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This is author-created pdf of accepted version of the article published in Rev Fish Biol Fisheries
The final publication is available at www.springerlink.com DOI 10.1007/s11160-011-9233-7
Fish hatching strategies: a review
Michał Korwin-Kossakowski
The Stanisław Sakowicz Inland Fisheries Institute in Olsztyn, Pond Fishery Department in
Żabieniec, 05-500 Piaseczno, Poland, e-mail: mkk@infish.com.pl, +48 22 7562044, +48 22
7562088
Abstract
The paper presents differences in the distribution
of hatching gland cells, and the location of egg envelope
digestion, the significance of hatching movements, and
the ways larvae escape from egg envelopes. A review of
the literature on the hatching orientation of 34 fish species
is compared. No correlation was seen between hatching
orientation and egg diameter or newly hatched larva
length, nor newly hatched larvae length ratio to egg
diameter. Photographs of twelve freshwater species
present the moment of hatching either head first or tail
first. Some differences were shown in swelling between
eggs incubated in commercial hatchery and developed in
natural conditions, as well as possible effect of these
differences on hatching.
Keywords: Hatching, Egg, Embryo, Egg
envelopes, Hatching enzyme, Teleost
Introduction
Hatching, or leaving the egg envelopes
(chorion), is the most important environmental
change fish experience during their lives. This
moment is usually regarded as the dividing line
between the embryonic and larval periods.
According to Fuiman (2002), hatching occurs
when the embryo reaches a size at which its
energy requirements for oxygen exceed the
diffusion capabilities of this gas through the egg
envelopes and perivitelline fluid. There are
however several species of fish that lay eggs
terrestrially and do not hatch on a set timetable
or a set size (Martin 1999). The comparison of
hatching between these fish species that hatch
according to genetic program and those species
with environmentally cued hatching (ECH) was
accurately described by Martin et al. (2011a),
while ECH across the broad range of animals
was analyzed by Warkentin (2011).
Nearly all environmental factors have an
effect on hatching, with temperature exerting
possibly the greatest effect on fish development
(Pepin 1991; Kamler et al. 1994, 1998;
Kamiński et al. 2006; Korwin-Kossakowski
2008). This factor also influences the activity of
the hatching gland cells, metabolism, and
oxygen requirements (Kamler 1992, 2002;
Kamler et al. 1998). The water oxygen content
can either shorten or lengthen embryonic
development to hatching competence (Czerkies
et al. 2001; Fuiman 2002; Ciuhandu 2005),
influences hatching enzyme secretion
(DiMichele and Taylor 1980), and also hatching
rate (Hassell et al. 2008). Light can affect both
the time to hatching as well as the duration of
the hatching time (Downing and Litvak 2002,
Brüning et al. 2010). Water pH, oxygen
saturation, chemical composition, and salinity
can all accelerate or delay, as well as prolong
hatching (Jezierska 1988; Oyen et al. 1991;
Griem and Martin 2000; Jezierska and Witeska
2001; Pyle et al. 2002; Bonisławska 2010).
Oxygen conditions may influence drugs effect
on hatching in Fundulus heteroclitus
(DiMichele and Taylor 1981). Heavy metals in
water inhibit the activity of hatching enzyme
(Jezierska et al. 2009). Similar effects can be
caused by acidified water (Salmo salar –
Waiwood and Haya 1983), which can also
inhibit the development of hatching gland cells
(Cyprinus carpio – Ostaszewska 2002).
Magnetic fields can retard hatching of Danio
rerio and desynchronize it (Skauli et al. 2000),
ultraviolet radiation negatively influences
hatching success in Oryzias latipes (Bass and
Sistrun 1997). Delayed hatching might also be
the result of toxins in the water, such as
1
naturally occurring brevetoxins (Kimm-Brinson
and Ramsdell 2001), or antropogenic toxins
such as herbicides (Villalobos et al. 2000),
insecticides (Mercy et al. 2000; Gonzáles-
Doncel et al. 2003), or endocrine-disrupting
chemicals (EDCs) (Ishibashi et al. 2005).
The mechanisms of the biochemical
processes occurring during hatching are well
described (Yamagami 1988, 1996, 1997;
Yasumasu et al. 1988, 2010; Kawaguchi et al.
2008, 2009, 2010). Far less information is
available regarding the distribution of the
hatching gland cells and its relation with the
location of egg envelope digestion, as well as
embryonic movements prior to hatching, and
strategies for larvae to escape from egg
envelopes. The study presented in this paper
was an attempt to focus attention on these
phenomena.
Hatching gland cells
The digestion of egg envelopes happens
thanks to the hatching enzyme (chorionase)
released from enzyme granules located in
unicellular hatching glands (Yamagami 1988).
Rudiments of hatching gland cells usually
appear early in embryos at the end of the
gastrula stage (Hippoglossus hippoglossus –
Helvik et al. 1991a; D. rerio – Melby et al.
1996; O. latipes – Inohaya et al. 1999).
