Causes of Mortality in Bald Eagles (Haliaeetus leucocephalus) in The Canadian Maritime Provinces, 1991-2016 - Canadian Wildlife Biology ...

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Causes of Mortality in Bald Eagles (Haliaeetus leucocephalus) in The Canadian Maritime Provinces, 1991-2016 - Canadian Wildlife Biology ...
CWBM 2020: Volume 9, Number 2                                                                                 ISSN: 1929–3100

     Original Research

 Causes of Mortality in Bald Eagles (Haliaeetus
 leucocephalus) in The Canadian Maritime
 Provinces, 1991-2016
 Amélie MATHIEU1, E. Jane PARMLEY2,3, Scott MCBURNEY4, Colin ROBERTSON5,
 Helene VAN DONINCK6, and Pierre-Yves DAOUST4
 1
   British Columbia Ministry of Forests, Lands, Natural Resource Operations and Rural Development, 205 Industrial Rd. G,
 Cranbrook, British Columbia, V1C 7G5, Canada.
 2
   Department of Population Medicine, Ontario Veterinary College, University of Guelph, 50 Stone Rd. E, Guelph, Ontario,
 N1G 2W1, Canada.
 3
   Canadian Wildlife Health Cooperative, CWHC National Office, University of Saskatchewan, 52 Campus Drive, Saskatoon,
 Saskatchewan, S7N5B4, Canada.
 4
   Canadian Wildlife Health Cooperative, Department of Pathology and Microbiology, Atlantic Veterinary College, University
 of Prince Edward Island, 550 University Avenue, Charlottetown, Prince Edward Island, C1A 4P3, Canada.
 5
   Department of Geography and Environmental Studies, Wilfrid Laurier University, 75 University Avenue West, Waterloo,
 Ontario, N2L 3C5, Canada.
 6
   Cobequid Wildlife Rehabilitation Centre, 2220 Irwin Lake Rd, Brookfield, Nova Scotia, B0N1C0, Canada ̶ Posthumously.

         Abstract
         This article summarizes the results of necropsy findings on 420 bald eagles (Haliaeetus leucocephalus) from the 3
         Canadian Maritime provinces over a 26-yr period. It shows that, as in other regions of North America, anthropogenic
         factors dominate the diagnosed causes of mortality in this species, representing close to 50% of the cases. These factors
         included vehicular collision (n=57; 14%), electrocution (n=47; 11%), poisoning (n=38; 9%), snares and other trapping
         devices (n=35; 8%), gunshot (n=20; 5%), and other (n=5; 1%). At least some cases of trauma of unknown cause (n=79;
         19%) and some unknown causes of death (n=53; 13%) may have also involved anthropogenic factors. As in several

         Correspondence: Pierre-Yves Daoust, Canadian Wildlife Health Cooperative, Department of Pathology and
         Microbiology, Atlantic Veterinary College, University of Prince Edward Island, 550 University Avenue,
         Charlottetown, Prince Edward Island, C1A 4P3, Canada. Email: daoust@upei.ca.
Causes of Mortality in Bald Eagles (Haliaeetus leucocephalus) in The Canadian Maritime Provinces, 1991-2016 - Canadian Wildlife Biology ...
MATHIEU et al.                                                                                                              160

        other regions of North America, lead continued to be the most common source of poisoning in this species. Other
        causes of mortality identified, such as conspecific fights (n=11; 3%) and drowning / hypothermia (n=4; 1%), are
        natural challenges faced by these birds. Although bald eagles are not considered a species at risk in Canada, results of
        this study indicate that human-related causes of death are an ongoing issue in the Maritime region as elsewhere.
        Therefore, mitigating measures aimed at their reduction, for example those in relation to lead-based ammunition and
        fishing tackle, pesticide use and trapping, should continue to be implemented and expanded.

         Key Words: Anthropogenic factors, Bald Eagle, Canada, Haliaeetus leucocephalus, Maritimes, Mortality.

