Aquaculture 256 (2006) 521 – 528
www.elsevier.com/locate/aqua-online
Use of salt during transportation of air breathing pirarucu
juveniles (Arapaima gigas) in plastic bags
L.C. Gomes a,⁎, Edsandra Campos Chagas a , Richard Philip Brinn b , Rodrigo Roubach c ,
Carlos Eduardo Coppati d , Bernardo Baldisserotto d
a
Embrapa Amazônia Ocidental, Manaus, AM, Brazil
Florida International University, Miami, FL, USA
Instituto Nacional de Pesquisas da Amazônia, Manaus, AM, Brazil
d
Universidade Federal de Santa Maria, Santa Maria, RS, Brazil
b
c
Received 14 October 2005; received in revised form 23 December 2005; accepted 1 February 2006
Abstract
The farming of the Amazonian air breathing fish, Arapaima gigas, has been growing substantially over the last decade in Brazil
and other South American countries. Previous study demonstrated that transportation of pirarucu juvenile in plastic bags is a
suitable procedure, although it stimulated some stress responses. Therefore the objective of this study was to investigate the
addition of salt as a stress mitigator in pirarucu juveniles during transportation in plastic bags. Fish were reared for a month in
earthen pond and held in 3 indoor 2000-L depuration tanks for 24 h to allow complete gastrointestinal evacuation, then placed in
30-L polyethylene bags with 10 L of water at a density of 12 fish/bag (40 g/L) with different table salt (NaCl, 97%) concentrations
in the water: 0, 1, 3, 5 g/L (3 replicates each concentration). Transportation took 3 h and afterwards fish were transferred to 1-m3
floating cages installed inside an earth pond for recovery. Fish stress responses were evaluated before, during and after
transportation procedure, and the analyses performed were: cortisol, glucose, lactate, haematrocrit and waterborne net Na+, Cl−,
K+, and Ca2+ fluxes. No mortality was recorded in any treatment during transportation and recovery periods. Cortisol exhibited an
increase after transport with 1g salt/L and at 24 h after transportation for all treatments showing a latency period in their response.
Glucose exhibited a similar pattern for all treatments with a significant increase before and after transportation, returning to basal
levels in 24 h. Lactate concentrations increased before transportation and after transportation, presenting a significant decrease in all
treatments. Addition of salt in the transport water increased Na+, Cl− and Ca2+ net fluxes in pirarucu. Using salt during pirarucu
juvenile transportation should be avoided since there is no reduction on stress responses and causes osmoregulatory disturbances.
© 2006 Elsevier B.V. All rights reserved.
Keywords: Stress; Net ion fluxes; Cortisol; Glucose; Pirarucu
1. Introduction
⁎ Corresponding author. Present address: Departamento de Ecologia
e Recursos Naturais, Universidade Federal do Espírito Santo, Vitório,
ES, Brazil. Tel.: +55 92 3621 0381; fax: +55 92 3621 0300.
E-mail address: [email protected] (L.C. Gomes).
0044-8486/$ - see front matter © 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.aquaculture.2006.02.004
Monitoring physiological parameters during stressful
operations, like transportation can provide valuable data
for the establishment of adequate management practices,
even for situations where there is no fish mortality
(Sulikowski et al., 2005). For successful fish handling
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L.C. Gomes et al. / Aquaculture 256 (2006) 521–528
and transportation, a stronger effort towards the animal
well-being is more desirable than surveying for fish
mortality (Gomes et al., 2003c). Usually a severe stress
condition could compromise fish adaptive capacity to the
environment and even result in a temporary growth
disruption and higher susceptibility to parasites and
infections (Wedemeyer, 1996).
Fish respond to stress in a proportional way that
reflects the severity and duration of the stressor (Barton,
1997). These responses prepare the organism to the socalled “fight or flight” response, which is an attempt to
escape from the adversity (Morgan and Iwama, 1997).
Consequently the fish physiological reactions to that
specific type of stressor needs to be analyzed, both in
relations to the response, as to its intensity (KrigerAzolini et al., 1989).
