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Fisheries Science
ISSN 0919-9268
Volume 81
Number 5
Fish Sci (2015) 81:891-897
DOI 10.1007/s12562-015-0901-8
Effect of temperature and salinity on
hatching and larval survival of yellowfin
tuna Thunnus albacares
Yang-Su Kim, Darys Isabel Delgado,
Ing.Amado Cano & Yoshifumi Sawada
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Fish Sci (2015) 81:891–897
DOI 10.1007/s12562-015-0901-8
ORIGINAL ARTICLE
Effect of temperature and salinity on hatching and larval survival
of yellowfin tuna Thunnus albacares
Yang‑Su Kim1 · Darys Isabel Delgado2 · Ing. Amado Cano3 · Yoshifumi Sawada1
Received: 26 October 2014 / Accepted: 2 June 2015 / Published online: 26 June 2015
© Japanese Society of Fisheries Science 2015
Introduction
Water temperature and salinity are crucial abiotic environ-
mental factors that have the greatest effect on the whole life
history of fish [1–3]. In particular, at embryonic and early
larval stages, water temperature and salinity independently
and/or interactively affect survival by influencing the phys-
iological state [4–7]. Previous studies have investigated
the optimal water temperature conditions (optimal values
ranged 23.3–31.0 °C) for yellowfin tuna Thunnus albac-
ares (YFT) eggs and larvae [8–10]. In addition, more than
22 mg/L of dissolved oxygen, between 1 and 2 × 10−8 m−2
s−3 of micro turbulence and 24 h lighting of photoperiod,
were reported to affect egg and larval survival and larval
growth [10–12]. However, the interactive effects of factors
such as water temperature and salinity remain to be inves-
tigated to explore the optimal environmental conditions for
YFT early life stages.
During early life stages, sensitivity to environmental fac-
tors have been described as species-specific and life stage-
specific in teleosts [2, 13, 14]. It is known that embryos of a
variety of fish species have a stronger tolerance for sudden
changes in water temperature and salinity at the stage of
complete closure of the blastopore than during the earlier
blastomere stage [15–22]. Therefore, sudden changes of the
environmental conditions of fertilized eggs before comple-
tion of the blastopore stage will adversely affect the hatch-
ing rate and larval development as compared to the use of
fertilized eggs after the blastopore stage. In addition, data
on environmental control for the improvement of the hatch-
ing rate and larval development will potentially be appli-
cable to high density intensive egg management systems
for mass larval production. Therefore, our study aimed to
contribute information on the suitable egg incubation and
early larval rearing environment for YFT for technological
Abstract Effects of temperature and salinity on hatching
rate and normal larval rate at hatching, and survival of fast-
ing larvae after hatching (survival activity index; SAI) were
investigated using spontaneously spawned eggs of captive
yellowfin tuna (Thunnus albacares, YFT). Within the range
of experimental temperatures, 23–35 °C, at 32 psu salinity,
hatching and normal larval rates and SAI were highest at
23 and 26 °C. In the experiment exploring the most suitable
salinity within the range 23–38 psu, 35 and 38 psu gave the
highest hatching rate and normal larval rate; however, SAI
was highest at 26 psu. The results of multi-factor experi-
ments in each temperature (23, 26, and 29 °C) with each
salinity (32, 35, and 38 psu) indicated interactive effects of
temperature and salinity on the three indices and within the
experimental ranges gave an optimal combination of 23 °C
and 38 psu for YFT hatching and survival.
Keywords Yellowfin tuna · Hatching rate · Normal larval
rate · Survival activity index · Temperature · Salinity ·
Interaction
Aquaculture
* Yang-Su Kim
yskim0535@gmail.com
1 Oshima Branch, Fisheries Laboratories, Kinki University,
Oshima, Kushimoto, Wakayama 649-3633, Japan
2 Aquatic Resources Authority of Panama, Bella Vista, Panama
City, Republic of Panama
3 Aquatic Resources Authority of Panama, Achotines
Laboratory, Las Tablas, Los Santos Province, Republic
of Panama
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892 Fish Sci (2015) 81:891–897
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development of tuna aquaculture and to obtain information
on tuna early life history. This study examined the rates of
hatching and normal larval development, and the survival
activity index (SAI) of YFT larvae by rearing under vari-
ous temperatures and salinities after the blastopore stage.
