Content uploaded by Laurent Bahou
Author content
All content in this area was uploaded by Laurent Bahou on Apr 11, 2017
Content may be subject to copyright.
I.J.A.B.R, VOL. 6(4) 2016: 476-487 ISSN 2250 –3579
476
REPRODUCTIVE BIOLOGY OF FEMALE FRIGATE TUNA AUXIS
THAZARD (LACEPÈDE, 1800) CAUGHT IN COASTAL MARINE WATERS
OF CÔTE D’IVOIRE
aLaurent Bahou, aCélestin Atsé Boua, bMarie-Anne d’Almeida and bTidiani Koné
aLaurent BAHOU, Département Ressources Aquatiques Vivantes, 1Célestin ATSÉ BOUA, Département Aquaculture, Centre de Recherches
Océanologiques, Rue des pêcheurs, Treichville, Tel. (225) 21355014 / Fax. (225) 21351155 BP V18 ABIDJAN, Côte d’Ivoire.
bMarie-Anne d’ALMEIDA, Laboratoire de Biologie Cellulaire, 2Tidiani KONÉ, Laboratoire d’Hydrobiologie, UFR Biosciences, 22 BP 582
Abidjan 22, Université Félix HOUPHOUET-BOIGNY, Côte d’Ivoire.
*Corresponding Author Email: lbahoucrothon@yahoo.fr
ABSTRACT
Some biological features (length-weight relationship, size at first sexual maturity, eggs variation in diameter, gonado-
somatic index, hepato-somatic index, somatic condition and fecundity) and histological characteristics of frigate tuna Auxis
thazard were studied. The study was carried out on 496 female fish caught in gillnets and measuring in size between 25
and 48 cm FL (centimetre Fork Length) collected from January to December 2004. The results indicated that female frigate
tuna reach maturity at 29.88 cm FL. Spawning started in June while females at stage IV numbered 36.36% but it lessened
in November. The peak value of gonado-somatic index, GSI (3.21 ± 0.93%), was attained in August and GSI thereafter
decreased gradually from September to December. There is a direct correlation between GSI and hepato-somatic index
(HSI), and an inverse correlation of these factors to the somatic condition (Kc). Absolute fecundity has linear relationship
with the weights of specimens (AF = -9.3792 + 0.5485хW) as well as with the weights of ovaries (AF = 136.11 +
13.416хOW). Eggs-frequency distribution within the maturity stages III (maturing or developing), IV (spawning), and V
(post spawning) were also shown in the study.
KEYWORDS: Absolute fecundity, Gillnets, Gonado-somatic index, Hepato-somatic index, Somatic condition.
INTRODUCTION
Frigate tuna (Auxis thazard) are epipelagic and neritic fish
(Collette and Nauen, 1983), yet scarcely migratory species
(Cayré et al., 1988). They are amongst the most important
commercial fishes targeted by a small-scale fishery
operating with canoes in continental shelf waters of Côte
d’Ivoire, a Western African country (Bahou, 2001; Bahou
et al., 2007). Several studies regarding the reproductive
biology of frigate tuna have been carried out in West
Africa (Caverivière et al., 1976; Alekseev and Alekseeva,
1980; Rudomiotkina, 1984). Long ago, previous studies
attributed to reproduction in frigate tuna the possibility to
occur in some West African marine waters with
temperature above 24°C (Frade and Postel, 1955; Conand,
1970). By implication, frigate tuna could mainly reproduce
in suchlike waters. However, observation of the gonadal
status of females and males frigate tuna along with
juveniles Auxis spp. ingested as prey by large tunas,
especially during the cool season when the Sea surface
temperature (SST) are usually the lowest between June
and October (Varlet, 1958; Verstraète, 1970; Morlière and
Rébert, 1972), led us to conclude otherwise. The overall
objective of the current study was therefore to investigate
the reproduction in frigate tuna in relation with
temperatures other than 24°C (between 22 and 29°C),
depending on marine-water-season and regardless of
cooling. A specific goal was to propose a maturity scale
based on histological observations of the female gonads, in
addition to macroscopic description.
MATERIALS & METHODS
Study area, Sample collection and SST measure
Specimens of the fish Auxis thazard were obtained from a
commercial small-scale fishery, in the manner described
by Bahou et al.(2007). Tuna were caught with gillnets of
25 and 35 mm mesh by a fishery that operated at night
with canoes powered by 40 hp motors, at the edge of the
continental shelf of Côte d’Ivoire (Fig. 1). In addition, the
Sea surface temperature (SST) were measured daily at 7
am, 11 am and 15 pm for their important role in the
distribution of species within a given area. For that
purpose, a thermometer was immersed for 10 mn in
seawater collected in a 5 to 10-liter capacity container, at a
suitable place. The procedure permitted using of an
average SST-value as a result of three thermometer-
readings each day.
