Growth of juvenile striped seabream, Lithognathus mormyrus
(Teleostei: Sparidae) in the Adriatic Sea
Sanja Matić-Skoko, Josipa Ferri, Miro Kraljević and Jakov Dulčić
Institute of Oceanography and Fisheries; Meštrovićevo Šet. 63, P.O.Box. 500,
21000 Split, Croatia
Fax: +385 21 358 650
Corresponding author: sanja@izor.hr
Summary
Growth of juvenile Lithognathus mormyrus from the Duće Glava, eastern
Adriatic Sea, was analysed. A total of 2133 juveniles, ranging in total lenght from
0.8 to 10.3 cm, were caught. Most individuals (99.53%) belonged to the 0+ cohort.
The first settlers, aged 1.5-2.0 months, were recorded at the end of August.
Relationship between total length and weight indicates positive allometric growth
(b = 3.141). The condition factor, as a consequence of length-weight relationship,
was CF = 1.245. The Gompertz (c = 0.080 mm day-1; R2 = 0.962) and linear
equation (c = 0.051 mm day-1; R2 = 0.956) seem to be the most appropriate for the
description of young L. mormyrus growth.
Introduction
The larval period is profoundly important in the life of fishes. During this
time the new cohort is reduced dramatically to the rare survivor that goes on to
reproduce and add to the population’s persistence (Jones, 2002). Growth which
estimation can provide a descriptive parameter of the conditions surrounding a
population (Planes et al., 1999), is the most sensitive parameter to enviromental
1
conditions (Weatherly and Gill, 1987). Using the analysis of size-frequency
distributions (Barry and Tegner, 1989), growth of juveniles can be estimated from
the increase of the mean size of fish in a “cohort” within year-classes (Planes et
al., 1999). Different growth models can be used to construct growth curve. Data
on juvenile fish growth rates are still scarce in the literature, although they are
crucial for a better understanding of species population dynamics (Lasker, 1985).
The striped seabream Lithognathus mormyrus is a demersal marine fish
belonging to the Sparidae family. It is widely distributed in the Mediterranean
(absent in the Black Sea), Atlantic (from Bay of Biscay to Cape of Good Hope),
Red Sea and southwestern Indian ocean (Bauchot and Hureau, 1986), occurring
predominatly over unvegetated sand habitats (Guidetti, 2000). L. mormyrus is a
gregarious species, entering exceptionally in coastal lagoons (Suau, 1970;
Tortonese, 1975). In spite wide distribution, juvenile striped seabream has never
been the object of intensive investigation. Majority of published studies deal with
aspects of adult L. mormyrus reproduction, age and growth so these have been
studied in the central–east Atlantic (Lorenzo et al., 2002; Pajuelo et al., 2002), in
eastern Spanish coastal waters (Suau, 1955, 1970), in Thracian Sea, Greece
(Kallianiotis et al., 2005) and in the northern and middle Adriatic Sea (Kraljević
et al., 1995; Kraljević et al., 1996). Froglia (1977), Jardas (1985) and Badalamenti
et al. (1992) studied feeding habits of adult striped seabream. It is also known that
fecundity of L. mormyrus greatly increased from May to June, reaching a
maximum at the beginning of June (Suau, 1970) and that this species is a
proteandric hermaphrodite (Besseau, 1990). However, nothing is known about the
2
growth of juvenile striped sea bream in the Adriatic Sea and other areas of its
wide distribution.
Therefore, the aim of the present work was to estimate growth of juvenile
L. mormyrus from the Croatian waters, and to test different models for estimating
juvenile fish growth.
Materials and mathods
Duće Glava (43°26′3″N 16°41′E) is a small south-facing sandy beach on
the Croatian Adriatic coast (~ 20 km south of Split) within the River Cetina
estuary. The sampling area was characteristically sandy and partially overgrown
with Cystoseira barbata and Ulva rigida.
Samples were collected monthly from April 2000 to March 2001. Fish
samples were collected using a 22 m long beach seine with wings of 7.5 m and
central collecting area of 7 m. The outer wings were of 4 mm mesh size and the
central sac of 2 mm. The net was always hauled from the depth (max. 2 m depth)
to the shallow. Collected striped seabream juveniles were preserved in 4%
buffered formalin, identified according to Jardas (1996).
