee Lund and Hindar, 1990; DeMartini, 1991). Egg size in sh is also
affected=modulated by the nutritional status of the female during ovarian recrudescence
(Bromage et al., 1990; Tyler et al., 1994) and in asynchronous spawners, the size of eggs
ovulated in the later batches is often smaller, a phenomenon associated with the diminishing
resources of the female (Hsiao et al., 1994). In Atlantic cod, their spawning strategy
indicates that egg size takes priority over fecundity (Kjesbu et al., 1996). It has been
suggested that, in the wild, larger hatchlings that result from larger eggs, have a survival
advantage during the rst few days of their lives, as they have larger yolk reserves (Blaxter
and Hempel, 1963), may have higher growth rates (Moodie et al., 1989), are able to avoid
predators more effectively (Miller et al., 1988; Hinckley, 1990; Wootton, 1994), and eat a
wider variety of food items (Hunter, 1981; Webb and Weihs, 1986). Other authors, however,
indicate that this is not necessarily so, arguing that larger offspring would be more
noticeable as prey (Kjesbu et al., 1996). Furthermore, as larger eggs often take longer to
hatch than smaller eggs, they are at risk from predation or adverse abiotic conditions for
longer periods of time; the smaller eggs hatch earlier and the mobile larvae may then avoid
adverse conditions (Miller et al., 1988). In cultured rainbow trout, egg size does not appear
to be an important indicator of egg quality (Bromage et al., 1992; Brooks et al., unpublished
data). Bromage et al. (1992) showed that larger eggs did produce larger fry, but this size
advantage was soon masked by other environmental determinants of growth.
Age of sh and egg quality
Studies on mammals have shown that reproductive age can affect egg quality (Koenig
and Stormshak, 1993; Navot et al., 1994). For example, in pigs, the incidence of embryo
Egg quality in sh
399
mortality in pubertal gilts (experiencing the rst oestrous cycle) is greater than that of
gilts mated after one or more oestrous cycles (Young and King, 1981; Archibong et al.,
1992). Cytogenetic evaluation of ova from pubertal and third-oestrus gilts revealed that
gilts at rst oestrus ovulated a greater proportion of immature ova than gilts at third
oestrus. In addition, the estimated frequency of meiotic nondisjunction was greater for
gilts at rst oestrus than at third oestrus (Koenig and Stormshak, 1993). In older humans,
the reverse is seen; there is a 50% decrease in human female fecundity from age 25 to
35, which appears to be linked to a deterioration in oocyte quality (Navot et al., 1994).
Studies of this nature in sh have not been reported, but our recent work in the rainbow
trout has indicated that over their rst two spawning seasons, females produce betterquality eggs in the second season (Brooks et al., unpublished data). Similarly, Bromage
and Cumaranatunga (1988) found that the survival to eyeing of eggs from female
rainbow trout ovulating for the second time (as 3-year-olds) was signicantly higher
compared with eggs from females spawning for the rst time (as 2-year-olds; 75% versus
58% survival, respectively). A general improvement in egg quality, quantied as survival
to hatching, in successive spawning seasons has also been observed in European sea bass
(D. labrax; Navas et al., 1995).
Environmental inuences on egg quality
Comparisons of wild and captive sheries show, consistently, that egg quality is higher in
wild sh compared with that in captive stocks. As an example, studies on wild and
captive Atlantic salmon (Salmo salar, Salmonidae) have shown that eggs from wild
salmon have up to 25% higher fertilization and hatching success, which is associated
with greater size and survival of embryos and alevins, compared with their captive
counterparts (Srivastava and Brown, 1991). The superior quality of wild eggs over
farmed eggs is believed to be largely a function of environmental inuences.
Environmental factors that may affect egg quality in sh include the diet of the
broodsh and the physiochemical conditions of the water in which the eggs are incubated
(temperature, salinity and pH of the water, etc.). In aquaculture, the photoperiod to which
the broodsh have been exposed and the quality of the husbandry factors such as the
level of stress to which the broodstock are exposed, the fertilization procedures adopted,
overripening of eggs in the body cavity and bacterial colonization of fertilized eggs
can all affect egg quality (Fig. 3). In both wild and captive sheries, exposure of
maturing females, or exposure of the eggs or developing embryos to envrionmental
pollutants may affect egg and fry survival (Smith and Cole, 1973; Mauck et al., 1978;
Westin et al., 1985; van Leeuwen et al., 1986; Von Westernhagen et al., 1989; Matsui et
al., 1992; Miller, 1993). More subtle features of the environment may also affect
spawning. For example, in the ayu (Plecoglossus altivelis, Plecoglossidae), sensitivity to
hormone signals is affected by the physical features of the spawning environment
(Soyano et al., 1993). The known inuences of these environmental factors on egg
quality are discussed in more detail below.
DIET
Difference in egg quality as a consequence of diet, especially the diet's lipid content, is
one of the most researched aspects concerning egg quality and viability. Dietary
components as diverse as polar and non-polar lipids (Watanabe et al., 1991a,b), fatty
400
acids (Harel et al., 1994; Carrillo et al., 1995), protein (Washburn et al., 1990; Harel et
al., 1995) and ascorbic acid (Dabrowski and Blom, 1994; Blom and Dabrowski, 1995)
have all been shown to affect egg and embryo survival.
Egg quality was found to be improved in the European sea bass by altering the lipid
composition of broodstock diet (Carrillo et al., 1995). Eggs considered to be of better
quality had a higher content of total n3 fatty acids, which included enhanced levels of
both decosahexaenoic acid and eicosapentaenoic acid. In gilthead seabream, broodstock
fed on a diet decient in n3 highly unsaturated fatty acids for a period of 10 days
shortly before spawning, produced eggs with a reduced viability. Further, it was shown
that the levels of n3 highly unsaturated fatty acids supplied in the diet were directly
correlated with levels in both the polar and neutral fractions of egg lipid (Harel et al.,
1994). In contrast to these studies, an analysis of the lipid and fatty acid composition of
Atlantic halibut eggs showed that batches of eggs with widely differing viabilities had
very similar lipid compositions (Bruce et al., 1993).
Dietary proteins and carbohydrate also appear to inuence egg quality (Washburn et
al., 1990; Harel et al., 1994, 1995), although these components have received less study
than the lipids. In sh, although carbohydrates are relatively poorly utilized, and the
main sources of energy are protein and lipid (Walton and Cowey, 1982), in rainbow
trout, broodstock fed on a diet low in carbohydrate had a reduced relative fecundity
(they produced fewer eggs per kg body weight), and the eggs had a reduced survival to
the eyeing stage and a reduced hatchability (Washburn et al., 1990). Proteins act as a
source of amino acids and as a reservoir of materials used during the many biosynthetic
activities that are essential for the early stages of embryogenesis (Metcoff, 1986).
Successful embryonic development in sh has been shown to be dependent on the
balance of amino acids present in the egg (Fyhn and Serigstad, 1987; Fyhn, 1989).
Most studies on diet and egg quality in sh have focused on the bulk dietary
components; that is, the proteins, fats and carbohydrates. There have been few studies
on the `minor' dietary constituents. Some of the trace elements and vitamins have been
linked with egg quality (Takeuchi et al., 1981; Hardy, 1983; Sandnes et al., 1984), but
there have been very few comprehensive studies on their importance. The most detailed
studies on trace dietary components have been conducted on ascorbic acid deposition in
rainbow trout eggs (Dabrowski and Blom, 1994; Blom and Dabrowski, 1995). These
authors have shown that vitamin C is an essential nutrient, and that a deciency of this
vitamin in the diet results in eggs that show considerably higher mortalities than eggs
from females fed on diets enriched with vitamin C. Watanabe et al. (1991a,b)
demonstrated that red seabream (Pagrus major, Sparidae), which were fed on
commercial sh diets supplemented with phosphatidyl choline, astaxanthins and
vitamin E shortly before spawning, produced eggs that had signicantly improved
viability and hatching rates. From these studies, the authors concluded that the principal
factors aiding red seabream reproduction were free radical scavengers, such as the
supplement they added to their diet.
There is little doubt that broodstock sh fed on `natural diets' often produce eggs of
better quality than those on formulated commercial diets, and sometimes these
differences are considerable. For example, studies in the gilthead seabream have shown
the sh fed on squid (which contains a very similar essential amino acid composition to
the main proteins in sea bream eggs) produced three times more viable eggs than sh
fed on a commercial, wheat-gluten-based diet (Harel et al., 1994). Unfortunately it is
Egg quality in sh
401
not clear if egg quality was improved because of the amino acid composition of the
diet or because of the other dietary constituents. Despite the considerable efforts that
have been directed towards unravelling the importance of dietary components in
determining egg quality, the evidence that diet can directly affect egg quality is very
limited; the different methods used to evaluate egg quality, and the different timings of
the provision of the diets in the life of the sh, make it difcult to isolate any real
improvements that are a function of diet alone.
In formulating commercial diets, it would be benecial to look more closely at the
natural diet of the species in question, and what nutrients are contained within the eggs
of that species. In the very few studies that have been carried out using this approach,
there appear to be differences, sometimes substantial ones, in the nutrient composition
of eggs from different sh species. As an example, if we consider lipid in eggs, some
sh eggs appear to be totally devoid of lipid droplets (Wallace and Selman, 1981),
whereas in others, such as the gourami (Trichogaster cosby, Belontiidae), over one third
of the weight of an oocyte may be wax ester (Kaitaranta and Ackman, 1981).
Substantial differences in the patterns of utilization of the various lipid class by
embryos and larvae have also been observed in different sh species (Ronnestad et al.,
1994; Wiegand, 1996b). In summary, it appears that different sh species may have
different dietary requirements and that diets for broodstocks should be tailor-made to
ensure good egg quality. To assess the roles of the various dietary constituents on egg
quality, however, requires experiments with large numbers of sh, extensive tank and
hatchery facilities, and the studies are both labour and time intensive; there are very
few research establishments that have these facilities.
P H OTO P E R I O D A N D P H Y S I O C H E M I C A L P RO P E RT I E S O F T H E WAT E R
It has been suggested that environmental factors such as photoperiod, temperature,