INTRODUCTION                                                      retrospective study identifies the causes of death that bald
                                                                  eagles have encountered in the Canadian Maritime provinces
  Identifying, monitoring and mitigating potential causes of
                                                                  (New Brunswick [NB], Prince Edward Island [PEI], Nova
morbidity and mortality in wildlife are important activities
                                                                  Scotia [NS]) over a 26-yr period (1991-2016), based on data
that contribute to conservation. Bald eagles (Haliaeetus
                                                                  from a long-term wildlife health surveillance program
leucocephalus), like many other raptors, can be negatively
                                                                  carried out by the Canadian Wildlife Health Cooperative
affected by human activities. Once hunted as pests or
                                                                  (CWHC; www.cwhc-rcsf.ca).
trophies, bald eagles are now protected under provincial
jurisdiction in Canada, and by the Bald and Golden Eagle
Protection Act and the Migratory Bird Treaty Act in the           MATERIAL & METHODS
United States (US) (U.S. Fish & Wildlife Service 2018a,             Carcasses of bald eagles found dead or in poor health and
2018b). However, these regulations do not preclude harm           subsequently euthanized were submitted by conservation
from environmental contaminants, day-to-day human-                officers, park wardens, biologists, wildlife rehabilitation
related activities, poaching, or habitat fragmentation and        centre staff, or the public to the Atlantic regional centre of
destruction from urban and agricultural encroachment. This        the CWHC, Atlantic Veterinary College, University of
became evident in the mid-20th century when the population        Prince Edward Island, where they were necropsied. All
of bald eagles plummeted in the US as a consequence of            necropsies were performed by 3 experienced wildlife
breeding failure due to the extensive use of                      pathologists who provided a consistent level of examination
dichlorodiphenyltrichloroethane (DDT), poaching, and              over the 26-yr duration of the study. Individual necropsy
habitat loss (Fraser 1985; Richardson and Miller 1997). The       reports were reviewed carefully by 2 of the 3 pathologists
species was listed as “endangered” under the US Endangered        and, for each carcass evaluated, the following information
Species Preservation Act in 1967, but it subsequently             was collected: province of origin; month and year when the
recovered and was delisted in 2007 (U.S. Fish & Wildlife          bird died or when the carcass was found; history of the
Service 2019). Its recovery across North America is largely       circumstances under which the bird was found; age class
attributed to the ban on general use of DDT in Canada and         (nestling, immature [
Causes of Mortality in Bald Eagles (Haliaeetus leucocephalus) in The Canadian Maritime Provinces, 1991-2016 - Canadian Wildlife Biology ...
MATHIEU et al.                                                                                                             161

original cause of the problem that had led to the bird’s          performance liquid chromatography, with a detection limit
capture could be clearly identified.                              of 1.0 μg/g.
  Primary causes of death were divided into 10 categories:          Statistical analyses were conducted using SAS 9.4
trauma, electrocution from power lines, emaciation,               (Copyright © 2002-2012; SAS Institute Inc., Cary, North
poisoning, conspecific fight, infection, idiopathic disease       Carolina, USA). Univariable exact logistic regression
(disease process identified, but cause undetermined),             models were fitted to examine associations between the odds
nestling mortality, drowning / hypothermia, and unknown           of being diagnosed with select causes of death (i.e., trauma,
(no cause of death identified). Criteria for each of these        electrocution from powerlines, emaciation, poisoning, all
categories are defined in Table 1. Lead concentration in liver    human-associated causes of death) and the following
or kidney (on a wet weight basis) was determined by atomic        variables: age, sex, body condition, season, and province.
absorption spectroscopy, with a detection limit of 0.25 μg/g      Significance level was set at α=0.05 for these models, and
in early years, improving over time to
Causes of Mortality in Bald Eagles (Haliaeetus leucocephalus) in The Canadian Maritime Provinces, 1991-2016 - Canadian Wildlife Biology ...
MATHIEU et al.                                                                                                            162

