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1 Introduction

The use of avian tissues for biomonitoring of contaminants has widely been used. Avian tissues are usefully used indicator because the concentration level of heavy metals in their tissues reflects their exposure and may also be indicative for trend of the past exposure. Initially, internal organs were collected after sacrificing a live bird, but more recently the demand of noninvasive technique leads to the use of feathers, eggs, and feces for biomonitoring of heavy metals (Burger 1993). Feathers and eggs are very special for metal accumulation studies not only because they can be collected without affecting the life of a bird but also for they have certain important information which is not possible to acquire otherwise (Dauwe et al. 1999). The use of feathers and eggs for heavy metal monitoring in soil has their own respective limitations, but eggs have certain several advantages over the other noninvasive biomonitoring matrices because they are easier to collect and can be preserved for a long time. In addition, eggs are relevant to a specific portion of the population, called as egg-laying female birds; they are formed during a specific duration of the life of a female and hence proven as a very good indicator for local exposure. Prior to egg laying, females of all the bird species from temperate and tropical zones spend a lot of time in their breeding grounds feeding on local resources for egg production (Dauwe et al. 2005). Unlike feathers, the composition of an egg is advantageous because its composition is highly consistent which does not change with size, age, or the position of the body. Eggs have been widely used for many of the recent biomonitoring studies, and it has been a proven fact that collecting a single egg in favorable circumstance has produced negligible effects on population parameters of the species (Furness 1993).

Soil is an important medium to support the life on earth. It is an essential part of biosphere which provides space for animal and plant anchorage and growth and regulates the cycles of nutrients and water. Since the advent of industrial revolution, the concentration of heavy metals increases alarmingly in the soil. As a result of rampant discharge of agricultural and industrial waste, the concentration level of heavy metals like most of the pollutants suddenly touched to the threatening threshold. Municipal waste, ore smelting, and the use of pesticide and fertilizers are the major anthropogenic sources through which toxic heavy metals are introduced in the soil (Meli et al. 2013). Heavy metals are carried from the source to the distant areas through water currents or land/soil movement. Soil is the ultimate medium which receives heavy metals from different sources and deposits them for a long time. Being the largest supporting medium for heavy metal deposition, soil and sediments serve as an archive and reservoir for metal deposition and their subsequent dissemination in plants and animal body parts through their feed. Most of the heavy metals particularly mercury, cadmium, and lead readily adsorbed on dead organic matter, waxy plant material, animal’s membranes, fats, and oppositely charged soil particles. After adsorption, the bioavailability of these toxic heavy metals for an organism will either depend on the properties of the metals and/or the physical, chemical, and biological properties of the medium into which it is released (Gamberg et al. 2005). Elevated concentration of heavy metals in soil greatly affects the capability of the soil to sustain its biological productivity, regulate the local environment, and provide the best condition for the growth of animals and plants and betterment of human health.

Heavy metals present in soil are taken by plants and animals through absorption and ingestion, respectively. Birds being the agile group of vertebrates receive metals during their lifetime exposure to soil. The concentration level in eggs of a species is a very good indicator for local exposure to soil. This is because of the reason that an egg is the only development in birds which is produced during a particular period of time by an egg-laying female fraction of a population. For breeding, birds are either sedentary (remain in their same habitat) or migratory (migrate toward their breeding grounds for breeding). Before egg laying, females build an actively defended breeding/nesting territory and exploit the local resources to the balance of nutrients during egg-laying season. Burger and Gochfeld (1995) reported that the concentration of metals in eggs represents the circulation level of respective metals in the blood which in turn reflects the recent exposure. Metals usually accumulate in the eggshell and/or egg contents during metal sequestration by the female (Mora 2003). Similarly, Burger (1993) said that eggs are the most vulnerable part to be affected with heavy metals and it exhibits the local exposure of the adult female which has laid them. Different studies reported the direct relation between the heavy metal concentration in soil and the level recorded in eggs of different bird species. The concentration of metals such as Pb and Cd concentration was found to be correlated in the soil and egg which suggests that soil is an important source for these elements (Waegeneers et al. 2009a, b). Similarly, the concentrations of Pb, Cd, and Cu in the eggs of gray heron (Ardea cinerea) and black-crowned night heron (Nycticorax nycticorax) were found indicative for their respective concentration in sediments of Nallihan Bird Paradise, Turkey (Ayaş 2007). In this way, an egg has been proven as a very useful biomonitoring tool for heavy metal contamination in soil.