Pirarucu (Arapaima gigas) is an exclusively air
breathing fish native from the Amazon basin. Pirarucu
farming is booming in some South and Central America
countries mainly due to its growth rate, reaching from 7
to 10 kg in a twelve-month cycle (Imbiriba, 2001;
Pereira-Filho et al., 2003). With the increasing demand
for pirarucu to grow-out operations the determination of
an appropriate, simple, reliable, and inexpensive method
for an efficient transportation with the lowest stress
possible for the fish is required. Previous results obtained
by Gomes et al. (2003c) demonstrated that plastic bag
with pure oxygen is a feasible method for pirarucu transportation, although fish exhibited some stress
responses.
The use of salt during transportation helps fish to
maintain homeostasis by reducing the osmotic gradient
between plasma and external environment and by
increasing mucus production (Wurts, 1995) which has
been demonstrated to reduce stress responses for some
fish species like rainbow trout (Oncorhynchus mykiss)
(Barton and Peter, 1982) and matrinxã (Brycon cephalus) (Carneiro and Urbinati, 2001), but has not been
tested for pirarucu transportation. Therefore this study
analyzed several parameters (blood glucose, lactate,
cortisol, haematocrit and ion fluxes) in an attempt to
evaluate the effect of salt on physiological homeostasis
of pirarucu during transportation of juveniles in plastic
bags.
2. Material and methods
Brazil) to feed train them to accept a commercial
(extruded) fish diet. After 100% acceptance of extruded
feed they were reared for 1 month in a 200-m3 earth
pond and fed four times a day with a commercial
pelleted feed with 45% crude protein (TR 45; Nutron®,
São Paulo, Brazil).
Fish (weight 32.79 ± 2.35 g, n = 162) were caught
from the earth pond and held in three indoor 2000-L
depuration tanks (one for each replicate) for 24h to allow
gastrointestinal emptying. Fish were placed in 30-L
polyethylene bags with 10 L of water at a density of 12
fish per bag (40 g/L). Commercial table salt (NaCl, 97%)
was added to the water at: 0, 1, 3, 5 g/L (3 replicates for
each concentration). Bags were then inflated with oxygen, tied with rubber strings and packed in styrofoam
boxes. Transportation proceeded though paved roads for
3h. After transportation fish were transferred to 1 m3
floating cages installed in an earth pond for recovery.
Fish from each bag were kept in separate cages for the
subsequent monitoring. Fish density (385 g/m3) in the
recovery cage was in the appropriate range for rearing
this species (Cavero et al., 2003).
Fish stress responses were evaluated in the earth
pond (control; before disturbance [BD], n = 9); before
transportation in the depuration tanks ([BT], n = 3 for
each tank); immediately after transportation ([AT], n = 3
for each replicate) and at 24, 48, and 96h after transportation ([24 AT], [48 AT] and [96 AT] n = 3 for each
replicate). To avoid unaccounted cumulative stress
responses occasioned by repeated disturbance during
48 and 96AT, fish were individually captured in the
recovery cage with a hand net when they came for
surface air. Therefore the fish that remained in the cage
were minimally disturbed.
2.2. Water sampling and analyses
During the transportation total ammonia, measured
by the endophenol method (APHA, 1992) and water ions
levels, were assessed. Rigid cannulas were inserted
through the opening of the bags before closing and at the
end of these tubes weights were attached to prevent
floating. Water was sampled (400 mL) through a small
valve, every hour during the transport process. Four bags
containing the same salt concentrations, temperature and
pH as all the treatments were used to replenish the
volumes sampled.
2.1. Experimental procedure
2.3. Ion fluxes
Pirarucu juveniles were obtained from a commercial
supplier and transferred to a 2000 L indoor tank at the
Embrapa fish culture sector (Manaus, Amazonas,
Water Na+ and K+ levels were measured directly in
a B462 flame photometer (Micronal, Brazil), Ca2+
L.C. Gomes et al. / Aquaculture 256 (2006) 521–528
0 g/L
Cortisol (ng/mL)
with an AA-1475 atomic absorption spectrophotometry (AAS VARIAN, Australia) after dilution in
lanthanium chloride and Cl− levels by the colorimetric
assay described by Zall et al. (1956). Net ion fluxes
were calculated according to Gonzalez et al. (1998),
and the replacement of water every hour (as explained
in the previous item) was considered for the final
calculation.