more subjective and also implies the need to look further for   proportion of human-related causes of death relative to the
a cause of death. Causes of death thought to have been          total number of submissions (Figure 2)
human-related were also grouped. These included all known         Sixty-six of the 79 birds diagnosed with trauma of
causes of trauma (trauma of unknown cause excluded),            unknown cause had bone fractures and/or internal
electrocution and poisoning.                                    hemorrhage. Most of the remaining birds had focal acute or
  The same univariable regression modelling approach was        chronic superficial soft tissue lacerations. The hemorrhage in
used to examine associations of select causes of mortality      2 birds was of a diffuse nature without good evidence for the
with characteristics of the locations in which the birds were   source of blood, suggesting the possibility of anticoagulant
found. Human population density (persons per km 2) of           poisoning (Murray 2011). Liver analysis for the presence of
dissemination areas (small areas with populations of 400-700    anticoagulant rodenticide was done on 1 of these 2 birds and
persons) was extracted from the 2016 Canadian census            was negative. In 4 birds, the severity, distribution and nature
(Statistics Canada 2019) as a proxy for anthropogenic risks     of soft tissue trauma (epidermal, dermal and soft tissue
to bald eagles. A road network dataset was used to examine      necrosis) was considered compatible with electrocution and
potential effects of major roads on bald eagles (ESRI Data &    survival of the birds for some time post-injury. The history
Maps 2019). Finally, locations of contaminated lands were       available for 1 of the 79 birds with trauma of unknown cause
obtained from the Federal Contaminated Sites Inventory          suggested a lightning strike. This bird was observed to
which tracks known sources of environmental contamination       “simply fall” from the sky during a severe thunder storm and
that could pose a risk to human health or the environment       hit the ground with its wings folded and feet bent back
(Treasury Board of Canada Secretariat 2019). Human              toward its tail. Necropsy revealed a large internal blood clot,
population density was categorized as low (≤50 persons/km2)     compatible with trauma from the bird’s impact on the ground.
or higher (>50 persons/km2); distance to roads was                Trauma was confidently attributed to a human cause in 117
categorized as near road (0 ̶100m from a road) or off-road      of 196 (60%) total cases of trauma (Table 1), vehicular
(>100m from a road); distance to contaminated lands was         collision being most common (57/196, 29%). Non-target
categorized as near (
Causes of Mortality in Bald Eagles (Haliaeetus leucocephalus) in The Canadian Maritime Provinces, 1991-2016 - Canadian Wildlife Biology ...
MATHIEU et al.

Table 1. Primary causes of mortality in 420 bald eagles (Haliaeetus leucocephalus) submitted for necropsy from the 3 Canadian Maritime provinces between 1991
and 2016.
                                                                                                                                                                163
Causes of Mortality in Bald Eagles (Haliaeetus leucocephalus) in The Canadian Maritime Provinces, 1991-2016 - Canadian Wildlife Biology ...
Table 1. Primary causes of mortality in 420 bald eagles (Haliaeetus leucocephalus) submitted for necropsy from the 3 Canadian Maritime provinces between 1991
and 2016 (Cont’d).
                                                                                                                                                                MATHIEU et al.
                                                                                                                                                                164
Causes of Mortality in Bald Eagles (Haliaeetus leucocephalus) in The Canadian Maritime Provinces, 1991-2016 - Canadian Wildlife Biology ...
MATHIEU et al.                                                                                                             165

  Figure 2. Number of bald eagles submitted, percent of eagle submissions due to human-related mortality causes and three-
  year moving average of percent of eagle submissions due to human-related mortality causes in the Maritime provinces,
  1991-2016.

vascular fibrinoid necrosis, as described in waterfowl by        involving the head and neck with puncture wounds or
Wobeser (1997). Lead levels in kidney or liver were also         fracture of the skull in 3 of them. The 6th bird may have been
determined for 100 of the 392 bald eagles with a diagnosis       drowned by the conspecific; its plumage was very wet, and
other than lead poisoning. Of these, 2 birds had lead levels     it had puncture wounds in the skin and muscle mass of its
above 2 µg/g indicative of elevated lead exposure, but less      right leg. Four of the remaining 5 birds suspected of having
than levels considered clinically toxic (Wobeser 1997;           died following a fight with a conspecific had severe soft
Wayland and Bollinger 1999); 1 died of carbofuran                tissue trauma involving the head and neck, including a skull
poisoning and the other of electrocution. Five other birds had   puncture in 2 of them. The 5th bird had only subcutaneous
lead levels between 1 and 2 µg/g; 2 died of emaciation, 1        congestion of the head, but another eagle had been seen
from trauma of unknown cause, 1 from vehicular collision,        “picking up its head” shortly before it died.
and 1 was euthanized because of suppurative polyarthritis.          Nine of 10 cases of infection consisted of locally extensive
Exposure to organophosphates and carbamates (OP/CM)              infectious processes, such as pododermatitis, arthritis, and
accounted for 7/38 (18%) cases of poisoning, and                 cellulitis, at least some of which may have resulted from
barbiturates accounted for 3/38 (8%).                            local trauma with secondary bacterial infection.
  All 11 deaths attributed to conspecific fighting involved      Staphylococcus aureus was isolated from 4 of 7 cases in
adult birds (6 females, 5 males). Nine of these deaths           which bacterial cultures were attempted. Pasteurella
occurred during the nesting season (April and May). This         multocida was isolated from 1 case, and bacteriology results
cause of death was confirmed in 6 birds based on a case          were inconclusive in 2 cases. The only generalized infection
history of direct observation of an aggressive interaction       considered to have resulted from a systemic process was a
between 2 birds, in one case involving 2 males that both died    case of suppurative polyarthritis involving the left elbow
during the encounter. Lesions in 5 of these 6 birds consisted    joint and both tarsometatarsal joints from which S. aureus
of extensive skin lacerations and subcutaneous hemorrhage,       was isolated; the source of this infection was not determined.
Causes of Mortality in Bald Eagles (Haliaeetus leucocephalus) in The Canadian Maritime Provinces, 1991-2016 - Canadian Wildlife Biology ...
MATHIEU et al.                                                                                                          166

