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Early Growth and Survival Rate of Hybrids from Male

Meagre (Argyrosomus regius) × Female Shi Drum
(Umbrina cirrosa) Compared to their Parent Species
Bilge Karahan*, Kutsal Gamsız, Emel Özcan Gökçek

Ege University, Fisheries Faculty, Aquaculture Department, Bornova,

35100 Izmir, Turkey

(Received 3.12.12, Accepted 8.2.13)

Key words: hybridization, heterosis, meagre, Argyrosomus regius, shi

drum, Umbrina cirrosa

Abstract
Growth performance and survival rates of hybrid meagre × shi drum and
purebred offspring of their parents were compared. Hybrids were produced
from eggs of hormone-induced shi drum females (Umbrina cirrosa), artificially
fertilized by frozen meagre (Argyrosomus regius) sperm. For comparison,
purebred offspring were obtained from both species by natural spawning from
hormone-manipulated breeders. Growth and survival were observed for 120
days after hatching. The hybrid offspring grew significantly faster than the
purebred. On day 120, the mean weights were 12±1 g for the meagre, 5±0.5
g for the shi drum, and 22±1 g for the hybrid juveniles. The mean daily
growth coefficients were 1.9 for the meagre, 1.3 for the shi drum, and 2.1 for
the hybrids. Estimations of growth heterosis, the extent to which the hybrids
outperformed their parent species, showed high hybrid vigor: heterosis for
mean weight was 159% and for daily growth coefficient was 31%. The
hybrids also had better survival rates than either of the purebred juvenile
populations: 49±0.03% for the meagre, 34±0.02% for the shi drum, and
78±0.02% for the hybrids. Therefore, heterosis for survival rate was 86%.
According to the growth performance and survival rate, crossing of these two
species is strongly suggested.

*Corresponding author. Tel.: +90-533-2474184, fax: +90-232-3883685, e-mail:

bilge.nomm@ege.edu.tr
2 Karahan et al.

Introduction
Mediterranean aquaculture is based on European sea bass and gilthead sea bream. Labor
costs in the Mediterranean area are high while prices of cultured fish are decreasing due
to surplus production. One reaction of aquaculturists is to diversify (Libertini et al.,
1998).
Hybridization is used to produce strains with desirable traits such as improved growth
rate and environmental tolerance or to transfer desirable traits such as induced sterility
and improved disease resistance from one species to another. Heterosis, the extent to
which a hybrid individual outperforms its parents with respect to one or many traits, can
be attained by crossing closely related species (Bartley et al., 2001; Lutz, 2001).
Production of hybrid fish constitutes a significant proportion of the aquaculture
production in some countries. For example, in Israel, tilapia are hybred (Oreochromis
niloticus X O. aureus) to produce predominantly male offspring and, thus, reduce
unwanted natural reproduction in growout ponds (Rosenstein and Hulata, 1993). Other
examples include hybrid striped bass in the USA, hybrid clarid catfish in Thailand, and
hybrid characids in Venezuela.
In this study two purebred drum species are of interest: meagre (Argyrosomus regius
Asso, 1801) and shi (Umbrina cirrosa Linnaeus, 1758), both of which are candidate
species for European and Mediterranean aquaculture. Meagre is commonly produced in
Italy, France, Spain, and Turkey (Gamsiz et al., 2008; Monfort, 2010) and has huge
culture potential due to its fast growth, FCR, environmental tolerance, and flesh quality
(Poli et al., 2001). Reproduction of meagre starts around the end of April when the
temperature reaches 19°C and lasts until the water temperature drops below 21°C. Shi
drum is widely distributed in the Mediterranean and Black Seas and in the eastern
Atlantic from the Bay of Biscay and Gibraltar to southern Morocco (Chao and Trewavas,
1990). It is a demersal fish that inhabits sandy and rocky bottoms in marine and brackish
coastal areas; in nature, it feeds on benthic invertebrates (Koumoundouros et al., 2005).
The shi drum reproduces from spring to the end of July when the water temperature
ranges 17-28ºC (Mylonas et al., 2004).
The purpose of this study was to compare growth and survival rates of male meagre
× female shi drum hybrids with purebred stocks of each parental species.