Hatching gland cells usually appear after
embryonic blood circulation begins, which is
linked most frequently with the appearance of
eye pigments (Clupea harengus – Rosenthal and
Iwai 1979; Stizostedion lucioperca –
Ostaszewska 1989; C. carpio – Ostaszewska
1998; Leuciscus idus – Rechulicz 2001). As the
embryo hatches and leaves the egg envelopes,
the hatching gland cells degenerate and
disappear (Yokoya and Ebina 1976; Schoots et
al. 1982a; Helvik et al. 1991a; Ostaszewska
1998, Iwamatsu 2004, Martin et al. 2011a).
The distribution of hatching gland cells
on fish embryo differs between species. In C.
harengus (Rosenthal and Iwai 1979) hatching
gland cells are located on the head and back; in
Oncorhynchus mykiss, Esox lucius, and L. idus
(Winnicki et al. 1970; Schoots et al. 1982a;
Rechulicz 2001) on the head and the upper and
front parts of the yolk sac; in S. lucioperca
(Ostaszewska 1989) on the head, the yolk sac,
and in small numbers on the body; in C. carpio
(Ostaszewska 1998) on the head, the yolk sac,
and pectoral fins; in some salmonids (Yokoya
and Ebina 1976) on the head, snout, gills, and
yolk sac; in Oreochromis niloticus (Morrison et
al. 2001) on the head, pectoral fins, upper part
of the yolk sac, and the tail; and in L. tenuis
(Martin et al. 2011a) along the lateral surface of
the body. Atypical hatching gland cells
distribution is noted in O. latipes, in which they
occur on the inside of the mouth cavity
(Yamagami 1997), in F. heteroclitus
(Kawaguchi et al. 2005) in pharyngeal cavity
and the periphery of the mouth, and in H.
hippoglossus (Helvik et al. 1991a, b) in which
they form a loop around the front of the yolk sac
and which is likely the only example of this type
of distribution.
Hatching enzyme and embryo hatching
movements
The hatching process is described most
frequently as the joint effect of the hatching
enzyme released by hatching gland cells and the
mechanical tearing of egg envelopes. Fraysse et
al. (2006) describe it as a combination of
biochemistry and behavior. The hatching
enzyme of euteleostean fishes consists of two
proteases; the high choriolytic enzyme that
causes swelling in the thick inner layer of the
egg envelope, and the low choriolytic enzyme
that digests this layer (Yasumasu et al. 1988,
2010; Kawaguchi et al. 2010). The thin outer
layer, which is not digested, can then be torn by
embryo.
Embryo movements intensify prior to
hatching; they increase respiratory demands and
in effect embryo moves more, what is helpful
for escaping the envelopes (Miller and Kendall
2009). These intensified movements may also
additionally aid respiration efficiency. It is
known that oxygen diffusion into the
perivitelline space depends on egg envelopes
thickness (Fuiman 2002). Comparing oxygen
consumption between intact eggs and
dechorionated embryos, Buznikov (1961)
showed that envelopes reduce oxygen
consumption, what happens especially before
hatching (Czerkies et al. 2002). Ciuhandu et al.
2
(2005) concluded that O. mykiss embryos
without egg envelopes moved more frequently
and grew faster than those developing inside
egg envelopes. Ninness et al. (2006) linked
increased oxygen consumption while hatching
in O. mykiss (by 19%) with substantial increases
in movement (by 50%) during this time. Much
bigger increase in oxygen consumption while
hatching (almost twice) was found in L. tenuis
(Martin et al. 2011a). Thus, mixing the
perivitelline fluid facilitates oxygen penetrating
into the egg, and it also accelerates the
distribution of hatching enzyme in the
perivitelline space. Embryo movement prior to
hatching serves the development of primary
behavioral reactions (Nechaev and Pavlov
2004). Inhibiting embryo movement in
Cichlasoma nigrofasciatum using d-
turbocurarine substantially prolonged the
development inside the egg envelopes and
increased mortality, which Nechaev and Pavlov
(2004) linked to the allegedly worsening oxygen
conditions in the egg. Since lowering oxygen
content generally accelerates hatching
(Rombough 1988; Ciuhandu 2005), it can be
concluded that, in this instance, the inhibition of
movement of C. nigrofasciatum had a greater
effect on time to hatching than did the lowering
of oxygen content. So that it appears that
embryonic movements improve oxygen supply
and accelerate embryo development and growth.
In a comparison of embryo movement in
11 teleost fish, Korzelecka (1999) noted that
after a period of intensified activity just prior to
hatching embryo somatic movement ceased.
This was linked to the final, local digestion of
the egg envelopes. Following a period of several
minutes of no movement, the egg envelopes tore
at the site that had been digested sufficiently.
Winnicki et al. (1970), Winnicki and
Korzelecka (1997), and Korzelecka and
Winnicki (1998) also reported increased motor
activity in the period prior to hatching, followed
by the embryo bodies adhering to the inner layer
of the egg envelopes for a period of time.
