Optimal period for the effective promotion of initial swim bladder inflation in yellowfin tuna, Thunnus albacares (Temminck and Schlegel), larvae

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SHORT COMMUNICATION
Optimal period for the effective promotion of initial swim
bladder inflation in yellowfin tuna, Thunnus albacares
(Temminck and Schlegel), larvae
Tomoki Honryo
1
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Michio Kurata
1
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Angel Guillen
2
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Yoshiki Tamura
3
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Amado Cano
2
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Maria S Stein
4
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Daniel Margulies
4
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Vernon P Scholey
4
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Yoshifumi Sawada
1
1
Oshima Station, Aquaculture Research Institute of Kindai University, Wakayama, Japan
2
Aquatic Resources Authority of Panama, Wakayama, Republic of Panama
3
Department of Fisheries, Faculty of Agriculture of Kindai University, Nara, Japan
4
Inter-American Tropical Tuna Commission, La Jolla, CA, USA
Correspondence
Tomoki Honryo, Oshima Station, Aquaculture Research Institute of Kindai University, Wakayama, Japan.
Email: t.honryo@kindaisuiken.jp
Present address
Angel Guillen, Open Blue Sea Farms, Panama, Panama
Funding Information
JST (Japan Science and Technology Agency); JICA (Japan International Cooperation Agency)
Keywords: mortality, surface-adhesion death, survival, swim bladder, yellowfin tuna
Many physoclistous fish larvae including yellowfin tuna (YFT), Thun-
nus albacares and Pacific bluefin tuna (PBF), Thunnus orientalis
inflate their swim bladder by gulping air at the water’s surface for
initial swim bladder inflation (ISI) (Honryo et al., 2016; Kurata et al.,
2012). The time period, or ‘window’, for larvae to gulp air for ISI is
finite, brief and occurs in the early larval stages with a physosto-
mous swim bladder. Oily surface films in rearing tanks can arise
from enriched rotifers introduced as food and leaching from
microalgae added to tanks; the surface films can inhibit larval ISI
success via impeding gulping air (Honryo et al., 2016; Kurata et al.,
2012). Failure to inflate the swim bladder results in the reduction
of growth, survival and vertebral deformation which have an impact
on seedling production (Chatain, 1989; Kitajima, Watanabe, Tsuka-
shima & Fujita, 1994). Mortality due to surface-adhesion death is
serious for tuna larviculture and can be prevented by creating an
oil film on the rearing water’s surface (Miyashita, 2002). However,
this countermeasure becomes a dilemma when the period of high
surface-adhesion death overlaps with the window as in PBF in
which both periods overlap at 3 days post hatch (Kurata et al.,
2012). In YFT larvae, it is still unclear whether the same dilemma
exists as it does in PBF. Ecological experiments with YFT larvae
have been conducted by the IATTC for many years (Margulies,
Scholey, Wexler & Stein, 2016), but larviculture aspects of YFT
rearing have not been emphasized to date. Hence, this study was
designed to examine the effect of the period of skimming of sur-
face film on ISI to determine the optimal period to effectively pro-
mote ISI, and on occurrence of surface death in YFT larvae.
Survival of larvae was also estimated during the study.