The concentration of heavy metals in eggs in relation to soil may be affected by several factors. As this relation is much dependent on food of the organism, difference in the food chain may exist. It also depends on the dietary preferences of the species during breeding period. Interspecies differences and spatiotemporal differences were recorded in several studies (Akearok et al. 2010; Burger 2002; Dauwe et al. 2004). The difference between the eggshell and egg contents also gives useful information. Usually, for toxic trace metals such as Pb, Cd, Se, and Hg, the eggshell has been suggested to be a better indicator, while egg contents could be used as a best indicator for essential elements such as Fe, Mn, Zn, etc. (Dauwe et al. 1999). Moreover, it is suggested that data for egg metals for the same species should be collected for a period of consecutive years to identify the addition or deletion of any point or nonpoint pollution source and also to record the past trends of exposure (Burger and Gochfeld 1993). This chapter relates the metal concentration in eggs which is indicating the pollution level at different habitats, factors which affect the soil to egg metal ratio and the inexplicability of egg to soil metal relation. Further, this chapter also discusses the pros and cons for an egg as a biomonitoring tool for metal contamination and its scope for future biomonitoring research.

2 Soil Characteristics and Metal Bioavailability for Birds

Depending on the ecosystem, either terrestrial or aquatic, pollutant dynamics are rather different. In terrestrial ecosystems, the ambient environment is usually soil (Burger et al. 2004; Lam et al. 2005; Shahbaz et al. 2013), while in an aquatic one, it is usually the water or the sediment (Boncompagni et al. 2003; Mora 2003; Mora et al. 2007). Once metals get into soil or sediment, they have long residence times before they are eluted to other compartments. Acidity has a marked effect on the solubility of metals in soils and water. The mobility of metals in soils is dictated largely by the clay contents, amount of organic matter, and pH. In general, the higher the clay and/or organic content and pH are, the more firmly bound the metals are and the longer their residence time is in soil. In water, the solubility of metals is strongly pH dependent. In aquatic systems, metals may become “blocked up” in bottom sediments, where they may remain for many years. However, if the pH falls, metal solubility increases, and they become more mobile and hence more bioavailable (Cotín Martínez 2012). As the acidity changes, the oxidation state changes accordingly, and as a result, heavy metals can generate or break bounds with organic compounds generating specific compounds such as methylmercury. Methylated compounds are taken up more readily than the unmethylated form, due to its high lipoaffinity (Cotín Martínez 2012).

Unlike organochlorides (another known family of pollutants), which are distributed widely among body tissues, largely in relation to their lipid contents, heavy metals tend to be held in one particular tissue at much higher levels than the others. The site specificity of metals has an important influence on the choice of tissue for monitoring studies. For example, although females can excrete mercury into eggs, the amount they shed in this way is usually small compared to the amount put into feathers during molting (Honda et al. 1986). There are several different approaches for measuring bioavailability. In vivo tests use an animal to measure absolute bioavailability and toxicity. In vitro tests are performed outside the organism (Furman et al. 2006).

3 Egg as a Biomonitor for Soil Heavy Metals from Different Ecosystems

Governmental agencies, tribal nations, policy makers, managers, and the general public are concerned about the health of different ecosystems of the environment and require bioindicators that assess the levels of contaminants in individual organisms, populations, and communities. Chemical use is increasing in our environment and may pose a threat to some species and populations. The levels of many chemicals have been elevated in aquatic ecosystems (wetland, islands, marine land, and coastal areas) and terrestrial ecosystems (agriculture, forest, rural and urban) by using eggs (Table 7.1) as a biomonitor (Burger et al. 2009; Hashmi et al. 2013; Lam et al. 2005; Mora et al. 2011; Shahbaz et al. 2013), because of the influx from rivers, as well as runoff and direct pollution (Furness and Rainbow 1990), and from atmospheric transport and deposition.