Studies conducted on O. mykiss indicated that
egg envelopes exhibited localized traces of
digestion (Ninness et al. 2006) and that they had
torn in these thinner places during hatching
(Winnicki et al. 1970). These results confirmed
the previous studies of Hayes (1942), which
confirmed that the egg envelopes of S. salar
were digested by hatching enzyme at locations
that were in direct contact with the embryonic
hatching gland cells. Hayes also explained the
significance of embryo contact with egg
envelopes, and concluded that the pH of the
perivitelline fluid was slightly acidic, while that
of the embryo epithelium was slightly alkaline.
Since hatching enzyme activity increases in an
alkaline environment (the optimum is at pH
9.6), the contact of hatching gland cells with the
egg envelopes creates localized environments
more proper for digestion. The maximum
proteolytic activity of hatching liquid was: in
Salmo trutta m. trutta at pH 9.0-9.4 (Luberda et
al. 1993), in Coregonus albula and C. lavaretus
at pH 8.5 (Luczynski et al. 1987) or at pH 9.4
and 9.6, respectively (Luberda et al. 1992). Shi
et al. (2006) reported however that lower levels
(pH 7) were optimal for choriolytic activity of
Paralichthys olivaceus hatching enzyme.
Thus, when hatching gland cells are in
direct contact with egg envelopes, hatching
enzyme digests them much faster than when it is
diluted in perivitelline liquid. Winnicki et al.
(1970) concluded that, with the exception of the
places where there was digestion from direct
contact, the egg envelopes of O. mykiss were of
the same thickness as before hatching, which
indicates that the enzyme diluted in the
perivitelline liquid had not yet digested them.
The active perivitelline liquid of S. salar
containing hatching enzyme digested through
the egg envelope in four minutes (Hayes 1942),
but when the hatching gland cells were in direct
contact with the envelope the digestion time
would probably be shorter. The time required to
digest envelopes undoubtedly depends on their
thicknesses (Kawaguchi et al. 2008), as well as
on the quantity of hatching enzyme, and thus on
the number of hatching gland cells, which is
dependent on species (Ostaszewska 1989, 1998;
Helvik et al. 1991a; Rechulicz 2001). Schoots et
al. (1982b) noted that the total number of
hatching enzyme granules in fish embryos
increased with egg envelope thickness.
Kawaguchi et al. (2009) also demonstrated that
the embryos of Clupea pallasii, which develop
in eggs with thick envelopes, have much higher
3
numbers of hatching gland cells than do
Engraulis japonicus, which have thin envelopes.
The period of egg envelope digestion also
depends on the degree to which the egg is
developed (Morrison et al. 2003).
The course of digestion is entirely
different in species in which there is no contact
between hatching gland cells and the egg
envelope. In effect, the hatching enzyme
contained in the perivitelline liquid caused
envelope thickness to thin over its entire surface
area. The egg envelopes of O. latipes
(Yamagami 1997) in which the hatching gland
cells are distributed in the mouth cavity are
digested equally over the entire internal surface
area. It is likely that envelope digestion happens
similarly in Ctenopharyngodon idella since its
tiny embryo has little contact with the egg
envelope (Korwin-Kossakowski, unpubl. data).
Hatching synchronization
Environmental factors like temperature,
oxygen and light are regarded as main natural
factors influencing hatching in nature
(Yamagami 1988). Nevertheless these factors
were applied more than once in commercial
hatcheries or in laboratory for controlling
development and hatching. Synchronized
hatching is desirable in commercial hatcheries
that incubate fish eggs. Since the hatching step
is a significant one and larvae are particularly
sensitive during the consecutive phase of
development, minimizing this time is desirable
(Korwin-Kossakowski 2008). Synchronization
can be achieved either by accelerating or
delaying the moment of hatching which results
in an increase of hatching events over a given
period of time. The oldest method used to
accelerate hatching is probably to reduce aquatic
oxygen content (Rombough 1988; Czerkies et
al. 2001; Ciuhandu et al. 2005), which also
effects increased hatching enzyme secretion
(DiMichele and Taylor 1980; Rothbard 1981;
Shireman and Smith 1983). This method is used
successfully in hatcheries culturing C. carpio.
Reducing the flow of water through Zuger jars
results in faster hatching that occurs nearly
simultaneously, and it does not cause increased
larval mortality (Korwin-Kossakowski 1988;
Horvath et al. 1992).
Hatching can be accelerated and
synchronized by increasing incubation
temperature, as was confirmed for
Chondrostoma nasus (Kamler et al. 1998),
Eupallasella percnurus (Kamiński et al. 2006)
and Gadus macrocephalus (Laurel et al. 2008).
At higher temperatures the time between the
beginning and the end of hatching process was
shorter than at lower temperatures. On the other
hand in L. idus embryos incubated at the
optimal temperature the hatching gland cells
were larger than at higher temperature
(Rechulicz 2001). Since the hatching gland cells
size is closely correlated with hatching enzyme
activity (DiMichele and Taylor 1981) it could
be expected that optimal temperature may in
effect synchronize hatching.
A significant factor regulating the
hatching process is light, which, through the
pineal organ, influences the hatching gland cells
(Helvik and Walther 1992; Forsell et al. 1997).