salinity and pH of the water inuence egg quality (Carrillo et al., 1989; Bromage et al.,
1992; Gillet, 1994; Brown et al., 1995). Photoperiod manipulation is commonly used in
aquaculture as a method for advancing or delaying spawning, to obtain a year-round
supply of eggs of salmonids and other sh species. Delaying spawning of pink salmon
(Oncorhynchus gorbuscha, Salmonidae) by light manipulation led to increased egg
mortality by the eyed stage from 5% (in the controls) to between 60% and 80%
(Dabrowski and Blom, 1994). In contrast, Pohl-Branscheid and Holtz (1990) found only
minor differences in egg quality estimated as percentage survival at the eyed stage in
female rainbow trout exposed to an articially compressed light regime that induced four
spawnings in 2 years; under a natural photoperiod, rainbow trout spawn once a year.
Gillet (1994) found that delaying ovulation in the Arctic charr (Salvelinus alpinus,
Salmonidae), by changing the photoperiod regime, improved egg quality. However, this
was probably because the delay in ovulation meant that the eggs were ovulated when the
water was 2 8C colder than normal, which reduced over-ripening of the eggs. The effect
of manipulating the rate of development of the ovary on the subsequent fertility and egg
quality in non-salmonid species is also controversial (Girin and Devauchelle, 1978;
Devauchelle, 1987; Carrillo et al., 1989; Gillet, 1994). Photoperiodic advancement of
ovarian development in sea bass has resulted in slightly poorer egg survival in some
studies (Girin and Devauchelle, 1978; Devauchelle, 1987), but not in others (Carrillo et
al., 1989). In summary, to what extent egg quality is affected by manipulating
402
photoperiod is not clear, but it may depend at what time of the year the advance=delay in
spawning occurs.
Water temperatures during spawning and the incubation of the eggs are particularly
important in affecting egg quality. Temperature may affect metabolism, activity and
structure of the developing embryo (Kinne and Kinne, 1961). Brown et al. (1995)
examined the effect of sea temperature on the spawning performance of Atlantic halibut
over two spawning seasons, both in terms of egg morphology and viability of the
subsequent embryos. The viability of eggs from females kept at a constant temperature
of 6 8C was consistently higher than those from females maintained under ambient,
uctating temperatures (Brown et al., 1995). In the wild, Atlantic halibut inhabit deep
waters that are characterized by fairly constant physical environmental conditions,
including low, relatively stable temperatures (Haug, 1990). Similarly, in the Arctic charr,
the viability of eggs from captive-reared females held under ambient temperatures was
lower than that of wild-caught females. However, when the water in which the female
charr were held was cooled to 5 8C where the sh spawn in the wild in Lake Geneva,
the temperature does not exceed 6 8C the viability of eggs produced by captive-reared
females did not differ from that of eggs from wild females (Gillet, 1994). The
temperature at which the eggs are incubated can affect not only their quality, but also
their growth rate and differentiation. Studies on salmonids have shown that both
vertebrae number and gill raker number have both a genetic and an environmental
component, the environmental component being the temperature at which the eggs are
incubated (Kubo, 1950; Kwain, 1975; Beacham and Murray, 1986). Thus, transfer of
developing embryos to different temperature regimes can inuence the number of
meristic elements formed (Ali and Lindsey, 1974; Fahy, 1976, 1983). In salmonids, the
temperature at which eggs are incubated has a signicant impact on survival and time
of hatching; excessively high or low incubation temperatures can induce substantial
embryo mortality during early development stages. Different stages of embryo
development exhibit different thermal stabilities (Kinne and Kinne, 1961). In most
species of sh studied, it appears that there is a period of low thermal stability during
early development (fertilization to gastrulation), followed by a phase of somewhat
increased stability and later, towards the end of embryonic development (heavypigmented-eye stage), there is a period of low stability again (Kinne and Kinne, 1961;
Bailey and Evans, 1971). The basis of this susceptibility to temperature changes is
unknown. It has been established, however, that profound changes in the pattern of gene
expression can be induced in cells and tissues by small temperature changes (Moreau et
al., 1991). These changes in gene expression are likely to affect development.
Salinity may also affect egg quality, and is capable of modifying the physiological
effects of temperature on embryo development in both marine and brackish-water sh
(Kinne and Kinne, 1961). For example, salinity affects the rate of embryo development
in plaice (Pleuronectes platessa, Pleuronectidae; Berghahn and Karakiri, 1990).
Hypertonicity can have major effects on embryo development and these changes may
result from altered gene expression (Burg and Garcia-Perez, 1992).
P O L L U TA N T S
Fish oocytes and eggs are particularly sensitive to environmental pollutants. As an

example, sh have a 100-fold greater sensitivity compared with mammals to induction of
specic mutations during oogenesis (Walker and Streisinger, 1983). There is considerable
Egg quality in sh
403
experimental evidence that the quality of sh eggs can be adversely affected by pollution.
Malformations and impaired development and viability may result from exposure to a
variety of environmental contaminants, including insecticides (van Leeuwen et al., 1986),
organochlorinated biphenyls (Smith and Cole, 1973) and polychlorinated biphenyls
(Mauck et al., 1978; Matsui et al., 1992). Exposure to these pollutants, and their
accumulation in the oocyte=egg, may occur when the oocytes are developing in the ovary
(Miller, 1993), or subsequently, when the eggs are released into the aquatic environment.
Gonads with high concentrations of chlorinated hydrocarbons yield eggs with lower
hatching success than less contaminated eggs (Westin et al., 1985; Von Westernhagen et
al., 1989). Some persistant environmental chemicals, for example chlorinated
hydrocarbons, polychlorinated biphenols, and some known endocrine disrupters (e.g.
DDT) are lipophilic and may be transported with lipid reserves into the developing
oocyte (Knickmeyer and Steinhart, 1989; Miller and Amrhein, 1995; Ungerer and
Thomas, 1995). Rates of mortality and deformities become particularly pronounced when
larvae from organochlorine-exposed females start to use their lipid reserves (Burdick et
al., 1964). Bioconcentration factors for PCBs from the water column into oocytes may be
up to 80 000 (Bruggeman et al., 1981). Studies on alligators, turtles and birds have
shown that exposure to oestrogenic xenobiotics (endocrine disruptors) during a specic
period of embryonic development can affect not only embryo survival but sexual
development too (Tyler et al., unpublished data). This is very likely to be the case from
embryonic development in sh also.
Reproduction in many commercial sheries takes place in waters that are
contaminated with pollution, for example, the coastal regions of the North Sea
(Cameron and Berg, 1992). It has been proposed that this pollution of surface waters is
a factor inuencing malformations and reduced viability in mackerel (Scomber
scombrus, Scombridae) eggs off the Atlantic Coast of the US (Longwell and Hughes,
1981; Longwell et al., 1992) and both cod and sprat (Sprattus sprattus, Clupeidae) eggs
in the Baltic (Grauman and Sukhorukova, 1982).
H U S BA N D RY O F C A P T I V E F I S H
There is little doubt that poor husbandry results in poor reproductive success of cultured
sh. It is surprising, therefore, that more attention has not been paid to the effects of
husbandry practices on egg quality. Key husbandry factors that are likely to have major
effects on egg quality are: to what extent the broodsh have been stressed, the
fertilization practices adopted, egg over-ripening, and bacterial colonization of eggs
(Bromage et al., 1992).
In captivity, connement and crowding of sh may affect egg quality. Both chronic
connement experienced during the nal stages of reproductive development, and
periods of acute stress, have been shown to disrupt the endocrinology underpinning
normal growth and development of the ovary in trout, and may result in signicantly
lower progeny survival rates (Campbell et al., 1994). Stress can lead to irregular
spawning intervals, low fertilization rates and increased occurrence of abnormal
embryos in Atlantic cod (Kjesbu, 1989; Wilson et al., 1995). How stressing broodsh
leads to deleterious effects on egg quality has not been established.
Some sh, when reared in captivity, do not usually oviposit (release) their eggs; the
eggs will then àge' or òver-ripen' within the body cavity. The time interval between
ovulation and fertilization will also affect the `ripeness' of the eggs. In rainbow trout,
404
there is approximately a one-week window for successful fertilization, in Atlantic