Body measurements, macroscopically and histological
observations of gonads
Fish Fork Length were measured to the nearest centimetre.
Specimens were weighed to the nearest gram and their
ovaries and liver were weighed to the nearest milligram.
Sex and maturity stage were determined through
macroscopic observation of the gonads of dissected
specimens. Maturity stages were based on external
features (morphological appearance, colour, consistency,
resistance of gonads to pressing) and histological
examination. Ovaries are consisted of either symmetrical
or dissymmetrical sacs (lobes) joined to each other by
intermixed membranes and by a posterior ovarian end that
Reproductive Biol. of Frig. Tuna
477
seems to taper off. Ovaries removed from those females’
abdominal cavity were subdivided into two main groups.
The former, made up with ovaries whose eggs were visible
with the naked eyes (ovaries at stages III, IV, and V), were
used for the measurement of eggs’ diameters. Two
sections, each of 1 cm in length (the former from the
central part and the later from the upper extremity of
gonads), were taken from one single ovary and stored in
10% formalin. Intra-ovarian eggs diameter was measured
using an ocular micrometer. Ovaries that constituted the
second group were fixed in Bouin’s fixative for two
weeks, underwent a series of different ethanol
concentration baths (in order to rinse off the picric acid)
and then were embedded in paraffin. They were used for
histological examination. Sectioning of the gonads was
carried out. Sections were cleared in Xylene, impregnated
in liquid paraffin wax (melted at 52-60°C) and poured into
metal rectangular Lucas moulds. The moulds were placed
under running tap water to harden and positioned in the
microtome for trimming. The samples were sectioned at
approximately 7 μm width with a microtome. Hardened
wax trimmings housing the gonads were stretched out
properly. With the help of a clean slide, the stretched films
of gonads were picked and placed on hot plate for about
30 minutes to dry up so as to properly attach to the slide.
Each slide was passed through Xylene (for about 10
minutes) and through descending concentrations of
ethanol (95, 90, and 70%). Then, the preparations were
stained with hematoxylin-eosin and mounted using
Distrene Platicizal Xylene (DPX). Sections were observed
under a binocular microscope at various magnifications
and photographed. The internal structure of the ovary and
the developmental stages of eggs were classified
depending on the observations.
FIGURE 1. Map of the fishing area (the centre of the fishing area is approximately 4°80’N -5°10’N and 4°30’W – 4°W) (BAHOU et
al., 2007)
Fecundity
Fecundity was estimated using portions of ovaries, 1 g
each, taken from the central part of the ripe ovaries and
immersed in Gilson fluid for 2 weeks to harden (which
caused eggs to disaggregate). Those ripe ovaries were
taken from thirty-one gravid females harvested from June
to October. When the Gilson fluid had been filled up as to
reach 50 ml, it was shaken vigorously for a while to make
it homogeneous. That resulted in separated connective
ovarian tissues. Then 1 ml sample was taken with a
Pasteur pipette and put in a tinny receptacle. Thereafter,
eggs were manually enumerated and recorded. That
procedure was repeated three times to enable choosing of
mean values. Absolute fecundity (AF) was taken as the
number of ripe oocytes in the female gonad prior to
spawning. Relative fecundity (RF) was the number of
oocytes per kilogram of fish body weight (Wootton,
1979). Absolute fecundity was calculated as follows:
AF = Number of oocytes (No) × 50 × Total weight of
ovaries (TW)
Reproduction
Gonado-somatic index, Hepato-somatic index and Somatic
condition were calculated using the formulae:
)(var)( 100)(var OWweightyOTWweightTotal OWweightyO
GSI
,
Gibson and Ezzi (1980)
)(var)( 100)( OWweightyOTWweightTotal LWweightLiver
HSI
3
)(
100)(var)(
FLlengthFork
OWweightyOTWweightTotal
KC
,
Htun-Han (1978).
The relationship between the absolute fecundity and fork
length was estimated. The Length-weight relationship was
I.J.A.B.R, VOL. 6(4) 2016: 476-487 ISSN 2250 –3579
478
determined according to Ricker (1980). Female fish at
stages IV and V were chosen to determine the size at first
sexual maturity (LF50), ranging them into 1 cm size classes
and calculating their proportions. The Statistica 7.1
software (Statsoft, Inc.) made it possible to estimate the
mean size at first sexual maturity by fitting the logistic
function to the proportion of these mature fish. Such a
function fits in with logistic regression and the probability
associated with it satisfies the following equation:
)(1 )(
log)]([log p
p
pit
Another option to the logistic regression was
found through the utilization of the exponential function as
expressed by the equation:
)(
)(
1
)(
e
e
p
, where αand βare two
constants.