 Table 2. Demographic, temporal and geographical data for all cause of mortality categories diagnosed among 420 bald
 eagles (Haliaeetus leucocephalus) submitted for necropsy from the 3 Canadian Maritime provinces between 1991 and
 2016.

 Table 3. Univariable exact logistic regression models estimating the associations between bald eagles being diagnosed with
 select causes of death (i.e., trauma [all causes], electrocution from power lines, emaciation, or poisoning) and age, sex,
 body condition, season, and province in which the birds were found (1991-2016). Significant associations are in bold
 characters.
Causes of Mortality in Bald Eagles (Haliaeetus leucocephalus) in The Canadian Maritime Provinces, 1991-2016 - Canadian Wildlife Biology ...
MATHIEU et al.                                                                                                                                       167

  A presumptive diagnosis of drowning / hypothermia was                                     human cause, but less likely to die of poisoning, than adults
made in 3 of 4 birds (excluding the bird presumably drowned                                 (Tables 3 and 4).
by a conspecific) based on the facts that their carcass had                                   No association could be found in our study between causes
been found ashore, that their plumage was very wet, and that                                of mortality and spatial variables examined (human
no significant gross lesion was found. The 4th bird was                                     population density, proximity to roads, and presence of
actually found alive in water. According to the conservation                                contaminated lands), except that emaciated birds were less
officers who picked it up, it could not get out and was having                              likely (OR=0.395, 95% CI: 0.182-0.827) to be found near
trouble staying afloat. It died shortly thereafter.                                         roads than farther away from roads.
  All 53 birds with an unknown cause of death were in
moderate to good body condition (Table 2). Eleven had                                       DISCUSSION
recently ingested food, raising the possibility of poisoning.
                                                                                               Bald eagles, as upper-trophic level piscivores and
The possible involvement of organophosphate, carbamate or
                                                                                            scavengers found in habitats often affected by human activity,
barbiturate poisoning was examined in 8 of these birds, and
                                                                                            are important bio-sentinels of environmental health and of
all results were negative. Nine birds were found under a
                                                                                            the impacts of human activity on wildlife. Monitoring their
power line or electrical transformer but showed no gross
                                                                                            health can help identify emerging threats to wildlife and
evidence of electrocution.
                                                                                            human health and may be used in the development of
  Based on univariable exact logistic regression models,
                                                                                            effective conservation programs. Identification of threats
birds in moderate to good body condition were more likely
                                                                                            associated with population declines of some avian species
to die of trauma due to human causes, of electrocution, and
                                                                                            (i.e., DDT and lead) have resulted in regulatory changes and
of all human-related causes combined, but less likely to die
                                                                                            population rebound (Avery and Watson 2009; Government
of poisoning, than birds in poor body condition (Tables 3 and
                                                                                            of Canada 2013; U.S. Fish & Wildlife Service
4). Females were less likely to die of electrocution than
                                                                                            2019). Documentation of on-going causes of death provides
males. Immature birds were more likely to die of trauma of

 Table 4. Univariable exact logistic regression models estimating the associations between bald eagles being diagnosed with
 select causes of death (i.e., trauma of human cause, trauma of unknown cause, or all human-associated causes of death) and
 age, sex, body condition, season, and province in which the birds were found (1991-2016). Significant associations are in
 bold characters.