Table 7.1 Biomonitoring of heavy metals using eggs from different areas and bird species
Full size table

3.1 Terrestrial Ecosystem

Terrestrial ecosystem exists only on landforms which may cover agricultural areas, forest areas, urban areas, and rural areas. Hence, terrestrial ecosystems are major hotspot for the chemical deposition from anthropogenic activities (agriculture and industrial) and natural processes. These anthropogenic activities and natural processes have not only affected terrestrial ecosystem services but also other living things (human, animals, etc.). Biomonitoring approaches using bird’s eggs as a bioindicator tool to probe out the integrity of different areas of terrestrial ecosystem have been used a few decades ago. Several research articles reported eggs as a suitable bioindicator of agricultural areas (Hashmi et al. 2013; Shahbaz et al. 2013), urban areas (Burger et al. 2004; Burger and Gochfeld 1995, 2004; Dev and Bhattacharjee 2010; Ek et al. 2004; Evers et al. 2003; Fu et al. 2014; Gochfeld 1997; Hui 2002; Lam et al. 2005; Mora 2003; Mora et al. 2007, 2011; Orłowski et al. 2010; Sekeroglu et al. 2013; Swaileh and Sansur 2006), rural areas (Kitowski et al. 2013; Orłowski et al. 2010), and industrial areas (Burger et al. 2004; Burger and Gochfeld 2004; Dauwe et al. 1999, 2005; Gochfeld 1997; Mora et al. 2011; Orłowski et al. 2010; Scheuhammer et al. 2001).

3.2 Aquatic Ecosystem

Aquatic ecosystems or environments are particularly sensitive to heavy metal contamination because aquatic physicochemical conditions can facilitate the conversion of unavailable forms of heavy metals into more bioavailable forms, which accumulate very efficiently in top predators. The life histories and ecological niches occupied by many aquatic birds predispose them to accumulating heavy metals, and the toxicology and merits/limitations of using eggs for monitoring heavy metals have been studied extensively. Aquatic ecosystems such as wetlands, islands, marine lands, and coastal areas provide breeding habitats for egrets, herons, and waterfowls and receive untreated effluents from agriculture and industries and cities from point and nonpoint sources of pollution. Hence, wetlands, islands, marine lands, and coastal areas act as a depository reservoir of organic as well as inorganic pollutants. Species that forage in aquatic environments are particularly vulnerable because of the potential for the rapid movement of contaminants in water, compared to the movement in terrestrial environments, and because chemicals can be stored in sediments in intertidal environments, providing a pool for years to come. A variety of toxic substances enter the water from surface runoff, industrial effluent, air pollution, wave action, the movement of organisms, and the high traffic of marine shipping entering these ports. Organisms that live in these estuarine systems can bioaccumulate organic and certain inorganic substances over time and are at risk from both lethal and sublethal effects, as their body burdens increase. Several studies used eggs as a biomonitor of heavy metal contamination in the soil and sediments of wetland ecosystems (Shahbaz et al. 2013; Hashmi et al. 2013; Jackson et al. 2011; Ayaş 2007; Kertész and Fáncsi 2003; Burger and Gochfeld 2004; Mora 2003; Mora et al. 2007 Boncompagni et al. 2003; Bischoff et al. 2002; Goutner et al. 2001), island ecosystems (Xu et al. 2011; Burger et al. 2009; Pereira et al. 2009; Burger et al. 2008; Ayaş et al. 2008; Agusa et al. 2005; Burger 2002; Gochfeld 1997; Sanpera et al. 2000, 1997; Burger and Gochfeld 1995), marine ecosystems (Akearok et al. 2010; Day et al. 2006), and coastal ecosystems (Pereira et al. 2009; Burger and Gochfeld 2003; Mateo et al. 2003). However, most of the published literature focused on the island and wetland ecosystems to monitor the heavy metal contamination by using eggs than the other ecosystems.

