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/�/00�*R�4.!>�4J+�4yJ+����%�����D/D/l#,���0�������������������������������������������������������������������������4���������6	?:	@Metal contamination in the eggs of Peafowl, Pavo cristatus and Grey Francolin, Francolinus pondicerianus in India

R. Jayakumar1*, S. Muralidharan2, V. Dhananjayan3 and C. Sugitha2

1Department of Environmental Science, GITAM University, Hyderabad Campus, Rudraram, Medak � 502 329, Andhra Pradesh, India.

2 Division of Ecotoxicology, S�lim Ali Centre for Ornithology and Natural History, Anaikatty, Coimbatore � 641 108, Tamilnadu, India.

3Industrial Hygiene & Toxicology Division, Regional Occupational Health Centre (S), ICMR, Kannamangala P.O., Bengaluru, 562 110, Karnataka, India



*Corresponding author
GITAM University, Hyderabad Campus, Rudraram, Medak � 502 329, Andhra Pradesh, India.
Mobile No. +91 7893871711
Telephone:  08455-220555/56/57
Fax:  08455-220046
Email: rjkumar8@yahoo.com
Abstract  
Metal concentrations in eggs from Pea Hen (Pavo cristatus) and Grey Francolin (Francolinus pondicerianus) were measured to monitor the environmental contamination.  The homogenized contents of each egg were analysed by atomic absorption spectrophotometer for levels of copper (Cu), cadmium (Cd), lead (Pb) and zinc (Zn).  Copper was at a significantly greater level (approximately two fold) in eggs from Grey Francolin than in those from Pea Hen. Levels for Cd, Pb and Zn were not significantly different between species. The difference in metal levels may be related to species differences in habit, habitat and metabolic activity.  Levels of Cu and Zn appear to be background levels; however, Pb and Cd exceeded background levels substantially for poultry and should be investigated further to evaluate potential population-level and trophic effects.

Key words:  Eggs, Metal contamination, Peafowl, Gray Francolin, 

Generally, the nonessential trace elements occur both in wild and commercial birds mainly due to inputs from human activity. The effect of trace element contamination may manifest in the form of suppression of egg production, kidney damage and testicular damage (Hui 2002). Further the deformities caused by metal contaminants are often multiple and may include missing or abnormal eyes, beaks, wings, legs and feet.   Previous studies (Dauwe et al. 2005; Ayas et al. 2008; Henny et al. 2008; Mierzykowski 2010) have authentically illustrated the fact that eggs can serve as better indicators of metal contamination.  In India, toxicological studies on Indian Avifauna (Muralidharan et al. 2008; Dhananjayan and Muralidharan 2010; Muralidharan and Dhananjayan 2010; Dhananjayan et al. 2011) have clearly indicated that their contamination exposure is varied and obvious.   Owing to contamination, mass mortality of bird species such as Indian White-backed Vulture, Spotted Pelican, Sarus Crane has been reported (Dhananjayan et.al, 2011)   Further, contamination studies on eggs are available in the Indian context with special reference to pesticides (Muralidharan et al. 2008) and metals (Dey and Dwivedi 2000; Bibhash et al. 2010). As the referred studies have revealed the contamination pattern of pesticides and metal only in poultry eggs and select species of birds, there is a need for better understanding towards the metal contamination in wild bird eggs. Further the latter provide better clues to anticipate the impact if any, at population level. 

The species considered for the present study are Indian Peafowl (Pavo cristatus) and Grey Francolin (Francolinus pondicerianus) which come from a common family Phasianidae. They bear common habitat and foraging features. They are found in small groups in open grounds of forests and scrub jungles.  Being omnivorous in diet, their exposure to anthropogenic contamination is anticipated because both the species are observed foraging in human cultivations near the adjoining areas of forest. Importantly, Indian Peafowl being the national bird of the country, its exposure levels to contaminants is of important concern.   Bearing these factors in mind, the present study attempts to monitor metal contamination in eggs and  understand the variations in metal levels of select species of wild birds such as Peahen (Pavo cristatus) and Grey Francolin (Francolinus pondicerianus) and  the levels are also compared with the studies elsewhere to  comment on its toxicological implications. 