In such a case, the probability for p (X) was attributed to
mature females and the values in middle of size classes
referred to X. Mature females counted 50% as LF50 = -
α/β. Relationships between any pair of variables were
determined. Statistical analyses were performed using
Statistical 7.1 software while 0.05 was adopted as level for
significance.
RESULTS
Biological characteristics
The length-weight relationship determined for female
frigate tuna was W = 0.723×10-5 (FL) 3,206. (r2= 0.98),
suggesting allometric growth, the value of “b” (3.206)
being superior to the commonly referred value “3” (“t”
statistics, F = 3.24; t = 12.173). First sexual maturity was
attained at 29.88 cm FL (LF50 = 73.939/2.47428), referring
to the equation for the curve that led to its calculation (y =
exp (-73.939 + (2.47428)*x)/(1 + exp(-73.939 +
(2.47428)*x), where “y” represents the percentage for
mature individuals and “x” the size of these individuals.
Therefore, all females larger than 30 cm in length were
mature.
Figure 2 shows the monthly variation of the maturity
stages in female frigate tuna. Though present throughout
the year, individuals at immature and maturing stages
fluctuated in number each month, especially the former,
among which juveniles were numerous, reached higher
percentages from June to September. Females at stage III
have been observed in varying percentages, 48.00% and
8.82%, between April and October, respectively. Gravid
females (stage IV) got numerous from June (36.36%) to
November (32.26%). Though fewer in July (9.76%), post
spawners (stage V) increased in November (54.84%) and
December (55.17%). Individuals at resting stage VI were
observed from December (20.69%) to March (36.00%),
yet more numerous in January (51.85%).
FIGURE 2. Proportion of females frigate tuna Auxis thazard by maturity stage and month. St = stage; St I (immature); St II (early
maturing); St III (maturing); St IV (spawning); St V (post spawning and spent); St VI (recovery and resting adult)
Variation of the GSI is shown in Figure 3A. Gonado-
somatic index increased gradually from 0.91 ± 0.13% in
January to 1.25 ± 0.36% in April as ovaries scarcely
increased in weight during the recovery and resting adult
period. From a relatively higher value in May (GSI = 1.50
± 0.20%), the GSI reached a peak in August (3.21 ±
0.93%). GSI thereafter decreased untill December (GSI =
0.92 ± 0.19%). Variations in GSI made it possible to
determine four main phases in the course of the
reproduction of frigate tuna. These are the resting phase,
the maturation, the spawning, and the post spawning
phases (Fig. 3A). As shown in Figure 3B, the increase in
HSI was scarce from January to April (HSI = 0.427 ±
0.003%) but it reached a peak in August (HSI = 0.429 ±
0.003%). Overall, HSI showed the same trend as GSI did.
The somatic condition (Kc) showed a tendency to increase
from January (Kc= 1.71 ± 0.02%) to April (Kc= 1.72 ±
0.02%) and from July (Kc= 1.69 ± 0.03%) to November
(Kc= 1.72 ± 0.03%) (Fig. 3C). Temperature scarcely
increased from January (27.44 ± 1.48°C) to May (28.53 ±
1.48°C) yet steadily decreased untill August (22.14 ±
1.49°C) (Fig. 4). Following a decrease due to cooling of
water masses, an increase in temperature occurred from
September (23.06 ± 1.51°C) to November (27.71 ±
1.46°C). Temperature thereafter scarcely decreased in
December (27.49 ± 1.52°C). Sea surface temperature
variation resulted in four hydroclimatic periods, of which
the minor cool season (mCS, from January to February),
the main warm-water season (MHS, from March to June),
the main upwelling season or main cool season (MUS,
from July to October), and the minor warm-water season
(mHS, from November to December).
0
10
20
30
40
50
60
70
80
90
100
J F M A M J J A S O N D
Month
Maturity stage (%)
St VI
St V
St IV
St III
St II
St I
Reproductive Biol. of Frig. Tuna
479
J F M A M J J A S O N D
Spawning period
0.5
1.0
1.5
2.0
2.5
3.0
3.5
4.0
4.5
Gonado-somatic index (%)
Resting period
A
Post spawning
Maturation period
J F M A M J J A S O N D
Month
0.422
0.424
0.426
0.428
0.430
0.432
0.434
Hepato-somatic index (%)
B
J F M A M J J A S O N D
Month
1.66
1.67
1.68
1.69
1.70
1.71
1.72
1.73
1.74
1.75
Condition factor (%)
mCS MHS MCS mHS
C
FIGURE 3. Monthly variation of GSI, HSI, and Kcin female frigate tuna caught with gillnets in Ivorian shelf waters from January to
December 2004. mCS = minor cool season; MHS = main warm water season; MUS = main upwelling season; mHS = minor warm water
season
I.J.A.B.R, VOL. 6(4) 2016: 476-487 ISSN 2250 –3579
480
FIGURE 4. SST variation on continental shelf of Côte d’Ivoire throughout the study period from January to December 2004. mCS =
minor cool season; MHS = main warm water season; MUS = main upwelling season; mHS = minor warm water season.
