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Biological indicators of stress in pacu (Piaractus mesopotamicus) after capture/Indicadores biologicos de estresse em pacu (Piaractus mesopotamicus) apos captura.

1. Introduction

There are many potential applications of the stress response. Experimental biologists need to know the baseline from which to assess whatever response they are studying. It is also important to know whether fish under intensive aquaculture are in or out of a stressed state. Aquaculture development depends on the establishment of appropriate management practices. Thus the features of the physiological stress responses can serve this purpose.

Various stressors, including fish capture (Mugnier et al., 1998; Arends et al., 1999; Barcellos et al., 2001; Rocha et al., 2004; Morales et al., 2005), are necessary components of modern intensive aquaculture (Wendelaar Bonga, 1997). The fish response to such stressors involves a series of physiological changes in an attempt to compensate for the challenge imposed upon it and, thereby cope with the stress. Such changes have been broadly categorized into primary, secondary and tertiary responses including hormonal, metabolic, osmoionic and hematological disturbances and have been used to characterize the degree of stress fish experienced (McDonald and Milligan, 1997; Wendelaar Bonga, 1997; Wojtaszek et al., 2002).

The majority of international research effort has gone into the stress responses of salmonids (McCormick et al., 1998; Ackerman et al., 2000; Barton, 2000), but other species such as carp (Cyprinus carpio L.) (Vianen et al., 2001), tilapia (Oreochromis niloticus L.) (Van der Salm et al., 2005), turbot (Scophthalmus maximus L.) (Van Ham et al., 2003) and sea bream (Sparus aurata L.) (Arends et al., 1999) have gained attention due to their potential for aquaculture in many countries. However, little research has been done on native South American fishes. Among the Brazilian farmed fish, research on stress has been carried out on matrinxa (Brycon cephalus) (Gunther, 1869) (Carneiro and Urbinati, 2001; Ide et al., 2003; Rocha et al., 2004; Urbinati et al., 2004), tambaqui (Colossoma macropomum) (Cuvier, 1818) (Gomes et al., 2003a), pirarucu (Arapaimas gigas) (Schinz, 1822) (Gomes et al., 2003b) and jundia (Randia quelen) (Quoy and Gaimard, 1824) (Barcellos et al., 2001). Despite pacu (Piaractus mesopotamicus) (Holmberg, 1887) being considered one of the most important native species (Queiroz et al., 2005) and studies on its reproduction (Romagosa et al., 1990), larviculture (Jomori et al., 2003), feeding and nutrition (Souza et al., 2000; Bechara et al., 2005; Takahashi et al., 2006; Abimorad et al., 2007) are available, there is sparse knowledge on the stress response of the species (Krieger et al., 1989; Martins et al., 2000; Takahashi et al., 2006). In the present study, the physiological responses (hormonal, metabolic, ionic and hematological) to capture (chasing, netting and air exposure) were investigated in the pacu.

2. Material and Methods

2.1. Fish and experimental procedure

Juveniles of pacu (132 fish, 49.7 [+ or -] 11.7 g) were randomly distributed in thirty three 100 L boxes (4 fish per box), with constant water and air flow, where they were kept for 15 days to acclimate to the experimental conditions. Feeding was stopped 24 hours before the capture that consisted in chasing, netting and exposed the fish to the air. Fish were submitted to the conditions: T1: undisturbed fish (control) (3 boxes), T2: chasing and 3 minutes of air exposure (15 boxes), T3: chasing and 5 minutes of air exposure (15 boxes). Nine fish of T2 and T3 (3 fish/3 boxes) were sampled at each sampling time (5, 15, 30, 60 minutes and 24 hours after handling). The control fish (n = 9) were sampled before handling. Fish were anesthetized (benzocaine, 66 mg.L-1) and bled by caudal vessels puncture and serum and plasma were separated. The four fish of each box were simultaneously anesthetized but only 3 were sampled.

2.2. Analyses

Glucose (King and Garner, 1947), hematocrit, red blood cell count (RBC), mean corpuscular volume (MCV) and hemoglobin were determined in total blood (Celm DA-500), chloride (kit Labtest) and osmolality (Osmometer Wescor Mod 505) in plasma and cortisol (RIA, kit Diagnostics Products Corporation), sodium, potassium and calcium (ion selector Iselab Drake) in serum.

Water temperature (29.1 [+ or -] 0.5 [degrees]C) and dissolved oxygen (4.4 [+ or -] 0.4 mg.L-1) (Yellow Springs Instruments, Yellow Springs, OH, USA, YSI 55), pH (10.2 [+ or -] 0.4) (YSI 63) and total ammonia (0.0102 [+ or -] 0.0054 mg.L-1, Nessler Reactive) were monitored throughout the experiment.