halibut the window is 4 to 6 hours, but in tilapia, over-ripening of eggs occurs very
quickly and the window for successful fertilization is only an hour or so post-ovulation
(Bromage et al., 1994). It is important, therefore, that broodsh are checked regularly
to ensure that they are stripped and the eggs are fertilized shortly after ovulation. For
both cultured sh species that release (oviposit) their eggs, and for wild sh, the time
to fertilization will depend upon the presence of a mature male. Over-ripening of eggs
is perhaps the most common reason for poor egg quality in captive broodsh.
After fertilization, dying or dead eggs become colonized with bacteria=fungus, and if
these eggs are not removed quickly from the incubation trays, viable eggs may also be
colonized. By incubating eggs in water of high quality, and by `picking' colonized eggs
at regular intervals, egg survival (and, therefore, overall egg quality) can be enhanced
considerably (Bromage et al., 1994).
Genetic inuences on egg quality
PA R E N TA L G E N E S
Fertility studies carried out both in humans and in domestic animals show that parental
genetics can strongly inuence fecundity and egg quality (Ezra et al., 1992; Almeida and
Bolton, 1993). Work on humans has shown that a major cause of poor egg quality and
infertility is that ova are either immature or have chromosomal abnormalities (Almeida
and Bolton, 1993). Another proportion of women produce oocytes which are not
immature and do not appear morphologically abnormal, yet are in some way defective,
perhaps because of defects in the zona pellucida or in the ooplasma (Ezra et al., 1992). A
number of studies in sh also indicate that maternal genetics the DNA provided by the
female may have signicant effects on egg quality (Reinitz et al., 1979; Brauhn and
Kincaid, 1982; Withler, 1987; Brooks et al., unpublished data). Preliminary data from
Brooks et al. (unpublished data) indicate that in a single population of rainbow trout,
females that produce better-quality eggs in their rst spawning season year, do so in the
subsequent season, suggesting that there are genetic inuences on egg quality. However,
genetic factors in sh that account for these differences have yet to be determined.
Studies on genetic inuences on egg quality need to take into account the `male
factor'; the complement of genes from the male will also affect embryo survival and
therefore, perceived ègg quality'. Designing experiments to separate the inuence on
egg quality of the paternal genetic component from the maternal genetic component,
however, is difcult. An experiment to examine the maternal genetic component would
require that all the females in the study were fertilized with a single pool of male milt
at the same point in time. In many sh species, however, in any one population,
females do not all ovulate at exactly the same time; as an example, in the rainbow
trout, two females within a population may ovulate 6 or even 8 weeks apart. Similarly,
separating the effects on egg quality of parental genetics and effects that are directly
attributable to the environment is also difcult. Some effects on egg quality that have
been ascribed to parental genetics may, in fact, be a function of environmental
inuences. For example, different sh farms may report considerable differences in egg
quality, and interpret this to mean that the basis for the variability was genetic
females on some farms produce better eggs than females on other farms. This may not
necessarily be so, however, and the reported variability in egg quality could, equally, be
Egg quality in sh
405
due to different husbandry practices on the different farms (i.e. an environmental

