Developmental changes in behavioral and retinomotor responses of Pacific bluefin tuna on exposure to sudden changes in illumination

doi:10.1016/j.aquaculture.2010.04.014

Aquaculture

Volume 305, Issues 1–4, 1 July 2010, Pages 73-78

https://doi.org/10.1016/j.aquaculture.2010.04.014 Get rights and content

Abstract

Schooling behavior traits during the process of retinomotor response from scotopic to photopic vision were examined in cultivated juvenile Pacific bluefin tuna (PBT) at 3 different ages. After a sudden change in illumination from darkness to 300 lx, retinal adaptations changed from scotopic to photopic vision. Retinomotor and schooling indices showed strong agreement, with juvenile PBTs forming polarized schools upon complete retinal adaptation to photopic vision. The behavioral and retinal adaptation to sudden illumination took 20, 15, and 10 min after illumination in PBT 25, 40, and 55 days after hatching (dah). At 40 dah, PBT took a longer time to adapt than fish aged 55 dah and showed the highest swimming speed, including momentary bursts of swimming immediately after illumination. This suggested that these fish were swimming at high speed under poor visibility conditions. In contrast, PBT at 55 dah showed a gradual increase in swimming speed that correlated with their retinal adaptation. Therefore, behavioral and retinal adaptation traits changed during growth, suggesting that the high mortality in PBT around 40 dah, due to collisions with the tank and net walls at dawn, may be because these adapt more slowly than fish at 55 dah and were swimming at a relatively high speed under conditions of poor visibility.

Introduction

Bluefin tuna aquaculture is of high commercial value and is carried out in many countries around the Mediterranean Sea, Mexico, Australia, and Japan. However, as most aquaculture industries are dependent on wild captured juvenile or young adult tuna, the negative impacts of aquaculture on the management of this stock have been reported (Miyake et al., 2003). Recently, the Fisheries Laboratory of Kinki University (FLKU) constructed a hatchery for Pacific bluefin tuna Thunnus orientalis in order to establish a stable supply of juvenile fish for aquaculture and to enhance fish stocks (Sawada et al., 2005). The construction of this hatchery has also enabled evaluation of PBT at all stages of the life cycle under appropriate conditions.

Although the entire life cycle of PBT has been established, the production of juvenile PBT is associated with high mortality as a result of sedimentation to the tank bottom, aggressive behavior, or collisions with the tank/net walls (Miyashita et al., 2000, Sawada et al., 2005, Sabate et al., 2010). Collisions with the tank/net walls occur frequently in juveniles between 30 and 60 days after hatching (dah) (40–140 mm body length [BL]) in the indoor tank (Miyashita et al., 2000) and immediately after the fish (around 45 mm BL) are transferred from the indoor tank to sea net cages (Ishibashi et al., 2009). Fewer deaths occur among wild captured juvenile PBTs (around 300 mm BL) that were caught and transferred to net cages than among hatchery-reared juvenile PBTs (Miyashita, 2002). These studies showed that growth stage is related to collision mortality. Torisawa et al. (2007) showed juvenile PBT (70–110 mm Standard length [SL]) depended strongly on vision for their schooling behavior. Ishibashi et al. (2009) reported PBT had relatively low scotopic vision sensitivity compared to other marine teleost fish such as grouper Epinephelus septemfasciatus, purplish amberjack Seriola dumerili, ocellate puffer Takifugu rubripes, and red sea bream Pagrus major; they suggested a method for preventing collisions by providing artificial lighting at night (Ishibashi et al., 2005). Masuma et al. (2001) performed histological studies to examine the time delay for the retinomotor response from scotopic to photopic vision and demonstrated that visual disorientation was caused by the additional time lag between the time required for the retinomotor response and the time taken for changes in ambient light intensity at dawn. These studies were successful in estimating the visual traits and behavior of juvenile PBTs during periods of high mortality risk and showed that lighting conditions and visual traits contributed to collision mortality. In order to elucidate the basis of this mortality, a scientific understanding of the relationship between lighting conditions and developmental changes in behavior and vision associated with growth during the pre-large reduction to post-large reduction periods due to the collision is required. However, only a few such studies have been attempted.