2.3. Statistical analysis

A completely randomized design (CRD) was employed and results were analyzed by a two-way analysis of variance (ANOVA), with 2 treatments (capture with 3 or 5 minutes air exposure) and 5 sampling times (5, 15, 30 and 60 minutes and 24 hours after capture) as the factors plus the resting condition (control fish). Data were expressed in means [+ or -] standard deviation of the mean. Means were compared by Tukey test (p < 0.05).

3. Results

No mortality was observed in any group during the experiment. There were hormonal and metabolic changes after the handling imposed on the fish. Serum cortisol concentrations in air-exposed fish either for 3 minutes (T2) or 5 minutes (T3) rose within 30 minutes (p = 0.0109) and then dropped until 24 hours later. The rise was higher in fish of treatment 3 (p = 0.0074) regardless of the sampling (Figure 1). Blood glucose in both air-exposed fish (T2 and T3) increased within 5 minutes (p = 0.0001) compared to control (undisturbed fish) and recovered the resting values within 24 hours (Figure 1). Capture elicited mild changes in ionic balance of pacu. Plasma chloride levels dropped in fish of treatments 2 and 3 within 60 minutes, not recovering the resting levels within 24 hours (p = 0.0291) (Figure 2). Serum sodium increased (p = 0.0026) at 15 and 30 minutes in both air-exposed fish (T2 and T3) and returned to resting levels 24 hours later (Figure 2). Potassium concentration (p = 0.2901) and osmolality (p = 0.5332) did not change after air exposure (Table 1). In fish of treatments 2 and 3, calcium levels did not differ significantly until 60 minutes after handling and decreased after 24 hours (p = 0.0001) compared to the other samplings but not to the control condition (Table 1). Excepting for MCV, which rose 30 minutes after capture and returned to resting levels 24 hours later (p = 0.0440), the hematocrit (Table 1), red blood cells count (RBC) and hemoglobin (Figure 3) were not affected by capture (p = 0.8382; p = 0.2980 and p = 0.5463, respectively).

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

4. Discussion

Stress is a biological response of adaptation to adverse conditions and fish respond by activating responses such as increased circulating cortisol and glucose (Wendelaar Bonga, 1997), changes in blood ionic balance (McDonald and Milligan, 1997) and hematological profile (Wojtaszek et al., 2002). Although laboratory studies can be criticized for lack of realism, they allow for a systematic determination of general behavioral and physiological principles of stress response that is not possible in the field.

Interactions of sequential stressors, as those to which the pacu was exposed in the present study, often cause increased stress in fish. Capture, for instance, includes the chasing and swimming of fish, physical injury provoked by the contact among fish and with the net and anoxia by air exposure (Mugnier et al., 1998; Arends et al., 1999; Ross and Ross, 1999; Barcellos et al., 2001; Morales et al., 2005). Confirming the literature regarding fish stress, elevated circulating cortisol and glucose of pacu were short-term responses in both air-exposed fish after capture and the recovery occurred within 24 hours. However, the magnitude of glucose responses was low (from 60 to 94 [mg.dL.sup.-1]) compared to values found previously in pacu in stressed state (Krieger et al., 1989; Martins et al., 2000). Air exposure of Sparus aurata for 3 minutes resulted, within 30 minutes, in an increase in plasma concentrations of cortisol and glucose. After 2 hours, plasma cortisol and after 12 hours plasma glucose had returned to control concentrations (Arends et al., 1999). On the other hand, netting and exposure of juvenile turbot to air for 1-4 minutes had no immediate effect on plasma cortisol concentrations (Mugnier et al., 1998). The stress response of pacu involved activation of the brain-pituitary-interrenal axis, as indicated by the cortisol and glucose elevations and it was probably elicited by the combined stimuli of fish swimming when chased, netting and the hypoxic condition provoked by air exposure.

[FIGURE 3 OMITTED]

Many stressors affect the ionic balance in fish (Wendelaar Bonga, 1997) facilitated by cathecolamine-induced increase of gill permeability responsible for chloride and sodium exchange with the environment (McDonald and Milligan, 1997). Decrease in plasma concentration of chloride and sodium were found in other stressed freshwater fish as in Brycon cephalus after transport (Carneiro and Urbinati, 2001; Urbinati et al., 2004). In our experiment, a partial and moderate disturbance of the ionic balance was found in both air exposed fish. In stressed pacu, chloride decreased 60 minutes after capture whereas sodium concentration increased transiently between 15 and 60 minutes after capture. Additionally, calcium and potassium levels and osmolality were not affected by the sequential stressors during capture. Apparently only a moderate and rather specific loss of permeability control occurred as consequence of capture.