4 Factors Influencing Accumulation of Soil Heavy Metals in Eggs

4.1 Interspecific Variations

Metal accumulation in eggs is different for different species of birds. Several factors such as age and health of the female, diet preferences during breeding season, taxonomic affiliation, and the trophic level of the species and metal concentration level in the surrounding environment either singly or synergistically influence the overall metal burden in egg of different bird species. Heavy metal accumulation in eggs of different species largely depends upon the metal availability, metal intake, and physiological mechanisms for metal circulation, accumulation in the parts of the body, regulation, and subsequent excretion. All of these factors vary for different species and/or within the species and hence cause intra- and interspecific variation for metal accumulation in eggs. Differences of heavy metal concentrations in the eggs of different species have been reported in several studies (Akearok et al. 2010; Boncompagni et al. 2003; Burger 2002). There are several possible reasons for interspecific metal variation in eggs. One of the most important is the difference of the habitats/locations which different species prefer for foraging during breeding season. As the choice and requirement of nutrients differ for species, they accumulate metals in different quantities in their eggs (Ayaş 2007). A study reported by Boncompagni et al. (2003) concluded that the dissimilar concentration level of heavy metals in the eggs of three egret species foraging in the same area was because the female may have to visit different habitats for foraging prior to or during breeding and egg formation. So the phenomenon of visiting different locations for the sake of fulfilling its nutrient requirement has proved to be the basic factor influencing the ratio of soil and egg concentration level of heavy metals for different species. The next question in this regard may be that why eggs of different species exhibit different concentrations of metals inhabiting the same location? There is no straightforward answer yet being provided through research. But it is described by the physiological mechanism differences for the circulation, regulation, excretion, and replenishment of metals for different species. In general, one can say that both of the abovementioned factors, i.e., the difference of location and difference of the regulation of body metal burden, markedly influence the metal concentration level in eggs.

4.2 Influence of the Trophic Levels

Concentrations of metals in eggs are mainly attributed to the diet of the organism. Shahbaz et al. (2013) reported that elevated concentrations of toxic metals such as Cd, Cr, and Pb and some essential elements, viz, Mn, Fe, and Zn, in the egg contents of cattle egret are directly related to the higher concentrations of these metals in prey and soil of their foraging sites. They also deduced that unlike feathers, the concentration of heavy metals in eggs is more influenced by the environmental condition and food items. Similarly, elevated concentrations of Pb and Cd in the diet and sediments were found to be directly associated with the higher concentration of these metals in herons of Korea (Kim et al. 2010). The higher concentration of strontium in the eggshell of passerine birds from Arizona was probably associated with the higher deposition of Sr in the surrounding of the nesting sites of these birds. These passerine birds feed on certain invertebrates and insects which were associated with the recycling of Sr in the soil (Mora 2003). While studying the accumulation of Hg in different species, Burger (2002) found that larger fish-eating birds tend to accumulate more metals in their eggs when compared to small fish eaters. Similarly, in comparison with carnivores, omnivores and invertebrate-eating species accumulate lower metal accumulation in their eggs and showed that for birds, certain metal concentration increases with the increase in the trophic position. But this is not true for all the metals nor for all species. Being higher on the food web, the concentration of Hg in the eggs of common tern (Sterna hirundo) was found twice than those of duck species (Akearok et al. 2010). Boncompagni et al. (2003) reported that the concentration level of different heavy metals in the eggs and different other tissues of egret species was indicative of the concentration of the respective metals in sediments and prey items. So the birds which feed on the prey which largely relies on metal-rich soil for their food should have more metal concentration in their eggs. In general, one can say that the concentration level of heavy metals increases with the increase in the trophic position of the species, but one has to keep in mind the respective food chain and food web to get a meaningful result.

