Birds as Intrinsic Bio-Indicators for Probing Heavy Metal Contamination Signatures in Polluted Environmental Matrices

Abstract

The purpose of this study is to provide a comprehensive summary of the major functions of avifauna as bioindicators of contamination and their impact on conservation. Birds have been utilised as bioindicators of contamination globally for a long time. When their functions and numbers are taken into account, bioindicators—species that are used to assess the health of the environment—are capable of evaluating the integrity of the ecosystem. Birds are excellent indicators because they are very noticeable and their existence is simple to spot in any setting. They are also equipped with the ability to fly, so they may flee from an environment if it does not meet their ecological needs. In addition, due to their widespread distribution, individual species are simple to recognise in classification. When their functions and numbers are considered, bioindicators can evaluate the integrity of the ecosystem. Birds are excellent indicators since they are simple to spot and observe in any environment. Although necessary for life, heavy metals can be harmful at high levels and disrupt behaviour and productive function. They can also be easily ingested and biomagnified through food or the food chain. Therefore, the use of birds as bioindicators depends on the features of interest and the resources available for ecological evaluation, which encourages the conservation of bird species for the next generation.

1. Introduction

Birds reflect the quantities of xenobiotics in the environment and have been utilised as bioindicators to assess the extent of developing contamination present in any particular ecosystem. Due to the omnipresence of the environment in the modern world, heavy metals produced due to anthropogenic pressure persists in the environment Elemental poisoning in the environment has increased in recent years, raising concerns that have not only afflicted industrialised countries in Southern Asia but also India [1]. Heavy metal deposition in soils is caused by natural geological processes, whereas atmospheric deposition, flooding, and industrial discharge are caused by anthropogenic sources. Higher-trophic level organisms absorb these elements from bacteria, macro-invertebrates, flora, and other abiotic elements, which are subsequently transferred to them [2]. Due to exposure parameters that are over acceptable limits, vital metals that would otherwise be necessary for the growth and development of the species throughout this process can instead become hazardous to the organism [3]. The contribution of heavy metal contamination to the terrestrial environment comes from several man-made sources, including urban activities, paint, manures, industrialisation, discharge from mines, biomedical and hazardous waste disposal, obnoxious use of fertilisers and pesticides, coal burning, vehicle exhausts, and open incineration [4]. Long-term accumulation of persistent toxicants in sediments exposes wildlife living in coastal environments to the effects of such toxicants, which can continue to occur for years [5]. Heavy metals, a significant ecotoxicological pollutant, have an impact on the diet, feeding habits, and evolutionary traits of several animals [6].

The first instance of using Aves as a biomonitor to assess environmental health was recorded in history in the 1960s [7]. Consumption of contaminated food is a significant method through which birds obtain metals [8]. Acute poisoning can cause adult birds to die [9], but chronic exposure to metals at low levels can continue to occur in birds with extended life spans [10]. Heavy metal toxicosis can cause physiological and genetic diseases, growth impairments, impaired development, reproductive issues, disease resistance, and population decrease [11, 12].

2. Background

Diverse marine bird and animal species have recently perished from anthropogenic causes and rare diseases. One of the primary causes of such events is anthropogenic sources. Animals may exhibit endocrine physiological problems as a result of several man-made substances. Toxicants can be deadly to animals, including birds, and can mess with their endocrine systems. One of these toxicants is organochlorine since it can penetrate all topical layers. Endocrine disruptive substances, such as polychlorinated biphenyls (PCBs) and organochlorine pesticides, can accumulate in the tissues of wildlife over time. Due to exposure to excessive quantities of hazardous compounds from different pesticides, wildlife has suffered as a result of mass fatalities. The incapacity of open-sea creatures like Albatrosses and cetaceans to metabolise hazardous persistent pollutants has been linked to higher levels of organochlorines in these creatures [13]. As a result of their quick adaptation to climate changes, birds are regarded as pioneer indicators for changes connected to global warming.