Reactions to light can differ diametrically
among different species. Light accelerates and
synchronizes the hatching of O. latipes
(Wakamatsu 1997), and also accelerates
hatching in Melanogrammus aeglefinus
(Downing and Litvak 2002). However, in H.
hippoglossus hatching is postponed over time in
light and the embryos continue to develop inside
the egg envelopes, but when they are moved
into the dark they hatch synchronously (Helvik
and Walther 1992, 1993a, b). Hatching occurs
then within an hour (with 70% of the stock
hatching within 20 min) although hatching
normally lasts for 2 days.
Natural synchronization of hatching
occurs also by tidal cues in F. heteroclitus and
L. tenuis, species that incubate eggs terrestrially
(DiMichele and Taylor 1980, Griem and Martin
2000, Martin et al. 2011b). Contact with water
is then a trigger for hatching which occurs very
fast.
An atypical method for synchronizing
hatching was used with Ctenopharyngodon
idella when the first individuals began to hatch
(Korwin-Kossakowski, unpubl. data). The eggs
were siphoned through a plastic tube with an
internal diameter of about 8 mm. As they
flowed through the tube their delicate egg
envelopes tore under the pressure of the
4
procedure, and all of the larvae hatched
simultaneously. The larvae induced to hatch
with this method inflated their swim bladders
and began exogenous feeding at the same time
as larvae that had hatched naturally, and
survival was comparable after 1 week of
feeding. Their further development and growth
was not studied.
Hatching synchronization can also be
achieved using electrical impulses as was
demonstrated with O. latipes (Yamamoto et al.
1979) or Coregoninae and E. lucius (Luczynski
1984; Luczynski and Bardega 1990).
Synchronization performed in that way turned
out to be a good method for collecting hatching
enzyme. The hatching enzyme of Coregoninae
and E. lucius was collected by synchronizing
the hatching of these specimens using electrical
impulses and special devices (Luczynski et al.
1987, Luczynski and Bardega 1990). The
hatching liquid collected was frozen at –20°C,
and it retained its proteolytic activity for 1 year.
In turn, hatching enzyme from O. latipes was
obtained, in low water capacity, by using light
to synchronize the hatching of larvae
(Wakamatsu 1997). The time of envelope
digestion using the enzyme solution collected
with this method was about 50 to 60 min. for O.
latipes. It was confirmed that the solution can be
stored on ice for 1 month or longer at a
temperature of –80°C.
Hatching in various species
Table 1 presents hatching methods
described by various authors. They are
presented according to species habitat and
increasing newly hatched larva (hatchling) size
in two groups that hatch either head first or tail
first. With the exception of Speer-Blank and
Martin (2004) as well as Ługowska and
Sarnowski (2011), all the remaining authors
reported their rough estimates rather than results
of exact quantifications. No dependencies were
identified between hatching orientation and egg
size, newly hatched larvae size, or the ratios of
the length of newly hatched larvae to the
diameter of the egg. Acanthopagrus cuvieri and
Puntius titteya, two of the smallest species
compared, hatched head first and tail first,
respectively. The two largest species also
differed with Barbus barbus hatching mainly
tail first and E. lucius hatching head first. The
hatching orientation didn’t depend on eggs size.
The hatching orientation was not also linked to
the ratio of length of the newly hatched larva to
egg diameter, even though the differences in
this were quite large ranging in different species
from 1.84 (L. cephalus) to 5.40 (Osmerus
eperlanus) (Table 1). No differences were noted
either between two closely-related species from
the suborder Clupeoidei, namely C. pallasii that
spawns adhesive, demersal eggs, and E.
japonicus that spawns pelagic eggs, and both of
which hatched head first (Kawaguchi et al.
2009). Miller and Kendall (2009) stated that
marine fish larvae hatched from large eggs tend
to emerge tail first, while those from small eggs
emerge head first. Marine fishes, not very
numerous in the presented list, belong mainly to
the head first hatching group with narrow range
of egg diameter. Such statement is not
confirmed however by, presented in Table 1,
results for freshwater species.
The photographs in Figs. 1-6 present
examples of head-first hatching, while those in
Figs. 7-12 present tail-first hatching in
freshwater fish. The hatching orientations
presented are those that were observed most
frequently, but in none of these instances were
the percentage shares calculated. All of the
species presented in the pictures, with the
exception of Clarias gariepinus, are from the
family Cyprinidae, thus it can be concluded that
the hatching orientation does not depend on
membership in a particular family. Hatching
orientation was also impossible to link to the
adhesiveness of the eggs since there were
species in both groups that had very adhesive
eggs such as Tinca tinca, Alburnoides
bipunctatus, C. carpio, and Carassius carassius,
as well as less adhesive, such as those of Vimba
vimba, L. cephalus, L. idus, and P. sachsi.
The hatching way of C. idella is unusual.
