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Antracol administration has disturbed the reproductive cycle of domestic pigeon Columba livia domestica.


All over the world different types of pesticides are being used for the control of different types of damages caused by pests. Propineb (polymeric-Zinc propylen-bisdithiocarbamate) is one of the broad spectrum fungicide currently widely used as a protective treatment for several crops to control various fungi, especially Oomycetes, Ascomycetes and fungi imperfecti [1]. Propineb, analog to other dithiocarbamtes (DTCs) has a tendency to conjugate with other molecules containing SH groups and form metal chelates, which have given them advantage to influence the enzymatic activities of different proteins, and their antioxidant properties have promoted a wide spread application of this class of compounds in many industrial processes [1] and in medicine [2, 3]. However, the extensive use of these chemicals in agriculture has raised concern for their effects as occupational and ecotoxicological hazards [4], despite their low acute toxicity [5]. DTCs by their lipophilic nature pass across the cell membrane easily, and also several studies have showed the teratogenic, goitrogenic and neurotoxic effects of these molecules and their metabolites [6, 7]. [8] showed that propineb induced the release of acetylcholine, which was mediated through the polymerization of actine cytoskeleton. Moreover, DTCs metal complexes induced dopamine oxidation and produced intraneuronal oxidative stress leading to neuronal damage [9]. Since DTCs chelate heavy metals as Cu, Zn and Fe leading to their intraneuronal accumulations, these metals have been implicated in promoting lipid peroxidation, oxidative stress and enzyme inhibition causing then neurotoxic effects [10, 11]. Maneb was found to induce nitric oxide production, lipid peroxidation and cause parkinson's like disease syndrome in mice [12]. On the other hand, there are several reports suggesting the endocrine disruptive actions of DTCs; by inhibiting spermatogenesis in rats [13] affecting ovarian function and disturbing the estrous cycle, leading to rat infertility [14]. Both thiram and disulfiram inhibit 11 P hydroxyl steroid dehydrogenase 2 and interfere with their receptors' binding [15].

The aim of the present study has been to investigate the effect of propineb, an organometallic fungicide, on the reproductive cycle of male domestic pigeons (Columba livia domestica). Thus, gonadal growth, total body weights, thyroxin levels, plumage moult and the testis histological profiles were investigated under long days (18L: 6D).


Animals and treatment:

Commercial formulation of dithiocarbamate fungicide propineb [Antracol, 70% wettable powder WP (bayer France)] was used as the test pesticide. Solutions of this pesticide were made by diluting commercial formulations with drinking water of pigeons to obtain the required concentrations, which then given to birds.

Twenty four male pigeons (Columba livia domestica) with an average total body weight of (298 [+ or -] 23 g) were acquired from Skikda (North-East Algeria) at the end of February. Pigeons were housed in aluminium cages (x60x54x52 cm) with 4 individuals per cage. Birds were acclimated for 15 days in the animal house with standard conditions of natural photoperiod, ambient temperature and humidity of 20 [+ or -] 2[degrees]C and 55% [+ or -] 4, respectively. Food (chick crumbs) and water were provided ad libitium. Birds were divided into three groups of 8 individuals each, where the first group was used as a control, but the second one has received 2 g/l of propineb (tech 70% purity); a concentration used in agriculture. However, the third group was given 0.2 g/l of propineb. All groups were held under artificial photoperiod of (18L: 6D) using electric horologe of an intensity of 72 watts. Hence, water containing propineb was renewed every 48h.

Laparotomy, blood sampling and molt scoring:

Gonadal status was assessed at the start of the experiment and subsequently at 2 week intervals by laparotomy. This was performed through a small incision in the body wall between the last pair of ribs after anesthetizing the incision with viscous lidocain. The width and length of the left testis was recorded to nearest 0.5 mm using calipers and the volume was calculated as V= 4/3 [pi] [a.sup.2] b; where a is half the width and b is half the length (long axis).

Blood samples were obtained by pricking a superficial wing vein and collecting approximately 2 ml of blood in heparinized tubes. Blood was centrifuged at 1500g/min for 10 min and the plasma was separated and stored at -20[degrees]C.

Molt scores were assessed as the mean of the number of the nine primary feathers lost on both wings, which are normally shed in regular sequence, at the time of reproductive regression.

Pigeons were killed at the end of the experiment and testes were dissected out and weighed and then they were fixed for histological studies.

Analytical procedures:

Plasma free thyroxine (FT4) was estimated by automated micro particle enzyme immunoassay (Architet CI8200, Laboratory Abott) using commercial kits.


After decapitation, tissues were immediately fixed in Bouin's fluid for 24h, hydrated in alcohol grades and cleared in toluene prior to embedding in paraffin wax. Sections of 5 pm thick were cut by microtome, stained with haematoxylin and Eosin and monted on diesterase phthalate xylene.