                                                                     Trauma-human             Trauma-unknown            Human COD
                                                                     [OR (95% CI)]             [OR (95% CI)]           [OR (95% CI)]
                                Age            Adult                      0.57                       1.75                   0.75
                                                                      (0.37, 0.95)               (0.97, 3.26)           (0.49, 1.16)
                                               Immature                     -                          -                      -
                                               (ref)1
                                Sex            Male                         0.64                      1.43                  0.85
                                                                        (0.39, 1.04)              (0.84, 2.42)         (0.557, 1.304)
                                          Female (ref)                        -                         -                     -
                                Body      Good                              6.86                      1.63                  3.26
                                condition                              (2.89, 19.88)              (0.82, 3.49)          (1.88, 5.79)
                                          Poor (ref)                          -                         -                     -
                                Season    Summer                            1.83                      0.64                  1.40
                                                                        (0.92, 3.62)              (0.30, 1.29)          (0.79, 2.49)
                                               Fall                         2.43                      0.41                  2.05
                                                                        (1.29, 4.61)              (0.18, 0.87)          (1.19, 3.57)
                                               Winter                       3.25                      0.69                  2.49
                                                                        (1.69, 6.33)              (0.32, 1.40)          (1.38, 4.54)
                                               Spring (ref)                   -                         -                     -
                                Province       New                          2.04                      1.14                  1.46
                                               Brunswick                (1.21, 3.44)              (0.60, 2.12)          (0.90, 2.37)
                                               Prince                       1.08                      1.53                  1.46
                                               Edward                   (0.57, 1.98)              (0.79, 2.92)          (0.86, 2.50)
                                               Island
                                               Nova Scotia                     -                         -                   -
                                               (ref)

                                1 ref, referent (the reference category to which the other categories are compared).
MATHIEU et al.                                                                                                            168