The perivitelline space in the egg of this species
can occupy as much as 99% of its volume
(Billard et al. 1986). The newly hatched larvae
are very small in comparison with the egg
diameter (4.9 and 3.3 mm, respectively;
Korwin-Kossakowski 2008); thus, the
embryonic epithelium does not come into close
5
TABLE 1
Sizes of eggs and newly hatched larvae and the hatching orientation observed among different fish
species
Species Habitat Egg
diameter
(mm)
Newly hatched
larva length
(mm)
Hatching
orientation
Source
Tinca tinca F 1.2 3.5 head Korzelecka-Orkisz et al. 2009a
Leuciscus cephalus F 1.9 3.5 head Korwin-Kossakowski, unpubl. data
Clarias gariepinus F 1.7/1.3
1
4.0 head Korwin-Kossakowski et al. 1999
Eupallasella percnurus F 1.4 4.3 head Kamiński et al. 2002
Alburnoides bipunctatus F 2.0 6.0 head Wolnicki and Korwin-Kossakowski
2003
Vimba vimba F 1.9 6.1 head Korwin-Kossakowski, unpubl. data
Scardinius erythrophthalmus F 1.4 6.7 head Korzelecka and Winnicki 1998
Esox lucius F 2.6 7.8 head Tański et al. 2000
Acanthopagrus cuvieri M 0.8 1.9 Head Hussain et al. 1981
Chrysiptera parasema M 1.35 3.0 head Olivotto et al. 2003
Abudefduf saxatilis M 0.95/0.55
2
3.1 head Shaw 1955
Engraulis japonicus M 1.4/0.7
2
3.5 head Kawaguchi et al. 2009
Lipophrys pholis M 1.3 5.0 head Faria et al. 2002
Clupea pallasii M 1.4 7.5 head Kawaguchi et al. 2009
Puntius titteya F 1.2 2.9 tail Korzelecka-Orkisz et al. 2009b
Puntius sachsi F 1.2 3.5 tail Korwin-Kossakowski and Kamiński
2001
Lota lota F 1.1 3.7 tail Kujawa et al. 2002
Barbus trevelyani F 1.5 3.7 tail Cambray 1985
Oryzias latipes F/M 1.2
3
4.0 tail Iwamatsu 2004
Leucaspius delineatus F 1.3 4.3 tail Bonisławska et al. 1999
Alburnus alburnus F 1.5 4.6 tail Winnicki and Korzelecka 1997
Oreochromis niloticus F 2.2/1.6
2
4.8 tail Morrison et al. 2001
Osmerus eperlanus F 1.0 5.4 tail Hliwa et al. 2007
Cyprinus carpio F 1.9 5.5 tail Korwin-Kossakowski 1998,
Oyen et al. 1991,
Ługowska and Sarnowski 2011
4
Carassius carassius F 1.5 5.8 tail Korwin-Kossakowski, unpubl. data
Leuciscus idus var. orphus F 2.2 5.9 tail Korwin-Kossakowski 1999
Leuciscus idus F 2.4 6.4 tail Korwin-Kossakowski 1999
Leuresthes tenuis M 1.6 7.0 tail Speer-Blank and Martin 2004
5
,
Martin et al. 2009
Heteropneustes fossilis F 1.3 3.4 tail or head Korzelecka-Orkisz et al. 2010
Gymnocephalus cernuus F 0.9 3.9 tail or head Bonisławska et al. 2004
Oncorhynchus mykiss F/M - 4.5 tail or head Ługowska and Sarnowski 2011
6
Barbus barbus F 2.9 9.0 tail, head or
mixed
Ługowska and Sarnowski 2011
7
,
Korwin-Kossakowski, unpubl. data
Ctenopharyngodon idella F 3.4 4.9 specific Korwin-Kossakowski 2008
Hippoglossus hippoglossus M 3.3
8
5.9
8
specific Helvik et al. 1991a
F – freshwater fish, M – marine fish, F/M – two habitats fish
1
African catfish eggs resemble flattened discs with a hemisphere attached to one side; measurements are diameters of
larger and smaller parts
2
longer and shorter axes of elliptical egg
3
diameter of unfertilized egg
4
about 79% of embryos hatched tail first
5
about 68% of embryos hatched tail first
6
about 56% of embryos hatched tail first
7
about 73% of embryos hatched tail first
8
measured from calibrated photographs
6
Figs 1-6 Hatching head first (freshwater species): 1. Vimba vimba, 2. Leuciscus cephalus, 3. Tinca tinca, 4.
Alburnoides bipunctatus, 5. Eupallasella percnurus, 6. Clarias gariepinus (photographs by Michał Korwin-
Kossakowski)
contact with egg envelope. Envelope tearing is
also different in C. idella than it is in other
Cyprinidae. The envelope becomes limp so the
moment of its rupture is not visible, and the
larvae swim out of them without difficulty. It is
difficult in this case to classify this hatching
way as head first, even if the head is the first to
leave the envelope.
The hatching of H. hippoglossus is
unique (Helvik et al. 1991b). The hatching
gland cells are distributed in a narrow belt on
the front of the yolk sac. The egg envelope is
digested as the result of direct contact with the
7
Figs 7-12 Hatching tail first (freshwater species): 7. Leuciscus idus, 8. Leuciscus idus var. orphus, 9.