The low magnitude of glucose responses, mild chloride and sodium disturbances, and the lacking potassium, calcium and osmolality responses indicated low activation of the brain-sympathetic-chromaffin cell axis, and hence a low release of catecholamines, which seemed though to occur to a higher extent at severe stressors (Mazeaud and Mazeaud, 1981). Several studies are known to initiate catecholamine secretion in fish including physical disturbance (Ristori and Laurent, 1985) and hypoxia (Ristori and Laurent, 1989). However, the degree of hypoxia required to initiate the responses is highly variable. Studies have shown that there exist hypoxiatolerant species such as carp (Vianen et al., 2001) in contrast to hypoxia-intolerant species such as rainbow trout (Boutilier et al., 1988). A recent study that provided the first data on plasma catecholamines level in tropical fish (Perry et al., 2004) has shown that plasma catecholamines levels remained constant in pacu exposed to acute hypoxia, suggesting an inoperative or absent humoral adrenergic stress response in this species.

The results of the hematological assessement of stressed pacu confirmed the low degree of activation of the brain-sympathetic-chromaffin cell axis. Peripherical blood analysis has been used as a diagnosis to assess healthy state in fish and the effect of several stressors on them (Wojtaszek et al., 2002). The most significant effect of catechoalmines release during stress is to enhance blood O2 transport by increasing the carrying capacity (Wells and Weber, 1990) and by enhancing Hb-O2 binding affinity (Cossins and Richardson, 1985). No significant changes were found in the hematological parameters tested in pacu after the sequence of stressors during the capture. Concluding, the results of this work indicate that the submission of sequential stressors on pacu during capture activated the brain-pituitary-interrenal axis (cortisol and glucose responses) but the activation of the brain-sympathetic-chromaffin cell axis was apparently moderate (ionic and hematological responses).

Acknowledgements--We would like to thank Mrs. Damares Perecim Roviero for the technical support, to Piscicultura Aguas Claras (Mococa, SP) for the fish donation and to the Aquaculture Centre of Sao Paulo State University for the facilities.

Received August 17, 2007--Accepted January 30, 2008--Distributed May 31, 2009 (With 3 figures)

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Abreu, JS. (a), Takahashi, LS. (d), Hoshiba, MA. (c) and Urbinati, EC. (b,d) *

(a) Departamento de Zootecnia e Extensao Rural, Faculdade de Agronomia e Medicina Veterinaria--FAMEV, Universidade Federal do Mato Grosso--UFMT, Av. Fernando Correa da Costa, s/n, Coxipo, CEP 78060-900, Cuiaba, MT, Brazil

(b) Centro de Aquicultura--CA, Universidade Estadual Paulista--UNESP Via de Acesso Prof. Paulo Donato Castelane, CEP 14884-900, Jaboticabal, SP, Brazil

(c) Instituto de Ciencias Sociais e Aplicadas e Zootecnia do Baixo Amazonas, Universidade Federal do Amazonas--UFAM, Rua Pa raiba, 2186, Campus Universitario do Baixo Amazonas, CEP 69152-010, Parintins, AM, Brazil

(d) Faculdade de Ciencias Agrarias e Veterinarias--FCAV, Universidade Estadual Paulista--UNESP, Via de Acesso Prof. Paulo Donato Castelane, CEP 14884-900, Jaboticabal, SP, Brazil

* e-mail: bethurb@caunesp.unesp.br
Table 1. Hematocrit, serum potassium and calcium and osmolality of
pacu undisturbed and air exposed for 3 and 5 minutes.Different
capital letters indicate differences among samplings and small
letters between treatments.

                                     Sampling times

                      Air exposure   5 minutes

                      Control
Hematocrit (%)        3 minutes      31.4 [+ or -] 2.22
                      5 minutes      34.9 [+ or -] 1.68
                      Means          33.2 [+ or -] [2.58.sup.A]

Serum                 Control
potassium             3 minutes      3.03 [+ or -] 0.74
(mEq.[L.sup.-1])      5 minutes      2.43 [+ or -] 0.35
                      Means          2.73 [+ or -] [0.61.sup.A]

Serum                 Control
calcium               3 minutes      1.48 [+ or -] 0.22
(mEq.[L.sup.-1])      5 minutes      1.45 [+ or -] 0.03
                      Means          1.46 [+ or -] [0.14.sup.A]

Osmolality            Control
(mOsmol.[L.sup.-1])   3 minutes      310.9 [+ or -] 6.2
                      5 minutes      314.5 [+ or -] 4.5
                      Means          312.7 [+ or -] [5.2.sup.A]

                                     Sampling times

                      Air exposure   15 minutes

                      Control
Hematocrit (%)        3 minutes      33,2 [+ or -] 2.22
                      5 minutes      34.2 [+ or -] 2.42
                      Means          33.7 [+ or -] [2.16.sup.A]

Serum                 Control
potassium             3 minutes      2.33 [+ or -] 0.32
(mEq.[L.sup.-1])      5 minutes      2.34 [+ or -] 0.44
                      Means          2.34 [+ or -] [0.34.sup.A]