inuence). One possible experimental approach to assess the effects of parental genetics
alone on egg quality, removing variation as a function of the inuences of the
immediate environment, would be to place batches of fertilized eggs from the same
females on different sh farms. The crucial elements in the design of such an
experiment are that each farm must be supplied with eggs from the same females and
that the eggs supplied from individual females to the different farms be derived from
the same batch of eggs. The resulting variation in ègg quality' in eggs from an
individual female and the variation between the different females on the different farms
would make it possible to determine the genetic component of egg quality in that strain
of sh. As with studies on the inuence of diet on egg quality, however, studies of this
nature require large numbers of sh, extensive hatchery facilities and are labour
intensive.
G E N E T I C M A R K E R S F O R E G G Q UA L I T Y
Recently, it has been suggested that differences in the content of yolk proteins in sh
eggs may be used as a genetic `marker' for egg quality (sea bass; Carnevali et al.,
unpublished data). This may not hold for all sh species, however, as preliminary studies
on rainbow trout demonstrated that extracts of yolk from different eggs contained the
same major lipoprotein components, regardless of the subsequent survival of that batch
of eggs. Furthermore, although there were differences in the phosphoprotein composition
of yolk extracts between batches of eggs, they did not appear to relate to egg quality
(Brooks et al., unpublished data). Nevertheless, in Atlantic salmon alevins of different
parental origin, there do appear to be different pathways for processing yolk proteins and
these differences may be related to the proportion of the progeny surviving (Olin and Von
der Decken, 1990). These ndings have prompted work to look for markers of egg
quality associated with the processing of yolk protein. Cathepsin D is the key enzyme in
the formation of yolk proteins, proteolytically cleaving vitellogenin into its component
polypeptides and digesting the yolk proteins during the early stages of embryogenesis to
release free amino acids for the developing offspring (Retzek et al., 1992). Studies are
now underway in a number of teleosts, to isolate and sequence the cDNA for cathepsin
D, with a view to its use as a potential genetic marker for egg quality.
C O N T RO L O F G E N E E X P R E S S I O N A N D E G G Q UA L I T Y
RNA in oocytes may be derived from transcription of the oocyte's own genes or
synthesized by the mother during oogenesis and accumulated in the oocytes (reviews:
Davidson, 1986; Amanai et al., 1994; Hales et al., 1994). The `maternal' RNA supports
oocyte protein synthesis during oogenesis and controls early embryonic development,
until transcription of the embryonic RNA begins after fertilization (Kaani, 1973;
Davidson, 1986). There is very little information on gene transcription and=or translation
of mRNA in sh oocytes=embryos, despite the fact that the products synthesized and the
mechanisms controlling their expression are likely to play a central role in determining
egg quality. Indeed, the highest mortalities in sh embryos are often seen within several
weeks of hatching, at a time when many embryonic genes are being activated (Kimmel,
1989).
In many animals, their early development within the egg is a result of changes in the
pattern of protein synthesis via a change in the translational activity or stability of an
406
mRNA (Sheets et al., 1994). Translational control has been shown to be critical for a
variety of developmental processes, including axis formation in Drosophila (Driever
and Nusslein-Volhard, 1988; Tautz and Pfeie, 1989) and sex determination in
Caenorhabditis elegans (Ellis and Kimble, 1994). The actual mechanisms underlying
regulation of mRNAs encoding proteins involved in cell cycle regulation and
development are virtually unknown in any animal. Experiments by various researchers
(Gallie, 1991; Simon et al., 1992; Wickens, 1992; Sheets et al., 1994) have, however,
demonstrated that increases in poly(A) tail length can activate translation, whereas
removal of poly(A) can prevent it. There is also evidence that mRNA translation is
regulated by proteins associated with the maternal mRNA (Spirin, 1994). These
masking proteins bind to specic short sequence elements within the 39 untranslated
region of the gene, acting as translational inhibitors until the proteins are modied or
destroyed at the appropriate stage during development, leading to normal translation of
the previously dormant mRNA (Murray et al., 1992; Standart, 1992; Bouvet and
Wolffe, 1994).
Studies on gene transcription in sh oocytes have been initiated by Nagahama and
co-workers, through the study of maturation promotion factor (MPF: Yamashita et al.,
1992; Nagahama, 1994). MPF switches the developing oocyte from the rst meiotic
arrest into second meiotic division, and hence nal maturation. The activation of MPF
in sh oocytes has been shown to be induced by maturation-inducing hormone through
the de novo synthesis of protein initiators, which include cyclin B (Goetz, 1983; Maller,
1985; in sh, MPF is a complex of cyclin B with cdc 2 kinase, Hirai et al., 1992).
In summary, little is known about transcription of the genes in sh oocytes or the
mechanism of regulation and translation of mRNAs. Studies on the role of maternal
RNA during oogenesis and embryogenesis, and studies on how and when the messages
are masked and unmasked for their developmental expression in sh oocytes, eggs and
embryos, have yet to be a focus for research. It is likely that hundreds, possibly
thousands, of genes are transcribed and RNAs translated during embryo development.
Some will be vital to development, whereas others will be less crucial. Inappropriate
expression of these genes, either in strength or timing, will likely lead to problems
during embryogenesis, and hence to a `poor-quality egg'. Most, possibly all, of the
factors shown to affect egg quality will do so by inuencing gene expression and RNA
translation in the egg. Studies of this nature on sh oocytes=eggs, therefore, are likely
to be of an increasing concern in unravelling what makes a `good-quality' egg.
Acknowledgement
Dr S. Brooks was supported by a grant from the European Union (AIR 2 93 1005).
References
Adkins-Regan, E., Ottinger, M.A. and Park, J. (1995) Maternal transfer of estradiol to egg-yolks alters
sexual differentiation of avian offspring. Journal of Experimental Zoology 271, 466470.
Ali, M.Y. and Lindsey, C.C. (1974) Heritable and temperature induced meristic variation in the
medaka, Oryzias latipes. Can. J. Zool. 52, 959976.
Almeida, P.A. and Bolton, V.N. (1993) Immaturity and chromosomal abnormalities in oocytes that fail
to develop pronuclei following insemination in vitro. Human Reproduction 8, 229232.
Egg quality in sh
407
Amanai, K., Suzuki, Y. and Ohtaki, T. (1994) Involvement of a maternally transcribed lectin gene in
the early development of Bombyx mori. Rouxs Archives of Developmental Biology 203, 397401.
Anderson, D.M. and Smith, L.D. (1978) Patterns of synthesis and accumulation of heterogeneous RNA
in lampbrush stage oocytes of Xenopus laevis (Daudin). Dev. Biol. 67, 274285.
Archibong, A.E., Maurer, R.R., England, D.C. and Stormshak, F. (1992) Inuence of sexual maturity
of donor on in vivo survival of transferred porcine embryos. Biology of Reproduction 47,
10261030.
Ayson, F.G. and Lam, T.J. (1993) Thyroxine injection of female rabbitsh (Siganus guttatus)
broodstock changes in thyroid-hormone levels in plasma, eggs, and yolk-sac larvae, and its
effect on larval growth and survival. Aquaculture 109, 8393.
Babin, P.J. (1987) Apolipoproteins and the association of egg yolk proteins with plasma high density
lipoproteins after ovulation and follicular atresia in the rainbow trout (Salmo gairdneri). J. Biol.
Chem. 262, 42904296.
Babin, P.J. (1992) Binding of thyroxine and 3,5,39-triiodothyronine to trout plasma lipoproteins. Am. J.
Physiol. 262, E712E720.
Bagenal, T. (1996) The relationship between food supply and fecundity in brown trout Salmo trutta. J.
Fish Biol. 1, 167182.
Bailey, J.E. and Evans, D.R. (1971) The low-temperature threshold for pink salmon eggs in relation to
a proposed hydroelectric installation. Fishery Bulletin 69, 587593.
Barker, G.A., Smith, S.N. and Bromage, N.R. (1989) The bacterial ora of rainbow trout, Salmo
gairdneri Richardson and brown trout, Salmo trutta L. eggs and its relationship to developmental
success. Journal of Fish Diseases 12, 281293.
Beacham, T.D. (1982) Fecundity of coho salmon (Oncorhynchus kisutch) and chum salmon (O. keta)
in the northeast Pacic Ocean. Can. J. Zool. 60, 14631469.
Beacham, T.D. and Murray, C.B. (1985) Effect of female size, egg size and water temperature on
chum salmon (Oncorhynchus keta) from the Nitinat River, British Columbia. Can. J. Fish. Aquat.
Sci. 42, 17551765.
Beacham, T.D. and Murray, C.B. (1986) The effect of spawning time and incubation temperature on
meristic variation in chum salmon (Oncorhynchus keta). Can. J. Zool. 64, 4548.
Beacham, T.D. and Murray, C. (1987) Adaptive variation in body size, age, morphology, egg size, and
developmental biology of chum salmon (Oncorhynchus keta) in British Columbia. Can. J. Fish.
Aquat. Sci. 44, 244261.
Berghahn, R. and Karakiri, M. (1990) Experimental induction of biological tags in otoliths of 0-group
plaice Pleuronectes platessa by starvation, temperature, and UV-B radiation. Marine Ecology
Progress Series 67, 227233.
Blaxter, J.H.S. and Hempel, G. (1963) The inuence of egg size on herring larvae (Clupea harengus
L.). J. Cons. Perm. Int. Explor. Mer 28, 211240.
Blom, J.H. and Dabrowski, K. (1995) Reproductive success of female rainbow trout (Oncorhynchus
mykiss) in response to graded dietary ascrobyl monophosphate levels. Biology of Reproduction
52, 10731080.
Bouvet, P. and Wolffe, A.P. (1994) A role for transcription and FRGY2 in masking maternal mRNA
within Xenopus oocytes. Cell 77, 931941.
Brauhn, J. and Kincaid, H. (1982) Survival of growth and catachability of rainbow trout of four
strains. N. Am. J. Fish. Manage. 2, 110.
Bromage, N.R. and Cumaranatunga, R. (1988) Egg production in the rainbow trout. In Muir, J.F.
and Roberts, R., eds. Recent Advances in Aquaculture. London and Sydney: Croom Helm,
pp. 63138.
Bromage, N.R., Hardiman, P., Jones, J., Springate, J. and Bye, V. (1990) Fecundity, egg size and total
egg volume differences in 12 stocks of rainbow trout, Oncorhynchus mykiss. Aquaculture and
Fisheries Management 21, 269284.
Bromage, N.R., Jones, J., Randall, C., Thrush, M., Davies, B., Springate, J., Duston, J. and Barker, G.
408
(1992) Broodstock management, fecundity, egg quality and the timing of egg production in the
rainbow trout (Oncorhynchus mykiss). Aquaculture 100, 141166.
Bromage, N.R., Bruce, M., Basavaraja, N. and Rana, K. (1994) Egg quality determinants in nsh: the
role of overripening with special reference to the timing of stripping in the Atlantic halibut
Hippoglossus hippoglossus. Journal of the World Aquaculture Society 25, 1321.
Brooks, S., Pottinger, T.G., Tyler, C.R. and Sumpter, J. (1995) Does cortisol inuence egg quality in
the rainbow trout Oncorhynchus keta. In Goetz, F.W. and Thomas, P., eds. Proceedings of the
Fifth International Symposium on the Reproductive Physiology of Fish. Austin, Texas, USA: Fish
Symposium '95, Austin, p. 180.
Brown, C.L., Doroshov, S.I., Nunez, J.M., Hadley, C., Vaneenennaam, J., Nishioka, R.S. and Bern,
H.A. (1988) Maternal triiodothyronine injections cause increases in swimbladder ination and
survival rates in larval striped bass, Morone saxatilis. Journal of Experimental Zoology 248,
168176.
Brown, C.L., Doroshov, S.I., Cochran, M.D. and Bern, H.A. (1989) Enhanced survival in striped bass
ngerlings after maternal triiodothyronine treatment. Fish Physiology and Biochemistry 7,
295299.
Brown, D.J.A. and Lynam, S. (1981) The effect of sodium and calcium concentrations on the hatching
of eggs and the survival of the yolk-sac fry of brown trout, Salmo trutta L. at low pH. Journal of
Fish Biology 19, 205211.
Brown, N.P., Bromage, N.R. and Shields, R.J. (1995) The effect of spawning temperature on egg
viability in the Atlantic Halibut ( Hippoglossus hippoglossus). In Goetz, F.W. and Thomas, P., eds.
Proceedings of the Fifth International Symposium on the Reproductive Physiology of Fish. Austin,
Texas, USA: Fish Symposium '95, Austin, p. 181.
Bruce, M.P., Shields, R.J., Bell, M.V. and Bromage, N.R. (1993) Lipid class and fatty acid
composition of eggs of Atlantic halibut, Hippoglossus hippoglossus (L.), in relation to egg quality
in captive broodstock. Aquaculture and Fisheries Management 24, 417422.
Bruggeman, W.A., Martron, L., Kooiman, D. and Hutzinger, O. (1981) Accumulation and elimination
kinetics of dichlorobiphenyls, trichlorophenyls and tetrachlorobiphenyls by goldsh after dietary
and aqueous exposure. Chemosphere 10, 811832.
Brummett, A.R., Dumont, J.N. and Larkin, J.R. (1982) The ovary of Fundulus heteroclitus. Journal of
Morphology 173, 116.
Burdick, G., Harris E., Dean, H., Walker, T., Skea, J. and Colby, D. (1964) The accumulation of DDT
in lake trout and the effects on reproduction. Trans. Am. Fish. Soc. 93, 127136.
Burg, M.B. and Garcia-Perez, A. (1992) How tonicity regulates gene expression. Journal of the
American Society of Nephrology 3, 121127.
Cameron, P. and Berg, J. (1992) Morphological and chromosomal aberrations during embryonic
development in dab Limanda limanda. Marine EcologyProgress Series 91, 163169.
Campbell, P.M., Pottinger, T.G. and Sumpter, J.P. (1994) Preliminary evidence that chronic
connement stress reduces the quality of gametes produced by brown and rainbow trout.
Aquaculture 120, 151169.
Carragher, J.F., Sumpter, J.P., Pottinger, T.G. and Pickering, A.D. (1989) The deleterious effects of
cortisol implantation on reproductive function in 2 species of trout, Salmo trutta L. and Salmo
gairdneri Richardson. General and Comparative Endocrinology 76, 310321.
Carrillo, M., Bromage, N., Zanuy, S., Serrano, R. and Prat, F. (1989) The effect of modications in
photoperiod on spawning time, ovarian development and egg quality in the sea bass
(Dicentrarchus labrax L.). Aquaculture 81, 351365.
Carrillo, M., Zanuy, S., Prat, F., Cerda, J., Mananos, E., Bromage, N., Ramos, J. and Kah, O. (1995)
Nutritional and photoperiodic effects on hormonal cycles and quality of spawning in sea bass
(Dicentrarchus labrax L.). Netherlands Journal of Zoology 45, 204209.
Chan, S.L., Tan, C.H., Pang, M.K. and Lam, T.J. (1991) Vitellogenin purication and development of
assay for vitellogenin receptor in oocyte membranes of the tilapia (Oreochromis niloticus,
Egg quality in sh
409
Linnaeus 1766). Journal of Experimental Zoology 257, 96109.