3. Consequences of environmental pollution

Due to heavy metal contamination, the environment has lost its capacity to support life and transmit its fundamental values. Heavy metals are present in the environment naturally, but because of human activity, their occurrence is considerably more extreme than it is. This puts the lives of humans, animals, and plants in danger. But it presents significant obstacles to our knowledge and way of life. Environmental contamination is the introduction of anything new to our environment. The primary causes of pollution in our environment are anthropogenic, or man-made, sources. The presence of pollutants in a region has the potential to disrupt the overall ecological equilibrium. Contaminants are the main type of environmental contaminant that harms our ecosystem. Pests, condensates, and other materials can carry bacteria, chemicals, and particulate contaminants. While adulteration brought on by environmental microbes causes content to decay and disease, chemical pollutants frequently induce harmful reactions. Heavy metals are metallic elements that are denser than water in comparison [14, 15, 16] asserts that arsenic, a metalloid, is hazardous when exposed at low levels and draws the assumption that toxicity and mass are related. A few of the environmental sources of heavy metals are the atmosphere, industries agriculture, geological pollution, pharmaceuticals, and home effluents [17].

Mine tailings, emissions from industrial regions, deposition of elemental waste produced by the paint, fertiliser, and pesticide industries, sewage, thermal power plant residues, petrochemical spillage, and atmospheric deposition are the principal sources of heavy metals and metalloids in soils. Regardless of where they come from, heavy metals are mostly absorbed by the soil. While inorganic contaminants like metals do not go through the oxidation process described above and stay relatively persistent in soils even after introduction, several organic contaminants do so as a result of microbial activity [18, 19].

Industrial, agricultural, and other anthropogenic activities harm aquatic ecology [20]. Metals continue to biomagnify in aquatic environments through the food chain and cause biological harm that poses a concern to humankind [21]. According to Canli and Atli [22], aquatic species occasionally accumulate heavy metals inside of them that is higher than ambient levels. Industrial discharges cause freshwater habitats to become more contaminated than other environments over time [23]. Numerous aquatic ecosystems may be able to withstand large levels of pollution, according to studies, however, those ecosystems may also suffer harm from the resulting living populations.

4. Bio-indicators

Bioindicators (Figure 1) are species that are used to assess the health of an ecosystem or the environment. They can assess the integrity of the environment based on their populations and functions. Monitoring the state of several ecological unit constituents is essential for protecting and managing the natural environment. Ecologists have utilised wild birds as indicators of heavy metal contamination over the years because they can gauge the impact of environmental heavy metal concentrations. In ecology and conservation science, surrogate species have been employed over time to ascertain the relationship between plants and animals in a particular geographic location [24]. Because managing ecosystems is challenging and there are few scientific tools available, conservation biologists have also employed target species as desirable shortcuts.

Figure 1.

Illustration of heavy metals and other toxic compounds which impacts avifauna, revering them as “bio-indicators.”

5. Biomonitoring using birds through the invasive method

5.1 Bones

Animals are exposed to accumulative sources of metals through food consumption, which elevates over time with rising metal concentrations. Fish that are exposed to trace concentrations of heavy metals over an extended period experience damage to their skeletal, renal, and respiratory systems [25]. According to clinical investigations Engström et al. and Rodríguez and Mandalunis [26, 27], Cadmium exposure increases the risk of bone deterioration, osteoporosis, and kidney impairment. Brzóska and Moniuszko-Jakoniuk [28] also noted that exposure to Cd causes a decrease in mineralisation, affecting the biomechanical characteristics and making the bones more prone to deformation and fracture. Long-term exposure to cadmium reduces bone volume, according to Chen et al. [4], however, Rodríguez and Mandalunis [27] found that it increases the number of tartrate-resistant acid phosphatase (TRAP) positive cells in tibial bone. According to Papa et al. [29], cadmium causes osteoblast apoptosis, which causes the cytoskeleton to rupture, as well as DNA fragmentation, a rise in the frequency of micronuclei, and reactive oxygen species [27, 30].