Data analysis:

All data were expressed as mean[+ or -]SEM. The statistical significance of all data was evaluated using both student's test and analysis of variance (ANOVA). The significance was defined as p [less than or equal to] 0.01.


Changes in testicular size:

Changes in gonadal size measured during the present study are shown in fig 1. At the beginning of the experiment, all birds had mean testicular size of 235.3 [+ or -] 77 [mm.sup.3]. Control birds that were kept on 18L: 6D; long photoperiod throughout the experiment, all maintained fully reproductive cycle, characterized by significant (p<0.01) increase in the volume of their testes at week 6, followed by spontaneous gonadal regression, with testes reaching a minimal size of 235.5 [+ or -] 62 [mm.sup.3] (p< 0.01) by week 10 of the experiment. Treated groups had also showed a fully reproductive cycle. However mean testes size were inferior in the treated pigeons compared to the control. Under long photoperiod and 2 g/l of propineb, testes' volumes were 424.8 [+ or -] 74 (p [less than or equal to] 0.05) at the 6th week. However, the reduction in testicular size occurred after the 8th week of experiment.

Testicular Mass:

The mean combined testicular mass is shown in Fig. 2. All individuals had fully regressed gonads. There were a significant (P>0.05) differences between the combined testicular masses of treated birds, but they were all, of course, considerably smaller (P<0.05) than the combined testicular mass of the control.

Liver Mass:

The mean combined liver mass is shown in Fig. 3. Immediately after dissection, livers of the propineb treated birds were clearly swollen and having a brown-yellowish color and elevation in their liver weight

Changes in total body weight:

Changes in total body weight illustrated in figure 4 showed that, at the beginning of the experimentation, all individuals had a total body weight close to 298[+ or -] 23g. However, control birds showed an increase in their total body weights. Contrary, pigeons treated with propineb showed a decrease in their total body weights during the first weeks of the experimentation, before they regain their initial weights at the sixth week of experiment.

Primary Moult:

At the beginning of the experiment none of the birds was moulting, and consequently all individuals had complete numbers of primary flight feathers. Control and treated group (0.2 g/l) had begun to molt at the sixth week. However, the 3rd group (2 g/l) had started moulting at the 8 week of experiment. It should be noted that means molt score of control was superior to than those of the treated groups.

Plasma thyroxin:

Plasma thyroxin level showed significant variation between groups (p<0.01; fig. 6). Control birds maintained throughout the experiment on 18L: 6D had the highest concentrations (3.3 [+ or -] 0.24 g/dl), while individuals from treated groups (0.2 and 2 g/l) had much lower plasmatic thyroxin levels. All birds placed under 18L: 6D had recorded the highest concentrations of thyroxin at the 6th week before they had a declined levels at the end of the experiment.

Histological studies:

The histological assessments were conducted on tissue sections collected after exposure to long days and propineb treatment; a testicular lesion was evident although the differing concentrations of propineb. Histological observation of the testes showed uniform diameter of seminiferous tubules with a thick basal blade and the absence of spermatozoa in the lumen of seminiferous tubules marking thus, gonads regression and a refractoriness period. Histological examination of the testes from 0.2 g/l treated pigeons showed irregular diameter of seminiferous tubules with a little small and a fine elongated basal blade. It is necessary to note the presence of spermatozoa in the lumen of the majority of tubules. Histological observations of the testes from birds treated with 2 g/l revealed a much sever testicular lesions reflected by elongated seminiferous tubules, detachment of the seminiferous epithelium and sloughing of germ cells into the lumen of the seminiferous tubules. A whitish-grey color was also seen.


