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