50
45
40
35
30
25
20
15
10
5
0
2.4. Blood analysis
BT
Glucose (mg/dL)
*
BD
7
Lactate (mmol/L)
3 g/L
*
100
90
80
70
60
50
40
30
20
10
0
BT
AT
5 g/L
* *
*
24AT
48AT
96AT
24AT
48AT
96AT
* * **
AT
*
6
5
4
** * * * *
*
3
2
* ** *
1
*** *
0
2.5. Statistical analysis
Haematocrit (%)
BD
Differences between treatments (salt concentrations)
and physiological stress indicators at different samplings
were compared against the control group (before disturbance; BD) by one-way ANOVA and Dunnett's test
(P b 0.05). Data for Na+ and Cl− fluxes were submitted to
linear regression. Ammonia concentrations and K+ and
Ca2+ fluxes were evaluated by two-way ANOVA (time
1 g/L
3 g/L
5 g/L
BT
AT
24AT
48AT
96AT
48AT
96AT
*
45
40
35
30
25
20
15
10
5
0
BD
0 g/L
1 g/L
*
BD
Blood was drawn from the caudal vasculature with
heparinized syringes in less than 1 min without anesthesia since till this date there are no non-lethal anesthetics
methods known for this species. Blood glucose was
measured using the digital Advantage™ blood glucose
system (Roche, Germany). Blood lactate was measured
using the digital Lactate-Pro system (Arkray Inc., Japan).
Haematocrit values were obtained with a microhaematocrit centrifuge. Plasma was separated by centrifugation
(3000 ×g, 10 min) and stored at − 20 °C for further
analysis. Cortisol was measured with an enzyme-linked
immunoassay method (ELISA, kit 55050, Human,
Germany) using a microplate reader, intra-assay coefficient of variation was 8.4%, the analytic sensitivity of the
assay was 1.1 ng/dL.
523
BT
AT
24AT
Period of transport
Ammonia (mg/L)
0.4
0.3
0.2
0.1
0
0
1
2
3
Time of transport (h)
Fig. 1. Total ammonia during 3 h transportation of pirarucu juvenile
Arapaima gigas in plastic bags with different salt concentrations in the
water. Data were analyzed by two-way ANOVA, statistical significances are in the text.
Fig. 2. Cortisol, glucose, lactate and haematocrit during transportation
procedure of pirarucu juvenile Arapaima gigas in plastic bags with
different salt concentrations in the water. Data are means ± SEM. BD —
before disturbance (n = 9) at the earth pond; BT — before transportation
(n = 9) at the depuration tank; AT — immediately after transportation
(n = 3 for each tree replicates within each salt concentration); 24AT,
48AT and 96 AT — at 24, 48 and 96 h after transportation (n = 3 for each
tree replicates within each salt concentration). Columns marked with *
are significantly different from the control (BD) (Dunnett's test;
P b 0.05).
of transport and salt concentration) and Tukey's test
(P b 0.05). All statistical analyses were performed with
the software Sigma Stat 3.0.1.
524
L.C. Gomes et al. / Aquaculture 256 (2006) 521–528
1500
3.1. Water quality and mortality
No mortality was recorded in any treatment during
transportation and the recovery period. Water quality
parameters before transportation were: DO: 5.32 mg/L;
temperature: 25°C, pH 5.8 and total ammonia 0.02 mg/
L. Ammonia concentration in the water increased
significantly with transportation time (P b 0.05), although with no effect from the different salt concentrations (Fig. 1).
