Elsevier

Aquaculture

Volume 532, 15 February 2021, 735981
Aquaculture

Effects of light cycle on motion behaviour and melatonin secretion in Haliotis discus hannai

https://doi.org/10.1016/j.aquaculture.2020.735981Get rights and content

Highlights

  • A specific method and unit for studying the behavioural ecology of abalone was established.

  • This study provided an initial quantitative description of abalone diurnal behaviour characteristics under different light cycles.

  • The intrinsic correlation between melatonin secretion and abalone behavioural rhythms was further investigated.

  • Certain references were provided for lighting control and feeding strategy during the aquaculture production of abalone.

Abstract

The abalone Haliotis discus hannai is a typical nocturnal marine invertebrate. In this study, a quantitative analysis was performed on the motion behaviour characteristics of abalones exposed to different light cycles (0 L:24D, 12 L:12D, 24 L:0D) using infrared camera and behavioural analysis software. A preliminary analysis of the intrinsic correlations between melatonin secretion and abalone behaviour rhythms was also conducted. The results showed that the cumulative moving distance and duration of movement for abalone in the 0 L:24D group were significantly higher than those in the 12 L:12D and 24 L:0D groups (P < 0.05). The mean and maximum moving velocities of abalones in the 12 L:12D group were significantly higher than those in the 0 L:24D group (P < 0.05). The maximum cumulative moving distance and duration of movement for abalone in the 12 L:12D and 24 L:0D groups occurred between 00:00–03:00. In the 0 L:24D group, peak cumulative moving distance and duration movement were recorded between 00:00–03:00 and 15:00–18:00. According to the results of cosine analysis, melatonin content and expression levels of aralkylamine N-acetyl transferase (AANAT) and N-acetylserotonin O-methyltransferase (ASMT) in the 12 L:12D and 24 L:0D groups showed significant circadian cosine rhythms (P < 0.05) and tended to be higher during the day and lower at night. Compared with the variation trend of melatonin, the expression levels of melatonin receptor (MTR) in each group showed significant circadian cosine rhythms (P < 0.05). Especially in the 0 L:24D group, the expression levels of MTR also tended to be higher during the day and lower at night, indicating that MTR may mediate other factors which participate in the regulation of abalone circadian rhythms. The results of this study provide a quantitative description of the motion behaviour characteristics of abalone exposed to different light cycles. The intrinsic correlation between melatonin secretion and abalone motion behaviour rhythms was also examined in this study, which in turn provides a reference for light regulation and feeding strategies in aquaculture production.

Introduction

Light is a critical environmental factor. The behaviours and physiological characteristics of aquatic organisms result from long-term adaptation to environmental factors such as changing light conditions and temperature, so that individual benefits are increased as much as possible (Badruzzaman et al., 2013). Light cycle is the primary factor influencing the timing of growth and development. Subject to the impact of alternate day and night, light environment factors are extremely complex and exhibit great variability over short time periods (Villamizar et al., 2011; Wei et al., 2019). In response to the periodic changes of the external natural environment, organisms can regulate their own motion behaviour which then evolves into regular behavioural characteristics, also known as “biological rhythms”. The most common rhythms in the biosphere are the 24 h circadian rhythms which occur as a result of the rotation of the Earth (Johnston et al., 2016).

The abalone Haliotis discus hannai is one of the most economically important marine shellfish species in China. In 2018, Chinese abalone aquaculture production was 163,300 tons, accounting for more than 90% of the total global yield (FAO, 2019). In the wild, abalones live in rocky reefs and hide in cracks in the rocks during the day and crawl out to feed and exercise at night, which is considered a typical circadian rhythm pattern (Wang and Wang, 2008). This nocturnal behaviour means that animals (e.g., abalone) do not have to move slowly or seek passive shell protection from predation by natural enemies. This behaviour can be attributed to the long-term environmental adaptation of abalone. Haliotis fulgens showed the highest growth rate in a 00:24 light: dark cycle (García-Esquivel et al., 2007). In a lightproof water tank, the growth rate of Haliotis rubra was 15.65% faster than that in light conditions (Day et al., 2004). In light conditions, the oxygen consumption rate and ammonia excretion rates of Haliotis discus discus were significantly higher than in a dark setting (Ahmed et al., 2008). These findings suggest that the circadian rhythm behaviours of abalone are closely associated with their physiological state. However, most studies on the motion behaviour of abalone are limited to experience-based judgment, without quantitative descriptions. It remains unclear whether abalone have an endogenous physiological regulation mechanism in place to drive body rhythms synchronized with cyclical environmental changes.

