Endocrine disrupting pesticides impair the neuroendocrine regulation of reproductive behaviors and secondary sexual characters of red munia (Amandava amandava)
Introduction
Reproductive success in vertebrates depends on display of sexual behaviors which coordinates fertilization and reproduction. Sexual behaviors are modulated by environmental/seasonal factors, such as changes in photoperiods, temperature, rain fall, humidity etc., during reproductive development and maintenance, in mammals and birds [1], [2]. In mammals, photoperiod-induced changes during gonadal growth/development have been correlated with occurrence of sexual behaviors, such as courtship, territoriality, copulation etc. [3]. Transfer of photoperiodic birds from short to long days, induces the testicular development and expression of male sexual behavior [4]. Photoperiod-induced changes in gonadal growth/development use to influence sexual differentiations and results in profound sex differences in courtship, territoriality, copulation etc. and also secondary sexual characters, such as plumage pigmentation and beak/toe color.
The avian brain exhibits a remarkable degree of steroid hormones induced/dependent neuroplasticity which is influenced by seasonal changes and other environmental factors. Development of sexual behaviors largely depends on sex steroids androgens and estrogens [5], [6]. In hypothalamus, sex steroids bind to their specific nuclear receptors, such as androgen receptors (ARs), estrogen receptors (ERs: α and β) and progesterone receptors (PRs), and regulate the mechanisms that are important for sexual development. Testosterone undergoes rapid catabolism into 5-α-dihydrotestosterone (5-α-DHT) and 17-β-estradiol (E2) in preoptic area/POA and brainstem regions of hypothalamus and affects male specific courtship behaviors [7]. E2 induces the caudal nucleus of the ventral hyperstriatum/HVc regions in telencephalon for song production as well as facilitates mating behaviors in many birds [8]. Sex steroids are regulated by pituitary gonadotropins luteinizing hormone/LH and follicle stimulating hormone/FSH. Both gonadotropins as well as gonadal steroids are under regulation of the neuroendocrine pathway hypothalamus-pituitary-gonadal (HPG) axis. Hypothalamic neuropeptides gonadotropin releasing hormone/GnRH and gonadotropin inhibitory hormone/GnIH are important homeostatic regulators of the HPG axis. GnRH up regulates synthesis/release of gonadotropins and gonadal steroids. GnIH down regulates the gonadotropin synthesis/release form pituitary and it also has been reported to inhibit sexual behaviors in white-crowned sparrows [9].
EDPs have adverse effects on reproductive performances of human as well as wildlife species [10], [11]. Birds are more susceptible to pesticides-induced disruption of the neuroendocrine system. Characteristics that have a profound influence on the toxicological and toxicokinetic consequence of an EDC exposure in avian species include high rates of food consumption, high metabolic rates, periods of starvation that mobilize lipid reserves, hormone-dependent behaviors, developmental strategies, and control of sexual differentiation [12]. Disruption of the neuroendocrine system such as that of HPG and hypothalamic-pituitary-thyroid (HPT) axes, therefore, may result in disruption of secondary sexual characters and sexual behaviors. Though pesticides have shown to disrupt the development of secondary sexual characters and sexual behaviors by affecting plasma profiles of sex steroids in fish [13], [14]; laboratory investigations on pesticides-induced disruption of sexual behaviors are lacking in other vertebrate, particularly in birds. The present study was thus focused on the pesticides-induced disruption of sexual behaviors and secondary sexual characteristics in a seasonally breeding male bird, red munia (Amandava amandava) during the reproductive phase (pre-breeding/preparatory and breeding/courtship stages) of reproductive cycle. Effects of two contemporarily used pesticides, a dithiocarbamate fungicide mancozeb/MCZ and a neonicotinoid insecticide imidacloprid/IMI, were studied as individual as well as combinatorial exposures. Effects of MCZ as individual exposure on the rat gonad [15] and in a mixture with four other pesticides epoxiconazole, prochloraz, tebuconazole and procymidone on spatial learning as well as mating behaviors have been demonstrated [16]. IMI is an agonist of the nicotinic acetylcholine receptor (nAChR) and can modulate normal reproductive behaviors by disrupting ACh in brain which stimulates sexual arousal [17], [18]. The effect on reproductive behavior was assessed through study of courtship behaviors (song tunes and mating patterns) and that of secondary sexual characters from beak color and plumage pigmentation. Plasma levels of pituitary hormones (LH, FSH and PRL) and sex steroids (testosterone and E2) as well as in situ expression of GnRH, GnIH and ARs in testis were assessed to correlate the sexual behavioral abnormalities to impairment of reproductive related hormones.
Section snippets
Experimental design
Male birds were collected in and around Allahabad, India (25°27′N 81°44′E), from a particular forest area away from croplands (to avoid background exposures to pesticides) during first week of July (preparatory stage) and first week of September (breeding/courtship stage). They were acclimatized for 10 days in the open air aviary under natural conditions of temperature and photoperiod with an ad libitum supply of food and water. Only adult birds were included in the study. All male birds were
Results
The effect of pesticides exposure on development and maintenance of secondary sexual characters and on sexual behaviors is summarized in Table 1.
Discussion
The present study revealed that exposures to dithiocarbamate MCZ and neonicotinoid IMI pesticides disrupt the development and maintenance of secondary sexual characters and sexual behaviors in a seasonally breeding wildlife bird red munia. More prominent effects in co-exposed groups indicated cumulative toxicity due to combinatorial actions of both pesticides (and/or their metabolites). Display of sexual behaviors and reproductive performances are under the regulation of neuroendocrine HPG
Conflict of interest
The authors declare that they have no conflicts of interest regarding this work.
Funding
This work was financially supported by University Grant Commission (UGC), New Delhi, as a Major Research Project (No. 39-600/2010(SR) Dt. 10/01/2011) to B. Mohanty.
Acknowledgement
Avian-specific antigens and androgen receptors were kindly provided by National Hormone and Pituitary Program (NHPP), USA.
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