Chen, T.T. (1983) Identication and characterisation of oestrogen-responsive gene products in the liver
of the rainbow trout. Can. J. Biochem. Cell Biol. 61, 802810.
Contreras-Sanchez, W., Schreck, C. and Fitzpatrick, M. (1995) Effect of stress on the reproductive
physiology of rainbow trout, Oncorhynchus mykiss. In Goetz, F.W. and Thomas, P., eds.
Texas, USA: Fish Symposium '95, Austin. p. 183.
Craik, J.C.A. and Harvey, S.M. (1984) Egg quality in rainbow trout. The relation between egg
viability, selected aspects of egg composition, and time of stripping. Aquaculture 40, 115134.
Cyr, D.G. and Eales, J.G. (1992) Effects of short-term 17-beta-estradiol treatment on the properties of
T4-binding proteins in the plasma of immature rainbow trout, Oncorhynchus mykiss. J. Exp. Zool.
262, 414419.
Dabrowski, K. and Blom, J.H. (1994) Ascorbic acid deposition in rainbow trout (Oncorhynchus
mykiss) eggs and survival of embryos. Comparative Biochemistry and Physiology 108A, 129135.
Davidson, E. (1986) Gene Activity in Early Development. Orlando, FL: Academic Press.
De Jesus, E.G., Inui, Y. and Hirano, T. (1990) Cortisol enhances the stimulating action of thyroid
hormones on dorsal n-ray resorption of ounder larvae in vitro. General and Comparative
Endocrinology 79, 167173.
De Jesus, E.G., Hirano, T. and Inui, Y. (1991) Changes in cortisol and thyroid hormone concentrations
during early development and metamorphosis in the Japanese ounder, Paralichthys olivaceus.
General and Comparative Endocrinology 82, 369376.
DeMartini, E.E. (1991) Annual variations in fecundity, egg size, and the gonadal and somatic
conditions of queensh Seriphus politus (Sciaenidae). Fishery Bulletin 89, 918.
Devauchelle, N. (1987) Four marine spawners in European hatcheries. In `Production Controlee en
Ecloserie. Synthase des papiers presentes dans le cadre du MEDRAP a Roviny-Zadar
(Yugoslavia)', pp. 50. Rapport FAO, Rome.
Ding, J.L., Hee, P.L. and Lam, T.J. (1989) Two forms of vitellogenin in the plasma and gonads of
male Oreochromis aureus. Comparative Biochemistry and Physiology 93B, 363370.
Dong, J., Albertini, D.F., Nishimori, K., Kumar, T.R., Lu, N. and Matzuk, M.M. (1996) Growth and
differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383, 531535.
Driever, W. and Nusslein-Volhard, C. (1988) A gradient of bicoid protein in drosophila embryos. Cell
54, 8393.
Ellis, R.E. and Kimble, J. (1994) Control of germ-cell differentiation in Caenorhabditis elegans. Ciba
Foundation Symposia 182, 179188.
Ezra, Y., Simon, A. and Laufer, N. (1992) Defective oocytes a new subgroup of unexplained
infertility. Fertility and Sterility 58, 2427.
Fahy, W.E. (1976) The morphological time of xation of the total number of vertebrate in Fundulus
majalis (Walbaum). J. Cons. Int. Explor. Mer 36, 243250.
Fahy, W.E. (1983) The morphological time of xation of the total number of caudal n rays in
Fundulus majalis (Walbaum). J. Cons. Perm. Int. Explor. Mer 41, 3745.
Feist, G., Schreck, C.B., Fitzpatrick, M.S. and Redding, J.M. (1990) Sex steroid proles of coho
salmon (Oncorhynchus kisutch) during early development and sexual differentiation. General and
Comparative Endocrinology 80, 299313.
Fluker, M.R., Sui, C.K., Gunby, J. and Daya, S. (1993) Cycle characteristics and outcome in relation
to ovarian response during in vitro fertilisation. Journal of Assisted Reproduction and Genetics
10, 504512.
Fyhn, H.J. (1989) First feeding of marine sh larvae are free amino-acids the source of energy.
Fyhn, H.J. and Serigstad, B. (1987) Free amino-acids as energy substrate in developing eggs and
larvae of the cod Gadus morhua. Marine Biology 96, 335341.
Gallie, D.R. (1991) The cap and poly(A) tail function synergistically to regulate messenger-RNA
410
translational efciency. Genes and Development 5, 21082116.