FIGURE 5. Frequency distribution of eggs diameter in the ovaries of frigate tuna A. thazard at stages III, IV, and V
Reproductive Biol. of Frig. Tuna
481
Eggs length frequency distribution is shown in Figure 5.
There appeared to be much more eggs measuring in size
from 0.3 to 0.7 mm in ovaries at stage III than there were
in ovaries at stages IV and V (Figs. 5A, 5B, and 5C). In
addition, ovaries at stage IV predominantly contained eggs
that measured between 0.8 and 1.2 mm. Although ovaries
at stage V contained eggs measuring in size from 0.3 to
1.2 mm, eggs of 0.5 mm seemed to be more abundant
within them (Fig. 5C). Overall, each stage was
characterized either by one or by two eggs-size-classes in
which eggs measuring 0.5 or 1.0 mm proved to be the
most numerous. Absolute fecundity was estimated for
frigate tuna (Fig. 6). This species can spawn up to 305,000
and 891,000 eggs (mean value = 544,920 ± 161 eggs) in
females measuring in size between 33 and 45 cm FL.
Relative fecundity was estimated to be 470-666 eggs/g
(mean value = 539 ± 42 eggs/g). Absolute fecundity was
positively correlated with body weight of specimens
(Figure 6A), which suggests that fecundity is likely to be
greater in larger females than in small ones. Absolute
fecundity was also found to correlate with ovary weight as
shown in Figure 6B through the equation AF = 136.11 +
13.416×OW.
Macroscopic and histological characteristics of the
ovaries of frigate tuna
Macroscopically observation of ovaries on the basis of
external features along with histological examination of
ovarian cells moved us to distinguish six stages in relation
to six types of ovaries as follows (Figs. 7-12):
(i) The immature stage (I): Ovaries were cylindrical,
almost threadlike, with two tapering ends (Fig. 7A).
Immature stage was also characterized by a large amount
of oogonia and pre vitellogenic oocytes which were very
small and spherical cells, each with thin and indistinct
peripheral cytoplasm (Fig. 7B).
(ii) At the onset of maturation (stage II), ovaries increased
in size and they were pinkish in colour (Fig. 8A). This
stage showed primary oocytes that were mostly oval or
round. Two rows of these oocytes separated by interstitial
conjunctive tissue (ICT) are shown in Figure 8B.
FIGURE 6. Relationships between AF and TW (A), AF and OW (B) in female frigate tuna sampled from January to December 2004 at
Abidjan fishing port
I.J.A.B.R, VOL. 6(4) 2016: 476-487 ISSN 2250 –3579
482
FIGURE 7. Ovaries of an immature female Auxis thazard (stage I). (A) Overall appearance and localization of the two-thread-like
immature ovaries. (B) Cross-section of an immature ovary showing two lobes of germ cells, with an interstitial conjunctive tissue (ICT)
keeping them apart. We can see pre vitellogenic oocytes (pr) with their nuclei (N), cytoplasm (Cyt), and oocyte membrane (OM). (M ×
200) (Hematoxylin and Eosin). MAC = muscles of abdominal cavity ; OV = ovaries.
(iii) At the developing or maturing stage (III), nearly ripe
ovaries were orange yellow in colour, with bloody vessels
on their surface that are conspicuous (Fig. 9A). Eggs were
distinguishable with the naked eye when looking through
the ovarian membrane. The maturing stage was also
featured by vacuolization (i.e. appearance of vacuoles) and
by the appearance of the zona radiata as constituent of the
oocyte wall. The vacuoles were at first few in number and
small in size, yet scattered within the oocytes’ cytoplasm
(Fig. 9B). At this stage, oocytes measured 0.59 ± 0.13 mm
in diameter (mean size).
(iv). At the spawning stage (IV), ovaries reached
maximum development in thickness and width, which
undoubtedly made blood vessels on their surface more
conspicuous (Fig. 10A). Ovaries occupied the entire length
of the body cavity, almost leaving little portion for the
viscera to display. With the ovarian membrane getting
thinner, eggs became more distinguishable with the naked
eye. The belly of some individuals got so swollen that a
slight pressing on the belly generally made eggs release
out. Follicles, or eggs, increased in diameter and reached
maximum size (mean value = 1.04 ± 0.15 mm across the
long axis). The vacuoles increased in size and intermixed
with the yolk granules. Both vacuoles and yolk granules
scattered within the cytoplasm (Fig. 10B).
