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60

weeks to months). Consequently, highest lead concentrations

are generally found in bone, followed by kidney and liver, with

intermediate concentrations in brain and blood, and lowest

concentrations in muscle (Longcore

et al.

1974a, Johnson

et al.

1982, Custer

et al.

1984, Garcia Fernandez

et al.

1995). However,

in cases of acute lead poisoning, concentrations in soft tissues

may be very elevated relative to those in bone. Blood lead is a

good indicator of recent exposure and usually remains elevated

for weeks or months after exposure. The degree and duration

of elevation of blood lead depends largely upon the amount

absorbed and the duration of exposure. While lead in bone

is less mobile than in other tissues, it can be mobilised under

certain conditions. For example, lead may be mobilised from

medullary bone together with calcium, when calcium is required

for eggshell formation (Finley and Dieter 1978).

The first measurable biochemical effect of lead, occurring at

very low blood lead levels, is inhibition of the activity of the

blood enzyme delta-aminolevulinic acid dehydratase (δ-ALAD),

necessary for haem synthesis in erythrocytes (Hernberg

et al.

1970,Tola

etal.

1973, Pain1987, 1989,Martinez-Lopez

etal.

2004).

While some reduction in ALAD activity appears to be tolerated

in birds, protracted inhibition in ALAD activity can be associated

with haemolytic anaemia (Pain and Rattner 1988, Mateo

et al.

2003). As in other animals, lead can affect a wide range of body

systems influencing reproduction, productivity, behaviour and

the immune system (for a selection of specific studies on a range

of bird species see Longcore

et al.

1974a, 1974b, Clemens

et al.

1975, Finley

et al.

1976, Finley and Dieter 1978, Dieter and Finley

1978, 1979, Kendall

et al.

1981, Veit

et al.

1983, Kendall and

Scanlon 1982, 1984, Chasko

et al.

1984, Fimreite 1984, Buerger

et

al.

1986, Pain and Rattner 1988, Trust

et al.

1990, Redig

et al.

1991,

Franson and Smith 1999, Fair and Myers 2002, and for reviews

see Scheuhammer 1987, Eisler 1988, Burger and Gochfeld 2000,

Franson and Pain 2011).

Many factors may affect an individual bird’s susceptibility to lead

poisoning including its sex and breeding condition, the physical

and chemical constituents of its diet and environmental factors

such as temperature and food stress. For example, in some

experimental studies, ingestion of just one lead gunshot has

been sufficient to cause ill health or death in birds (

e.g.

Holladay

et al.

2012, Pain and Rattner 1988), while in others, birds have

survived higher doses. It is therefore difficult to generalise about

the magnitude of impact on an individual bird of ingesting a set

amount of lead from ammunition (unless this is large). However,

it is currently considered that there are no identified “no

observed adverse effect levels” (NOAEL) or “predicted no effect

concentrations”(PNEC) for lead in humans (EFSA 2010) and thus

likely for other vertebrates.

While the dose-response relationship can vary among

individuals and species, the health impacts of exposure to

lead show great consistency across experimental studies.

When the large numbers of studies conducted are considered

together, particularly those studies that have examined large

numbers of birds over time, generalisations can be made. The

diagnosis of large scale and geographically extensive wildfowl

mortality from lead poisoning following gunshot ingestion

was first reported in the USA in the 1950s (

e.g.

Bellrose 1959),

supported by extensive

post mortem

data. These findings were

subsequently further supported by numerous experimental

studies where captive wildfowl were fed lead gunshot (see

above). Studies of survival of birds in relation to exposure to

lead gunshot have also been conducted. Tavecchia

et al.

(2001)

analysed recoveries between 1960 and 1971 of adult mallard

Anas platyrhynchos

ringed in the Camargue, France, for which

the amount and type of lead exposure (ingested or embedded

gunshot) had been determined by X-radiography. Ingested

gunshot was present in the gizzard of 11% of birds and

embeddedgunshot was present in 23%of birds. Annual survival

of mallards containing more than one gunshot in the gizzard

was 19% lower than in unaffected birds. Survival was also lower

by 19% for birds with any embedded gunshot and the effects

of gizzard and embedded gunshot together were additive.

Based upon the proportion of birds with gunshot in the gizzard

and the estimated effect of gunshot on survival, these authors

estimated that 1.5% of wintering mallards may die from lead

poisoning due to ingested gunshot every year in the Camargue.

Mortality from embedded gunshot and wounding would be

additional to this. Guillemain

et al.

(2007), analysed recovery

data from 40,000 teal

Anas crecca

that had been trapped and

X-rayed in the Camargue, France (1957–1978), and also found

reduced survival from one or more ingested pellets.

In addition to the direct impacts of lead on welfare and survival,

indirect effects are likely to occur. These may include: increased

susceptibility to infectious disease

via

lead’s immunosuppressive

effects (Grasman and Scanlon 1995, Trust

et al.

1990); and

increased susceptibility to death from a range of other causes,

such as collision with power lines (Kelly and Kelly 2005 –

via

its

effects on muscular strength and coordination) and being shot

(

e.g.

shown by Bellrose 1959, Heitmeyer

et al.

1993, Demendi

and Petrie 2006 and others).

Deborah J. Pain, Ruth Cromie & Rhys E. Green