supportive science-based evidence for the creation of new        other factors besides size are at play in this cause of death.
policies and practices that are needed to further protect bald   Immature raptors, being less experienced flyers and thus at a
eagles and other wildlife from preventable mortality             higher risk of mishaps when landing or taking off from an
associated with human activity (e.g., lead poisoning).           electric power structure, are commonly reported to be more
Trauma                                                           prone to electrocution than adult birds (Boeker and
   Trauma was the most commonly diagnosed cause of death,        Nickerson 1975; Fitzner 1978; Ferrer and Hiraldo 1992;
accounting for close to half of the carcasses examined (Table    Dawson and Mannan 1994). We did not identify an age
1). This high proportion is consistent with the findings of      predilection associated with electrocution, but we did
similar mortality studies in bald eagles and other raptors in    observe that bald eagles dying of trauma of human cause
North America (Coon et al. 1970; Deem et al. 1998; Driscoll      were more likely to be immature than adult. It is interesting
et al. 2004; Smith et al. 2018; Simon et al. 2020). However,     in this context that 1 adult female that died of electrocution
it contrasts with the low proportion of trauma reported for      had hepatic lead levels indicative of elevated exposure,
bald eagles in Saskatchewan (22%) where toxicosis was            suggesting that, as a neurotoxin, this amount of lead may
found to be the most prevalent cause of death (Scott and         have resulted in some degree of incoordination predisposing
Bollinger 2015).                                                 to this accident.
   A large proportion of the trauma cases were of unknown        Emaciation
cause; some of them could have been of human origin, such          The proportion of birds dying of emaciation in our study
as collisions with vehicles or power lines or from               (10%) is consistent with findings of other studies on causes
electrocution, while others may have had a natural cause,        of mortality in bald eagles in which the proportion of cases
such as collisions with trees. Vehicular collision, the most     of emaciation ranged from 3 ̶ 8% (Russell and Franson 2014;
commonly identified cause of traumatic injuries in this study,   Scott and Bollinger 2015; Smith et al. 2018; Simon et al.
may be more likely to occur when bald eagles scavenge road       2020). No effect of age or season on emaciation was detected,
kills. Non-target capture in snares or traps targeting           as was also found by Smith et al. (2018) in Ontario. It was
furbearers is generally only considered a minor cause of         nonetheless surprising that emaciation was rarely identified
trauma contributing to bald eagle mortality (Coon et al. 1970;   as a cause of death in winter, when food sources would be
Driscoll et al. 2004; Harris and Sleeman 2007; Scott and         expected to be least abundant (Table 2). However, bald
Bollinger 2015; Smith et al. 2018). However, the number of       eagles are semi-obligate scavengers and might benefit from
deaths from this cause in this study corroborates the findings   a time of year when animals of other species are more likely
by Fitzgerald et al. (2015) and Proulx et al. (2015) that such   to die from starvation.
non-target captures are an ongoing cause of bald eagle           Poisoning
mortality in Canada. It is also likely an underestimate since      Compared to some other Canadian reports, poisoning was
it was based in large part on voluntary reporting by trappers.   not a commonly identified cause of bald eagle mortality in
A number of measures aimed at mitigating this cause of           the Maritime provinces. Poisoning was only diagnosed in 9%
death in bald eagles have been proposed and implemented in       of the bald eagles in this study whereas it was diagnosed in
some, but not all, Canadian provinces (Fédération des            26% of bald eagles examined in Ontario (Smith et al. 2018)
trappeurs gestionnaires du Québec 2014; Fitzgerald et al.        and in 53% of those examined in Saskatchewan (Wayland
2015).                                                           and Bollinger 1999; Scott and Bollinger 2015). However, the
Electrocution                                                    possible presence of poisons was not systematically
   Electrocution, the second most commonly identified cause      determined in all birds for which this information would
of bald eagle mortality in our study, is a well-known cause      have been pertinent, such as some of the emaciated birds or
of death of large birds which, given their large body size and   those with an unknown cause of death.
wide wingspan, are at higher risk than small birds of              In this study, we determined that birds in poor body
spanning electrical components and thus contacting at least      condition were more likely to have died of poisoning than
2 points of energized or grounded hardware (Lehman et al.        those in moderate or good body condition. This can likely be
(2007). Ferrer and Hiraldo (1992) found that female Spanish      attributed to the fact that lead accounted for most cases of
imperial eagles (Aquila adalberti) were more prone to            poisoning (74%) and that half of the birds with lead
getting electrocuted on power lines than males and attributed    poisoning were emaciated, a typical manifestation of this
this difference to sexual dimorphism in this species, with       type of poisoning. Lead poisoning was also identified as the
females having a larger body size. In contrast, we observed      most common cause of poisoning in bald eagles in Ontario
that male bald eagles, which are typically smaller than          (14/23, 61%), in Michigan (176/185, 95.1%), and in several
females, were more prone to electrocution. This suggests that    American states combined (484/762, 63.5%) (Russell and
MATHIEU et al.                                                                                                              169