Na+ net flux (mmol/kg.h)
3. Results
1h
2h
3h
A
1000
500
0
-500
-1000
0
1
2
3
4
5
6
2
3
4
5
6
Cortisol exhibited a significant increase AT in the 1 g
salt/L treatment (29.66 ± 4.6 ng/mL) and at 24 AT for all
treatments, returning to basal levels (8.26 ± 3.9ng/mL)
on the next sampling period (48 AT) (Fig. 2). Glucose
concentrations exhibited similar levels for all treatments
with a significant increase BT and AT, returning to basal
levels (34.9 ± 2.8ng/mL) after 24h (Fig. 2). Lactate basal
levels were 3.8 ± 0.3 mmol/L and their concentrations
increased significantly at BT (5.04 ± 1.0 mmol/L). After
transportation lactate levels exhibited a significant
decrease for all treatments that persisted until the last
sample (Fig. 2). Haematocrit increased significantly in
the control treatment after 24 AT (41.0% ± 1.28%),
returning to basal level (30.4% ± 1.6%) on the next
sample, salt treatments were not associated with any
statistically significant differences at any sampling time
(Fig. 2).
Cl- net flux (mmol/kg.h)
1500
3.2. Metabolic and haematological disturbance
B
1000
500
0
-500
-1000
0
1
Salt in the water (g/L)
Fig. 3. Net Na+ (A) and Cl− (B) fluxes during 3h transportation of
pirarucu juvenile Arapaima gigas in plastic bags with different salt
concentrations in the water. Data are reported as mean ± SEM, and
values of net fluxes at 2 and 3h from fish exposed to zero salt in the
water are superimposed to 1h. Data are fitted to the following
equations:
A Z 1 h : y ¼ 30:56−72:17x r2 ¼ 0:880;
2 h : y ¼ −51:54 þ 230:63x r2 ¼ 0:970;
3.3. Ion fluxes during transportation
+
−
Net Na and Cl fluxes of fish transported in the
water without salt were near zero. The increase of salt
concentration in the transport water led to an increase of
Na+ efflux in the first hour of transport, and later to an
increase of Na+ influx. The increase of salt in the
transport water also increased Cl− influx throughout the
transport. In addition, there was a significant increase on
Na+ and Cl− influx after 2 or 3 h of transport compared
to after 1 h of transport in fish transported in the water
with 3 and 5g (Fig. 3). Pirarucu transported in water
with 0 and 1 g showed low net Ca2+ influx (except a low
efflux in fish transported in water with 1 g/L salt for 1h)
throughout the transport. Fish transported in water with
3 and 5 salt/L exhibited a significant increase on Ca2+
influx after 3 h of transport compared to Ca2+ fluxes
after 1h of transport (Fig. 4A). Net K+ flux was affected
significantly by treatments and time of transport. Fish
3 h : y ¼ −15:64 þ 157:42x r2 ¼ 0:998;
where y ¼ Naþ net flux ðmmol=kg hÞ
and x ¼ salt addition in the water ðg=LÞ
B Z 1 h : y ¼ −60:27 þ 53:77x r2 ¼ 0:440;
2 h : y ¼ −88:11 þ 198:87x r2 ¼ 0:863;
3 h : y ¼ 20:15 þ 141:79x r2 ¼ 0:985;
where y ¼ Cl− net flux ðmmol=kg hÞ
and x ¼ salt addition in the water ðg=LÞ:
transported in water without salt addition did not show
any significant change on K+ flux throughout the time
of transport. Addition of any amount of salt in the water
increased K+ efflux significantly after 1 h of transport,
but after 2 h of transport only pirarucu exposed to water
with 3 and 5 g salt/L showed significantly higher K+
influx compared to those transported in water with 0
and 1 g salt/L. After 3 h of transport, fish transported in
L.C. Gomes et al. / Aquaculture 256 (2006) 521–528
Ca2+ net flux (mmol/kg.h)
2,0
1,5
4.2. Metabolic and haematological disturbance
0 g/L
1 g/L
3 g/L
5 g/L
A
b
b
ab
1,0
ab
0,5
a
a
0,0
-0,5
-1,0
1
K+ net flux (mmol/kg.h)
0,2
2
B
3
a
B
b
B
0,1
A
a
B
B
a
B
b
B
A
A
0,0
-0,1
AB
-0,2
b
A
A
1
525
2
3
Time of transport (h)
Fig. 4. Net Ca2+ (A) and K+ (B) fluxes during 3h transportation of
pirarucu juvenile Arapaima gigas in plastic bags with different salt
concentrations in the water. Values are reported as mean ± SEM. Means
identified by different capital letters indicate significant difference
among treatments in the same time of transport (P b 0.05), while means
identified by different small letters indicate significant difference
among times of transport in the same treatment as determined by twoway ANOVA and Tukey's comparison of mean values.
water with 0, 1 and 3g salt/L salt exhibited K+ efflux,
while those transported in water with 5g salt/L showed
K+ influx (Fig. 4B).