Recently, there has been increased awareness of possible affects of environmental contaminants on male reproduction [16]. In the present study, propineb was applied to domestic male pigeons (Columba livia) at 0.2 and 2g/l under long days (18L: 6D). The obtained results show that under long photoperiod (18L: 6D); all experimented birds maintained a fully reproductive cycle characterized by full mature testes at the 6th week, followed by spontaneous gonadal regression. In birds, the gonadal growth and regression are highly seasonal and relate to environmental factors such as food availability and the photoperiod length [17]. Therefore, the day length has been well defined as the regulator of different metabolic and reproductive activities in many avian species [18, 19]. Since the work of Rowan [20], it has been clear that the primary environmental factor used by birds to time reproduction is the annual changes in photoperiod. Birds have extra-retinal photoreceptors which they use, in conjunction with a circadian clock, to measure photoperiod [21, 22]. Exposure to long days (18L: 6D) causes reproduction maturation and full breeding condition [23, 24]. The physiological mechanism underlying the photo-stimulation is that an increase in photoperiod elevates the rate of secretion of gonadotrophin-releasing hormone I (GnRH-I), leading to augmented gonadotrophin secretion, and hence gonadal maturation such as luteinizing hormone (LH) and follicule hormone (FSH) which in turn induce gonad growth and steroid hormone production [25]. Actually, considerable amount of evidence is known about the neuroendocrine mechanisms of photo-stimulation. In Japanese quail, maximal photo-induction occurs about 14h after dawn [26]. Thus, an increase in luteinizing hormone can be detected 22h after dawn and an increase in GnRH-I secretion from hypothalamic cultured in vitro can be detected at the same time [27]. However, continued exposure to long days causes photo-refractoriness. As a result, gonadotrophin-releasing hormone (GnRH) cell bodies in the brain shrink and fibers emanating from these towards the median eminence show a marked decrease in immunocytochemical staining for GnRH [28, 29]. This has also been demonstrated in the sparrow, passer domesticus [30]. Hence, pituitary release of the gonadotrophin- luteinising hormone (LH) and follicule-stimulating hormone (FSH) is reduced to a minimum level [31, 23] and then the gonads undergo marked regression. Other physiological effects associated with photo- refractoriness are a peak in plasma prolactin and postnuptial molt [32, 33].

However, the administration of propineb at a rate of 0.2 g/l and 2 g/l to male pigeons under long days, does not affect only the development of testes, but also the speed of gonads growth. It has been recorded a lower means in testes sizes during the experiment in treated birds compared to controls. At the physiological level, it is difficult to discuss the correlation between the inhibiting effect of pesticides and the reproductive cycle of birds, but it is possible to measure the photoperiod. Therefore they hadn't estimated the true photoperiod, and consequently all photoperiod would be regarded as being short. In this context, several studies showed the inhibiting effect of the short days on the sexual maturity in many birds, including sparrow of trees (Spizella arborea), and curdle (Couturnix couturnix japonica), which undergo a total regression in their testes during the 18th weeks of experiment [34]. In addition, prolonged exposure to propineb might have interfered with testis function and indirectly acted at the level of hypothalamus or pituitary gland, or also directly on the testis as number of pesticides have showed testicular toxicity. Some studies suggested that pesticide exposure disrupts the hypothalamic pituitary endocrine function and indicated that FSH and LH are the hormones most affected in males [35]. Moreover, [36] have reported that the insecticide chlorodimeform may destroy endocrinologic homeostasis by suppressing GnRH release. It has also been reported that xenobiotics may affect reproductive function by direct insult to the cell populations within the gonads resulting in a feedback mechanism impairment of the hypothalamus and the pituitary [37].

Paired testicular mass, is a valuable index of reproductive toxicity in male animals [38]. The weight of testes is largely dependent on the mass of differentiated spermatogenic cells, but the reduction of their weights, was consistent with elimination of germ cells [39]. In the present study, decreased weight of control testes is due to the refractoriness [29]. However in this study, the weight of testes decreased significantly with increasing fungicide concentrations, which may be owed to elongated and reduced tubule size, and the reduced number of germ cells [40]. The presence of spermatozoa in the semineferous tubules of treated birds by 0.2 g/l indicated that these pigeons were not in the refractoriness period; subsequently the drop in their testes mass is possibly related to the fungicide treatment. Similar study [41] has found that mice's receiving mankozeb had decreased testes weight with an inhibition of spermatogenesis reflected by the significant decrease in the number of spermatogenic cells and sperms. Other study revealed a testicular atrophy with damaged germinal epithelium, accompanied with reduced sperm motility and viability in male adult rats exposed to maneb and zineb [42]. It has been showed that the carbamate insecticide carbaryl has affected spermatogenic cells and caused leydig cells degeneration and altered serum testosterone and gonadotrophin levels [43]. [44] revealed that propineb may be a mutagen agent due to the observed rise in the frequency of sperm abnormalities in mouse. Few studies have been carried out on the mechanisms of organometallic fungicide action on target organisms. However, many studies have been reported on the effects of heavy metals alone in a variety of organisms [45]. Exposure to most metals result in metal accumulation in certain tissues and organs of the exposed organisms. Zn is well known to accumulate in two particular organs, namely liver and kidney, where they may cause biochemical and histopathological changes [46, 47]. In the present study, exposure to propineb resulted in liver weight elevation, probably because of residues accumulation, since liver is the primary organ for metabolism and detoxification of xenobiotics. Thus, immediately after dissection, livers of the propineb treated birds were clearly swollen and having a brown-yellowish color, an indication of severe inflammation. Similar to our results, the administrated propineb to rainbow trout for 14 days has led to liver weight augmentation. Thus the histological examination has showed liver cell necrosis, an increase of sinusoidal space, intracellular oedema and pycnotocis nucleus [48]. Moreover, the liver of pregnant females exposed to 400 ppm propineb showed a dilatation of the wall of the liver vena centralis lobule, as well as irregularity and degeneration of hepatocytes around the vein [49]. Besides, an increase in the number of vacuoles, hyalinization and dilatation of the sinusoids between the hepatocytes were also observed [49]. Similar effects were found for the liver of one-day old rat litters from propineb treated mother, except that an infiltration of clustered cells indicating the occurring inflammation [49], in addition to Zn accumulation in the organs of both litters and mothers.