(v) At the spent stage (V), there appeared to be a discharge
of a considerable amount of ripe ovaries in the course of
spawning (Fig. 11A). Ovaries were severely flaccid and
collapsed, which caused them to decrease in weight,
compared to the ones at the preceding stage.
Vascularization was prominent, which moved the ovaries
to be reddish in colour, as is generally the case in fish at
such a stage. The spent period was also characterized
chiefly by the presence of empty follicles. The ovary also
displayed various peculiarities at this stage of the
spawning season. It may closely resemble the ripe ovary in
having mature follicles that are not yet released. Besides
atretic oocytes, empty follicles can be observed. The
discharge of ripe ovaries during the spawning period
resulted in numerous empty follicles being present within
the ovaries (Fig. 11B).
(vi) The recovery and resting adult stage (VI) is the stage
at which some ovaries were reduced in size. They could
easily be likened to ovaries at stage II, had they not
slightly been more vascularized after spawning (Fig. 12A).
New generation of small oocytes made their appearance.
The number of atretic oocytes and empty follicles
increased, which made this stage different from the
preceding stage V (Fig. 12B).
Reproductive Biol. of Frig. Tuna
483
FIGURE 8. Ovaries of female Auxis thazard at stage II (onset of maturation). (A) Overall appearance of the ovaries of a female frigate
tuna A. thazard at Stage II. (B) Cross-section showing details of the observation of ovaries of frigate tuna at Stage II. Appearance of
primary vitellogenic oocytes (Ost-1) in addition to pre vitellogenic oocytes (pr). (M × 200) (Hematoxylin and Eosin). MAC = muscles of
abdominal cavity ; OV = ovaries ; N =nucleus ; Ost-1 = primary vitellogenic oocytes ; pr = pre vitellogenic oocytes ; ICT = interstitial
conjunctive tissue.
FIGURE 9. Ovaries of a specimen Auxis thazard at stage III (maturation). (A) Characteristics of the ovaries of a specimen A. thazard at
Stage III. The ovaries (OV) are orange yellow, with blood vessels (BV) on their surface. (B) Cross-section of an ovary of frigate tuna at
Stage III showing eggs nearing onset of secondary vitellogenic division (Ost-II). (M × 250) (Hematoxylin and Eosin). MAC = muscles
of abdominal cavity ; OV = ovaries ; BV = blood vessels ; alv = alveoli ; Cyt = cytoplasm ; N = nucleus ; Ost-II = secondary vitellogenic
oocyte ; AF = atretic follicle ; TQ = theca ; Vac = vacuoles ; YG = yolk granules ; ZR = zona radiata.
I.J.A.B.R, VOL. 6(4) 2016: 476-487 ISSN 2250 –3579
484
FIGURE 10. Ovaries of a specimen Auxis thazard at stage IV (spawning, gravid female). (A) Overall appearance of the ovaries in a
mature specimen A.. thazard at spawning stage IV. (B) Cross-section of the ripe ovary of a specimen frigate tuna at spawning stage.
Vacuoles (vac), alveoli (alv), and yolk granules (YG) are mixed up and they scattered within the cytoplasm (Cyt). The nucleus (N)
occupies a central position. (M × 250) (Hematoxylin and Eosin). MAC = muscles of abdominal cavity ; OV =ovaries; N nucleus ; pr =
pre vitellogenic oocyte; Vac = vacuoles.
FIGURE 11. Ovaries of a specimen Auxis thazard at post spawning stage V. (A) Overall appearance of the ovary of a specimen A.
thazard at post spawning stage V. (B) Cross-section of the ovary of a post spawner showing in central position a secondary yolk stage
follicle (FO) with its nucleus (N). The follicular epithelium (FE) underwent invagination after spawning. Atretic follicles (AF), follicles
in resorption state (FR), empty follicles (EF), and post-ovulatory follicles (POF) can be seen. (M × 200) (Hematoxylin and Eosin). MAC
= muscles of abdominal cavity ; OV = ovaries ; BV = blood vessels; AF = atretic follicle ; FR = follicle in resorption state ; POF = post
ovulatory follicle; FO = mature follicle ; EF = empty follicle ; N = nucleus ; invaFE = invagination of the follicular epithelium ; pr = pre
vitellogenic oocyte.
Reproductive Biol. of Frig. Tuna
485
FIGURE 12. Ovaries of a specimen Auxis thazard at stage VI (recovery or adult sexual rest stage). (A) Overall appearance and
characteristics of the ovaries of a resting adult A. thazard. (B) Cross-section of the ovary of a specimen frigate tuna at resting stage. (M ×
200) (Hematoxylin and Eosin). MAC = muscles of abdominal cavity ; OV = ovaries. AF = atretic follicle; FR = follicle in resorption
state ; pr = pre vitellogenic oocyte ; recICT = reconstitution of the interstitial conjunctive tissue.