Serum                 Control
calcium               3 minutes      1.54 [+ or -] 0.16
(mEq.[L.sup.-1])      5 minutes      1.51 [+ or -] 0.08
                      Means          1.53 [+ or -] [0.11.sup.A]

Osmolality            Control
(mOsmol.[L.sup.-1])   3 minutes      312.0 [+ or -] 3.9
                      5 minutes      314.8 [+ or -] 1.7
                      Means          313.4 [+ or -] [3.1.sup.A]

                                     Sampling times

                      Air exposure   30 minutes

                      Control
Hematocrit (%)        3 minutes      34.7 [+ or -] 1.35
                      5 minutes      32.8 [+ or -] 1.76
                      Means          33.7 [+ or -] [1.76.sup.A]

Serum                 Control
potassium             3 minutes      2.61 [+ or -] 0.48
(mEq.[L.sup.-1])      5 minutes      2.25 [+ or -] 0.55
                      Means          2.43 [+ or -] [0.50.sup.A]

Serum                 Control
calcium               3 minutes      1.88 [+ or -] 0.24
(mEq.[L.sup.-1])      5 minutes      1.60 [+ or -] 0.22
                      Means          1.74 [+ or -] [0.26.sup.A]

Osmolality            Control
(mOsmol.[L.sup.-1])   3 minutes      307.5 [+ or -] 1.8
                      5 minutes      314.8 [+ or -] 7.8
                      Means          311.2 [+ or -] [6.4.sup.A]

                                     Sampling times

                      Air exposure   60 minutes

                      Control
Hematocrit (%)        3 minutes      33.3 [+ or -] 1.10
                      5 minutes      33.8 [+ or -] 3.39
                      Means          33.5 [+ or -] [2.27.sup.A]

Serum                 Control
potassium             3 minutes      2.35 [+ or -] 0.42
(mEq.[L.sup.-1])      5 minutes      2.64 [+ or -] 0.40
                      Means          2.50 [+ or -] [0.40.sup.A]

Serum                 Control
calcium               3 minutes      1.74 [+ or -] 0.47
(mEq.[L.sup.-1])      5 minutes      1.79 [+ or -] 0.40
                      Means          1.77 [+ or -] [0.39.sup.A]

Osmolality            Control
(mOsmol.[L.sup.-1])   3 minutes      309.7 [+ or -] 7.1
                      5 minutes      306.3 [+ or -] 8.4
                      Means          308.0 [+ or -] [7.2.sup.A]

                                     Sampling times

                      Air exposure   24 hours

                      Control
Hematocrit (%)        3 minutes      37.1 [+ or -] 0.77
                      5 minutes      36.6 [+ or -] 1.30
                      Means          36.9 [+ or -] [0.99.sup.A]

Serum                 Control
potassium             3 minutes      2.95 [+ or -] 0.13
(mEq.[L.sup.-1])      5 minutes      2.77 [+ or -] 0.51
                      Means          2.86 [+ or -] [0.35.sup.A]

Serum                 Control
calcium               3 minutes      1.01 [+ or -] 0.19
(mEq.[L.sup.-1])      5 minutes      1.03 [+ or -] 0.08
                      Means          1.02 [+ or -] [0.13.sup.B]

Osmolality            Control
(mOsmol.[L.sup.-1])   3 minutes      298.1 [+ or -] 16.3
                      5 minutes      317.0 [+ or -] 4.6
                      Means          307.5 [+ or -] [14.9.sup.B]

                                     Sampling times

                      Air exposure   Means

                      Control        34.5 [+ or -] [3.21.sup.Aa]
Hematocrit (%)        3 minutes      34.0 [+ or -] [2.40.sup.a]
                      5 minutes      34.5 [+ or -] [2.31.sup.a]
                      Means

Serum                 Control        2.34 [+ or -] [0.49.sup.Aa]
potassium             3 minutes      2.66 [+ or -] [0.49.sup.a]
(mEq.[L.sup.-1])      5 minutes      2.48 [+ or -] [0.43.sup.a]
                      Means

Serum                 Control        1.30 [+ or -] [0.06.sup.ABa]
calcium               3 minutes      1.53 [+ or -] [0.39.sup.a]
(mEq.[L.sup.-1])      5 minutes      1.48 [+ or -] [0.31.sup.a]
                      Means

Osmolality            Control        306.0 [+ or -] [5.8.sup.Aa]
(mOsmol.[L.sup.-1])   3 minutes      307.6 [+ or -] [8.9.sup.a]
                      5 minutes      313.5 [+ or -] [6.3.sup.a]
                      Means
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Author:Abreu, J.S.; Takahashi, L.S.; Hoshiba, M.A.; Urbinati, E.C.
Publication:Brazilian Journal of Biology
Date:May 1, 2009
Words:4008
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