4. Discussion
4.1. Water quality
Pirarucu is highly tolerant to ammonia and able to
survive in waters with 30 mg/L of ammonia (Cavero et
al., 2004). Therefore ammonia concentrations did not
reach a critical level during this experiment. According
to Berka (1986) depuration procedure has a direct
relation to ammonia concentration during transportation,
with low ammonia concentration when fish are submitted to this procedure. The low values of ammonia
obtained at the end of our experiment can be explained
by an adequate depuration period to allow gastrointestinal evacuation.
There was a great latency period in pirarucu cortisol
responses. After transportation, a period of great
disturbances, cortisol levels remained unaltered (except
for 1g salt/L treatment) and 24 AT their levels increase
significantly in all treatments. Gomes et al. (2003c) also
obtained low cortisol responses after transportation of
pirarucu juvenile (1kg) in plastic bag without salt. This
great latency on cortisol response has also been shown
in sea raven (Hemitripterus americanus) (Vijayan and
Moon, 1994), pallid sturgeon (Scaphirhynchus albuns)
juvenile and the hybrid of pallid × shovelnose (S.
albuns × S. platorynchus) (Barton et al., 2000), and the
authors suggested that it can be related with the
neuroendocrine mechanisms involved on the corticosteroid responses to prevent the excessive mobilization of
energy stores to suit its life-style. Cortisol levels
returned to their basal values after disturbance (48 AT),
demonstrating that pirarucu is able to return to their
basal cortisol levels relatively quickly. This result is
similar to the one observed with tambaqui, which
exhibited a cortisol increase after transportation in
plastic bag and return to basal levels after 24 h (Gomes
et al., 2003a). On the other hand, some temperate fishes
such as salmonids species present a significant increase
in cortisol levels after 2 h transportation and maintain
their cortisol elevated for more than 48 h (Barton, 2000).
Addition of salt in the water reduced cortisol
secretion in tambaqui (Gomes et al., 2003b), matrinxã
(Carneiro and Urbinati, 2001) and rainbow trout (Barton
and Peter, 1982) during and after transportation. As the
treatments with salt and control exhibit the same cortisol
pattern, no evidence that salt decreases cortisol
production and excretion by pirarucu juveniles was
found.
Different than cortisol, glucose levels increased
significantly at the moment of greater disturbances
(BT and AT) for all treatments. Glucose levels normally
increase during acute stress which is intermediated by
catecholamines, which stimulates glycogenolysis in the
liver (Fabbri et al., 1998; Mommsen et al., 1999) and has
already been shown in some fish species, like common
dentex (Dentex dentex) (Morales et al., 2005), stellate
sturgeon (Acipenser stellatus) (Bayunova et al., 2002),
and red drum (Scianops ocellatus) (Robertson et al.,
1987). Glucose increase in BT indicates a cumulative
stress response to the several different stressors
including catching and handling between the pond
(BD) and depuration tank, and is a first stress response
during the different phases that compose the transportation procedure. This result is contrary to one obtained
526
L.C. Gomes et al. / Aquaculture 256 (2006) 521–528
by Gomes et al. (2003a) with tambaqui juveniles.
Glucose values remained elevated AT and returned to
basal levels at 24 AT, a similar pattern to other Amazon
fishes like the matrinxã (Carneiro and Urbinati, 2002),
that exhibit glucose elevation after 4h transportation and
returned to basal values after 24 h. Salt in the water is
efficient to mitigate glucose responses of matrinxã
transported at low density (100 kg/m3), although not for
fish transported at highest densities (200 and 300kg/m3)
(Carneiro and Urbinati, 2002). As for cortisol there is no
evidence that addition of salt in the water mitigates
pirarucu glucose responses.