DISCUSSION
Length-weight relationship is one of the commonest ways
for determining the type of growth in fishes. That
relationship generally is exponential-like, fitting in with
the equation of Le Cren (1951). According to Fréon
(1979), the coefficient “b” of that equation which varies
between 2 and 4, yet close to 3 in many cases, is an
indication of the overall body shape of fishes. In frigate
tuna where the coefficient “b” is superior to 3, it does
indicate a faster increase of the fish in weight rather than
in length (See Micha, 1973; Ricker, 1980). Konstantinova
and Chur (1976) reported sexual maturity to be 30 cm FL
for females and males frigate tuna. Therefore, size at first
sexual maturity for female Auxis thazard obtained here
would appear to be of the right order by comparison with
these results. Furthermore, patterns in the variations of
GSI and HSI reinforce this assertion. In fact, in continental
shelf waters of Côte d’Ivoire, most of individuals Auxis
thazard are immature or are in adult sexual rest phase
from December to May. Gonad maturation phase, which
occurs as gonads’ weights reach 2% of body weight
(Postel, 1950; Frade and Postel, 1955), started in May but
lingered on untill July. Starting June, gravid frigate tuna
appeared in the fishery, although spawning got intensified
in August and lessened (or weakened) in November.
Therefore, GSI which expresses gonads’ tendency to
increase or decrease, depending on whether fish in
spawning condition are numerous or not, showed varied
amplitudes according to months, of which the ones from
June to November coincided with higher GSI values.
Patterns in the proportion of fish by maturity
developmental stage suggested that spawning took place
from June to November with fish in spawning condition
only being observed during this period. During the gonad
maturation phase (from May to July) females frigate tuna
undoubtedly fed actively in order for them to store up
energetic reserves within the liver. Hence, during that
period, both the GSI and HSI increased. According to
Htun-Han (1978), the increase in the GSI is generally
associated with accumulation of higher levels of proteins
and lipids within the gonads. In fact, before gonads in
general or especially ovaries get mature, they undergo
various morphological and physiological modifications
whose final result is to get the fish ready for spawning.
According to Koné (2000), in order for them to
successfully get their gonads mature, fatty-fish actively
feed and, thereby, store up energetic reserves within their
muscles, their perivisceral mesenteries and beneath their
skins. Those energetic reserves thereafter first reach the
liver and then the gonads so as to provide for the further
energetic needs of the fish in the course of the
reproduction. For those kind of fish, the peak of GSI
coincides with that of the HSI (Lahaye, 1980), as show the
results we obtained.
The condition factor has been mentioned as a measure of
the degree of fatness, that of gonad development and of a
suitable environmental condition with regard to the
feeding conditions (MacGregor, 1959). Decrease of the
condition factor during the gonad maturation phase shows
that frigate tuna at that period got thinner, possibly
because they scarcely fed intensely. Energetic reserves
stored up within the liver were being used because energy
supply from food consumption insufficiently compensated
for energy requirements from muscular origin, which
contributed to the lessening of the condition factor.
However, the increase of the condition factor from July to
November was due to the increase in weight of frigate
I.J.A.B.R, VOL. 6(4) 2016: 476-487 ISSN 2250 –3579
486
tuna as a result of heavy consumption of food favoured by
the plankton bloom at that period (Binet, 1993).
The presence of gravid frigate tuna from June to
November showed that the spawning occurred within a
temperature range of 27.56°C and 28.53°C (during the
warm water season). It did occur during the cool water
season at temperatures varying from 22.14°C to 25.15°C.
For example, in Senegal (a western African country), the
spawning period of frigate tuna occurs from June to
November, with temperature of superficial layers of the
seawater over 24°C (Frade and Postel, 1955; Conand,
1970). Temperatures we mention in our study are among
the ones frigate tuna larvae can bear. According to
Valeiras and Abad (2010), frigate tuna larvae are tolerant
of a wide range of temperature as they can live in waters
with temperature between 21.6°C and 30.5°C. Tunas in
general are known to be batch spawners (Cayré, 1984;
FAO, 2012). This implies that various eggs at different
developmental stages be observed within each ovary,
which gives way for eggs with different diameter to
display. Hence, in the course of reproduction, not all eggs
are released right away. Only eggs with maximum size of
about 1.04 mm are such-like ones. Albaret (1976) explains
the multiple spawning process. Within the spawning
period a cyclic process that will occur repeatedly over a
certain time sets in. After normal maturation, which occurs
from stage I to stage V, the ovary functions as if returning
back to the end of stage III or the onset of stage IV. This
occurs a certain time throughout the spawning season
(Albaret, 1976). Additionally, the presence of modes in
eggs frequency distribution was observed in tuna species
such as yellowfin (Thunnus albacares), skipjack
(Katsuwonus pelamis) and bigeye tuna (Thunnus obesus)
(See Cayré et al., 1988).