Gillet, C. (1994) Egg-production in arctic charr (Salvelinus alpinus L.) broodstock effects of
photoperiod on the timing of ovulation and egg quality. Canadian Journal of Zoology 72,
334338.
Girin, M. and Devauchelle, N. (1978) Decalage de la periode de reproduction par raccourcissement
des cycle photoperiodiques et thermiques chez poissons marins. Ann. Biol. Anim. Biochim.
Biophys. 18, 10591065.
Goetz, F.W. (1983) Hormonal control of oocyte nal maturation and ovulation in shes. Fish
Physiology 9, 117170.
Gordin, H. and Zohar, Y. (1978) Induced spawning of Sparus auratus (L.) by means of hormonal
treatments. Ann. Biol. Anim. Bioch. Biophys. 18, 985990.
Grauman, G. and Sukhorukova, L. (1982) On the emergence of sprat and cod abnormal embryos in
the open Baltic. International Council for the Exploration of the Sea. C.M. 1982=J:7, 8.
Greenblatt, M., Brown, C.L., Lee, M., Dauder, S. and Bern, H.A. (1989) Changes in thyroid-hormone
levels in eggs and larvae and in iodide uptake by eggs of coho and chinook salmon,
Oncorhynchus kisutsch and Oncorhynchus tschawystscha. Fish Physiology and Biochemistry 6,
261278.
Hales, K.H., Meredith, J.E. and Storti, R.V. (1994) Transcriptional and posttranscriptional regulation of
maternal and zygotic cytoskeletal tropomyosin messenger RNA during drosophila development
correlates with specic morphogenic events. Developmental Biology 165, 639653.
Hansen, G.H. and Olafsen, J.A. (1989) Bacterial colonization of cod (Gadus morhua L.) and halibut
( Hippoglossus hippoglossus) eggs in marine aquaculture. Applied and Environmental Microbiology 55, 14351446.
Hardy, R. (1983) Salmonid broodstock nutrition. In Iwamoto, R. and Sower, S., eds. Salmonid
Reproduction. Seattle: Washington Sea Grant Program, pp. 98108.
Harel, M., Tandler, A., Kissil, G.W. and Applebaum, S.W. (1994) The kinetics of nutrient
incorporation into body tissues of gilthead seabream (Sparus aurata) females and the subsequent
effects on egg composition and egg quality. British Journal of Nutrition 72, 4558.
Harel, M., Tandler, A., Kissil, G.W. and Applebaum, S.W. (1995) The role of broodstock dietary
protein in vitellogenin synthesis and oocyte development, and its effects on reproductive
performance and egg quality in gilthead sea bream Sparus aurata. In Goetz, F.W. and Thomas, P.,
eds. Proceedings of the Fifth International Symposium on the Reproductive Physiology of Fish.
Austin, Texas, USA: Fish Symposium '95, Austin, p. 105.
Haug, T. (1990) Biology of the Atlantic halibut, Hippoglossus hippoglossus (L., 1758). Advances in
Marine Biology 26, 170.
Hinckley, S. (1990) Variation of egg size of walleye pollack Theragra chalcogramma with a
preliminary examination of the effect of egg size on larval size. Fishery Bulletin 88, 471483.
Hirai, T., Yamashita, M., Yoshikuni, M., Lou, Y.H. and Nagahama, Y. (1992) Cyclin B in sh oocytes
its cDNA and amino-acid sequences, appearance during maturation, and induction of P34cdc2activation. Molecular Reproduction and Development 33, 131140.
Hodson, R.G. and Sullivan, C.V. (1993) Induced maturation and spawning of domestic and wild
striped bass, Morone saxatilis (Walbaum), broodstock with implanted GnRH analogue and
injected hCG. Aquaculture and Fisheries Management 24, 389398.
Holliday, F.G.T. and Pattie Jones, M. (1967) Some effects of salinity on the developing eggs and
larvae of the plaice (Pleuronectes platessa). J. Mar. Biol. Ass. U.K. 47, 3948.
Hsiao, S.M., Greeley, M.S. and Wallace, R.A. (1994) Reproductive cycling in female Fundulus
heteroclitus. Biological Bulletin 186, 271284.
Hunter, J.R. (1981) Feeding ecology and predation of marine sh larvae. In Lasker, R., ed. Marine
Fish Larvae. Seattle: Washington Sea Grant Program, pp. 3377.
Hwang, P.P., Wu, S.M., Lin, J.H. and Wu, L.S. (1992) Cortisol content of eggs and larvae of teleosts.
General and Comparative Endocrinology 86, 189196.
Egg quality in sh
411
Hyllner, S.J., Oppenberntsen, D.O., Helvik, J.V., Walther, B.T. and Haux, C. (1991) Estradiol-17-beta
induces the major vitelline envelope proteins in both sexes in teleosts. Journal of Endocrinology
131, 229236.
Hyllner, S.J., Silversand, C. and Haux, C. (1994) Formation of the vitelline envelope precedes the
active uptake of vitellogenin during oocyte development in the rainbow trout, Oncorhynchus
mykiss. Molecular Reproduction and Development 39, 166175.
Kaani, C. (1973) Genome transcription in sh development. Advances in Morphogenesis 8, 209284.
Kaitaranta, J.K. and Ackman, R.G. (1981) Total lipids and lipid classes of sh roe. Comparative
Biochemistry and Physiology 69B, 725729.
Kimmel, C.B. (1989) Genetics and early development of zebrash. Trends in Genetics 5, 283288.
Kinne, O. and Kinne, E.M. (1961) Rates of development in embryos of a cyprinodont sh exposed to
different temperaturesalinityoxygen combinations. Can. J. Zool. 40, 231253.
Kjesbu, O.S. (1989) The spawning activity of cod, Gadus morhua L. Journal of Fish Biology 34,
195206.
Kjesbu, O.S., Solemdal, P., Bratland, P. and Fonn, M. (1996) Variation in annual egg production in
individual captive atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic
Sciences 53, 610620.
Kjorsvik, E. (1994) Egg quality in wild and broodstock cod Gadus morhua L. Journal of the World
Aquaculture Society 25, 2231.
Kjorsvik, E., Mangorjensen, A. and Holmefjord, I. (1990) Egg quality in shes. Advances In Marine
Biology 26, 71113.
Knickmeyer, R. and Steinhart, H. (1989) On the distribution of polychlorinated biphenyl congeners
and hexachlorobenzene in different tissues of dab (Limanda limanda) from the North Sea.
Chemosphere 19, 13091320.
Koenig, J.L.F. and Stormshak, F. (1993) Cytogenetic evaluation of ova from pubertal and 3rd-estrous
gilts. Biology of Reproduction 49, 11581162.
Kubo, T. (1950) A preliminary report of the study on groups of Oncorhynchus keta (Walbaum) (dog
salmon) and the numbers of their segments. Bull. Fac. Fish. Hokkaido Univ. 1, 111.
Kudo, S. (1992) Enzymatic basis for protection of sh embryos by the fertilisation envelope.
Experientia 4B, 277281.
Kwain, W. (1975) Embryonic development, early growth, and meristic variation in rainbow trout
(Salmo gairdneri) exposed to combinations of light intensity and temperature. J. Fish. Res. Board
Can. 32, 397402.
L'Abee Lund, J.H. and Hindar, K. (1990) Interpopulation variation in reproductive traits of anadromous
female brown trout, Salmo trutta L. Journal of Fish Biology 37, 755763.
LaFleur, G.J., Byrne, B.M., Kanungo, J., Nelson, L.D., Greenberg, R.M. and Wallace, R.A. (1995)
Fundulus heteroclitus vitellogenin: the deduced primary structure of a piscine precursor to
noncrystalline, liquid-phase yolk protein. J. Mol. Evol. 41, 505521.
Lam, T.J. (1994) Hormones and egg=larval quality in sh. Journal of the World Aquaculture Society
25, 212.
Le Menn, F. and Nunez-Rodriguez, J. (1991) Receptors mediate endocytosis of VTG in sh follicles.
In Scott, A.P., Sumpter, J.P., Kime, D.E. and Rolfe, M.S., eds. Proceedings of the Fourth
International Symposium on the Reproductive Biology of Fish. Norwich, UK: Shefeld University
Press, pp. 300302.
Leatherland, J.F. and Barrett, S.B. (1993) Investigations into the development of the pituitary-gland
thyroid-tissue axis and distribution of tissue thyroid-hormone content in embryonic coho salmon
(Oncorhynchus kisutch) from Lake Ontario. Fish Physiology and Biochemistry 12, 149159.
van Leeuwen, C.J., Espeldoorn, A. and Mol, F. (1986) Aquatic toxicological aspects of
dithiocarbamates and related compounds. 3. Embryolarval studies with rainbow trout (Salmo
gairdneri). Aquatic Toxicology 9, 129145.
Longwell, A. and Hughes, J. (1981) Cytologic, cytogenetic and developmental state of Atlantic
412
mackerel eggs from sea surface waters of the New York Bight, and prospects for biological
effects monitoring with ichthyoplankton. Rapp. P.-v. Reun. Cons. int. Explor. Mer 179, 275291.
Longwell, A.C., Chang, S., Hebert, A., Hughes, J.B. and Perry, D. (1992) Pollution and developmental
abnormalities of Atlantic shes. Environmental Biology of Fishes 35, 121.
McEvoy, L.A. (1984) Ovulatory rhythms and over-ripening of eggs in cultivated turbot. Scophthalmus
maximus L. J. Fish Biol. 24, 237448.
Maller, J.L. (1985) Regulation of amphibian oocyte maturation. Cell Differentiation 16, 211221.
Manning, A.J. and Crim, L.W. (1995) Variability in egg quality and production in a batch spawning
ounder, Pleuronectes ferrugineus. In Goetz, F.W. and Thomas, P., eds. Proceedings of the Fifth
International Symposium on the Reproductive Physiology of Fish. Austin, Texas, USA: Fish
Symposium '95, Austin, p. 238.
Matsui, M., Hose, J.E., Garrahan, P. and Jordan, G.A. (1992) Developmental defects in sh embryos
from Salton Sea, California. Bulletin of Environmental Contamination and Toxicology 48,
914920.
Mauck, W.L., Hehrule, P.M. and Mayer, F.L. (1978) Effects of the polychlorinated biphenyl
ArochlorTM 1254 on growth, survival and bone development in brook trout (Salvelinus fontinalis).
J. Fish. Res. Board Can. 35, 10841088.
Metcoff, J. (1986) Intracellular amino acid levels as predictors of protein synthesis. Journal of the
American College of Nutrition 5, 107120.
Miller, M.A. (1993) Maternal transfer of organochlorine compounds in salmonines to their eggs.
Canadian Journal of Fisheries and Aquatic Sciences 50, 14051413.
Miller, M.A. and Amrhein, J.F. (1995) Maternal transfer of organochlorine compounds in Lake
Superior siscowet (Salvelinus namaycush siscowet) to their eggs. Bulletin of Environmental
Contamination and Toxicology 55, 96103.
Miller, T.J., Crowder, L.B., Rice, J.A. and Marschall, E.A. (1988) Larval size and recruitment
mechanisms in shes: toward a conceptual framework. Can J. Fish. Aquat. Sci. 45, 16571670.
Moodie, G.E.E., Loadman, N.L., Wiegand, M.D. and Mathias, J.A. (1989) Inuence of egg
characteristics on survival, growth and feeding in larval walleye (Stizotedion vitreum). Can. J.
Fish. Aquat. Sci. 46, 516521.
Moreau, N., Lautredou, N., Nda, E. and Angelier, N. (1991) Cold-stress response in the amphibian
oocyte changes in synthesis and nucleocytoplasmic distribution of some proteins. Biology of
the Cell 71, 97103.
Murray, M.T., Schiller, D.L. and Franke, W.W. (1992) Sequence-analysis of cytoplasmic messenger
RNA-binding proteins of xenopus oocytes identies a family of RNA-binding proteins.
Proceedings of the National Academy of Sciences of the United States of America 89, 1115.
Mylonas, C.C., Magnus, Y., Gissis, A., Klebanov, Y. and Zohar, Y. (1996) Application of controlledrelease, GnRHa-delivery systems in commercial production of white bass 3 striped bass hybrids
(sunshine bass), using captive broodstocks. Aquaculture 140, 265280.
Nagahama, N. (1994) Molecular biology of oocyte maturation in sh. In Davey, K.G., Peter, R.E. and
Tobe, S.S., eds. Perspectives in Comparative Endocrinology. Ottawa: National Research Council
of Canada, pp. 193198.
Nagahama, Y. (1983) The functional morphology of teleost gonads. In Hoar, W.S., Randall, D.J. and
Donaldson, E.M., eds. Fish Physiology, Vol. IXA. Reproduction. New York: Academic Press,
pp. 223275.
Nagahama, Y. (1995) Teleost oocyte maturation actuality and potentiality. Aquaculture 135, 7576.
Naito, N., Dejesus, E.G., Nakai, Y. and Hirano, T. (1993) Ontogeny of pituitary cell types and the
hypothalamo-hypophyseal relationship during early development of chum salmon, Oncorhynchus
keta. Cell and Tissue Research 272, 429437.
Nakamura, M. and Nagahama, Y. (1993) Ultrastructural study on the differentiation and development
of steroid-producing cells during ovarian differentiation in the amago salmon, Oncorhynchus
rhodurus. Aquaculture 112, 237251.
Egg quality in sh
413
Nakamura, T., Takio, K., Eto, Y., Shibai, H., Titani, K. and Sugino, H. (1990) Activin-binding protein
from rat ovary is follistatin. Science 247, 836838.
Navas, J., Thrush, M., Ramos, J., Bruce, M., Carrillo, M., Zanuy, S. and Bromage, N. (1995) The
effect of seasonal alteration in the lipid composition of broodstock diets on egg quality in the
European sea bass (Dicentrarchus labrax). In Goetz, F.W. and Thomas, P., eds. Proceedings of the
Fifth International Symposium on the Reproductive Physiology of Fish. Austin, Texas, USA: Fish
Symposium '95, Austin, pp. 108110.
Navot, D., Drews, M.R., Bergh, P.A., Guzman, I., Karstaedt, A., Scott, R.T., Garrisi, G.J. and
Hofmann, G.E. (1994) Age-related decline in female fertility is not due to diminished capacity of
the uterus to sustain embryo implantation. Fertility and Sterility 61, 97101.
Ng, T.B. and Idler, D.R. (1983) Yolk formation and differentiation in teleost shes. In Hoar, W.S.,
Randall, D.J. and Donaldson, E.M., eds. Fish Physiology, Vol. IXA. Reproduction. New York:
Academic Press, pp. 373404.
Norberg, B., Valkner, V., Huse, J., Karlsen, I. and Grung, G.L. (1991) Ovulatory rhythms and egg
viability in the Atlantic halibut ( Hippoglossus hippoglossus). Aquaculture 97, 365371.
Olin, T. and Vonderdecken, A. (1990) Yolk proteins in salmon (Salmo salar) oocytes, eyed eggs, and
alevins differing in viability. Canadian Journal of Zoology 68, 895900.
Oppen-Berntsen, D.O., Gram-Jensen, E. and Walther, B.T. (1991) Origin of teleostean eggshell Zrproteins and their signicance during oogenesis: in vitro liver synthesis of eggshell proteins
induced by oestradiol-17b. In Scott, A.P., Sumpter, J.P., Kime, D.E. and Rolfe, M.S., eds.
Proceedings of the Fourth International Symposium on the Reproductive Biology of Fish.
Norwich, UK: Shefeld University Press, pp. 306308.
Oppen-Berntsen, D.O., Gram-Jensen, E. and Walther, B.T. (1992a) Zona radiata proteins are