Due to the time of spawning and the period of intensive settlement,
together with the duration of the larval stage of life (Raventos and Macpherson,
2001), which varies between one and two months, July 1st was assumed to be the
birth date of striped seabream. Age in months was determined as the difference
between the date of capture and the birth date. In the present paper, the term
“cohort” was used to describe groups of L. mormyrus of similar size, identified
monthly in each lenght-frequency distribution.
3
Empirical total size-frequency distributions were used to construct an agelenght key with 3 mm lenght intervals. The commonly used lenght-weight
relationship (W=aLtb) and condition factor (CF=100WLt-3) were applied (Ricker,
1979). Several growth models were tested: linear (Lt=a+ct), exponential (Lt=aect),
logarithmic (Lt=cLn(t)-a), parabolic (Lt=ct2+bt+a), von Bertalanffy equation
(VBGC) (Lt=L∞[1–e-c(t-t 0 )], Beverton and Holt, 1957) and the generalised
Gompertz growth equation (Lt=L∞e–be[exp-c
t)]
), Ricker 1979). Abbreviations in
upper equations are: Lt = total length (cm) at age t; L0 = total length when t = t0;
L∞ = asymptotic length (cm) at the end of the first growth season (Katsuragava
and Ekau, 2003); c = instantaneous growth rate when t = t0; t = age (months from
birthday or settlement); a, b = constants.
The equation was fitted (all individuals included) by an iterative method
with a non-linear (user specified) subroutine (StatSoft, 1996). Calculation of
determination coefficient (R2) provided a measure of goodness-of-fit (Sokal and
Rohlf, 1981).
Results
A total of 2133 juveniles of L. mormyrus, ranging from 0.8 to 10.3 cm Lt,
were analysed (Table 1). Most individuals (99.53%) belonged to the 0+ cohort.
First juveniles of L. mormyrus were sampled (962 individuals, 45.10% of the total
sample) at the end of August (August 28th), and ranged in length from 0.8 to 1.6
cm. The total weight of these individuals ranged from 0.01 to 0.13 g. According to
the spawning period of striped sea bream, their estimated birth date (July 1st) and
the duration of the larval stage, these individuals were probably 1.5 – 2.0 months
4
old. Juveniles of L. mormyrus were caught throughout the year and they left this
area mostly in June. Older individuals (>1+) were recorded in February, March,
April and June.
The slope (b = 3.141, R2 = 0.996) of the total length-weight regression
indicated positive allometric growth. By analysing values of b through length
frequencies, 3 periods of negative allometric growth have been determined (Table
2). The condition factor, as a consequence of the length-weight relationship, was
CF = 1.245. Linear regression of the mass and length logarithm values for every
length group hasn’t provided the uninterrupted order of dots lying on one straight
line. It has, actually, provided few fractures, or straight lines corresponding to the
physiological changes during the early stages of the striped sea bream (Fig. 1).
The results of using several different growth models are presented in Table 3. All
tested models gave different results. Among them, age length data of the juvenile
striped sea bream were well described by the growth curve of the Gompertz (c =
0.080 mm day1; R2 = 0.962; Fig. 2) and linear equation (c = 0.051 mm day-1; R2 =
0.956; Fig. 3).
Results of the growth increment analysis showed that growth rate of
juvenile L. mormyrus increased during the first five months of life although in the
period after settlement, in September, slower growth rates were noted. After first
five months, in January (mean 12.33°C) and in February (mean 12.31°C), the
limited growth was noted. In the period after February, new growth increment was
recorded. The growth slope was highest in October (Fig. 4a). Therefore, few
inflection points were evident, indicating the sigmoid growth of juvenile L.
mormyrus. The Gompertz and von Bertalanffy models, as usually used, fit the
5
data very well in first five months of life. After that period, Gompertz model
overestimated growth in comparison with the real growth slope less then the von
Bertalanffy model underestimated growth (Fig. 4b). The real growth slope was
calculated according to monthly mean length values of the cohort.