SAI values can be used as a practical indicator to evaluate
the larval tolerance to varying environmental conditions
[23–25].
Materials and methods
Broodstock and eggs collection
YFT fertilized eggs were obtained by spontaneous spawn-
ing in June 2011, May 2012, and October 2012 from wild-
caught broodstock maintained in a circulating cylindrical
tank (1361 m3 in volume) with re-circulating flow at the
Inter-American Tuna Commission’s Achotines Labora-
tory, located at the southern tip of the Azuero Peninsula
on the Republic of Panama’s Pacific coast. During the
spawning period, the broodstock were fed fresh sardines
and squid containing a vitamin mixture (Tuna Vitamin,
IATTC, USA) once a day (10:30). Temperature and salin-
ity during spawning were in the range of 28.3–28.8 °C and
31.7–32.0 psu, respectively. Fertilized eggs were collected
by a subsurface stationary plankton net and then were
transferred to 240 L circular incubation tanks at a density
of 300–350 eggs/L after rinsing and removal of sinking
eggs. Collected eggs were maintained in filtered seawater
within the same range of temperature and salinity as men-
tioned above. Approximately 11 h after spawning, eggs
developed to the Kupffer’s vesicle-disappearance stage
and were transferred to the seawater of each experimental
temperature and salinity treatment. This stage is soon after
the complete closing of the blastopore and has a stronger
tolerance to sudden changes of temperature and salinity as
mentioned above.
Experimental procedure
In the experiments, one hundred floating eggs on the water
surface of incubation tanks were transferred to 1 L beakers
filled with 800 mL of filtered seawater maintained at the
experimental temperatures and salinities. For the single fac-
tor treatment of temperature, treatments were adjusted to
23, 26, 29, 32, and 35 °C with a salinity of 32 psu (approxi-
mately equal to the spawning salinity at the Achotines
Laboratory). For salinity, it was adjusted to 23, 26, 29, 32,
35, and 38 psu with a temperature of 29 °C (approximately
equal to the spawning temperature at the Achotines Labo-
ratory). For the two-factor treatment of water temperature
and salinity, after considering the results of the two single
factor analyses, three different temperatures of 23, 26, and
29 °C were combined with three different salinities of 32,
35, and 38 psu for incubation. The experimental treatments
were carried out for each of the three spontaneous spawn-
ings. All single and two-factor experiments were conducted
in triplicate for each treatment. Water was not changed and
aeration was not conducted in beakers during the experi-
ment. Each experimental temperature was maintained by a
water bath using heaters (Seapalex300, Nisso, Japan) and
chillers (DSHP-4-WC, Aqua Logic Inc., USA), and each
salinity was maintained by using mixtures of artificial sea
salt powder (Sea life, Marine Tech Co. Ltd, Japan) and
groundwater (salinity ≤0.2 psu). The dissolved oxygen
saturation in the treated water was measured at the start
of egg stocking and after all dead larvae were collected;
the mean values for these stages were 83.8 ± 4.2 % and
83.1 ± 1.5 %, respectively.
Data calculation
In the larval SAI examination all the surviving larvae after
hatching were used to obtain the SAI value in the same
beakers as the incubation trials. From one day after hatch-
ing (DAH), all the larvae with morphological abnormalities
and dead larvae were carefully removed daily from each
beaker using a pipette and their number was counted. The
hatching rate, normal larval rate, and SAI were calculated
by the following equations [26]:
where N is total number of larvae, UE is the number of
unhatched eggs at 14 h after the start of hatching, M is
the number of morphologically abnormal larvae, hi is the
accumulated mortality by the i-th day and k is the number
of days elapsed until total larval mortality under fasting
conditions.