Lactate was the most pronounced metabolic stress
response after pirarucu transportation, and their levels
did not reach basal values until the final sampling. The
response of lactate levels in stress situations is a rapid
and severe rise as a consequence of muscle glycogen
hydrolysis (Vijayan et al., 1997). In accordance to
previous description lactate levels increase BT, however
at all others sampling times lactate levels diminished in
all treatments (except for 0g salt/L at 24 AT) and the
levels maintained lower throughout the experiment. The
main explanation for this decrease is the hepatic lactate
capacity used as a gluconeogenic precursor in stressed
fish with a lactate clearance from the circulation for
glycogen replenishment in the liver of stressed fish as
suggested by Vijayan et al. (1994). Basal levels of
lactate in pirarucu are higher than the majority of known
basal lactate in fishes (Barton et al., 2002), suggesting
their use as important fuel product to liver metabolism
during stressful situations in pirarucu. Another air
breathing (facultative) Amazon fish the armored cat
fish (Glyptoperichthys gibbceps) also presents this
response pattern with a lactate depression under stressful
situation like acute hypoxia (Almeida Val et al., 2006)
and common carp (Cyprinus carpio) present the same
pattern under prolonged hypoxia (Zhou et al., 2000), the
authors suggest that these fish species reduce accumulation of lactate and save on the use of energy reserves in
the face of stressor, as probably occurs with pirarucu.
According to Morales et al. (2005) changes in
secondary stress responses as haematocrit normally are
not displayed in handling stress (acute stressor), being
more responsive to chronic stress situations. Our results
are in accordance as pirarucu submitted to an acute
stress (rapid transportation) presents just a slight
alteration in their haematocrit 24 AT.
The low disturbance procedure used to sample fish
during recovery period to avoid cumulative stress responses was efficient, as the results of cortisol, glucose
and haematocrit during samples at 48 AT and 96AT
show values similar to basal levels.
4.3. Ionic flux disturbance
The stress of handling or confinement led to an
increase of ion branchial efflux and high Na+ loss in
rainbow trout (McDonald et al., 1991).Therefore, the
use of adequate amounts of salts (as NaCl) in the water
for transport could reduce the plasma–water gradient
and consequently the loss of ions from fishes into the
environment (Wurts, 1995). However, in the present
study pirarucu transported in water without addition of
salt did not show any significant loss of ions (except for
K+ after 3 h), because ion net fluxes were close to zero.
If the fish would loose ions through transport, there
would be a significant net ion efflux. Consequently, the
use of salt in the water to avoid Na+ or Cl− loss is not
necessary. Moreover, there was a significant increase of
Na+, Cl− and Ca2+ influxes in fish transported in the
water with higher amounts of salt, and these influxes
increased up to 2 h of transport. This was expected, since
all osmoregulatory effort of freshwater fishes consists of
obtaining these ions from the water (or avoids ion loss)
(Baldisserotto, 2003), and when transferred to water
with higher salt content freshwater fish must adapt to the
new conditions, i.e., reduce ion influx.
The use of salt in the transport water for pirarucu
juveniles, instead of protecting them from ion body loss,
obliged them to provide a fast osmoregulatory adaptation to cope with an environment with higher salt
content. The lack of adaptation to this osmoregulatory
change may lead to death if the transport lasts for a
longer period of time, as was observed in silver catfish
(Rhamdia quelen): addition of salt in the transport water
(6g/L) increased Na+ body levels in this species and led
to death after 12 h of transport (Gomes et al., 1999).
4.4. Final remarks
Our data suggests that the use of salt as a stress
mitigation did not work for this species and should be
avoided, since there are no signs of improvement both
on the metabolic or hematological parameters analyzed
and the increase of salt concentration causes an
osmoregulatory disturbance.
Acknowledgements
This study was supported by CNPq grant # 475093/
2003-8 and # 506943/2004-6 and Embrapa (MP2). The
authors are thankful to students and technical staff of
Embrapa Amazônia Ocidental. R. Roubach and B.
Baldisserotto are research fellowship recipients from
CNPq.
L.C. Gomes et al. / Aquaculture 256 (2006) 521–528
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