Discussion
Growth models are necessary for describing the development of one or a
number of populations and interactions with the environment. The choice of an
appropriate growth model depends on which species is being studied and also on
the aims of the study or the research possibilities (Gamito, 1998). There are
numerous contradictory studies dealing with the use of appropriate models for
estimating juvenile growth.
Analysing the results obtained by applying several growth models to
juvenile striped seabream, during the period after settlement, we found that the
Gompertz (c = 0.080 mm day-1; R2 = 0.962) and linear equation (c = 0.051 mm
day-1; R2 = 0.956) best described juvenile growth of this species according to R²
and its biology. We have already proposed Gompertz equation for this purpose
(Matić, 2001, Matić-Skoko et al., 2004, Matić-Skoko et al., 2006) and it has been
previously recommended by several authors (Regner, 1980, Monteiro, 1989,
Andrade, 1992; Gamito, 1998). On the other hand, Planes et al. (1999) have
recommended linear model for juveniles from Diplodus genus, and while this
model gave us relatively good estimation of growth for young L. mormyrus, for
other tested sparids obtained results in terms of the determination coefficient were
not acceptable. The von Bertalanffy growth equation is widely used for estimating
6
growth of adult individuals. However, the VBGC give poor adjustment in the case
of this species by underestimating the value of growth slope during whole
investigation period. The VBGC has the disadvantage of not being accurate for
describing first growth years with exception for species, which estimated t0
doesn’t differ from zero, such as Diplodus annularis (Gordoa and Molí, 1997).
For species with t0 different to zero, Gordoa and Molí (1997) recommended use of
the exponential model. But, obtained curves by both, exponential and logarithmic
models didn’t follow real growth of analysed species. As a conclusion, a
combination of Gompertz equation to describe the first year of growth, with the
seasonal von Bertalanffy model to describe the following years, might be the
outlet for an adequate description (Gamito, 1998).
There is a lack of information about growth of juvenile fish species based
on Gompertz models in the literature. Using the Gompertz model, Pallaoro et al.
(1998), estimated the growth rate of Oblada melanura to be 0.083 mm day-1 and
Gamito (1998) found that Sparus aurata has a growth rate of 0.003 mm day-1.
Matić-Skoko et al. (2004) reported about relatively slow growth of juvenile
salema, Sarpa salpa (0.047 mm day-1) in the Adriatic, and it is due to the fact that
salema settled from ichthyoplankton in November and spent the whole winter in
shallow coves with lower temperatures than the open sea. Slower growth of
Diplodus puntazzo (0.038 mm day-1) than that of Sarpa salpa can be attributed to
the lack of smaller and larger specimens in the sample (Matić-Skoko et al., 2006).
Planes et al. (1999) estimated growth rate of sparid juveniles of the genus
Diplodus using a linear model and their values are for D. vulgaris c = 0.202 mm
day-1 and D. puntazzo c = 0.160 mm day-1. However, it is not recommendable to
7
compare directly growth slopes of different species. The differences in size at age
and evident growth rate may be result of methodology imperfections caused by
use of small beach seine, slower growth in relatively colder Adriatic Sea (MatićSkoko et al., 2006) or wrong age interpretation. For that reason, the otolith
techniques, which can give us more precise information about the duration of
juvenile stage, are welcomed and proposed by Villanueva and Molí (1997).
On this sampling area, surface water temperatures follow seasonal cycle
with a maximum in July (23.0°C) and a minimum in February (12.3°C). D.
puntazzo, D. vulgaris and S. salpa, which spawn in autumn (Matić, 2001),
exhibited lower growth than, related species, such as Diplodus sargus settling in
May (Matić-Skoko et al., 2004) and striped seabream settling in August. So,
growth is directly and indirectly related with temperature fluctuations.