4.3 Temporal Variations (Inter-clutch and Intra-clutch Differences)

Temporal variation in egg metal content describes the time-based changes in the level of metal concentration and hence the difference in the local exposure. Temporal variation in the egg metal level provides information that can be useful for understanding the sudden shift of metals which in turn can be used to find any new addition in the metal pollution source (Burger and Gochfeld 2003). It is usually recommended to collect year-wise data for the same species for consecutive years to get a better understanding about the trends of metal accumulation. Significant differences in the concentration of heavy metals such as Pb, Cd, Se, and Hg were recorded in eggs of herring gulls (Larus argentatus) between the years 1998 and 1994. But the concentration level of metals in eggs rarely remains consistent for any metals between the years because of the changing metal pollution level for the location which the female is visiting for foraging prior to egg laying (Burger 1994). Furthermore, seasonal variation in the availability of heavy metals is obvious, so the exposure varies between different species and seasons. This is because the onset of breeding period is not the same for all the species, so the female of the different species may be exposed to the varying levels of heavy metals and hence accumulate different levels of metals in their egg. Seasonal bioavailability of heavy metals in soil is largely based on soil characteristics and local environmental condition and weather attributes. Besides inter-clutch variation in metal concentration, intra-clutch variation has also been observed for several metals. Custer et al. reported that sometimes systematic trends of metal concentration could be observed with egg-laying order, but it is not consistent for all the species nor for all the metals. Usually, the early laid egg has higher concentration of metals than later ones. Dauwe et al. (2004) reported that the time difference for laying eggs in any one breeding season has no significant effect on the metal accumulation in the female egg and hence on the number of sperm stored in perivitelline layer of the egg. Conversely, the concentration of several trace metals varied significantly between the home-produced chicken eggs in autumn and spring, but this temporal discrepancy of metals has not solely depended upon the concentration of these metals in soil (Waegeneers et al. 2009a). Similarly, temporal trends were recorded as spatial and temporal variations of Hg in the egg contents of gannet (Morus bassanus) between the years 1974 and 2004 from Bass Rock (North Sea) and Ailsa Craig (eastern Atlantic) (Pereira et al. 2009). Intra- and inter-clutch variations in the Hg level in the eggs of marine birds were reported and attributed to the diet switching of these marine species during their clutch periods. It is also proposed that an early clutch could be a better representative of the environmental state because it exhibits maximum metal load in females, metal burden which may be transferred to the offspring, and metals available for the predator (Akearok et al. 2010). The selenium level increases more than twofolds in the eggs of Florida scrub jays (Aphelocoma coerulescens) from 1996 to 2001 (Burger et al. 2004). No intra-clutch variation in the egg Hg level was reported in some piscivore and insectivore birds. The reason for this could be the body replenishment of Hg during egg-laying season mainly through ingestion and/or partly from the stored methylmercury in tissues and muscles (Brasso et al. 2010). Burger et al. (2008) reported that the clutches with more number of eggs exhibit variation than those with less number of eggs. In other words, the metal concentration varies within and among clutches, but no consistent trend has yet been observed. The lack of inconsistency among clutches of consecutive years is primarily attributed to the difference in the metal pollution level at the site where females visit during breeding season and partly may be due to species-specific responses toward metal burden in the consecutive years. Females may replenish the metal deficiency after laying the first egg and make up the metal deficiency effectively from the surrounding environment after each egg laid.

4.4 Geographical Difference

Metal contamination in egg is also influenced by the metal distribution level in the surrounding environment. Although not true for all the cases, the metal concentration level in egg is greatly influenced by the overall metal pollution burden of the surrounding environment and produces certain impairments in the egg. Differential exposure of species to soil heavy metals affects the total metal burden of the eggs and may produce certain abnormalities in the egg which in turn may affect reproduction. The exposure to the extreme level of heavy metals did not affect the egg of blue tit (Parus caeruleus) (Dauwe et al. 2002), while substantial impairments were observed in the eggs of pied flycatcher (Ficedula hypoleuca) and great tit (Parus major). It was also concluded that poor forest soil with less nutrient in combination with acidification affects the metal accumulation in egg and hence effects on egg quality (Eeva and Lehikoinen 1996). The soils with greater heavy metal pollution have been reported with lower sperm quality in males, poor mobility, and subsequent trapping in the perivitelline layer of the egg (Dauwe et al. 2002). Roodbergen et al. (2008) noted that the concentration of heavy metals such as Hg, Pb, and Cd was greater in soil, in earthworms, and subsequently in the egg of black-tailed godwit (Limosa limosa) at a polluted site which is contrasting to the reference site and suggested a direct transport of metals from the soil to the eggs through earthworm which is the primary prey of black-tailed godwit. Sekeroglu et al. (2013) reported that the metal concentration in eggs from the village chicken of Turkey is directly proportional to the distance from the roadside. Similarly, the concentration of toxic metals such as Pb, Cu, and Zn increases in the eggs of black kite (Milvus migrans) and decreases in distance from the solid waste incinerator (Blanco et al. 2003). Concentrations of heavy metals in the eggs of egret species were found higher in cosmopolitan areas where the metal pollution level was quite higher than relatively pristine areas (Boncompagni et al. 2003). Locational differences of Hg and Cd and Pb, As, Se, and Mn contamination in common tern (Sterna hirundo) eggs were recorded from five different locations of Barnegat Bay, New Jersey (Burger and Gochfeld 2003). It is evident from the above discussion that soil from different locations has the varying capacities of heavy metals which it can offer to plants, small invertebrates, and higher organisms. The greater the metal pollution sources, the higher the concentration in soil, and consequently more metals reached to the avian tissues and sequestered in egg which truly represents the local environmental state.