In the present study, indices of schooling and retinomotor were used to evaluate behavioral and retinomotor responses of PBT at three different ages to sudden changes in illumination. School formation generally requires accurate sensory functions in order to perceive the motion of neighbors (Partridge and Pitcher, 1980), and accordingly, PBT depends on their vision, with retinomotor responses being involved in schooling when lighting conditions change (i.e., at dawn, dusk, and with changes in artificial light). In the current study, time-related changes in PBT schooling behavior and retinomotor response were examined after sudden illumination, and the changes in these indices were compared in fish of different ages. The aim of this study was to determine whether the response to sudden illumination was different between the periods of pre-large reduction, large reduction, and post-large reduction due to collision.

Section snippets

Behavioral experiment

The juvenile PBTs used in the behavioral experiment were obtained from the Oshima station of FLKU. We studied the behavior of juvenile PBTs of three different ages, namely, 25, 40, and 55 days after hatching (dah). A period of large reduction caused by collisions with the tank walls was associated with each age of PBT (40 dah, 77 ± 11 mm BL, 7.5 ± 3.4 g body weight [BW]; pre-large reduction periods at 25 dah, 36 ± 4 mm BL, 0.7 ± 0.2 g BW; the latter half of the large reduction periods at 55 dah, 146 ± 9 mm BL,

Behavior of juvenile PBTs after a time interval from exposure to illumination

Under dark conditions, juvenile PBTs did not exhibit schooling behavior regardless of growth stage. In addition, the fish swam at relatively slow speeds as compared to speeds measured after illumination (Fig. 3). Under light conditions, behavioral traits differed among the growth stages. At the 25 dah stage, relatively slow S_Sws and no parallel swimming were observed (Fig. 3, Fig. 5). The fish aggregated immediately under the halogen light like a patch group, as evidenced by the I_NN value

Discussion

On the basis of a recent report by Ishibashi et al. (2005), culture of juvenile PBT at FLKU has been performed with artificial night time lighting to reduce the death rate from collisions with the walls of the tank and net. However, mass mortality occurred one night due to a power failure, with FLKU experiencing approximately 10% mortality on that occasion. We consider that the cause of this high mortality was the sudden change in illumination due to the power failure. In the present

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Previous studies showed that sinking death is influenced by their capability for continuous swimming (Ina et al., 2014). The swimming characteristics of juvenile stage tuna have been evaluated by calculating the positions of individuals using video analysis (Torisawa et al., 2007; Fukuda et al., 2010a, b; Torisawa et al., 2011; Takagi et al., 2013). Although the vertical distribution of PBT larvae affects sinking death, which depends on the swim bladder conditions and body shape characteristics such as an aspect ratio of the caudal fin (Ina et al., 2014), a quantitative analysis of the swimming characteristics at the larval stage has never been performed.
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Photoreceptor movement is typically reliant on the presence of a fully functional signal from mature rods (Hodel et al., 2006) which may not yet be apparent in young T. maccoyii larvae. The retinomotor response in juveniles of T. orientalis and T. thynnus has received intense investigation as it has been suggested that juveniles display visual disorientation during the transition from scotopic to photopic vision (Fukuda et al., 2010; Masuma et al., 2011; Torisawa et al., 2011; Torisawa et al., 2007). The consequence of visual disorientation can result in mortality as the explosive acceleration observed in tuna species generates sufficient power that impact against the tank wall often results in mortality (Ishibashi et al., 2013).
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In aquaculture situations, these physiological and morphological changes could increase mortality because of collisions causing dislocation or fractures, or both, of the vertebral column, parasphenoid, premaxilla, or frontal bones (Miyashita et al., 2000; Higuchi et al., 2014). Several factors, including the poor scotopic vision of PBF juveniles and visual disorientation during ambient light conditions, have been found to contribute to collision deaths (Masuma et al., 2001; Ishibashi et al., 2009; Fukuda et al., 2010b; Honryo et al., 2013). However, this mortality caused by the unique ontogeny of PBF still obstructs the practical production of Bluefin tuna.
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The yellowfin tuna (Thunnus albacares) (YFT) exhibits strong potential as a candidate species for full-life-cycle aquaculture. The Inter-American Tropical Tuna Commission (IATTC) has maintained a spawning population and studied the reproductive biology and early life history of YFT for research purposes at its Achotines Laboratory, Republic of Panama, since 1996. The broodstock YFT have spawned in land-based tanks at near-daily intervals as long as water temperatures have exceeded 23.3 °C. Courtship and spawning behaviors and the effects of physical and biological factors on spawning dynamics have been studied, and growth and survival rates of broodstock fish have been estimated. Experimental investigations of the early life history from the egg stage to 115 days after hatching (dah) have been conducted. The larval and early-juvenile stages are characterized by fast growth, high metabolic requirements, and high mortality. The refinement of rearing protocols that increase survival in the yolksac and first-feeding larval stages, and the development of improved artificial diets and sea cage rearing of juveniles, will hold the key to successful development of full-life-cycle aquaculture of YFT.
Organogenesis of digestive system, visual system and other structures in Atlantic bluefin tuna (Thunnus thynnus) larvae reared with copepods in mesocosm system
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During the following weeks, Pacific bluefin tuna juveniles improve scotopic vision though these early juveniles have low scotopic vision in comparison with other farmed fish (Ishibashi et al., 2009). It has been suggested that a relatively slow retinal adaptation during sunrise could cause visual disorientation contributing to the collisions with the tank wall (Fukuda et al., 2010; Ishibashi et al., 2013). Complementary studies may be performed by using visual pigments (opsins/photoreceptors) and other neurochemical macromolecules as specific markers selectively expressed by retinal cell types from different layers (e.g., calretinin, parvalbumin, glutamine synthetase, and protein kinase C) to obtain a more precise information on the maturation of different cell types and the related physiological retinal functionality (Bejarano-Escobar et al., 2010).
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Citation Excerpt :
Masuma et al. (2001) performed histological studies with juvenile PBT (50–100 mm TL) to examine the time delay for the retinomotor response from scotopic to photopic vision and demonstrated that visual disorientation was caused by the additional time lag between the time required for the retinomotor response and the time taken for changes in ambient light intensity during the dawn period. In fact, juvenile PBT (30–150 mm BL) swam at relatively high speeds, including momentary burst swimming, immediately after sudden illumination in indoor experimental tanks, when they had poor visibility due to visual maladaptation (Fukuda et al., 2010). Therefore, our results strongly suggest that collision deaths occur during dawn due to the slow retinal adaptation from scotopic to photopic vision of juvenile PBT in sea cages.
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Aquaculture