Statistical analyses
Percentage data are given as mean ± standard deviation
(N = 3) in the tables and figures. For all statistical analy-
sis, the percentage data (hatching rates, normal larval rates)
from each experiment were converted into arcsin % val-
ues. Hatching rates, normal larval rates, and SAI values
obtained in the single factor experiments were statistically
analyzed using one-way analysis of variance (ANOVA),
and values obtained in the two-factor experiment were ana-
lyzed using a two-way ANOVA (salinity and temperature
Hatching rate (%)
=
N/(N
+
UE)
×
100
Normal larval rate (%)
=
(N
−
M)/(N
+
UE)
×
100
SAI
=
k
i=1(N−hi)×i
N,
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893Fish Sci (2015) 81:891–897
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were both fixed factors). Where significant differences
(p < 0.05) in Levene’s test for homogeneity of variance
were found in any experiment by one- or two-way ANOVA,
the values of one-factor experiments were tested post hoc
by the Tukey test (p < 0.05). If a significant interaction
(p < 0.05) between temperature and salinity by two-way
ANOVA was observed, then the simple main effect in each
factor was analyzed to determine the individual mean dif-
ferences by the Tukey test (p < 0.05). All statistical analy-
ses were carried out using the IBM SPSS statistics program
version 20 (IBM SPSS Inc., Chicago, USA) for Windows.
Results
In the single factor experiment of temperature (conducted
at 32 psu salinity), the rates of hatching, normal larval
development, and SAI were significantly higher at 23 and
26 °C (Table 1), both of which were lower than the spawn-
ing temperature at the Achotines Laboratory (ca. 29 °C).
In the single factor experiment examining the effects
of salinity (conducted at 29 °C), salinities of 35 psu and
38 psu indicated significantly higher rates of hatching of
82.7 % and 95.6 % and of normal larval rate of 76.8 % and
92.2 %, respectively. As compared to those, at the salinity
of 23–32 psu, the hatching rate was 46.1–55.7 %, and the
normal larval rate was 10.6–40.4 % (Table 2). Furthermore,
the SAI was significantly higher at 26 psu (18.5) than other
salinities (≤11.0).
In the two-factor experiment conducted after analysis of
the results of the single factor experiments, temperatures
and salinities which showed higher hatching and normal
larval rates in the single factor experiment were selected for
testing; those were relatively lower temperatures of 23, 26,
and 29 °C, and relatively higher salinities of 32, 35, and
38 psu during YFT spawning. The highest rate of hatching
(100.0 ± 0.0 %) and normal larvae (99.7 ± 0.5 %) were
observed at 23 °C/38 psu among the combinations exam-
ined (Figs. 1, 2). Temperature, salinity, and their combi-
nations examined in this study were confirmed to have
Table 1 Hatching rate, normal larval rate, and survival activity index
(SAI) of yellowfin tuna under different temperatures
Data are shown as the mean ± standard deviation (N = 3). Mean val-
ues in the same vertical line with different superscript letters are sig-
nificantly different by Tukey’s test (p < 0.05)
* All the temperatures were examined at the salinity of 32 psu
Temperature
(°C)*
Hatching rate
(%)
Normal larval rate
(%)
SAI
35 16.5 ± 7.0d1.7 ± 1.6d1.2 ± 1.1c
32 38.1 ± 9.0c25.6 ± 8.4c9.0 ± 2.9b
29 74.9 ± 9.0b68.2 ± 7.7b11.5 ± 0.2b
26 94.5 ± 4.3a87.7 ± 5.8ab 19.0 ± 3.9a
23 100.0 ± 0.0a97.2 ± 4.0a23.7 ± 0.4a
Table 2 Hatching rate, normal larval rate, and survival activity index
(SAI) of yellowfin tuna under different salinities
Data are shown as the mean ± standard deviation (N = 3). Mean val-
ues in the same vertical line with different superscript letters are sig-
nificantly different by Tukey’s test (p < 0.05)
* All the salinities were examined at the temperature of 29 °C
Salinity
(psu)*
Hatching rate
(%)
Normal larval rate
(%)
SAI
38 95.6 ± 4.1a92.2 ± 2.7a8.5 ± 2.6b
35 82.7 ± 5.3ab 76.8 ± 8.4a9.6 ± 2.9b
32 55.7 ± 15.3b40.4 ± 14.4b5.3 ± 3.4b
29 46.3 ± 19.0b32.8 ± 12.9bc 11.0 ± 2.8b
26 48.7 ± 11.4b22.8 ± 9.4bc 18.5 ± 0.4a
23 46.1 ± 19.9b10.6 ± 3.4c8.4 ± 0.4b
Fig. 1 Hatching rate (%) of
yellowfin tuna under different
combinations of temperature
and salinity. Bars indicate
standard deviation (N = 3).
a, b, c Significant differences
between salinities within same
temperature (p < 0.05). A, B
Significant differences between
temperatures within same salin-
ity (p < 0.05)
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894 Fish Sci (2015) 81:891–897
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significant effects on the hatching and normal larval rates
by two-way ANOVA (p < 0.05, Table 3). Temperature
solely (p < 0.000), and combinations of temperature and
salinity (p = 0.032) significantly affected SAI (two-way
ANOVA, Table 3). Furthermore, at 23 °C significantly
higher SAI values than 29 °C were found without a signifi-
cant difference among the examined salinities by simple
main effect analysis (p < 0.05, Fig. 3).