synthesized by rainbow trout (Oncorhynchus mykiss) hepatocytes in response to estradiol-17-beta.
Journal of Endocrinology 135, 293302.
Oppen-Berntsen, D.O., Hyllner, S.J., Haux, C., Helvik, J.V. and Walther, B.T. (1992b) Eggshell zonaradiata-proteins from cod (Gadus morhua) extraovarian origin and induction by estradiol-17beta. International Journal of Developmental Biology 36, 247254.
Oppen-Berntsen, D.O., Olsen, S.O., Rong, C.J., Taranger, G.L., Swanson, P. and Walther, B.T. (1994)
Plasma levels of eggshell zr-proteins, estradiol-17-beta, and gonadotropins during an annual
reproductive cycle of Atlantic salmon (Salmo salar). Journal of Experimental Zoology 268,
5970.
Pohl-Branscheid, M. and Holtz, W. (1990) Control of spawning activity in male and female rainbow
trout (Oncorhynchus mykiss) by repeated foreshortened seasonal light cycles. Aquaculture 86,
93104.
Prat, F., Sumpter, J.P. and Tyler, C.R. (1996) Validation of radioimmunoassays for 2 salmon gonadotropins
(Gth-I and Gth-II) and their plasma concentrations throughout the reproductive cycle in male and
female rainbow trout (Oncorhynchus mykiss). Biology of Reproduction 54, 13751382.
Regan, L., Owen, E.J. and Jacobs, H.S. (1990) Hypersecretion of luteinizing hormone, infertility, and
miscarriage. Lancet 336, 11411144.
Reinitz, G., Orme, L. and Hitzel, F. (1979) Variations in body composition and growth among strains
of rainbow trout. Trans. Am. Fish. Soc. 108, 204207.
Retzek, H., Steyrer, E., Sanders, E.J., Nimpf, J. and Schneider, W.J. (1992) Molecular cloning and
functional characterization of chicken cathepsin D, a key enzyme for yolk formation. DNA and
Cell Biology 11, 661672.
Ronnestad, I., Koven, W.M., Tandler, A., Harel, M. and Fyhn, H.J. (1994) Energy metabolism during
development of eggs and larvae of gilthead sea bream (Sparus aurata). Marine Biology 120,
187196.
Rothbard, S., Moav, B. and Yaron, Z. (1987) Changes in steroid concentrations during sexual
ontogenesis in tilapia. Aquaculture 61, 5974.
Sampathkumar, R., Munro, A.D., Lee, J. and Lam, T.J. (1993) Exogenous cortisol promotes survival of
414
Asian seabass (Lates calcarifer) hatchlings exposed to hypersalinity but not hyposalinity shock.
Sandnes, K., Ulgenes, Y., Braekkan, O.R. and Utne, F. (1984) The effect of ascorbic acid
supplementation in brood-stock feed on reproduction of rainbow trout (Salmo gairdneri).
Sargent, R.C., Taylor, P.D. and Gross, M.R. (1987) Parental care and the evolution of egg size in
shes. American Naturalist 129, 3246.
Selman, K., Wallace, R.A. and Barr, V. (1986) Oogenesis in Fundulus heteroclitus. IV. Yolk vesicle
formation. J. Exp. Zool. 239, 277288.
Selman, K., Wallace, R.A., Sarka, A. and Qi, X.P. (1993) Stages of oocyte development in the
zebrash, Brachydanio rerio. Journal of Morphology 218, 203224.
Sheets, M.D., Fox, C.A., Hunt, T., Vandewoude, G. and Wickens, M. (1994) The 39-untranslated
regions of c-mos and cyclin messenger-RNAs stimulate translation by regulating cytoplasmic
polyadenylation. Genes and Development 8, 926938.
Simon, R., Tassan, J.P. and Richter, J.D. (1992) Translational control by poly(A) elongation during
Xenopus development differential repression and enhancement by a novel cytoplasmic
polyadenylation element. Genes and Development 6, 25802591.
Sire, M.F., Babin, P.J. and Vernier, J.M. (1994) Involvement of the lysosomal system in yolk protein
deposit and degradation during vitellogenesis and embryonic development in trout. Journal of
Experimental Zoology 269, 6983.
Smith, J.C., Price, B.M.J., Vannimmen, K. and Huylebroeck, D. (1990) Identication of a potent
Xenopus mesoderm-inducing factor as a homolog of activin-A. Nature 345, 729731.
Smith, R.M. and Cole, C.F. (1973) Effects of egg concentration of DDT and dieldrin on development
in winter ounder (Pseudopleuronectes americanus). J. Fish. Res. Board Can. 30, 18941898.
Soyano, K., Saito, T., Nagae, M. and Yamauchi, K. (1993) Effects of thyroid hormone on
gonadotropin-induced steroid production in medaka, Oryzias latipes, ovarian follicles. Fish
Physiology and Biochemistry 11, 265272.
Specker, J.L. and Sullivan, C.V. (1994) Vitellogenesis in shes: status and perspectives. In Davey,
K.G., Peter, R.E. and Tobe, S.S., eds. Perspectives in Comparative Endocrinology. Ottawa,
Canada: National Research Council of Canada, pp. 304315.
Spirin, A.S. (1994) Storage of messenger RNA in eukaryotes: envelopment with protein, translational
barrier at 59 side, or conformational masking by 39 side? Molecular Reproduction and
Development 38, 107117.
Springate, J.R.C., Bromage, N.R., Elliot, J.A.K. and Hudson, D.L. (1984) The timing of ovulation and
stripping and their effects on the rates of fertilisation and survival to eyeing, hatching and swimup in the rainbow trout (Salmo gairdneri). In Cowey, C.B., Mackie, A.M. and Bell, J.A., eds.
Nutrition and Feeding in Fish. London: Academic Press, pp. 371391.
Srivastava, R.K. and Brown, J.A. (1991) The biochemical characteristics and hatching performance of
cultured and wild Atlantic salmon (Salmo salar) eggs. Can. J. Zool. 69, 24362441.
Srivastava, R.K. and Brown, J.A. (1993) Assessment of egg quality in Atlantic salmon, Salmo salar,
treated with testosterone biochemical composition. Canadian Journal of Zoology 71, 109115.
Standart, N. (1992) Masking and unmasking of maternal mRNA. Seminars in Developmental Biology
3, 367379.
Suzuki, K., Nagahama, Y. and Kawauchi, H. (1988) Steroidogenic activities of 2 distinct salmon
gonadotropins. General and Comparative Endocrinology 71, 452458.
Tagawa, M. and Hirano, T. (1987) Presence of thyroxine in eggs and changes in its content during
early development of chum salmon, Oncorhynchus keta. General and Comparative Endocrinology
68, 129135.
Tagawa, M. and Hirano, T. (1991) Effects of thyroid-hormone deciency in eggs on early development
of the medaka, Oryzias latipes. Journal of Experimental Zoology 257, 360366.
Takeuchi, T., Watanabe, F., Ogino, C., Saito, M., Nishimura, K. and Nose, T. (1981) Effects of low
Egg quality in sh
415
proteinhigh calorie diets and deletion of trace elements from a sh meal diet on reproduction of
rainbow trout. Bull. Jap. Soc. Scient. Fish. 47, 645654.
Tanaka, M., Tanangonan, J.B., Tagawa, M., Dejesus, E.G., Nishida, H., Isaka, M., Kimura, R. and
Hirano, T. (1995) Development of the pituitary, thyroid and interrenal glands and applications of
endocrinology to the improved rearing of marine sh larvae. Aquaculture 135, 111126.
Tata, J.R. (1986) Coordinated assembly of the developing egg. BioEssays 4, 197200.
Tautz, D. and Pfeie, C. (1989) A non-radioactive in situ hybridization method for the localization of
specic RNAs in drosophila embryos reveals translational control of the segmentation gene
hunchback. Chromosoma 98, 8185.
Tyler, C.R. (1991) Vitellogenesis in salmonids. In Scott, A.P., Sumpter, J.P., Kime, D.E. and Rolfe, J.,
eds. Proc. Fourth Int. Symp. Reprod. Physiol. of Fish. Shefeld, UK: Shefeld University Press,
pp. 295299.
Tyler, C.R. and Lancaster, P. (1993) Isolation and characterization of the receptor for vitellogenin from
follicles of the rainbow trout, Oncorhynchus mykiss. Journal of Comparative Physiology 163B,
225233.
Tyler, C.R. and Sumpter, J.P. (1996) Oocyte growth and development in teleosts. Reviews in Fish
Biology and Fisheries 6, 287318.
Tyler, C.R., Sumpter, J.P. and Campbell, P.M. (1991a) Uptake of vitellogenin into oocytes during early
vitellogenic development in the rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish
Biology 38, 681689.
Tyler, C.R., Sumpter, J.P., Kawauchi, H. and Swanson, P. (1991b) Involvement of gonadotropin in the
uptake of vitellogenin into vitellogenic follicles of the rainbow trout Oncorhynchus mykiss. Gen.
Comp. Endocrinol. 84, 291299.
Tyler, C.R., Nagler, J.J., Pottinger, T.G. and Turner, M.A. (1994) Effects of unilateral ovariectomy on
recruitment and growth of follicles in the rainbow trout, Oncorhynchus mykiss. Fish Physiology
and Biochemistry 13, 309316.
Uchiyama, H., Nakamura, T., Komazaki, S., Takio, K., Asashima, M. and Sugino, H. (1994)
Localization of activin and follistatin proteins in the Xenopus oocyte. Biochemical and
Biophysical Research Communications 202, 484489.
Ungerer, J. and Thomas, P. (1995) Transport and ovarian accumulation of o,p9-DDT in the Atlantic
croaker (Micropogonias undulatus) during gonadal recrudescence. In Goetz, F.W. and Thomas, P.,
eds. Proceedings of the Fifth International Symposium on the Reproductive Physiology of Fish.
Austin, Texas, USA: Fish Symposium '95, Austin, p. 190.
van Leeuwen see Leeuwen
Vieira, A.V., Sanders, E.J. and Schneider, W.J. (1995) Transport of serum transthyretin into chicken
oocytes a receptor-mediated mechanism. Journal of Biological Chemistry 270, 29522956.
Von Westernhagen, H., Cameron, P., Dethlefsen, V. and Janssen, D. (1989) Chlorinated hydrocarbons
in north-sea whiting (Merlangius merlangus L.), and effects of reproduction. 1. Tissue burden and
hatching success. Helgolander Meeresuntersuchungen 43, 4560.
Wahli, W. and Ryf, G.U. (1985) Xenopus vitellogenin genes. In McLean, N., ed. Oxford Surveys on
Eukaryotic Genes, Vol. 2. Oxford: Oxford University Press, pp. 95120.
Walker, C. and Streisinger, G. (1983) Induction of mutations by gamma rays in pre-gonial germ-cells
of zebrash embryos. Genetics 103, 125136.
Wallace, R.A. (1985) Vitellogenesis and oocyte growth in non-mammalian vertebrates. In Browder,
L.W., ed. Developmental Biology, Vol. 1: Oogenesis. New York: Plenum Press, pp. 127177.
Wallace, R.A. and Hollinger, T.G. (1979) Turnover of endogenous, microinjected, and sequestered
protein in Xenopus oocytes. Expl Cell Res. 119, 277287.
Wallace, R.A. and Selman, K. (1981) Cellular and dynamic aspects of oocyte growth in teleosts. Am.
Zool. 21, 325343.
Wallace, R.A. and Selman, K. (1990) Ultrastructural aspects of oogenesis and oocyte growth in sh
and amphibians. Journal of Electron Microscopy Technique 16, 175201.
416
Walton, M.J. and Cowey, C.B. (1982) Aspects of intermediary metabolism in salmonid sh.
Comparative Biochemistry and Physiology 73B, 5979.
Wang, S., Smith, D.E. and Williams, D.L. (1983) Purication of avian vitellogenin III: comparison
with vitellogenins I and II. Biochemistry 22, 62066212.
Washburn, B.S., Frye, D.J., Hung, S.S.O., Doroshov, S.I. and Conte, F.S. (1990) Dietary effects on
tissue composition, oogenesis and the reproductive performance of female rainbow trout
(Oncorhynchus mykiss). Aquaculture 90, 179195.
Watanabe, T., Fujimura, T., Lee, M.J., Fukusho, K., Satoh, S. and Takeuchi, T. (1991a) Nutritional
studies in the seed production of sh. 21. Effect of polar and nonpolar lipids from krill on quality
of eggs of red seabream Pagrus major. Nippon Suisan Gakkaishi Bulletin of the Japanese
Society of Scientic Fisheries 57, 695698.
Watanabe, T., Lee, M.J., Mizutani, J., Yamada, T., Satoh, S., Takeuchi, T., Yoshida, N., Kitada, T. and
Arakawa, T. (1991b) Nutritional studies in the seed production of sh. 20. Effective components
in cuttlesh meal and raw krill for improvement of quality of red seabream Pagrus major eggs.
Nippon Suisan Gakkaishi Bulletin of the Japanese Society of Scientic Fisheries 57, 681694.
Webb, P.W. and Weihs, D. (1986) Functional locomotor morphology of early life history stages of sh.
Trans. Am. Fish. Soc. 115, 115127.
West, C.J. and Mason, J.C. (1987) Evaluation of sockeye salmon (Oncorhynchus nerka) production
from the Babine Lake development project. In Smith, H.D., Margolis, L. and Wood, C.C., eds.
Sockeye salmon (Oncorhynchus nerka) population biology and future management. Canadian
Special Publication of Fisheries and Aquatic Sciences 96, 176190.
Westernhagen, H. Von see Von
Westin, D.T., Olney, C.E. and Rogers, B.A. (1985) Effects of parental and dietary organochlorines on
survival and body burdens of striped bass larvae. Transactions of the American Fisheries Society
114, 125136.
Wickens, M. (1992) Forward, backward, how much, when: mechanisms of poly(A) addition and
removal and their role in early development. Seminars in Developmental Biology 3, 399412.
Wiegand, M.D. (1996a) Composition, accumulation and utilization of yolk lipids in teleost sh.
Reviews in Fish Biology and Fisheries 6, 259286.
Wiegand, M.D. (1996b) Utilization of yolk fatty acids by goldsh embryos and larvae. Fish
Physiology and Biochemistry 15, 2127.
Wilson, C., Crim, L. and Morgan, M. (1995) The effects of stress on spawning performance and larval
development in the Atlantic cod, Gadus morhua L. In Goetz, F.W. and Thomas, P., eds.
Texas, USA: Fish Symposium '95, Austin, p. 198.
Withler, R.E. (1987) Genetic variation in survival of chinook salmon (Oncorhynchus tshawytscha)
alevins exposed to an unidentied agent of mortality. Genome 29, 839845.
Woods, L.C. III and Sullivan, C.V. (1993) Reproduction of striped bass, Morone saxatilis (Walbaum),
broodstock: monitoring maturation and hormonal induction of spawning. Aquaculture and
Fisheries Management 24, 211222.
Wootton, R.J. (1994) Life histories as sampling devices: optimum egg size in pelagic shes. J. Fish
Biol. 45, 10671077.
Yamagami, K. (1992) Studies on the hatching enzyme and its substrate, egg envelope, of Oryzias
latipes. Zoological Science 9, 1131.
Yamashita, M., Fukada, S., Yoshikuni, M., Bulet, P., Hirai, T., Yamaguchi, A., Lou, Y.H., Zhao, Z. and
Nagahama, Y. (1992) Purication and characterization of maturation-promoting factor in sh.
Developmental Biology 149, 815
Young, L.G. and King, G.J. (1981) Reproductive performance of gilts bred on rst versus third estrus.
Journal of Animal Science 66, 1925.
Accepted 3 July 1997