Material and Methods

During the year 2007-08, a total of 25 non-viable eggs of Indian Peafowl (n=8) and Grey Francolin (n=17) collected from abandoned nests for a specific study that monitored environmental contaminants in Indian Avifauna at S�lim Ali Centre for Ornithology and Natural History (Ministry of Environment and Forests, Govt. of India), Anaikatty, Coimbatore were shared for the present exercise.  They were collected from nests in the study areas (Coimbatore-11.16�N 76.58�E; Anaikatty Forests - 11�52�N 75�50�E; Chinniyampalayam 11�3�21�N 77�4�17�E; Karamadai -11�14�33�N76�57�36�E; Manipal - 13�20�49�N 74�47�17�E). At laboratory, the eggs were examined for any visible external crack or fissure. The external dirt was gently wiped using cotton dipped in high quality cleaning solution (Labolene-Glaxo India Limited) and cleaned with double distilled water. The egg was then gently broken by excising a mid-ventral line crack with the help of a scalpel and the contents were poured in a pre-cleaned beaker, coalesced to have a homogenous yolk and albumen. 

About 0.5 to 1g of the mixed contents were weighed using a top loading electronic balance (Mettler A E 240) and digested in Microwave Digestion System (Milestone, MLS 1200) using 10 ml HNO3 (69% GR) for 10 min, 1 ml HClO4 (70% GR) for 5 min and 5 ml H2O2 (30%GR) for 10 min at 250 W magneteron power settings. All reagents used in digestion were of analytical grade (Merck). The digested solutions were filtered using Whatman No.1 filter paper and stored in well-cleaned polythene vials in refrigerator and subsequently analysed using a double beam Atomic Absorption Spectrophotometer (Perkin Elmer, Model AAnalyst800). Atomic absorption spectrometry standards for metals, namely copper (99.9%pure), lead (99.5% pure), zinc (99.9% pure) and cadmium (99.5% pure) manufactured by Sisco Research Laboratories Pvt. Ltd., India were used for calibration. In order to validate calibration during measurements, after every ten samples, blank and calibration standards were read three times and % relative standard deviations were computed. While the detection limit for copper was 0.002 ppm, the same for cadmium, lead and zinc was 0.001, 0.03 and 0.02 ppm respectively. The quantification limits of metals were three times the detection limit. Recovery rates for copper, lead, zinc, and cadmium were performed through standard addition method. Ten recovery tests were performed for recovery and keeping the reference value as 1, the recovery rates for copper: 86% (0.86�0.019), lead: 85% (0.85�0.11), zinc: 90% (0.90�0.23) and cadmium: 88% (0.88�0.01). The results were not corrected for per cent recovery and expressed in �g/g of wet weight. 

The data was subjected to statistical analysis using Statistical Package for Social Sciences (SPSS) software version 17.0.  The distribution of the data was viewed employing Shapiro-Wilk W Test. As the distribution of data was not normal, non-parametric test such as Mann � Whitney U Test explored the variation in metal contamination among the species. The variation was considered significant at P < 0.05. The results were presented in ppm wet weight.

Results and Discussion

Twenty-five eggs belonging to two species, namely Grey Franclin (Francolinus pondicerianus) and Pea Hen (Pavo cristatus) were analyzed for metal contaminants, namely copper, lead, zinc and cadmium and the variation in metal contamination between the eggs of two species of birds was tabulated (Table 1). The concentrations presented in this study are in �g/g on fresh weight basis and corrected for moisture loss.  The present values were compared with studies elsewhere which reported the values on dry weight basis by converting them to wet weight using dry weight divided by three (Burger and Gochfeld 2004). It is inferred that the differences arising out of dry weight to wet weight conversion is very low and generally wet weight concentrations are slightly higher than fresh wet weight (Mierzykowski 2008).  