Franson 2014; Smith et al. 2018; Simon et al. 2020), but not       sodium pentobarbital for euthanasia of domestic animals can
in Saskatchewan (20/121, 16.5%) where OP/CM were the               result in secondary intoxication of these birds if carcasses of
more common cause of poisoning (Scott and Bollinger 2015).         euthanized animals have been improperly disposed of
In this study, potential subclinical effects of lead did not       (Langelier 1993; Russell and Franson 2014; Simon et al.
appear to be common among 100 bald eagles with a cause of          2020).
death determined to be something other than lead poisoning         Other causes of mortality
in which hepatic or renal lead levels were determined.               Conspecific fights, infectious or idiopathic diseases,
  Our findings, along with those in other provinces, indicate      nestling mortality, and drowning/hypothermia were
that lead poisoning continues to pose a threat to bald eagles      infrequent individual contributors to mortality in our study,
in Canada. Although the use of lead ammunition to hunt             which is similar to findings in other studies of causes of
migratory game birds, including waterfowl, was banned in           mortality in raptors (Coon et al. 1970; Deem et al. 1998;
Canada in 1999, it is still used for hunting upland game birds     Morishita et al. 1998; Driscoll et al. 2004; Harris and
and small and large game mammals (Martin et al. 2008).             Sleeman 2007; Russell and Franson 2014; Scott and
Therefore, as semi-obligate scavengers, bald eagles continue       Bollinger 2015; Smith et al. 2018; Simon et al. 2020). No
to be exposed to lead through consumption of unretrieved           birds were diagnosed with either avian cholera or infection
carcasses or discarded offal from animals killed with lead         by West Nile virus, which were the 2 most frequently
ammunition (Stauber et al. 2010; Bedrosian et al. 2012;            diagnosed infectious diseases of bald eagles in Saskatchewan
Cruz-Martinez et al. 2012). Lead fishing tackle also               and Ontario, respectively (Scott and Bollinger 2015; Smith
represents an ongoing threat (Scheuhammer et al. 2003). It         et al. 2018). Most cases of infection were of a focal nature
is predicted that, in the absence of a legislative change, the     and could have been secondary to local trauma, and some of
use of lead ammunition will increase over the next decade,         them could potentially have been linked to human activities.
and the level of lead released annually into the environment       Human-related mortality
will increase from 5,000 tons (in 2016) to 5,800 tons by 2025        Human-related causes of mortality, including trauma,
in Canada (Government of Canada 2018a). Alternatives to            electrocution and poisoning, accounted for approximately
lead ammunition and fishing gear, made from materials such         half (48%) of the bald eagle mortalities in this study. This
as copper or copper-zinc alloy, steel, tungsten or bismuth, are    proportion may be overestimated since carcasses are more
safer for the environment and are available commercially           likely to be found and reported in populated areas and these
(Government of Canada 2018b).                                      areas are where mortality events are more likely to be due to
  Exposure to OP/CM accounted for 18% of the cases of              human-related activity (Scott and Bollinger 2015).
poisoning and nearly 2% of all eagle mortalities in our region.    Conversely, it may be underestimated since some cases of
Organophosphates and carbamates, introduced as an                  trauma of undetermined cause and some cases with an
alternative for pest management following the ban on               unknown cause of death may have been related to human
organochlorine insecticides in the early 1970s, are widely         activities. Regardless, our findings are consistent with other
used pesticides that often result in the non-target exposure of    human-related mortality patterns reported for bald eagles in
bald eagles and other wildlife (Henny et al. 1987; Allen et al.    North America that range between 30 ̶ 74% (Coon et al. 1970;
1996; Elliott et al. 1996; Fleischli et al. 2004; Wobeser et al.   Harris and Sleeman 2007; Russell and Franson 2014; Scott
2004; Cowan and Blakley 2015). Poisoning of bald eagles by         and Bollinger 2015) and indicate that anthropogenic factors
OP/CM commonly results from scavenging on livestock                continue to play a dominant role in mortality of this species
carcasses illegally laced with OP/CM used as coyote (Canis         in North America. The fact that birds in moderate to good
latrans) baits to prevent livestock predation (Allen et al.        body condition were more likely to die of human-related
1996; Cowan and Blakley 2015). Continuous monitoring of            causes (specifically, trauma and electrocution) than birds in
the use of OP/CM and increased public awareness of the             poor body condition indicates that most traumatic injuries
consequences of illegally baiting wildlife with OP/CM-laced        were acute and that birds were otherwise healthy at the time
carcasses are needed to mitigate future poisonings. In their       of death.
recent study, Hertz-Picciotto et al. (2018) highlighted the        Study limitations
human health hazards associated with organophosphate                 By the nature of the data involved, particularly the
pesticides and advocated for a global ban on their                 identification and collection of carcasses, this and other
agricultural and non-agricultural use.                             similar wildlife mortality studies are often limited by strong
  Three bald eagles in our study were identified as having         biases such as observer density and awareness and the size,
died from barbiturate poisoning. Because of bald eagles’           visibility and degree of preservation of carcasses (Coon et al.
reliance on scavenging, the use of barbiturates such as            1970). Carcass counts alone most often underestimate actual
MATHIEU et al.                                                                                                               170