According to Morais et al. [31], a high Ni concentration inhibits alkaline phosphatase activity, which has an impact on bone mineralisation [32]. However, it was concluded by Rodríguez and Mandalunis [27] that there is no literature on the effects of Nickel poisoning on human skeletal tissue or in vivo experimental models. Studies on Goldfish indicate that methylmercury directly affects and lowers the metabolism of scale bone cells, increases the production of metallothionein, and decreases the expression of calcaemic and oestrogen receptors [33]. According to Yachiguchi et al. [34], there is a decrease in TRAP and alkaline phosphatase (ALP) expression along with an increase in the production of metallothioneins. Mercury would thus inhibit both osteoclast and osteoblast function. According to Abd El-Aziz [35], experimental models with methylmercury injection into laboratory animals slowed ossification and had detrimental effects on foetus development. According to Rodríguez and Mandalunis [27], there is a dearth of information on the impact of mercury on mammal skeletal tissue, with only a few studies having been conducted.

According to Bier et al. and Ma et al. [36, 37], lead (Pb) blocks the signalling pathway, which in turn limits osteoblastic activity. The findings of Lv et al. [38] mentions that Pb’s autophagy can protect osteoblast apoptosis and it induces osteoblasts to apoptosis. Exposure to aluminium (Al) causes osteomalacia, osteoporosis, and renal osteodystrophy. Chappard et al. [39] found that in the hydroxyapatite crystals of exostotic patients, Ca²⁺ was replaced by Al³⁺ and Fe³⁺.

5.2 Tissues

Due to industrial, agricultural, and urbanisation-related activities that injure organisms, the environment is polluted with both essential and non-essential metals including Zn, Cu, Cd, Cr, and Pb. The food chain helps to mitigate the impacts on the raptors, even when they are not deadly. Studying the risk effects on the species and the degrees of contamination in their habitat is aided by the degree and extent of metal concentration in tissues [40]. Because of their biological behaviour, several species are exposed to the contamination that can be found if abiogenic sampling is not done. According to Jagar et al. [41], data on the degree of contamination and the movement of contaminants through the food chain could be obtained from raptors during large-scale sampling. When compared to other species of a similar kind, some aerial species are more exposed to pollution [42]. Information on temporary and geographical exposure to pollutants was proposed by Burger et al. and Pérez-López et al. [43, 44]. According to Rothschild and Duffy [45], the habitat, distribution, feeding habits, and life span of wild birds can all be used as indicators of environmental contamination. Only a few wild bird species, according to Movalli [42], can serve as bioindicators on a larger scale and be used to predict future environmental changes [46]. Burger et al. [43] claimed that because birds are such sensitive species to specific pollutants, they can provide information regarding spatial and temporal exposure to certain pollutants. According to Kler et al. [47] soft tissues of birds, such as their muscle, kidney, spleen, liver, heart, lungs, blood, and brain, can be widely employed as bioindicators to identify metal contamination in studies. Since different organs contain different amounts of metal, it is required to estimate different tissues for evaluation at the population level.

According to Jin et al. [48], metals that are not needed by the living organism do not dissolve and occasionally accumulate in the body, causing negative effects. Additionally, the ionisation of these ions causes them to react with biological components like protein or nucleic acid, which has an impact on how enzymes are activated and how three-dimensional protein structures are formed. Additionally, sometimes essential metals that are centrally situated in metalloenzymes are replaced by heavy metals. Furness and Greenwood [49] concluded that birds can be utilised as biological indicator species for determining the degree of heavy metal contamination and its negative effects.

According to Fisher et al. [50], the main sources of lead discharge into the environment are mining, industries, and hunting activities. According to Snoeijs et al. [51], persistent exposure to high concentrations had an impact on the wild birds’ reproductive rates, immunity, and physiological systems. Cadmium was listed as one of the harmful trace elements by Battaglia et al. [52] due to its toxicity and persistence in both food and the environment. According to references [53, 54], cadmium accumulation in birds’ bodies caused harm to their renal tubular cells and a decline in their physical conditions. It was concluded by Carpenter et al. [55] that copper (Cu) and manganese (Mn) have positive effects on biological processes as well as negative effects at greater concentrations on the kidneys, reproductive health, and the potential to cause mortality. According to Kim and Oh [56], determining the extent of accumulation worldwide as well as excretion patterns allowed for the conclusion of contamination levels and unfavourable reactions to certain species.