Significant variation in contamination could be observed for copper levels between the two species (Table.1) and the copper concentration in Grey Francolin was twice the Pea Hen levels.  The copper values reported in the species studied were comparable with the studies elsewhere.  Copper concentration in egg contents of Great and Blue tits collected from several sites of  Antwerp, Belgium closer to the proximity of metal smelter were 1.04 �g/g wet weight (Dauwe et al. 2005) and  it ranged between 0.44 to 1.10 �g/g in common tern eggs of relatively less polluted Maine Islands (Mierzykowski et al. 2008).  Further, a study on Piping Plover�s eggs from Delaware showed that the copper concentrations were 0.73 �g/g wet weight (Mierzykowski 2010). The background level for copper in avian eggs was approximately 1.1 �g/g wet weight (Seiler et al. 2003) and the present levels appeared as background levels. Significant variation in copper contamination could be due to the metabolic activity of the species in elimination or accumulation of copper (Becker 2001). The diet of Gray Francolin contains cereal grains, plant shoots, seeds of weeds and small insects and sometimes human excreta. Thus, the exposure to copper-rich diet must have eliminated the excess of copper in egg.  Although it is understood that, being omnivorous diet Pea Hen is more vulnerable to copper contamination, the body size and metabolic activity should be accounted. Comparatively Gray Francolin is smaller in size and has better chances to eliminate the excess copper through egg which has for high concentrations.

Lead values were found to be higher in Gray Francolin than Peahen with no significant variation (Table.1).Previous studies on Water bird�s eggs showed that lead levels were either in detection limits or in very low concentration (ranged between 0.13 to 2.2 �g/g wet weight) comparable to our findings (Hui 2002; Boncompagni et al. 2003; Dauwe et al. 2005). These results suggest low environmental inputs and the levels must have come only from the female and not from any external atmospheric deposition. Adult birds contain about four times more lead than in one month old juveniles and two times higher than in eggs (Hui 2002).   Studies done by Dey and Dwivedi (2000) reported concentrations of lead in Hen�s egg were ranged between 0.142 and 0.936 �g/g.   Further, the levels reported in Grey Francolin  higher when compared with  studies on domesticated avian eggs  particularly the chicken (0.14 �g/g wet weight) and quail (0.25 �g/g wet weight) which have a similar diet (Salwa and Shuhaimi-Othman 2011).  In the present study majority of the samples had lead concentration that exceeded the normal back ground concentration of lead (0.020 �g/g).  It should be noted that many studies that examined the partitioning of metals between egg contents and egg shell (Agusa et al.2005; Ikemoto et al.2005; Lam et al. 2005) have contradictory findings.  Owing to the differential binding nature of the metals, generally homogenised egg contents were preferred to examine the metal concentration.   However, egg shells are also found to accumulate fair concentration of metals (Dauwe et al. 2005; Kristy 2010) which is not examined in the present study.  Hence, the lead toxicity on the embryo could not be commented holistically.  

Of all the metals, zinc was found to be uniformly high in both species with no significant variation (Table.1). The background levels for zinc in avian eggs is approximately 10 �g/g wet weight (Seiler et al. 2003) and the present levels appear to be as background levels. Although the zinc values were higher among the four metals of this current study it is comparably lower than in the earlier reports (Dauwe et al. 1999; Mierzykowski 2010). Further the result also indicates that these high values are not attributable to any significant problem to the egg as it has been proved that zinc has more affinity towards yolk proteins and gets built into the embryo during embryogenesis (Morera et al.1997). Moreover, zinc was also found to be an essential element for the embryo growth, and zinc accumulation and body metabolism are carefully controlled (Nam et al. 2004). Thus it is logical to postulate that high values of zinc do not indicate any problem.