Discussion
After completion of closure of the blastopore stage of many
fish species including Pacific bluefin tuna (PBT) Thunnus
orientalis [22], eggs are reported to have a higher toler-
ance to variations in environmental conditions compared
with the blastomere stage [15–21]. Though the effects of a
sudden change of incubation environmental conditions on
hatching and normal larvae rates in each development stage
Fig. 2 Normal larval rate (%)
of yellowfin tuna under different
combinations of temperature
and salinity. Bars indicate
standard deviation (N = 3).
a, b, c Significant differences
between salinities within same
temperature (p < 0.05). A, B
Significant differences between
temperatures within same salin-
ity (p < 0.05)
Table 3 Summary of two-way analysis of variance for the effects of
combinations of three temperatures (T) and salinities (S) on yellowfin
tuna hatching rate (arcsin %), normal larval rate (arcsin %), and sur-
vival activity index (SAI)
SS Sum of squares, df degrees of freedom, MS mean square
SS df MS f p
Hatching rate
T 1454.778 2 727.389 21.603 0.000
S 1548.538 2 774.269 22.995 0.000
T × S 831.916 4 207.979 6.177 0.003
Normal larval rate
T 1515.849 2 757.924 15.033 0.000
S 2125.943 2 1062.972 21.083 0.000
T × S 899.504 4 224.876 4.460 0.011
SAI
T 1259.975 2 629.987 44.146 0.000
S 19.063 2 9.532 0.668 0.525
T × S 192.120 4 48.030 3.366 0.032
Fig. 3 Comparison of yellowfin
tuna larvae survival activity
index (SAI) under different
combinations of temperature
and salinity. Bars indicate
standard deviation (N = 3). A,
B, C Significant differences
between temperatures within
same salinity (p < 0.05)
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895Fish Sci (2015) 81:891–897
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of YFT fertilized eggs have not been detailed in the litera-
ture, the effects may be similar to the observed results in
the congeneric scombrid species PBT [22]. In addition, as
a preliminary study [27] the observed egg development in
YFT fertilized eggs within the blastomere stage after fer-
tilization was rapid, and the required time to the Morula
stage (late cleavage) was just 1 h 10 min after fertilization
in 28 °C. From a YFT mass seeding production point of
view, the collection of blastomere stage eggs from a large
tuna broodstock tank or a net cage is considered to be diffi-
cult to enable the various procedures (eliminate impurities,
sterilization, rinse, removal of unfertilized eggs, counting,
etc.) for egg management as YFT eggs have a fast devel-
opment speed. Therefore, YFT fertilized eggs in the blasto-
mere stage which are assumed to have low environmental
tolerance may be unsuitable for egg management proce-
dures, and the obtained results of this study using Kupffer’s
vesicle-disappearance stage of YFT fertilized eggs would
be more appropriate for the various procedures for mass
YFT seedling production; however, this requires further
verification.