6. Biomonitoring using birds through the non-invasive methods

6.1 Feathers

Raptors have been the most frequently used species in biomonitoring research on the environment because of their wide geographic spread for foraging purposes and also because of their higher position on the food chain, which can reflect the number of contaminants flowing through it [57]. However, because a number of raptor species are protected, non-invasive methods can be used. According to Dauwe et al. [58], sampling of feathers is simple, and feathers have already been used in numerous research [59]. According to Burger’s research, heavy metals have the propensity to bind to protein molecules during the brief embryonic stage of a feather when tiny blood capillaries connect it to the bloodstream. References [58, 59] came to the conclusion that after the formation of the feathers, the blood vessels become weak and physically detach from the bird. Birds shed a sizable amount of heavy metals during the moulting process through their plumage [57]. Some interior tissues begin displaying decreased metal levels as soon as the metals are sewn into the feathers. When a moult is finished, the internal level of a few heavy metals rises until the next moult, which is a constant process [60]. According to research by [61], if the overall amount of heavy metals in a bird’s body is reflected in the feathers as they form, the feathers that are moulted at the conclusion of the process should do so with lower concentrations than those that are moulted at the beginning. The concentration of various heavy metals inside the body of the bird during moulting may vary, being higher at the start and lower towards the end of the process. Birds also deposit toxins like Cd, Cr, and Pb into their developing feathers, which attach to the keratin in feathers and become biologically separated [62]. In addition, the accumulation of these metals into the calcareous tissues is a significant way for female birds to eliminate Pb [63], but Zn and Cu are favourably deposited in the feathers when concentrations surpass permitted limits [64]. Studies by [65, 66], revealed that during the brief period of egg hatching and while it matures, hatchling feathers can indicate local contamination that may result from their parents consuming food from the area [65].

6.2 Eggs

Over time, it has been discovered that the presence of metals in feathers, excrement, and eggs also causes harm to the bird population [65]. Hashmi [67] reported using feathers and eggs for biomonitoring soil, but due to their lengthy storage times and ease of sampling, this method is related to one’s own. Additionally, it was determined that because eggs are formed at a specific point in a female bird’s life cycle, they can act as a superb signal for local exposure in addition to belonging to a particular subset of egg-laying birds. According to Jayakumar and Muralidharan [68], anthropogenic inputs are the cause of the presence of unnecessary trace elements in both domestic and wild birds. The harmful effects of metal pollution might include everything from kidney and testicular damage to reduced egg production [69]. Bird eggs, according to reference [68] are among the most complex and distinctive types of reproductive cells. They have a protective coating (or shell) that encloses albumin and yolk contents that vary greatly in volume, shape, weight, and amount. From tropical to temperate zones, according to reference [57], female bird species tend to forage on their breeding grounds before to egg production after egg laying. According to reference [67], utilising eggs as a biomonitoring technique provides a number of benefits over using feathers since eggs are more stable and do not change with age, size, or body structure. Eggs have recently been employed in a number of biomonitoring studies, and it has thus been demonstrated that the collection of a single egg without harming the environment has a negligible impact on the population of the species [5]. A given metal’s circulation concentration in birds, which is then reflected in egg quality, can be closely correlated with recent exposure [67]. According to reference [70], the egg shell and egg content are typically where metals collect throughout the female’s metal deposition. In a similar vein, Burger et al. [43] came to the conclusion that heavy metal exposure from the parent’s local environment is what puts eggs in the greatest danger of being harmed.

6.3 Excreta

According to reference [47], investigations on heavy metal contamination in birds are extremely rare in nations like India. Additionally, the Wildlife Protection Act of India (1972) forbids the capture and sacrifice of birds, which makes it challenging for scientists to conduct any analytical research on eggs and tissues. Excreta might therefore be chosen as a different source that can provide clear information on environmental contamination [47, 71]. Birds are exposed to heavy metals through contaminated water sources, excessive metal concentrations in the atmosphere, and food sources close to point sources [72]. The rate of heavy metal absorption varies according to the physiology of the species and is influenced by the metals’ bioavailability and other factors. By storing them in the salt gland, uropygial gland, or excreta, birds can get rid of heavy metals [47]. Bird excretions are the best indicator of the environment’s level of heavy metal contamination since they excrete more metals than other animals [73]. Excreta from birds serve as helpful non-destructive bioindicators and provide information on the bird’s diet [74]. It also details the kinds of metals absorbed and removed [75].