Cyprinus carpio, 10. Carassius carassius, 11. Puntius sachsi, 12. Barbus barbus (photographs by Michał
Korwin-Kossakowski)
hatching gland cells, and the larvae hatch
frontally through an opening that is only slightly
smaller than the diameter of the yolk sac. The
authors explain this hatching method by the
weakly developed H. hippoglossus embryo
(especially musculature) at the hatching stage.
Reasons for differences
It is plausible that the hatching
orientation is largely dependent on the
distribution of hatching gland cells. An
indisputable example is that of H. hippoglossus,
in which the envelope is digested in a precisely
determined place that results from the
8
distribution of the hatching gland cells (Helvik
et al. 1991a,b). These authors suggest that
“restricted digestion” of a limited area in the
egg envelope can also occur in C. harengus
since the hatching gland cells are distributed on
the frontal part of the head (Rosenthal and Iwai
1979). The egg envelopes of O. mykiss, in
which the hatching gland cells are distributed
mainly on the head (Winnicki et al. 1970), tore
at hatching along places in which hatching
enzyme had created a groove. Similarly, C.
pallasii and E. japonicus, in which the hatching
gland cells are located on the heads (Kawaguchi
et al. 2009), hatched head first; however,
differences were noted. The envelope of C.
pallasii digested throughout the head region,
while that of E. japonicus had a slit digested by
the hatching gland cells located at the edge of
the head. Cyprinus carpio hatches tail first even
though the hatching gland cells are distributed
on the front of the body (Ostaszewska 1998);
this leads to the expectation that hatching will
be head first. Similarly, tail first hatching is
noted in L. idus (Korwin-Kossakowski 1999),
and, again, like in C. carpio, the hatching gland
cells are located on the head and on the front of
the yolk sac (Rechulicz 2001). Possibly, the
envelopes of these species are digested in spots
thanks to direct contact with head and then these
weakened spots are teared by tails. Such method
of escaping egg, with tail “employed” to break
envelopes was mostly observed in L. tenuis
(Speer Blank and Martin 2004). Such way of
hatching was linked to its hatching glands
location, along the lateral surface of the body
(Martin et al. 2011a).
In some fish, the hatching method is
dictated by the shape of the egg and the way in
which it is incubated. The elliptical eggs of
Chrysiptera parasema are attached to substrate
by adhesive filaments. Before hatching, the
embryo inverts itself so the head faces the distal
end of the egg, and, consequently, the larva
hatch head first (Olivotto et al. 2003). A similar
egg shape and attachment method is noted in
Perccottus glenii. The embryos are also located
along the egg axis, but their heads are in the
proximal end of the egg throughout embryonic
development (Korwin-Kossakowski, unpubl.
data). Unfortunately, nothing is known about
the hatching orientation of this species, but the
positioning of the embryo leads to the
expectation that it will occur tail first.
It sometimes happens that hatching form
may be described differently by various authors,
and one example is Lipophrys pholis. Faria et al.
(2002) reported that this species hatched head
first, but also noted that Qasim (1956) described
this same species (formerly Blennius pholis) as
hatching tail first. Since the percentage of a
population or experimental group of a given
species that employs a typical hatching way is
almost never calculated, it probably happens
that one hatching orientation is described as the
basic one, or even the only one. Speer-Blank
and Martin (2004) as well as Ługowska and
Sarnowski (2011) are the only researchers to
have quantified different hatching ways. In their
study, Speer-Blank and Martin (2004) described
the four hatching ways of L. tenuis, which
include tail first hatching in 67.8% of
individuals; head first in 10.3% of individuals;
partial tail first (the tail tore the envelope, but
the head emerged first) in 12.6% of individuals;
and head and tail emerging simultaneously in
9.2% of individuals. In the current study, B.
barbus was noted to employ also the last way
(see illustration Fig. 12). Although most of the
individuals of this species hatched tail first, the
"mixed" method of tail and head emerging
simultaneously, was also noted. Ługowska and
Sarnowski (2011) described three ways of
hatching in B. barbus; tail first (about 73%),
head first (about 17%) and yolk sac first (about
10%), as well as two ways of hatching in C.
carpio (79% tail first and 11.6% head first) and
in O. mykiss (56.4% tail first and 24.4% head
first. Thus, it is likely that most species employ
both the head and tail first hatching positions,
but with one of these figuring as the dominant
and reported as the only method. Sometimes
only, two hatching positions are reported, but
one is recognized as being typical. This was
precisely what happened with regard to G.
cernuus described by Bonisławska et al. (2004)
and H. fossilis described by Korzelecka-Orkisz
et al. (2010) (Table 1). Most authors conducting
research on early fish development do not
describe hatching orientation in detail, usually
9
only report one position, or sometimes neglect
to mention it at all.