4.5 Eggshell or Egg Content Differences

Eggshell is thought to be associated with the sequestration of most of inorganic elements (Dauwe et al. 1999) and usually exhibits greater metal concentration of most of the inorganic elements when compared with egg contents. Mora (2003) reported that the concentration of most of the studied metals including Ba, Ni, Sr, Zn, Mn, and V was 2–35 times higher in eggshells of yellow-breasted chats (Icteria virens) and willow flycatchers (Empidonax traillii extimus) when compared with egg contents. Similar results for higher eggshell/egg content ratio were recorded in black-tailed gulls (Larus crassirostris) in Japan (Agusa et al. 2005) and for little egret (Egretta garzetta) and black-crowned night heron (Nycticorax nycticorax) in Hong Kong (Lam et al. 2004). Metals sequestered through eggs depend upon the requirement of the respective metals for embryonic development and need for metal regulation and excretion. Ayaş (2007) reported that the metal concentration in the eggshell itself is a very good indicator for the metal concentration level in egg content. The level of metal contents in the eggshell and egg content is different for different metals. Dauwe et al. (1999) draw an important conclusion that there is a discrepancy for metal sequestration between the egg contents and eggshell. They reported that essential metals such as Zn and Cu were greater in egg contents of great tit (Parus major) and blue tit (Parus caeruleus), whereas the nonessential metals such as Cd, Pb, and As were higher in the eggshell. No significant difference between the polluted and reference site was recorded. Further, they deduced that the eggshell being highly associated with sequestered nonessential metals is a good indicator as compared to egg content. Similarly, the concentration of Zn, Cu, Hg, and Mn was found 80–99 % lower in the eggshell of Audouin’s gulls (Ichthyaetus audouinii) than in egg contents (Morera et al. 1997). It is reported that eggshells are important for the excretion of heavy metals in birds (Burger 1994; Hashmi et al. 2013). The greater concentration level of essential nutrients in egg content is evidently associated with the regulation mechanism of these metals in the egg contents, whereas nonessential metals are sequestered in the eggshell for excretion. But the elevated concentration of these nonessential metals in the respective soil would tend to accumulate more metals in different bird tissues and subsequently sequester in the eggshell at a higher rate and affect egg quality and hence reproduction.