A total of five types of pollution indicator species were identified by [76] which are represented in Table 1.

S. no	Type of species	Function
1	Sentinels	These extremely vulnerable animals were introduced into a specific area to provide early warning signs of ecosystem contamination
2	Detectors	These are species that are unique to a particular area and exhibit demonstrable responses to environmental changes, such as adjustments in behaviour, mortality, or age-class structure. In addition, it is anticipated that the species would react quickly to changes in the environment
3	Exploiters	These are the kinds of species that, by virtue of their very existence, can signal environmental damage. The ability of exploiter species to make use of a polluted environment determines whether or not they will survive. Because rivals cannot survive in the distorted environment, they frequently thrive in disturbed or contaminated places
4	Accumulators	These are species that accumulate pollution in significant amounts in their skin, feathers, lungs, liver, and kidney tissues

Table 1.

Type of pollution indicator species.

7. Advantages of Avifauna as indicator species in probing heavy metal pollution

Birds have historically served as reliable environmental indicators. Despite the fact that they still have a limited capacity for directly and quickly altering the features of ecosystems and for altering the behaviour of other taxa [77, 78]. The advantages of utilising bird species as indicators are:

1. They can be easily observed in any given environment.

2. Due to their diurnal nature and ability to call, they are easily recognisable.

3. Avifaunal classification and speciation make them easily identifiable across any field.

4. Birds prefer different habitat niches and are widely distributed geographically over a wide range of areas. Thus, their foraging activities constantly expose them to heavy metals present in the atmosphere, or in any given environment according to their habitat preferences.

5. They are top-level predators which makes them susceptible to the changes going on in the food chain and food web at the producer, primary consumer and secondary consumer levels.

6. Birds are great pollinators and help in seed dispersal, thereby maintaining the ecological balance in the ecosystem. In a polluted environment, plants sequester heavy metals into their fruits through their roots and upon consuming these fruits, birds are either exposed to heavy metals or continue to accumulate them in their system.

8. Disadvantages of using Avifauna as indicator species in probing heavy metal pollution

1. Because birds are mobile, it is possible to see them on a wide range. Making it simple for researchers to link their responses to particular alterations in the environment.

2. Bird species are very mobile in comparison to other terrestrial animals, and they use resources in three dimensions as opposed to other animals, which leads to erroneous reactions to environmental change.

3. Birds are similarly affected by secondary or tertiary changes in stressor components, which lessens the value of birds as bioindicators.

4. In comparison to other animals, they also possess behavioural and physiological characteristics that make them less vulnerable to changes in the ecosystem. For instance, birds have significantly greater control over the amount of fat and metal present in their body tissues than do invertebrates.

9. Conclusions

High levels of toxicity in some heavy metals can disrupt behaviour and productive function. Lead poisoning can be triggered by the presence of heavy metals, impairing the immune system and harming the nervous system. Birds’ ability to reproduce and grow can both be affected negatively by Cadmium. In addition, methylmercury can hinder bird reproduction, resulting in a decrease in egg size, fertility, and hatchability. Once a certain heavy metal’s allowable limit is exceeded, the aforementioned impacts of heavy metals on bird species are immediately apparent. As a result, wild birds are good markers of environmental heavy metal pollution. A function of the features of interest and resources available for ecological evaluation, using birds as bioindicators encourages the conservation of bird species for future generations. It is crucial to investigate potential mechanisms through which heavy metals may be to blame for the development of illnesses in wild birds. This will most certainly support the protection of threatened and endangered bird species.

Acknowledgments

The author is thankful to the Department of Environment Sciences, GITAM Institute of Science for providing basic infrastructure, library, and technical support and to the University Grants Commission (UGC) Rajiv Gandhi National Fellowship for funding the current work.

Conflict of interest

The authors declare no conflict of interest.

Acronyms and abbreviations

PCB
Cd
TRAP	tartrate-resistant acid phosphatase
ALP
Pb
Zn
Cu
Al
Cr
Mn
Ni