The optimal temperature range (23–26 °C) for hatch-
ing rate and normal larval development rate obtained in
this study was different from the previously reported one
for YFT by Harada et al. [8]. Harada et al. [8] obtained the
highest hatching rate (≥78 %, including dead and deformed
larvae) and normal larval development rates (≥58 %) at a
temperature range of 26.4–27.8 °C without information on
salinity. Although it is not possible to elucidate correctly
the cause of this difference, it may be attributable to differ-
ences in the experimental methods, e.g., differences in the
fertilization process (artificial and natural), stability of the
treatment temperature, whether the beakers were aerated
or not, the egg development stage at each treatment, and
differences between the broodfish groups used (genetic,
age, dietary factors, etc.). Regarding larval survival, the
SAI in our study was significantly higher at 23 °C (23.7)
and 26 °C (19.0) than for the other higher temperature
groups (1.2–11.5, Table 1). This optimal temperature range
(23–26 °C) obtained in this study is within the tempera-
ture range of the YFT spawning in the Central and Eastern
Pacific (21.5–30.5 °C) and the Western Pacific (24–29 °C)
where the main grounds of YFT fishing and spawning
occur [10, 28–31], and where YFT larvae are normally dis-
tributed (≥24 °C) [32–36]. In addition, the optimum tem-
perature range (23–26 °C) obtained in this study is within
the higher temperatures of the preferred temperature range
(20.5–25.8 °C) of adult YFT in the Atlantic, Pacific, and
Indian oceans [31], and it is at a slightly lower part of the
spontaneous spawning temperature range (21.5–30.5 °C)
in previous reports [9, 29] and is similar to the spawning
temperature range (24–25 °C) in the Western and Cen-
tral Pacific for YFT [30]. These indicate that the optimal
temperature for incubation of YFT fertilized eggs in this
study is in the intermediate range between the temperature
of the feeding area and spawning grounds, and this phe-
nomenon may be due to the evolutionary consequences of
the survival strategy for reducing energy consumption hav-
ing a long distance spawning migration behavior from the
feeding area to the spawning grounds.
Salinity of 35–38 psu gave the optimal range for hatch-
ing rate and normal larval development rates in this study,
and it was higher than that of broodstock spawning in Acho-
tines (≒32 psu). The previously proposed positive effect of
higher salinity during YFT embryonic development was
related to the prevention of their sedimentation and better
dispersion of floating eggs by increased buoyancy in the
higher salinity water [9, 37], which has a positive effect on
the survival of embryos and larvae [38]. Adverse effects
on hatching and normal larval development in the lower
salinity water has been reported in many other species
[39–41]. As one of the causes of this phenomenon other
than decreased buoyancy, some researchers have stated that
the low hatching rate in low salinity water is caused by the
induction of poorly developed tail musculature of embryos
resulting in difficulty for larvae to break away from the
egg chorion [4, 39]. The salinity in the YFT’s main habi-
tats (fishing grounds) and spawning grounds in the Pacific
and the Indian oceans is known to range 34.8–35.0 psu and
35.3–35.7 psu, respectively [28, 42]. These ranges are sim-
ilar to the optimum range observed in this study. Salinity
is known to affect the standard metabolic rate of hatched
larvae of many species through osmotic stress, and on lar-
val growth performance by the energy consumption for
osmoregulation [2, 3, 43, 44]. The highest SAI at 26 psu is
possibly better for YFT larvae to save energy expenditure
due to osmoregulation.
In the experiment for the combined effect of the tem-
perature and salinity, the hatching rate and normal larval
rate of 38 psu consistently showed the highest values as
compared to those of 32 psu and 35 psu regardless of the
temperature treatment, and the normal larval rate at 23 °C
was significantly higher than that at 29 °C. On the other
hand, the SAI was solely dependent on the water tempera-
ture and the SAI at 23 °C showed the highest value in all
the tested salinities. These results indicate that within the
ranges tested, the combination of 38 psu and 23 °C is the
most effective and optimal water temperature and salinity
combination for improving the hatching rate and increasing
the survival rate in the hatching of the YFT fertilized eggs.
Furthermore, the sensitivity to the temperature and salinity
during the embryonic period and that for hatching larvae
of YFT seem to differ among each life stage. That is, in
the embryonic period effects of combined temperature and
salinity occur, while hatching larvae are affected solely by
temperature (that is, relatively higher salinity tolerance than
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896 Fish Sci (2015) 81:891–897
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the embryonic stage). In terms of the YFT seedling produc-
tion, these results (preference for low water temperature)
may be applied to the development of technology to reduce
occurrences of mass mortality during the early larval stage
of tuna larvae [45]. However, Wexler et al. [10] found that
the water temperature range where fast growth of the YFT
larvae occurs is between 26 and 31 °C, and future studies
for reducing the gap between the improved survival rate
and the increased growth will need to be made.
Acknowledgments The authors would like to thank the staff of the
Achotines Laboratory of the IATTC and the staff of the Japan Inter-
national Cooperation Agency Panama Office for their cordial support
throughout the experiment. This study was supported by the Science
and Technology Research Partnership for Sustainable Development
(SATREPS) program of the Japan Science and Technology Agency
and the Japan International Cooperation Agency.
Appendix
See Figures 4, 5, and 6
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