Endocrine disrupting pesticides impair the neuroendocrine regulation of reproductive behaviors and secondary sexual characters of red munia (Amandava amandava)

doi:10.1016/j.physbeh.2017.01.030

Physiology & Behavior

Volume 173, 1 May 2017, Pages 15-22

https://doi.org/10.1016/j.physbeh.2017.01.030 Get rights and content

Highlights

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Pesticides impair sexual behaviors and secondary sexual characters in seasonal birds.
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Pesticides induced the disruption of the neuroendocrine HPG and lactotropic axes.
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Imbalance of pituitary and testicular hormones are linked to behavioral impairments.
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Testicular GnRH-/GnIH-ir revealed disruption of respective receptors/neuropeptides.

Abstract

The exposure effects of two endocrine disrupting pesticides (EDPs), mancozeb/MCZ and imidacloprid/IMI of the group dithiocarbamate and neonicotinoid respectively, on reproductive behaviors and secondary sexual characters have been studied in a seasonally breeding wildlife bird, red munia (Amandava amandava). Adult male birds were exposed to both the pesticides individually (0.25% LD₅₀ of each) as well as co-exposed (MIX-I: 0.25% LD₅₀ of each and MIX-II: 0.5% LD₅₀ of each) through food for 30 d in preparatory (July–August) and breeding (September–October) phase of reproductive cycle. Singing and pairing patterns started decreasing from 2nd week to complete disappearance during 4th week of pesticides exposures at both the phases of reproductive cycles. Similar trend was observed in the disappearance of spots on the plumage as well as color of both plumage and beak which turned black/gray from red. Pesticides caused impairment of the lactotropic as well as hypothalamic-pituitary-testicular (HPT) axes as there was increased plasma PRL and decreased LH, FSH and testosterone levels. Testicular expressions of GnRH and androgen receptor/AR were significantly decreased but that of GnIH significantly increased as compared to control. Significant differences among individually- and co-exposed groups were also present. Abnormalities in sexual behaviors and secondary sexual characteristics could be linked to inhibition of HPT axis and/or direct toxicity at the level of hypothalamus, pituitary and testis. In addition, pesticide-induced hyperprolactinemia as well as impaired thyroid hormones might have also affected maintenance of reproductive behaviors. On co-exposures, the more distinct impairments might be due to cumulative toxicity of pesticides.

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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Endocrine disrupting pesticides impair the neuroendocrine regulation of reproductive behaviors and secondary sexual characters of red munia (Amandava amandava)

Highlights

Abstract

Introduction

Section snippets

Experimental design

Results

Discussion

Conflict of interest

Funding

Acknowledgement

Front. Zool.

Physiol. Behav.

Trends Endocrinol. Metab.

Front. Neuroendocrinol.

Brain Res.

Horm. Behav.

Horm. Behav.

Reprod. Toxicol.

Horm. Behav.

Chemosphere

Horm. Behav.

Neurotoxicology

Peptides

Toxicol. Appl. Pharmacol.

J. Steroid Biochem. Mol. Biol.

Neuroendocrine regulation of gonadotropin secretion in seasonally breeding birds

Front. Neurosci.

Sex differences in survival costs of reproduction in a promiscuous primate

Behav. Ecol. Sociobiol.

Low sex steroids, high steroid receptors: increasing the sensitivity of the nonreproductive brain

Dev. Neurobiol.

Impact of endocrine disrupting chemicals in gynecology

Hum. Reprod. Update

Factors considered in using birds for evaluating endocrine-disrupting chemicals

ILAR J.

Antiandrogenic pesticides disrupt sexual characteristics in the adult male guppy (Poecilia reticulata)

Environ. Health Perspect.