Materials and Methods

Base population. Parent shi drum and meagre breeders were caught in the east Aegean
Sea, pit-tagged, and kept in separate 30-ton tanks under a natural photoperiod. In May,
sperm was stripped from three male meagre and frozen until further use. Gonad
development of shi drum females was checked from the beginning of June until the end
of July. Females with oocytes that had a migrating germinal vesicle were selected for
hormonal manipulation and stripping.
Breeding and husbandry. Frozen meagre sperm (10 ml) was used to artificially
fertilize 1000 g eggs, obtained by hormonal treatment with 10 µg/kg LHRHa (Mylonas et
al., 2004). Eggs were mixed with the sperm for 30 s, then 2 l sterilized sea water was
added. After 2 min, the egg-sperm mixture was rinsed in sea water, floating eggs were
separated, and the percent fertilization was calculated. Three batches of 100 g fertilized
eggs, each, were incubated in 350 l black plastic tanks and covered to protect them from
light. Ambient sea water was gradually added to the tanks until the temperature
decreased from 24°C to 20.5°C and the salinity reached 30 ppt. After that, the water
exchange was regulated at 300% per day. The larvae were transferred to 4-ton
cylindrical tanks one day after hatching and held under the same environmental
conditions.
Three days after hatching, and as soon as the mouth opened, larvae started to be fed
algae and rotifers (Fig. 1). From day 7 to day 20, Artemia were provided together with
the rotifers and algae. The same protocol was used to rear purebred meagre and shi
drum offspring. Except that the hybrids were raised in smaller tanks, water conditions,
stocking density, light intensity and duration, etc., were the same for all groups.
 Growth and survival of male meagre × female shi drum hybrids 3

Data collection. Groups of meagre, shi-

drum, and hybrid offspring (n = 60 for each
of three replicate tanks) were weighed every
10 days from hatch to growout for 120 days.
Larvae were weighed in groups to reduce
sampling errors because it is impossible to
tag such small fish. The behavior of the
larvae in the tanks and their morphological
characteristics were observed. Growth was
evaluated by mean daily growth coefficient,
which is more accurate for differing sample
groups measured at different times than
weight gain and specific growth rate. Daily
Day growth coefficients give constant growth
Fig. 1. Rearing conditions (salinity, rates regardless of the live weight of the fish
temperature, feeding of algae, rotifer, and and the time interval used in the calculation,
Artemia) for larvae of purebred and hybrid thus its use for growth rate estimation in
meagre × shi-drum (Argyrosomus regius × aquaculture is recommended (Bureau et al.,
Umbrina cirrosa) larvae. 2000). The daily growth coefficients were
were calculated as 100(mean final body wt -
mean initial body wt)/days (Cho, 1992). Growth performance data were analyzed using
one-way ANOVA followed by the Duncan’s multi-comparison of means test (p≤0.05).
Data were transformed logarithmically to correct effects of non-homogenous initial
weights.
The hatching rate was defined as no. hatched eggs/total no. eggs. The survival rate
was calculated on day 120 as no. survived larvae/total no. hatched eggs. Heterosis was
assessed as 100(avg F1 hybrid - avg parents)/avg parents (Tave, 1986).

Results
Hatching rates between groups did not significantly differ (88±0.09%). The meagre × shi
drum hybrids were fusiform shaped like their purebred parents, but had marked
differences (Fig. 2). Meagre offspring had a large terminally-located mouth while the shi
drum mouth was subterminal. The hybrid’s mouth was also subterminally located but it
was larger than that of the shi drum.
Depending on the light intensity, meagre offspring swam near the tank walls as a
group and there was significant cannibalism among them. The shi drum swam close to
the corners and bottoms of the tanks, indicating that they were stressed but no
cannibalism was observed among the shi drum offspring. In contrast, the hybrids were
distributed homogeneously in the tanks and had nonaggressive behavior.
Data collection of weights began on day 25. The hybrids had the highest mean weight
on day 120 (Table 1). The hybrids grew faster than the purebred larvae while the
logarithmic weight gain of the hybrids was significantly higher than those of the parent
lines when the mean weights were corrected according to Log10 (Fig. 3). The logarithmic
weight gain was positively correlated with the initial larvae weight. The survival rate of
the hybrid offspring was significantly higher than those of the purebred populations and
the hybrids seemed to have better stress tolerance.

a b c

Fig. 2. Larvae of (a) meagre (Argyrosomus regius), (b) shi drum (Umbrina cirrosa), and (c)
meagre × shi drum hybrids.
4 Karahan et al.