Egg Quality in Fish - What Makes A Good Egg

Încărcat de

Informații document

Titlu original

Drepturi de autor

Formate disponibile

Partajați acest document

Partajați sau inserați document

Opțiuni de partajare

Vi se pare util acest document?

Este necorespunzător acest conținut?

Drepturi de autor:

Formate disponibile

Egg Quality in Fish - What Makes A Good Egg

Încărcat de

Drepturi de autor:

Formate disponibile

Reviews in Fish Biology and Fisheries 7, 387416 (1997)

Egg quality in sh: what makes a good egg?

Author to whom correspondence should be addressed (e-mail: Suzanne.Brooks@brunel.ac.uk).

Brooks, Tyler and Sumpter

and=or mRNA translation in sh oocytes=embryos. This is surprising because the

Fig. 1. A scheme showing the coordinated assembly of a sh egg.

Brooks, Tyler and Sumpter

Brooks, Tyler and Sumpter

maintained in eggs in chum salmon (Oncorhynchus keta, Salmonidae) until hatching,

Brooks, Tyler and Sumpter

Brooks, Tyler and Sumpter

It has been suggested that environmental factors such as photoperiod, temperature,

Brooks, Tyler and Sumpter

Fish oocytes and eggs are particularly sensitive to environmental pollutants. As an

Brooks, Tyler and Sumpter

there is approximately a one-week window for successful fertilization, in Atlantic

due to different husbandry practices on the different farms (i.e. an environmental

Brooks, Tyler and Sumpter

Brooks, Tyler and Sumpter

Linnaeus 1766). Journal of Experimental Zoology 257, 96109.

Brooks, Tyler and Sumpter

translational efciency. Genes and Development 5, 21082116.

Brooks, Tyler and Sumpter

Brooks, Tyler and Sumpter

Brooks, Tyler and Sumpter

Accepted 3 July 1997

S-ar putea să vă placă și