The bimodal eggs-frequency distribution revealed the
existence within the ovaries of more than a single cohort
of eggs awaiting discharge. In addition, the observation of
histological slides showed gradual phases in eggs growth
where the most evolved eggs (i.e. mature follicles) are the
ones that contain the most vacuoles. Vacuoles are tiny
holes where diverse inclusions store up. Vacuolization (i.e.
vacuoles occurrence) coincides with the developmental
phase at which peripheral vacuoles and zona radiata
coexist within the eggs. The zona radiata sustains the
oocyte’s (i.e. the egg’s) wall (Mohamed and Al-Absawy,
2010). Ovaries at post spawning and adult rest stages give
us much more insight regarding the type and
characteristics of the spawning of Auxis thazard. In fact,
ovaries at these stages enclose, besides atretic follicles and
follicles in resorption state, numerous tiny cells that are a
part of a new generation of eggs that are to be released
later. The existence of such a cellular arrangement lies in
the batch spawning that is peculiar to multiple spawners,
of which frigate tuna (Chur, 1972; Rudomiotkina, 1983;
Collette and Nauen, 1983; Valeiras and Abad, 2010).
Acknowledgements
The authors wish to thank the anonymous referees for their
valuable suggestions.
REFERENCES
Albaret, J. J. (1976) Reproduction de l’albacore (Thunnus
albacares, Bonnaterre, 1788) dans le golfe de Guinée.
Thèse de Doctorat 3iè Cycle, Biologie Animale –Zoologie
Expérimentale, Université Paris 7, 1976/11/10.
Alekseev, F. E. and E. I. Alekseeva (1980) Some problems
of reproductive biology of oceanic and neritic tunas of the
Tropical Atlantic. Collective Volume of Scientific Papers,
pp 695-703, ICCAT 9 (3).
Bahou, L. (2001) Les thonidés débarqués par la pêcherie
artisanale au filet maillant dérivant au port de pêche
d’Abidjan (Côte d’Ivoire). Mémoire de Diplôme d’Etudes
Approfondies, Université de Cocody.
Bahou, L., T. Koné, V. N'Douba, K. J. N'Guessan, E. P.
Kouamélan and G. B. Gouli (2007) Food composition and
feeding habits of little tunny (Euthynnus alletteratus) in
continental shelf waters of Côte d'Ivoire (West Africa) –
ICES J Mar Sci 64, 1044-1052.
Binet, D. (1993) Zooplancton néritique de Côte d’Ivoire,
in Environnement et Ressources aquatiques de Côte
d’Ivoire. Le Loeuff, P., E. Marchal and J. B. Amon
Kothias (eds.), pp 167-193, 1. Le Milieu Marin.
ORSTOM, Paris.
Caverivière, A. F., F. Conand and E. Suisse de Sainte
Claire (1976) Distribution et abondance des larves de
thonidés dans l’Atlantique tropico-oriental. Etude des
données de 1963 à 1974. Documents scientifiques du
Centre de Recherches Océanographiques, Abidjan,
ORSTOM, 7 (2), 49-70.
Cayré, P. (1984) Biologie et comportement du listao, in Le
Listao de l’Atlantique. Pianet, R., P. Cayré, F. X. Bard and
A. Fonteneau (eds.), pp 5-13, Extrait de « La Pêche
Maritime » 1274/1275.
Cayré, P., J. B. Amon Kothias, T. Diouf and J. M. Stretta
(1988) Biologie des thons, in Ressources, Pêche et
Biologie des Thonidés Tropicaux de l’Atlantique Centre-
Est. Fonteneau, A. and J. Marcille (eds.), pp 157-268,
FAO, Document Technique sur les Pêches 292.
Chur, V. N. (1972) Some biological characteristics of little
tuna (Euthynnus alletteratus Rafinesque, 1810) in the
Eastern part of Tropical Atlantic. Collective Volume of
Scientific Papers, pp 491-500, ICCAT, SCRS / 72 / 51,
Volume 1.
Collette, B. B. and C. E. Nauen (1983) FAO Species
Catalogue. Volume 2. Scombrids of the world. An
annotated and illustrated catalogue of tunas, mackerels,
bonitos and related species known to date. FAO Fish.
Synop. (125).
Conand, F. (1970) Distribution et abondance des larves de
quelques familles et espèces de poisons des côtes
sénégambiennes en 1968. Document Scientifique
Reproductive Biol. of Frig. Tuna
487
Provisoire du Centre de Recherches Océanographiques de
Dakar-Thiaroye, ORSTOM, (26).