Melatonin is a kind of indole monoamine transmitter hormone. Secretion peaks at night and degrades in the daytime when light conditions are available. Its synthesis is regulated by light signals and the nervous system. The synthesis of melatonin involves two enzymes aralkylamine N-acetyl transferase (AANAT) and N-acetylserotonin O-methyltransferase (ASMT). AANAT is a key rate-limiting enzyme that catalyses the conversion of serotonin-to-melatonin and can acetylate the amino of 5-hydroxytryptamine and ultimately produces melatonin under the action of ASMT (Rath et al., 2016; Tan et al., 2016). The melatonin released in the blood can be transported to all tissues and organs in body and bind to melatonin G protein-coupled receptors on target cells as a means of participating in the regulation of circadian rhythms (Slominski et al., 2018). The addition of exogenous melatonin into water would change the motion period of Girardia tigrina, cause a dramatic reduction in the moving velocity of Caenorhabditis elegans, and along with the increase in melatonin injection dosage, the cumulative moving distance, steps and duration of cumulative movement of Apostichopus japonicus would also significantly decrease (Ding et al., 2019; Omond et al., 2017; Tanaka et al., 2007). However, the physiological regulation of melatonin depends on melatonin receptors. Two subtype receptors of melatonin, MT1 and MT2, mainly exist in the retinal neurons and ganglion cell layers and are closely associated with the rhythmic expression of the circadian clock gene. MT1/MT2 receptor will form a heterodimer, activate the phospholipase C/protein kinase (PLC/PKC) pathway, and inhibit cAMP-related signalling pathways, resulting in the altered expression and phase of the circadian clock gene (Baba et al., 2013; Lee et al., 2018). To date, the intrinsic correlation between melatonin secretion and the motion behaviour of abalone has not yet been reported. In addition, the impact of light cycle on melatonin secretion and the expression of its receptor genes has not been investigated.

In this study, the motion behaviour characteristics of abalone were quantitated using infrared camera technology and professional behavioural analysis software, to identify the characteristics of melatonin secretion and the expression of its receptor genes under different light cycles. The inherent relation between melatonin secretion and abalone motion behaviour was also analysed. These findings will provide a theoretical reference for light regulation and feeding strategy selection in aquaculture production systems.

Section snippets

Source and acclimation of experimental abalones

Juvenile abalones (shell length: 9.13 ± 0.69 cm, body weight: 89.92 ± 2.16 g) were purchased from Fuda Abalone Aquafarm (Jinjiang, Fujian, China). All experimental abalone were sourced from the same batch after artificial hatching. Prior to the experiment, abalones were placed in two culture tanks (0.8 m length × 0.4 m width × 0.4 m height), with the predefined light cycle 12 L:12D to acclimatise for 10 days. The seawater in the tanks was exchanged once a day and continuously aerated. Water

Abalone motion behaviour under different light cycles

The results of continuous 24-h monitoring showed that light cycle had a significant effect on the cumulative movement distance of abalone (Fig. 1a, P < 0.05). Cumulative movement distance was longest in the 0 L:24D group, at 38,533 ± 3203 mm. The cumulative movement distance was lowest in the 24 L:0D group, at just 12,925 ± 3461 mm. The duration of movement varied greatly from group to group (Fig. 1b, P < 0.05). The maximum duration was recorded for the 0 L:24D group with 27,301 ± 2325 s of

Discussion

Behaviour is the external response of animal to changes in the internal and external environments. Organisms can form endogenous rhythms that are similar to the periodic changes of the external environment as a way to adapting to environmental changes during evolution, with 24-h circadian rhythms being the most common of these (Dunlap et al., 2004; Gleiss et al., 2017). As a typical nocturnal creature, the motion behaviour of abalone is often observed by the naked eye and judged by experience,

Author statement

XLG, CHK and WWY conceived the project. XL and GWP participated in the design of the study and discussed the results. Measurement of growth and RNA extraction were conducted by GWP. XLG carried out data analyses and wrote the manuscript. All authors have read and approved the final manuscript.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have influenced the work reported in this paper.

Acknowledgements

This research was supported by grants from the Chinese Ministry of Science and Technology through the National Key Research and Development Program of China (2018YFD0901400), Fujian Ocean and Fisheries Research Grant (FJHJF-L-2020-7), Earmarked fund for the Modern Agro-industry Technology Research System (CARS-49), China Postdoctoral Science Foundation Grant (2019M650153), and the Outstanding Postdoctoral Scholarship from the State Key Laboratory of Marine Environmental Science at Xiamen

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