Environmental pollution of heavy metals represents a threat to ecosystems as it is responsible for numerous pathologies in living organisms, leading to impaired survival and reproduction in wildlife (Lucia et al., 2010). Birds have played a prominent role in the biomonitoring of different pollutants since the early 1950s with the realisation that the insecticide dichlorodiphenyltrichloroethane (DDT) was causing mass wildlife poisoning, especially of birds, through bioaccumulation (Furness, 1993). Biomonitoring of certain heavy metals is an established method to quantify pollutant abundance and bioavailability, as pollutants accumulate to higher levels in animals than those in the surrounding environment. Although many biomonitoring studies have collected internal tissues to assess chronic exposure (Aloupi et al., 2017, Gochfeld and Burger, 1987, Kalisińska et al., 2004, Di Giulio and Scanlon, 1984b), studies using non-destructive methods such as measuring concentrations in blood (Maia et al., 2017, Binkowski and Meissner, 2013), eggs (Hashmi et al., 2013, Dolci et al., 2017), and feathers and faeces (Dauwe et al., 2000, Karimi et al., 2015, Tsipoura et al., 2011) have increased in popularity, despite still being quite limited for comparison.
Researchers have found evidence of diverse heavy metal related impairments in birds. Cd is one of the most abundant nonessential metals within the environment due to its industrial uses. It became a national concern with the historical use of phosphate fertiliser in New Zealand, which up until the 1990s was contaminated with high Cd levels (Taylor, 1997). It is known to induce kidney and liver toxicity, disruption of calcium metabolic pathways, lesions of intestinal tissue, and thinning of eggshells (Cain et al., 1983, Burger, 2008, Furness, 1996). Cu, although involved in many biological processes including serving as an essential cofactor for several oxidative stress- related enzymes (Stern, 2010), can result in toxicity at high doses. It predominantly affects the liver, causing hepatocellular necrosis as well as erosion of the epithelial lining of the gastrointestinal track, and acute tubular necrosis in the kidney (Camakaris et al., 1999, Tchounwou et al., 2008). The most extensively studied heavy metal is Pb, as its route into the environment is often linked with hunting activities (Pb ammunition). Known as a potent toxin, in poisoned individuals it causes haemolytic anaemia and behavioural impairments, results in adverse effects on reproduction, such as decreased egg production and plasma calcium, and impairs growth and survival of chicks and nestlings (Burger and Gochfeld, 1993, Scheuhammer, 1987, Taggart et al., 2009, Pain, 1996).
Blood is the tissue of choice for non-destructive biomonitoring when determining recent exposure to pollutants, as it is obtained quickly and easily without high risk of permanent damage (Maia et al., 2017). Blood has the potential to be a good indicator of environmental exposure due to the high correlations between many metal levels in blood and other tissues (Wayland et al., 2001,
Chapter Two
Burger and Gochfeld, 1993). Unlike internal tissue collection, blood sampling allows studies of survival rate in relation to contaminant load. By allowing repetitive sampling of individuals, exposure in relation to life stage, reproductive activities, and seasonal effects can be monitored.
When interpreting metal concentrations in avian blood, the age of the bird should be considered (Garcá-Fernández et al., 1996, Burger and Gochfeld, 1997a). Since juvenile (hatch year) birds feed within a more localised area compared to adults, they provide data on metal pollution for a limited period and territory. This effect is more exaggerated within altricial nestlings, although precocial juveniles are also likely to demonstrate similar patterns (Dauwe et al., 2000, de la Casa- Resino et al., 2014). Adults, on the other hand, are more likely to have accumulated contaminants over their lifetime; an increase with age has been reported in many studies examining internal tissues (Berglund et al., 2011, Burger and Gochfeld, 1997a). Some studies suggest that sex can affect the accumulation of heavy metals in the body in birds, with females having lower concentrations due to their ability to excrete toxins into eggs (Gochfeld and Burger, 1987, Aloupi
et al., 2017). In contrast, a review on sex-related differences in metal loads in wildlife concluded that in most cases sex did not affect metal accumulation in birds, highlighting that significant differences are often sporadic and conflicting within the literature (Burger, 2007). Concentrations of heavy metals in blood have been reported less frequently, although Binkowski and Meissner (2013) studied the blood concentrations of seven metals (Fe, Zn, Zu, Cr, Ni, Pb, Cd) in mallards from Poland, which did not differ between the sexes. It should be noted that when differences between sexes have been reported, they are often small compared to the high level of variation between individuals (Furness, 1993).
Eggshell formation and laying is recognised as a mechanism that allows female birds to off-load environmental contaminants (Gochfeld and Burger, 1998, Burger, 1994), thus concentrations in eggs can potentially be used for pollutant monitoring. Pollutants excreted to eggs derive from both stored body burden, and food choice of the female during egg formation (Burger and Gochfeld, 1993). It is therefore assumed that eggshell concentrations can provide information on the degree of exposure within a female’s breeding area. Concentrations of trace elements in eggshells have been useful in long-term studies of geographical, geochemical and temporal trends of environmental pollution (Burger, 2002, Dolci et al., 2017, Kitowski et al., 2017a). Although the transfer rates of contaminants are thought to be related to the body load of the female, and ultimately to the exposure of pollutants in the female’s environment (Dauwe et al., 2005), there is some debate about the transfer of certain metals such as Cd into eggshells. Although differential toxin offloading can be a major disadvantage for the use of eggshells as a bioindicator, eggshells remain a tool for monitoring the movement of certain pollutants passed to subsequent generations, which could have effects on chick growth and survival (Lam et al., 2005, Agusa et al., 2005, Burger, 1994).
Chapter Two
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Within New Zealand there is a lack of research into the movement of pollutants between the environment and wildlife. The data presented here are the results of a survey aiming to assess potential heavy-metal contaminations of two spatially distinct populations of mallards in New Zealand, using non-destructive biomonitoring methods. Concentrations of one essential heavy metal, copper (Cu), and two nonessential heavy metals, cadmium (Cd) and lead (Pb), were determined from blood samples from mallards taken at two time points and in eggshells collected from hatched or abandoned nests. The objectives of this study were to (i) obtain a baseline level of contaminants in the bloods of mallards in New Zealand, (ii) assess the rate of maternal transfer of heavy metals during egg formation, and (iii) evaluate the feasibility of using non-destructive methods for monitoring contaminants in wildlife.