Table 1. Traits of larvae from meagre (Argyrosomus regius), The meagre × shi drum
shi drum (Umbrina cirrosa), and meagre × shi drum hybrids. hybrids had high vigor in
Meagre × terms of growth and survival
Meagre Shi drum
Trait
purebreds purebreds
shi drum rate. The heterosis values
hybrids were significantly high for
Initial wt day 25 (g) 0.11 0.04 0.14
Mean wt day 120 (g) 12±1 5±0.5 22±1
mean weight (159%), daily
Daily growth coefficient 1.9 1.3 2.1 growth coefficient (31%),
Survival (%) 49 34 78 and survival rate (86%).

a b

Logarithmic mean growth (g)

Mean growth (g)

Day Day
Fig. 3. Mean (a) growth and (b) logarithmic growth of larvae of meagre, shi drum, and
hybrid meagre × shi drum from day 25 to day 120.

Discussion
Our study shows that viable offspring of male meagre × female shi drum perform better
than purebred offspring of their parent species. Improved growth rate is an especially
desirable trait for genetic breeding in aquaculture and results from the dominance
variance of one allele over another (Tave, 1986) and/or a higher number of polymorphic
loci that produces a higher level of heterozygosity. The existence of a positive genetic
correlation between these traits is possible and could be studied using molecular tools
and fixed optimized factors.
Domestication is another important trait that gives rise to fish that perform better
under culture conditions (Lorenzen et al., 2012). Cannibalism was reported amongst
meagre in the early life stages regardless of stocking density (Roo et al., 2010). In our
study, the hybrid offspring had lower stress with higher survival and better growth than
purebred offspring of their parents. In addition, observations of behavior indicate that the
hybrids were more domesticated than the purebred offspring. However, in some species,
survival rates and growth are better in purebred offspring than in hybrids (Henderson-
Arzapalo and Maciorowski, 1994; Wolters and DeMay, 1996). The heterosis values in our
hybrids were positive with significantly higher growth and survival rates than the
purebred offspring. In combinations of different strain or species, as in our study,
expression of heterosis is related to the genetic distance between the parent species and
results from the successful combination of common and imported alleles (Zak et al.,
2007).
Interspecies hybridization has been experimented with many marine and freshwater
species (Hulata, 1995a). Within freshwater species, the crucian carp × common carp
hybrid has shown sufficiently high performance to be cultured in significant quantities in
China (Vandeputte et al., 2008). A crossed line of Oreochromis aureus males × O.
niloticus females, with an extremely high proportion of males and high growth rates, is
commercially cultured in Israel (Rothbard, 1996). The most famous commercial crossed
anadromous fish is the hybrid striped bass. Morone species were hybridized with striped
bass, but none produced as successful results as the striped bass × white bass cross,
either as a sport fish or as a cultured species (Hodson, 1989).
There is a general impression that inter-species hybridization is not a good way to
improve fish. But at the same time, this method can be a tool to eliminate the negative
 Growth and survival of male meagre × female shi drum hybrids 5

effects of inbreeding caused by selective breeding or uncontrolled reproduction and other

genetic modifications. Indeed, one project examined the potential for exploiting the
hybrid vigor of heterosis for yield in Pacific oysters by crossbreeding inbred lines using
family selection (Langdon et al., 2003; Hedgecock and Davis, 2007). Especially in marine
culture systems, sterile fish resulting from interspecific hybridization may be preferred
due to concern that fish may escape into the marine and coastal environment (Dunham
et al., 2001). For example, the use of sterile salmon should be carefully appraised, given
its potential to reduce direct genetic effects of escapees on wild salmon populations
(Thorstad et al., 2008). Besides that, sterility may be an important quality for marine
aquaculture due to improved growth rates and overall performance in cage culture
(Hulata, 1995b).
In conclusion, hybridization is not the only method of genetic improvement but, as
seen in this study, it is a simple method that can produce immediate gains while selective
breeding studies require long periods and many generations. This study produced hopeful
results but several issues need to be considered before the results of this experiment can
be transformed into commercial scale production: the genetic structure of the broodstock
species, goals and possible gains, detailed profit and loss analysis. In addition,
interspecies hybridization often results in sterile offspring or diminished reproductive
capacity due to problems with gonad development or chromosome pairing (Bartley et al.,
2001). Thus, gonad development of the interspecies crossed line is also worth studying.

Acknowledgements
We would like to acknowledge that the study was supported by the two marine fish
hatcheries, Egemar A.Ş. and Akvatek Ltd.

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