Finally, it is worth mentioning
differences in the swelling of adhesive eggs
incubated in commercial hatcheries and under
natural conditions. In commercial hatcheries the
adhesive eggs of such species as C. carpio, T.
tinca, or C. carassiuss, are treated with special
solutions to eliminate stickiness (Woynarovich
1962). C. carpio eggs with eliminated stickiness
swell significantly more (mean diameter by
about 20%, and thus internal volume by about
80%), than do eggs that develop without such
treatment (Korwin-Kossakowski, unpubl. data).
In effect, the developing embryo has much more
space and movement is easier. This can have an
influence on the metabolism of the embryo
(Ninness et al. 2006), and on its growth rate
(Ciuhandu et al. 2005). Just the opposite
situation occurred with Vimba vimba
incubation. Slightly adhesive eggs were treated
for 20-30 min with water only, what is sufficient
for stickiness elimination in that species. At the
end of treatment eggs were plunged for a short
time in tanine solution. In effect eggs with
eliminated stickiness swelled significantly less
than untreated (Korwin-Kossakowski, unpubl.
data). It is plausible that there are differences in
mortality and the percentage of deformities
between embryos developing in commercial
hatcheries and under natural conditions
stemming from the differences in the amount of
space in which the embryos develop.
Covering of adhesive eggs with
suspended particulates can influence their
swelling, especially in natural waters.
Bonisławska et al. (2011) found that presence of
suspended particulates in water is responsible
for worse swelling of eggs, as well as earlier
hatching and reduced survival of E. lucius
embryos.
Results of differences
Head first hatching allows larvae to exit
the egg envelopes quickly. Teleost fish have
specialized escape behavior that is called the
coordinated escape response, or the C-start
(Gibb et al. 2007), which is in operation at the
moment of hatching. Hatching head first permits
larvae to exit egg envelopes immediately after
they tear open. One of the faster hatchers from
the Cyprinidae family is T. tinca (Korwin-
Kossakowski, unpubl. data); the larvae burst
free from the egg envelopes as soon as they are
perforated. Hatching tail first poses certain
problems for the larvae. After the egg envelope
tears, the perivitelline fluid flows outside the
egg capsule thus halting hatching enzyme
activity. The heads of the hatching larvae are
often imprisoned in the egg envelopes for a
certain period (Figs. 7-12), and the time it takes
them to break free depends on these larvae
strength and vitality. These larvae are more
visible to predators and are easier prey than they
were when inside the egg. L. tenuis escape very
quickly in about two seconds (Speer-Blank and
Martin 2004). This species, however, incubates
terrestrially above the water line, and must
hatch after it is washed into the water with high
tides (Martin 1999; Martin et al. 2009). Chances
of survival decrease the longer the heads of the
larvae remain in the egg envelopes. The larvae
of A. alburnus, which hatch tail first, free
themselves of the egg envelopes within a few
movements (Winnicki and Korzelecka 1997).
The present author's own observations also
indicate that the heads of the imprisoned larvae
of C. carpio free themselves from the egg
envelope within a few minutes, while the larvae
of B. barbus usually take about a minute to do
this. Single individuals, usually the weakest or
anomalously developed, could remain for much
longer with their heads inside the torn egg
envelope. Studies of the time required for the
larvae to escape from the egg envelopes have
not yet been undertaken widely, and the work of
Speer-Blank and Martin (2004) is the exception.
The differences in speed of hatching
process between species with “restricted
digestion” and “general digestion” (terms
according to Helvik 1991a) are not described. It
could be expected that digestion in spot will
proceed faster than digestion of whole envelop.
There is however to many factors affecting the
speed of this process and such expectation could
be speculative only.
Finally, it is worth noting that the
hatching method also impacts the state of the
egg envelopes after hatching. The discarded egg
envelopes of species that use direct embryonic
10
contact with the envelope to digest spots in
them (Winnicki et al. 1970, Helvik et al. 1991b,
Kawaguchi et al. 2009) are decidedly thicker
than in species that digest the entire inner
surface of the envelope. While this is of no
consequence in the wild, this can affect
hatcheries by straining filters with high egg
envelope biomass.
Hatching abnormalities
Although hatching orientation is largely
species specific, atypical or pathological
situations can occur. Kimm-Brinson and
Ramsdell (2001) concluded that the embryos of
O. latipes hatch head first, and not tail first as
they normally do, when exposed to brevetoxin.
In embryos of C. carpio, B. barbus and O.
mykiss hatched tail first, what is typical for
examined species, Ługowska and Sarnowski
(2011) found statistically less deformed
specimens than in embryos hatched head first.
Hatched yolk sac first B. barbus embryos were
all deformed. It is highly possible that
deformities were the reasons of such atypical
way of hatching.
Oppen-Berntsen et al. (1990) suggested
that the proper hatching in S. salar is
determined by the state of the external zona
pellucida. Although it is thinner and weaker
than internal zona radiata, the outer layer is
resistant to hatching enzyme and is thus a
barrier against this leaking outside of the egg.
During hatching, the enzyme digests the thicker,
tougher zona radiata, followed by the
mechanical tearing of the zona pellucida by the
hatching embryo (Kawaguchi et al. 2008, 2010).