In the current study, mean values for cadmium were found to be near equal in both species and were found to be higher than the back ground levels (0.005�g/g) reported for poultry. Dey and Dwivedi (2000) had documented 0.072 � 0.004�g/g in the commercial Hen�s eggs.   Further the levels are comparably four times greater than the values  reported in chicken (0.018 �g/g wet weight) and quail eggs (0.03 �g/g wet weight) (Salwa and Shuhaimi-Othman 2011). It is known that Gray Francolin have a diet similar to that of a commercial egg laying Hen, but the exposure to contamination might vary. Further, being a wild inhabitant, Gray Francolin has better chances of exposure to the contaminated foraging grounds. It is also reported that Gray Francolin feeds on human feces which might serve as a plausible source of contamination. Trace metals such as cadmium and lead may interact with the metabolic pathway of calcium. Consequently, they may be incorporated more easily in the egg shell (Guitart et al. 2004).

Absence of significant variation between the two species shows that they should have gained a uniform and equal amount of contaminant exposure. Both the species bear a similar dietary habit and habitat which could scourge for cadmium contamination. The varying concentrations of metal in eggs in select species of birds could be due to many factors such as habit and habitat. Variation in metal contamination could also be due to metabolic activity of species. Gray Francolin have a similar diet to that of a commercial egg laying Hen, though the exposure to contamination might vary. Further, being wild inhabitants, Gray Francolin and Pea Hen have better chances of exposure to the contaminated foraging grounds. This study has clearly outlined the metal contamination pattern in the eggs of two species of birds, and except lead and cadmium levels, the concentrations of other metals do not create any toxicity. Further, the lead and cadmium concentrations have exceeded the normal levels prescribed for the poultry and hence these eggs if consumed intentionally by poaching are speculated to create an impact on humans in the long term which needs further systematic study. At this juncture, these results can be considered as starting points for expanding our investigations at population level in the context of Indian avifauna as there exist no report on the metal concentrations in the eggs of Indian birds. This study justifies the continuation of the exercise of using eggs as excellent indicators of metal contamination.

Acknowledgments�We sincerely thank the Ministry of Environment and Forests, Govt. of India for providing financial assistance. We also gratefully remember the founder director Dr VS Vijayan, SACON, Coimbatore for providing support. One of the author (Dr R Jayakumar) wishes to express his gratitude the Dr. MVVS Murti President, Prof G Subramanyam, Vice-Chancellor, Prof D Harinaryana Pro Vice-Chancellor and Prof. M Potharaju, Registrar of GITAM University for their kind support.  Further, we also appreciate Mr. S. Patturajan for his assistance in the laboratory.

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�d�gdc=d��7$8$H$gd��Muralidharan S, Dhananjayan V, Risebrough R, Prakash V, Jayakumar R, Bloom PH (2008) Persistent organochlorine pesticides residues in tissues and eggs of white- backed vulture, Gyps bengalensis from different locations in India Bull Environ Contam Toxicol 81:561�565
Nam D, Koo T (2004) Factors causing variations of lead and cadmium accumulation of Feral Pigeons (Columba livia). Environ Monitor Assess 95:23-35
Salwa AA, Shuhaimi-Othman M (2011) Metals concentrations in eggs of domestic avail and estimation of health risk from eggs consumption. J Biological Sciences 11:448- 453
Seiler RL, Skorupa JP, Naftz DL, Nolan BT (2003) Irrigation-induced contamination of water, sediment, and biota in the western United States � synthesis of data from the National Irrigation Water Quality Program U.S. Geological Survey Professional Paper 1655. 123 pp

Table 1 Variation in metal contamination (mean in �g/g �S.E on fresh wet weight basis) among the eggs of two species of birds

Species Copper Lead Zinc CadmiumGray Partridge
 (N = 17)1.51�0.16 
(0.53 � 2.52)0.82�0.43 
(BDL � 7.57)9.31�1.59 
(1.05 � 19.20)0.27�0.01
(0.19 � 0.35)Pea Hen
(N = 8)0.76�0.14 
(0.31 � 1.65)0.65�0.21 
(BDL � 1.70)10.67�1.58
3.83 � 18.62) 0.28�0.02
(0.22 � 0.36)Mann-Whitney U Test29.00
(p=0.023)38.00
(p=0.552)56.00
(p=0.485) 65.00
(p=0.861)Range (minimum and maximum) is given in the parenthesis 










 PAGE   \* MERGEFORMAT 8




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