5 Heavy Metals in Soil and Eggs: An Equivocal Relation

Egg laying may be an additional excretory pathway for heavy metals available to laying female birds. Contaminant levels in eggs are useful bioindicators of exposure because they potentially represent different periods of exposure. The concentrations of metals in eggs are derived from females and represent the recent exposure in waters close to the breeding grounds, as well as mobilization of stored metals from the past intake (Burger 1994; Burger and Gochfeld 1996). However, the contaminant concentration in the eggs is also influenced by the presence of contaminants in nonbreeding areas (Burger 2002). Eggshell formation and egg laying are recognized as a means of excreting environmental contaminants (e.g., metals) by oviparous females (Burger and Gochfeld 1995; Gochfeld and Burger 1998; Lam et al. 2004, 2005), and thus contaminant concentrations in eggs can potentially be used as a surrogate for contaminant monitoring in egg-laying wildlife. Besides metals, bird eggs are also useful for evaluating lipophilic persistent organic pollutants (Connell et al. 2003). However, the contaminant concentrations in the eggs can also be influenced by contaminants present in areas utilized by these birds outside the breeding seasons (Burger 2002). Further, heavy metal content in the bird’s egg reflects local pollution levels (Burger 2002); because hens live in close contact with the outside environment, they are exposed to contaminants (Furness et al. 1993). Also, numerous studies have related the heavy metal contents of bird’s eggs and internal organs come from environmental pollution (Burger 2002; Burger et al. 2004; Hui 2002; Mora 2003; Sekeroglu et al. 2013). Hence, eggs are not influenced directly by soil heavy metal contamination, and there are no reports which suggest a direct relationship between soil heavy metal contamination and eggs (Day et al. 2006). However, several reports suggested eggs as bioindicator of soil heavy metal contamination by food chain (Boncompagni et al. 2003; Ikemoto et al. 2005; Mora et al. 2011; Shahbaz et al. 2013) or by intake of heavy metals from air into birds. The literature published so far on eggs as indicator of soil heavy metal contamination considered the food chain. Then, the birds after the regulation of heavy metals in the internal body excrete or maternally transfer heavy metals in the eggs or eggshell. Scheuhammer (1987) suggests that the transfer to the eggs only takes place if the concentration in the tissues of the female is high. Egg heavy metal contamination suggested that maternal transfer, food chain, and inhalation of metals could be responsible. However, some reports suggested that eggshells (Burger 1994) and egg contents (Lewis et al. 1993; Monteiro and Furness 1995; Monteiro et al. 1995) are important for the excretion of some trace elements in birds. Hence, eggshells and egg contents may be suitable to assess burdens of trace elements in mother birds during the period of egg development (Fossi et al. 1994). Hence, the published literature discussed here indicated that heavy metals in soil and eggs exhibited an equivocal relation.

6 Scope of Egg as a Biomonitor of Soil Heavy Metals

The egg in birds is a self-sustained life support system which comprised of the egg contents and eggshell. The bird’s egg virtually serves as a good indicator for heavy metal pollution in the environment. Heavy metals are sequestered by the females during egg production (Burger 2002). But the sequestration of heavy metals is not consistent; cadmium, for example, is reported to be transmitted to the egg in a very limited quantity (Burger 1993). So, the use of egg for biomonitoring of those metals which are not sequestered properly by females will be limited. Scheuhammer (1987) suggested that the transfer of heavy metals to eggs takes place only if the concentration of the respective metals is very high in body tissues. In this way, females predominately sequester only those elements which are present in higher concentration in their body tissues, and the information about the other elements would be masked. So far, very limited information on the maternal transfer rate of heavy metals is available which means that the percentage of heavy metals in the egg to the whole body burden of metals has rarely been studied. To fill this gap of knowledge, extensive research on the maternal transfer rate of heavy metals to the eggs should be studied which will not only enhance the pool of existing knowledge on metal soil to egg metal ratio but will also provide the information about the extent to which eggs could be useful for biomonitoring of heavy metals in soil. Moreover, the concentration level of most of the essential metals such as Cu, Zn, and Fe in the eggs could partly be explained by the internal regulatory mechanism of the body. Some metals may be mobilized by the female body during the egg production from the stored metals in different tissues in the body which the organism has ingested elsewhere not from the local soil. For example, Pb sequestered in egg may reflect the mobilization of lead from accumulated mass during the previous breeding season from the same area. Therefore, concentrations of certain metals are not necessarily linked to the soil metal level. For a meaningful interpretation of the results, one has to take care about all these possible discrepancies. As the egg provides information only about the concentration in the soil of breeding grounds, the information about the metal addition at wintering grounds would be missing. Before using egg as a biomonitoring tool for heavy metal accumulation through soil, one must know the characteristics and history of the local soil, especially the turnover rate of sediments. By using these information and egg-related discrepancies, one could give the evocative description on soil to egg metal transfer.