FAO. 2012. FAO Fisheries and Aquaculture. Tuna and
tuna-like species group.
Frade, F. and E. Postel (1955) Contribution à l’étude de la
reproduction des Scombridés et thonidés de l’Atlantique
tropical. Rapport de Pêche V. Réunion CIEM, 137: 34-35.
Fréon, P. (1979) Relations tailles –poids, Facteur de
condition et Indices de maturité sexuelle : Rappels
bibliographiques, interprétations, remarques et
applications. Documents Scientifiques du Centre de
Recherches Océanographiques de Dakar-Thiaroye, 08,
114-171.
Gibson, R. N. and I. A. Ezzi (1980) The biology of the
scaldfish Arnoglossus laterna (Walbaum) on the West
Coast of Scotland. J Fish Biol 17, 565-575.
Htun-Han, M. (1978) The reproductive biology of the dab
Limanda limanda (L.) in the North Sea: gonado-somatic
index, hepato-somatic index and somatic condition. J Fish
Biol 13 (1), 369-378.
Koné, T. (2000) Régime alimentaire et reproduction d’un
tilapia lagunaire (Sarotherodon melanotheron Rüppel,
1852) dans la rivière Bia et le lac de barrage d’Ayamé
(Cöte d’Ivoire). Thèse de Doctorat, Katholieke University,
Leuven, Belgium.
Konstantinova, M. P. and V. N. Chur (1976) Comparative
biological characteristics of tunas of genus Auxis. Tropical
Atlantic Nauchno-Issled Institute, Rybn-Khoz,
Oceanography 65, 125-135.
Lahaye, J. (1980) Les cycles sexuels chez les poissons
marins. Cahiers ORSTOM,Série Océanographie 6 (7),
637-654.
Le Cren, E. D. (1951) The length-weight relationship and
seasonal cycle in gonad weight and condition in the Perch
(P. fluviatilis). J Animal Ecol 20, 201-219.
MacGregor, J.S. (1959) Relation between fish condition
and population size in the sardine (Sardinops caerulea).
U.S. Fish and Wildlife Services, Fish Bull 166, 215-230.
Micha, J. C. (1973) Etude des populations piscicoles de
l’Ubangui et tentatives de sélection et d’adaptation de
quelques espèces à l’étang de pisciculture. Centre
Technique Forestier Tropical, Nogent-sur-Marne, France.
Mohamed A, Al-Absawy EG. (2010) The reproductive
biology and the histological and ultrastructural
characteristics in ovaries of the female Gadidae fish
Merluccius merluccius from the Egyptian Mediterranean
Water. Afric J Biotech 9 (17), 2544-2559.
Morlière, A. and J. P. Rébert (1972) Etude hydrologique
du plateau continental ivoirien. Documents Scientifiques
du Centre de Recherches Océanographiques, Abidjan, 3,
1–30.
Postel, E. (1950) Note sur les thonidés de la presqu’île du
Cap Vert. Bulletin du Service Elevage Industriel et Animal
de l’Afrique Occidentale Française (2-3), 3-41.
Ricker, W. E. (1980) Calcul et interprétation des
statistiques biologiques des populations de poissons,
Bulletin Fish Res Board, Canada 32, 1369-1381.
Rudomiotkina, G. P. (1983) New data on reproduction of
Auxis spp. in the gulf of Guinea. Collective Volume of
Scientific Papers, pp 465-467, ICCAT, SCRS / 83 / 75, 15
(2).
Rudomiotkina, G. P. (1984) New data on reproduction of
Auxis spp. in the Gulf of Guinea. Collective Volume of
Scientific Papers, pp 465-468, ICCAT 20 (2).
Valeiras, L. and E. Abad (2010) Description de l’auxide
(FRI) / Biologie de la reproduction de Euthynnus
alletteratus. In : Mannuel ICCAT, Commission
Internationale pour la Conservation des Thonidés de
l’Atlantique, 1iè Édition (janvier 2010), Chapitre 2.1.10.3.
Description de l’auxide, pp 226-234./ Chapitre 2.1.10.5.
Thonine, pp 244-251. Dernière mise à jour : 4 septembre
2006.
Varlet, F. (1958) Le régime de l’Atlantique près
d’Abidjan. Etudes Eburnéennes 7, 97–222.
Verstraète, J. M. (1970) Etude quantitative de l’upwelling
sur le plateau continental ivoirien. Documents
Scientifiques du Centre de Recherches Océanographiques,
Abidjan, 1(3), 1–17.
Wootton, R. J. (1979) Energy costs of egg production and
environmental determinants of fecundity in teleost fishes.
Symposium of the Zoological Society, London 44, 133-
159.
