Introduction
Food consumption and energy homeostasis are crucial physiological processes in fish that provide adequate energy for development, behaviour, and reproduction (Saravanan et al., 2012, Conde-Sieira and Soengas, 2017). Multiple regulatory networks that play a role in regulating food intake and energy balance have been identified in vertebrates. Ghrelin is a 28-a.a. peptide associated with the brain-gut axis, secreted from the stomach and intestine that promotes food intake and metabolic changes in part through the growth hormone secretagogue receptor (GHS-R) within the arcuate nucleus of the brain in mammals (Howard et al., 1996, Nakazato et al., 2001). In addition to its stimulatory effect on appetite and the secretion of growth hormone (GH) and prolactin in vertebrates, including fish (Kaiya et al., 2003, Unniappan and Peter, 2005), ghrelin is also implicated in the regulation of reproductive processes in vertebrates. For instance, ghrelin inhibits testosterone secretion and sperm cell factor (Barreiro et al., 2004, Tena-Sempere et al., 2002), reduces the frequency at which gonadotropin-releasing hormone (GnRH) neurons fire (Farkas et al., 2013) in rats, and inhibits luteinizing hormone (LH) and follicle-stimulating hormone (FSH) secretion in normal as well as ovariectomized rats (Fernández-Fernández et al., 2004; Furuta et al., 2001). In contrast, ghrelin treatment stimulates LH release in the carp Cyprinus carpio and the goldfish Carassius auratus (Sokołowska-Mikołajczyk et al., 2009, Unniappan and Peter, 2005; Grey et al., 2010) and promotes the number of fully grown follicles in the benni Barbus sharpeyi (Mabudi et al., 2011).
In addition, ghrelin protein or GHS-R1a (a ghrelin receptor) is expressed in the testes of rats and sheep (Barreiro et al., 2002, Gaytan et al., 2004, Miller et al., 2005, Kheradmand et al., 2009), and ghrelin mRNA is identified in the ovaries of the chicken Gallus gallus domesticus (Sirotkin et al., 2006). Among fish, ghrelin or ghrelin receptor-like immunoreactivity is observed in the ovaries of the goldfish C. auratus and the zebrafish Danio rerio (Sirotkin et al., 2006, Shepperd et al., 2012). Although GHS-R1a expression has been detected in the brains of different teleosts, including tilapia (Airapetov et al., 2021), ghrelin mRNA expression is not detected in either the testes or ovaries of the Nile tilapia Oreochromis niloticus (Parhar et al., 2003).
It is apparent from these studies that there are species-specific discrepancies in the effects of ghrelin on the reproductive axes of mammals and fish. The influence of ghrelin on the hypothalamic-pituitary-testis (HPT) axis and associated alterations in the food consumption rate are still unclear in teleosts. In contrast to mammals, fish have a distinctive mechanism of cystic spermatogenesis, wherein germ cells are generated within cysts located within the lobules of the testis before the release of spermatozoa into the lumen (Uribe et al., 2015). A literature survey reveals that there are no systematic studies on the influence of ghrelin on fish spermatogenesis. Tilapia (O. mossambicus), a commercially significant food fish, exhibits year-round spermatogenesis, making it an ideal model for studying the impact of ghrelin on the HPT axis.
The objective of this investigation is to elucidate whether treatment with the ghrelin agonist ipamorelin acetate (IPA), a selective GHS and agonist of the ghrelin receptor GHS-R1a, influences food consumption and the HPT axis of the fish O. mossambicus.
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Experimental design
Adult males of O. mossambicus inhabiting the ponds around Dharwad (75° 01′ E, 15° 27′ N) were procured from the local fishermen and acclimated to laboratory conditions for one month. The fish were kept in 75 L aquaria (36 × 12 × 18 in.) with a stock size of five fish per aquarium under natural conditions (11.58 ± 0.02 h photoperiod, 30.12 ± 1.02 °C water temperature, pH 7.45). Daily water renewal was monitored to prevent algal growth. Fish weighing 26–34 g were fed food pellets (Taiyo pet feed,
Food consumption rate, body weight, body length, and gonadosomatic and hepatosomatic indices
The mean food consumption rate increased (P<0.001) in 5 and 30 μg IPA-treated fish in a dose-dependent manner (Fig. 1a). No significant difference was detected between the IBW and FBW or between the IBL and FBL in the controls or in the 5 or 30 μg IPA-treated fish (Fig. 2a and b). There was no significant difference in the mean GSI among the different experimental groups (Fig. 3a), whereas the fish treated with 5 μg IPA exhibited a decrease (P<0.001) in the mean HSI compared to both the control
Discussion
Previous studies have revealed that the treatment of goldfish acyl ghrelin or human ghrelin and ghrelin-C10 peptide stimulates food intake in teleosts, goldfish C. auratus and tilapia O. mossambicus, respectively (Unniappan et al., 2004, Riley et al., 2005; Matsuda et al., 2006). The present study revealed the effect of exogenous treatment with the ghrelin-agonist pentapeptide IPA (Aib-His-D-2-Nal-D-Phe-Lys-NH2) on both food intake and the reproductive axis of tilapia. The results of the
Conclusions
In conclusion, our results indicate that treatment with the ghrelin agonist IPA promotes germ cells at the meiosis-I stage, possibly through LH release at the hypophysial level and 11-KT and androgen receptor protein expression at the testicular level in tilapia. In addition, testicular steroidogenesis, LH release, and testicular growth may be influenced by increased food consumption in tilapia. The physiological impact of ghrelin on testicular activity reported in the present study is very
CRediT authorship contribution statement
C.B. Ganesh: Writing – review & editing, Supervision, Conceptualization. Mallikarjun Gouda: Writing – original draft, Methodology, Formal analysis, Data curation.
Declaration of Competing Interest
The authors declare that there are no conflicts of interest.
Acknowledgments
The first author expresses gratitude towards Karnatak University, Dharwad, for granting a University Research Studentship (URS/2021/626). We thank Dr. Ishwar Parhar, Monash University, Malaysia, for the generous gift of the GnRH antibody. We would like to express gratitude for the infrastructural facilities provided by the Science and Engineering Research Board–Department of Science and Technology (SERB-DST), New Delhi, Government of India.
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