Analysing the values of b through length frequencies, 3 periods of
negative allometric growth have been estimated, and they can be connected with
periods in the first year in life of juvenile striped sea bream. First period of
negative allometric growth was determined in September (Lt=0.6-2.5 cm) in the
phase of initial adaptation. Next period (Lt=5.6-7.5 cm) was related to wintertime
and low mean temperatures (12.3°C). Finally, third period of negative allometric
growth (Lt=9.6-10.5 cm) fitted the process of recruitment related with movement
from this shallow area and association with adults in deeper waters. Disharmony
phases represent crucial periods in the growth of the species. By linear regression,
three disharmony phases have been estimated in early life of juvenile striped
seabream. Those three phases are settlement, initial adaptation and recruitment,
8
and they are connected with three periods of negative allometric growth and
growth increment analyses, also previously mentioned.
Settlement intensity of L. mormyrus juveniles in area of Cetina Estuary
was highest at the end of August suggesting there was no bigger differences in
time when majority of settlers entered in shallow. Knowing the spawning period
of this species on the eastern coast of the Adriatic Sea (Kraljević et al., 1995), it
comes out that settlement occurred on whole Adriatic area in almost the same
time. Consequently, this small difference in settlement shouldn’t have influence
growth.
Furthermore, only ten adult specimens were found in the investigated area,
pointing out that juvenile L. mormyrus do not compete with adults for habitat.
These juveniles recruited in very shallow water forming a small number of
monospecific shoals. Macpherson (1998) reported that monospecific shoals of
such juvenile sparids never mix with the shoals of adults if they were present in
the nursery area.
Number of L. mormyrus specimens declined from one month to the next
one, especially after December when sea temperatures drastically fall down. We
presume that most of these individuals have been recruited at about 6-7 cm of
total length, changing cold shallow waters for deeper habitats with more stabile
conditions. Also, smaller individuals cannot be retained in codend while older,
more agile individuals are more capable to avoid net. Therefore, the impacts of
sampling by small beach seine on the success of the recruitment have to be clear
away. Consequently, using a technique less destroying such as visual census will
be more acceptable. Only difficulty may show in size estimation of smaller
9
individuals in first few months after settlement (2-3 cm of total length). In
addition, such high decrease of sampled individuals after December may result
from natural mortality due to predation (Bailey and Houde, 1989) or starvation.
Juveniles that stayed in this shallow area until next summer probably were too
small or exhausted to left shallow waters with others in December.
There are at least two reasons for the fast juvenile fish growth as this of L.
mormyrus: predator avoidance and earlier sexual maturity achievement. For this
species hypothesis “the bigger is better” given by Bailey and Houde (1989) seems
to be true. It is evident that earlier recruitment, after age of five or six months, is
achieved as a predator avoidance strategy or looking for “calmer” habitat instead
of daily and seasonally varying estuarine areas because L. mormyrus spawned
after second year of life (Kraljević et al., 1995). Shallow waters of Duće area are
inhabited by species of total length around 20–40 cm (Sparids, Labrids, Mugilids)
and since maximal vulnerability was attained when the relative size of the fish
larvae was 10% of the predator size (Paradis et al. 1996), it is crucially important
for L. mormyrus juveniles to reach lengths of over 40 mm as soon as possible.
Future studies should try to determine growth patterns modifications of
species at different stages of development caused by different habitat conditions,
as was previously proposed by Gordoa and Molí (1997). It is also very important
to incorporate juvenile growth into studies of adult population growth.
Acknowledgements
10
The authors gratefully acknowledge to Ministry of Science and
Technology of Republic Croatia for the financial support of this study through the
project “Adriatic”. Also, we want to acknowledge dr. Melita Peharda (IOR,
Croatia) for her efforts in English editing.
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TABLES
1. The length frequency distribution (with 3 mm intervals) of juvenile L.
mormyrus in
Croatian waters
2. The results of analysing allometric growth through length frequencies for
juvenile L.
mormyrus
3. The results of using several different growth models for juvenile L. mormyrus
16
FIGURES
1. Disharmony phases during the early stages of the striped sea bream
2. Gompertz growth curve of juvenile L. mormyrus from the Adriatic Sea
3. Linear growth curve of juvenile L. mormyrus from the Adriatic Sea
4. A. The monthly growth increment analysis of juvenile L. mormyrus; B.
Comparison of the real (■) (by monthly mean length), Gompertz (♦) and von
Bertalanffy (▲) growth curves of juvenile L. mormyrus
17