The experiment was conducted at the Inter-American Tropical
Tuna Commission’s (IATTC’s) Achotines Laboratory in the Republic
of Panama. Yolk sac larvae were randomly stocked into twelve
1000-L tanks (dark green colour wall and 135 cm in internal diame-
ter, 1.3 m
2
and surface area) at a density of 6.9 larvae/L. In order to
elucidate the optimal period for surface skimming to promote ISI, we
began surface skimming at four different ages of the larvae: 3 dph
(SF3D), 4 dph (SF4D), 5 dph (SF5D) and 6 dph (SF6D). Each treat-
ment was conducted in triplicate. The experimental duration was
from 3 to 7 dph when the proportion of swim bladder inflation
reached a plateau in previous studies and all surviving larvae were
counted at 8 dph; the survival was estimated for each tank after
adjusting for previous sample removals (Margulies, 1989). A few
drops of fish oil (Ueda oils and fats MFG. CO., Ltd, Hyogo, Japan)
Received: 17 October 2016
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Revised: 22 February 2017
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Accepted: 10 March 2017
DOI: 10.1111/are.13355
Aquaculture Research. 2017;1–4. wileyonlinelibrary.com/journal/are ©2017 John Wiley & Sons Ltd
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were added to each experimental tank every day and night to cover
the water surface. Surface skimmers (20 cm 945 cm, rectangular
shape with an air blower trap) settled near the tank wall were uti-
lized during photophase from 0600 to 1800 hours (12 hr), and sur-
face skimming was conducted in three-hour interval under a 12-hr
light and 12-hr dark cycle. Air diffusers (100 mm long, 23 mm diam-
eter) were placed at the tank bottom; nighttime aeration was
increased to 1.0 L/min, while daytime aeration was maintained at
0.3 L/min. These air flow rates were controlled using a flow meter
(KOFLOC, Kyoto, Japan). Daytime light intensity was measured at
4,000 lx in the centre of each tank at the water surface provided by
fluorescent bulbs hung above the rearing tank (wavelength was not
measured). Sand-filtered UV treated sea water was added to the
rearing tank from a water inlet placed near the tank wall just below
the water surface. Water was discharged from the centre of the tank
bottom through a 500 lm-mesh screen. Rearing water was
exchanged at the rate of 1000 L/day. Enriched (Algamac 3050,
Aquafauna Bio-Marine, Hawthorne, CA USA) rotifers were fed daily
at a density of 8–10 rotifers/mL, and cultivated fresh Nannochlorop-
sis oculata was also added at cell densities between 0.5 and
1.0 910
6
cells/ml. Water quality parameters were monitored twice
a day and were similar among treatment (Table 1.). At 3, 4, 5, 6 and
7 dph, 15–20 larvae were randomly collected from 0 to 20 cm depth
in each tank at 21:00 (3 hr after darkness) to determine the propor-
tion of larvae with inflated swim bladders using a microscope
(SZX16, Olympus, Tokyo, Japan). The fish that died and were discov-
ered at the water’s surface were removed and counted every day at
two-hour interval to determine the daily frequency of surface
deaths. Mortality due to surface death (%) was calculated from the
formula: total number of dead fish removed from rearing water’s sur-
face/total number of dead fish 9100. Total number of dead fish
was calculated from survival and initial number of stocked larvae.
Final parameters were tested statistically using ANOVA with Tukey’s
HSD test to examine differences among the treatments in water
quality parameters and survival. Mortality due to surface death and
proportions of larvae with inflated swim bladders were tested by a
repeated ANOVA with Tukey’s HSD test between the treatments
and among ages. Prior to testing, the data except water quality
parameters were arcsine transformed.
In this study, we elucidated that the optimal period to effec-
tively promote ISI by surface film skimming is the first day after
initial feeding (4 dph). A few larvae with inflated swim bladders
were observed at 3 dph; however, the percentages were not
increased and statistically similar among SF4D, SF5D and SF6D at
7 dph (Figure 1, upper). In addition, the proportions of SF3D and
SF4D were significantly higher than that of SF5D and SF6D at
4 dph and were statistically similar thereafter in the SF4D group
(Figure 1, lower). This point should be examined further in future
by improved sampling regime including increased sample size.
TABLE 1 Water quality parameters, survival and the mortality due to surface death of yellowfin tuna (Thunnus albacares) larvae reared
under the different timing of start surface skimming
Treatment Temperature (°C) Dissolved oxygen (mg/L) Salinity (g/L) Survival (%)
Mortality due to
surface death (%)
SF3D 27.8 0.1 6.49 0.04 33.9 0.1 11.4 6.4 1.8 0.8
SF4D 27.9 0.2 6.48 0.03 33.9 0.1 15.5 2.5 1.8 1.6
SF5D 27.8 0.1 6.49 0.01 33.9 0.1 6.7 0.1 0.4 0.2
SF6D 27.9 0.1 6.46 0.03 33.9 0.1 11.0 4.1 0.7 0.5
Values of percentage survival and mortality due to surface death are shown by mean SD (n=3).
No significant differences were detected among the treatment.
Rearing water surface was skimmed to remove fish oil from 3 (SF3D), 4 (SF4D), 5 (SF5D) and 6 dph (SF6D).