Abstract

Introduction

Section snippets

Behavioral experiment

Behavior of juvenile PBTs after a time interval from exposure to illumination

Discussion

References (20)

Artificial lighting prevents high night-time mortality of juvenile Pacific bluefin tuna, Thunnus orientalis, caused by poor scotopic vision

Aquaculture

Onset and development of cannibalistic and schooling behavior in the early life stages of Pacific bluefin tuna Thunnus orientalis

Aquaculture

Video analysis of fish schooling behavior in finite space using a mathematical model

Fisheries Research

The ocular structure, retinomotor and photo-behavioural responses of juvenile Pacific salmon

Canadian Journal of Zoology

Distance to nearest neighbor as a measure of spatial relationships in populations

Ecology

Ontogenetic changes in schooling behaviour during larval and early juvenile stages of Pacific bluefin tuna Thunnus orientalis

Journal of Fish Biology

Evaluating developmental changes in schooling behaviour in cultivated Pacific bluefin tuna Thunnus orientalis using a mathematical model

Contributions on the Theory of Fishing Gears and Related Marine Systems

Method for preventing abnormal behavior of tuna. Japanese patent application 2005-014358, JP4081092, PCT application PCT/JP2006/301176

Change in the visual threshold with development of rods in ayu Plecoglossus altivelis

Bulletin of the Japanese society of scientific fisheries

Retinomotor response and change in shape discrimination of Japanese parrotfish during light adaptation

Bulletin of the Japanese society of scientific fisheries

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Analysis of sinking death using video images of the swimming performance of Pacific Bluefin tuna (Thunnus orientalis) larvae

Retinal adaptations of southern bluefin tuna larvae: Implications for culture

Blood chemistry of Pacific bluefin tuna (Thunnus orientalis) juveniles showing abnormal swimming behavior

Research on the Reproductive Biology and Early Life History of Yellowfin Tuna Thunnus albacares in Panama

Organogenesis of digestive system, visual system and other structures in Atlantic bluefin tuna (Thunnus thynnus) larvae reared with copepods in mesocosm system

Causes of heavy mortality of hatchery-reared Pacific bluefin tuna Thunnus orientalis juveniles in sea cages