On other hand, the recorded increase in total body weight of the control birds during the actual study is certainly due to the reproductive activity. Previously, it has been reported a positive correlation between the total body weight and the reproductive activity [50]. On the other hand, oral administration of propineb at 0.2 g/l and 2 g/l to domestic pigeons involved a decrease in total body weight, especially in the first weeks of the experiment. In this study chronic diarrhea was clearly observed in birds exposed to propineb, especially in the highest dose, and this may well be one reason for the observed weight loss in male pigeons at the 4th week of the experimental period. Accordingly, the results of [51] were in line with our findings, in which the propineb subchronic exposure of male and female rats resulted in a drop of weight gain accompanied with severe diarrhea. Furthermore, propineb was found to cause diarrhea in birds, which is a well- known clinical picture for acute Zn overload [46].

The thyroid gland plays an essential role in the etiology of seasonal reproduction in birds [24, 29]. Thus, the active thyroid function is essential for this process, leading to the occurrence of refractoriness under long days. However, thyroidectomized birds stay fully mature under long days [32]. Termination of the refractory condition by thyroidectomy has also been observed in tree sparrows [34]. Plasma thyroxin concentrations increased when starlings were transferred from short to long days [52]. Though, treatment by exogenous thyroxin into sexually mature starling held under 11L: 13D induced overt manifestations of the refractory condition such as spontaneous gonadal collapse, decreased plasma gonadotrophin concentration, plumage molt, and increased plasma prolactin levels [33]. Therefore, it appears suitable to estimate the variation of thyroxin rates during this experimentation. So, the significant increase in plasmatic thyroxin at week 6 is due to the exposure to long days, which induces an increase in the thyroidal activity, and subsequently leads to increased levels of plasma thyroid hormones. This, in turn, could trigger an as yet unknown process in the central nervous system leading to photo-refractoriness and hence reduce GnRH output and gonadal regression [29]. Pigeons treated with propineb showed an increase in plasma thyroxin at the 6th week. However, these rates were smaller than those recorded in control birds. These results suggest that the inhibiting effect of the fungicide passes through the regulating process of the thyroid activity. It is known that propineb inhibited thyroid peroxidase and thus induced thyroid cancer in laboratory animals [53]. [54] also considered the common thyroid toxicity of propineb. It is important to note that any imbalances in the levels of thyroid hormones, in particular thyroxin disturb gonads development at many species of birds. Indeed, treatment by inhibiting compounds of thyroxin (carbimazol) or by exogenous thyroxin, have led to the inhibition of gonads growth in japaness quail [55] and in starlings [29]. Other physiological effect associated with photo-refractoriness is the post-nuptial moult [32, 33].

Therefore, moult scores readings were taken throughout the experimental period. By using the time of the onset of photo-refractoriness, the moult data supported the trends indicated by the testicular volume data in both control and 0.2 g/l treated pigeons. The delay of the onset of moult in birds treated by 2 g/l of propineb indicates that the regression of testes size is due to the propineb toxicity, excluding however the refractoriness effect.


Article history:

Received 11 June 2014

Received in revised form 21 July 2014

Accepted 20 August 2014

Available online 2 December 2014


Authors are grateful to the PNR projects, Algiers for the financial support. Thanks are given to the laboratory of animal ecophysiology, in which this work was carried out.


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(1) Souheila Slimani, (2) Mohamed Salah Boulakoud, (2) Cherif Abdennour and 1Doria Gueddah

(1) Department of Biology, Faculty of Sciences, University of 20 August 1955, Skikda, Algeria

(2) Laboratory of Animal Ecophysiology, Department of Biology, University Badji Mokhtar-Annaba, Annaba 23000, Algeria

Corresponding Author: Cherif Abdennour, Laboratory of Animal Ecophysiology, Department of Biology, University Badji Mokhtar-Annaba, Annaba 23000, Algeria

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Author:Slimani, Souheila; Boulakoud, Mohamed Salah; Abdennour, Cherif; Gueddah, Doria
Publication:Advances in Environmental Biology
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Date:Dec 1, 2014
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