0.0
20.0
40.0
60.0
SF3D
SF4D
SF5D
SF6D
Percentage of swim bladder inflation (%)
a
a
b
b
a
a
b
b
a
b
bc
c
a
ab
b
b
0.0
20.0
40.0
60.0
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SF3D
SF4D
SF5D
SF6D
Days post hatch
Percentage of swim bladder inflation (%)
A
B
AB
AB
B
B
AB
AB
C
B
B
AB
BC
B
B
B
B
FIGURE 1 The percentage of swim bladder inflation of yellowfin
tuna (Thunnus albacares) larvae reared at different initiation times of
surface skimming. Surface skimmer use was initiated at 3 dph (○;
SF3D), 4 dph (●;SF4D), 5 dph (□;SF5D) and 6 dph (■;SF6D). Values
indicate mean of pooled values from replicate tank treatments
(n=3). Different letters indicate significant differences between the
treatments at different age (a,b,c p<.05, upper) and among the age
in the treatment (A,B,C p<.05, lower). Error bars are not shown in
order to simplify the figure
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HONRYO ET AL.

Delaying the skimming by as little as 1 day (5 dph) resulted in a trend
towards lower percentage of swim bladder inflation. Therefore, sur-
face skimming to effectively promote ISI should be performed during
this brief period in YFT larviculture. Additionally, a peak of mortality at
the surface occurred at 4 dph, overlapping the brief period for ISI pro-
motion in SF4D (Figure 2), as reported in PBF (Kurata et al., 2012),
implying that larval access to the water’s surface to gulp air for ISI may
be a trigger for surface-adhesion death.
In the present study, the maximum proportion of larvae with
inflated swim bladders did not exceed 60% and was similar to the
proportion (50 0.5%) reported in Partridge et al. (2011) under a
12-hr lighting photoperiod. In contrast, Kurata et al., 2015 reported
that PBF larvae need to gulp air for successful ISI during a three-
hour period prior to onset of darkness at 3 dph with over 80% of
inflation frequency. This window corresponded to the twilight period
when light intensity was gradually decreased. Therefore, YFT larvae
probably require the twilight period and scotophase conditions for
ISI success.
There were no significant differences among treatments in sur-
vival at 8 dph or the mortality due to surface death in this study
(Table 1). These results for YFT indicated that the impact of mortality
due to surface deaths was less than the mortality due to other factors
such as sinking syndrome and malnutrition. The swim bladder is known
as a buoyancy-regulating organ, but it is thought that the effect of ISI
promotion on survival was diminished when nighttime aeration was
increased as a countermeasure to prevent sinking syndrome (Naka-
gawa, Kurata, Sawada, Sakamoto & Miyashita, 2011). However, as
Kurata et al., 2014 reported, there is a significant relationship between
ISI success and larval survival on PBF reared in 20 and 30 kl tanks in
which surface area was 20.3 and 28.3 m
2
respectively. They suggested
that larval survival was enhanced by ISI promotion in mass-scale PBF
larviculture due to prevention of sinking syndrome. In addition, it is
anticipated that the impact of surface death on overall mortality would
increase when larvae are reared in larger tanks due to the increase in
surface area; however, it has not been investigated yet. Moreover,
Takashi et al., 2006 suggested that larval body density with deflated
swim bladder of PBF increased with days post hatch. This indicated
that the potential mortality by sinking syndrome due to ISI failure
would increase without ISI success. Further studies are needed to
develop the rearing techniques that satisfy ISI success and suppress
mortality due to surface adhesion.
ACKNOWLEDGMENTS
The authors thank the staff of the IATTC’s Achotines Laboratory in
the Republic of Panama for their assistance. This study was finan-
cially supported by JST (Japan Science and Technology Agency) and
JICA (Japan International Cooperation Agency).
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How to cite this article: Honryo T, Kurata M, Guillen A,
et al. Optimal period for the effective promotion of initial
swim bladder inflation in yellowfin tuna, Thunnus albacares
(Temminck and Schlegel), larvae. Aquac Res. 2017; 00:1–4.
https://doi.org/10.1111/are.13355
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HONRYO ET AL.