Oppen-Berntsen et al. (1990) noted numerous
failed hatching attempts among S. salar that
were linked to perforations in the zona pellucida
caused by low-grade fungal infections, while
problems with hatching noted among Gadus
morhua and H. hippoglossus were linked to
damage caused to this membrane by microbial
infections. Barnes et al. (2009) described
degradation of external membrane as an effect
of Flavobacterium columnare infection in O.
mykiss eggs. Hatching rates in bacterially
infected eggs were found to be improved both
by water UV treatment and aeration (Komar et
al. 2004) as well as by antibiotic treatment
(Barnes et al. 2009).
It was found by Wedekind (2002) that
Coregonus sp. hatched earlier in water being
earlier in contact with eggs infected with
Pseudomonas fluorescens. As the author stated
there were no differences in mortality between
intacted and nonintacted eggs. Earlier hatching
could then be sometimes an attempt to avoid
egg infection by escaping of larvae from
endangered zone. Shorter incubation time was
found also in E. perenurus embryo when eggs
groups were more aggregated on glass plates
(Kamiński et al. 2006). Such hatching
acceleration could be the effect of locally
worsened oxygen condition in the boundary
layers as suggested by Ambühl (1959). It may
be also, referring to Wedekind (2002) results,
reaction to fungal infections, occurring often in
adhesive eggs excessively aggregated on
substrate, especially if some of them are dead.
Problems with successful hatching were
found in C. albula after prolonged hypoxia
(Czerkies et al. 2001). Embryos were too weak
to move and tear zona radiata externa however
the zona radiata interna was completely
digested by hatching enzyme. Increased salinity
of sand could be an inhibitor of hatching in
terrestrially incubating L. tenuis (Matsumoto
and Martin 2008). Delayed hatching in this
species could take place also if water does not
reach eggs during high tide – embryos can then
delay development inside egg to the next high
tide (Martin 1999; Martin et al. 2009). On the
other hand, constant immersion of F.
heteroclitus eggs in water caused a delay in
hatching in contrast to air-exposed embryos
(Tingaud-Sequeira et al. 2009).
Hatching problems are also noted among
some Pomacentridae, the elliptical eggs of
which attach to substrates. Chrysiptera
parasema embryos that do not invert properly
cannot hatch because the proximal end of the
egg is not pliable (Olivotto et al. 2003). Some
Abudefduf saxatilis embryos that began hatching
tail first were unable to complete the process;
however “a number of them did succeed” (Shaw
1955).
Helvik et al. (1991a) published a report
about a very specific cause of hatching
11
difficulties noted in H. hippoglossus. Hatching
gland cells form into a loop that gradually
migrates over the frontal part of the yolk sac as
the embryo develops. If this process is disrupted
or halted, then the loop remains small resulting
in too small a diameter of digested part of egg
envelope that made hatching impossible.
Unsuccessful hatching is an extreme
form of hatching abnormality, and it can result
from developmental problems or environmental
conditions such as water temperature, oxygen
saturation, salinity, or toxic substance content
that exceed permissible ranges.
Conclusions
Hatching head first permits larvae to
immediately escape and hide, while larvae that
hatch tail first are sometimes immobilized for a
period of time. Knowledge of how the larvae of
a certain species hatch permits making a more
realistic estimate of the danger posed by
predators at this step of development. It should
also be borne in mind that there might be
differences in hatching timing and method
between the same species developing under
natural and hatchery conditions. Adhesive eggs
are attached to vegetation or substrates,
therefore they remain in one position during
development of embryos. Also numerous non-
adhesive pelagophilic eggs sink at last to the
bottom and remain in one position. In
hatcheries, the adhesiveness is removed from
eggs and they are usually incubated in flowing
waters that generate constant movement. It is
also plausible that under controlled conditions
the water during incubation is better oxygenated
than it is under natural conditions. Perhaps this
reduces the frequency of embryonic movements
and perhaps the length of the development time
in the egg. It is difficult to confirm if hatching
enzyme is more efficiently distributed in the
perivitelline fluid by embryonic movements or
by the turning of the whole egg and if this has
an effect on the method and duration of egg
envelope digestion. The second important
difference between eggs incubated under natural
or commercial hatchery conditions is that eggs
with eliminated stickiness swell to larger size
or, depending on the method used, may swell
less. Significant differences in perivitelline
space volume that permit embryos to move
more or less freely definitely influence
development and possibly influence the
hatching of these species. Hence, incubation
technology may influence development,
improving conditions inside eggs (vide C.
carpio) or probably worsening it (vide V.
vimba). Although the hatching process is a
common one and much is known about it, many
aspects of it have yet to be explained and the
field for further study is wide especially as
concernes differences between hatchery
“produced” and naturally developed species.
Acknowledgments
I would like to express my sincere gratitude to Ewa
Kamler for her critical reading of the manuscript. I
warmly thank two anonymous reviewers who helped
to improve the manuscript. The study was supported
financially by project number S001 of the Inland
Fisheries Institute in Olsztyn.
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