mortality by a large margin (Ponce et al. 2010), and estimates    the current Maritime ecosystem, which is likely facilitated
of overall total mortality, even moderately accurate, are         by its scavenging feeding habits, the diversity of its diet, and
difficult to achieve (Loss et al. 2014). The cost of some         the abundance of shoreline. Nonetheless, human-related
diagnostic tools to identify more subtle causes of mortality      causes of death, either direct or indirect, are an ongoing issue
may also limit their use to only a subsample of cases. For all    in the Maritime provinces (MacDougall 2005), as they are in
these reasons, the proportion of various causes of mortality      other Canadian provinces, and should not be ignored,
identified in this study may not be fully representative of the   especially if mitigating measures are available. Reduction of
Maritime population of bald eagles at large, but more of the      negative human impacts (e.g., through updated policies
segment of that population in relative proximity to human         pertaining to lead-based ammunitions and fishing tackle,
habitation.                                                       pesticide use and trapping methods) is needed to better
   Our failure to identify associations between causes of         protect bald eagles and their habitats across Canada.
mortality and various spatial variables, for example between
trauma of human cause and proximity to roads, does not rule       ACKNOWLEDGEMENTS
them out. Further studies would require a more detailed
                                                                    We wish to thank all the people from the 3 Maritime
understanding of habitat characteristics and their change
                                                                  provinces, particularly the provincial conservation officers
over time, possibly through satellite-based detection
                                                                  and park wardens, who submitted carcasses of bald eagles
methods. Moreover, the location at which an eagle carcass
                                                                  over the many years of this project, and Darlene Weeks and
is found may not represent the area where the factor that
                                                                  Fiep de Bie, who helped in the necropsy of these carcasses
caused its death was encountered, even in the recent past.
                                                                  throughout the duration of this project. Dr. María Forzán
Therefore, foraging and yearly movements of the birds must
                                                                  also contributed substantially to the work involved.
also be considered. For example, bald eagle nesting habitat
(i.e., the home range in which they tend to display aggression
toward other eagles) is small and varies between 1 and 2 km       LITERATURE CITED
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Wayland, M., and T. Bollinger. 1999. Lead exposure and           AVC to complete a joint residency in morphologic and
 poisoning in bald eagles and golden eagles in the Canadian      wildlife pathology in 1994. Scott then became a wildlife
 prairie provinces. Environmental Pollution 104: 341 ̶ 350.      pathologist and the first staff member for the Canadian
Wobeser, G. A. 1997. Diseases of wild waterfowl. 2nd             Wildlife Health Cooperative, Atlantic Region. His primary
 edition, Plenum Press, New York, New York, USA.                 focus is using scanning and targeted wildlife health
Wobeser, G., T. Bollinger, F.A. Leighton, B. Blakley, and        surveillance to develop evidence-based management
 P. Mineau. 2004. Secondary poisoning of eagles following        strategies for the protection of wildlife health throughout
 intentional poisoning of coyotes with anticholinesterase        Canada.
 pesticides in western Canada. Journal of Wildlife Diseases        Colin Robertson is an
 40: 163 ̶ 172.                                                  associate professor in the
ABOUT THE AUTHORS                                                Department of Geography and
                                                                 Environmental Studies at
  Amélie Mathieu is a wildlife
                                                                 Wilfrid Laurier University and
veterinarian with the British
                                                                 an associate with the Canadian
Columbia Ministry of Forests,
                                                                 Wildlife Health Cooperative
Lands,     Natural      Resource
                                                                 (National Office). Colin is
Operations       and       Rural
                                                                 interested in understanding the
Development. She received her
                                                                 role that environmental change has on the health of human
Doctor of Veterinary Medicine
                                                                 and animal populations and how GIS and spatial modelling
degree from the Université de
                                                                 tools can help to understand the wildlife health.
Montréal in 2012, after which
                                                                   Helene Van Doninck was a wildlife veterinarian and the
she     completed      veterinary
                                                                 founder of the Cobequid Wildlife Rehabilitation Centre.
internships in small animal medicine, zoo medicine and
                                                                 Dr. Van Doninck saw far too many cases of lead poisoning
wildlife health and a combined residency (ecosystem health
                                                                 in avian wildlife. She became a leader in promoting the
and conservation medicine) and master’s program (Master of
                                                                 elimination of lead
Science in Veterinary Preventive Medicine) at the Ohio State
                                                                 in ammunition and
University, the Columbus Zoo and Aquarium and The Wilds.
                                                                 fishing tackle, not
  Jane Parmley is an associate professor in the Department
                                                                 only in this region,
                          of Population Medicine at the
                                                                 but also in the rest
                          University of Guelph and an
                                                                 of Canada and in
                          epidemiologist with the Canadian
                                                                 the United States.
                          Wildlife     Health    Cooperative
                                                                 She     is    sorely
                          (National     Office).   Jane     is
                                                                 missed.
                          interested in messy but fascinating
                                                                   Pierre-Yves Daoust is a wildlife pathologist with a
                          health challenges and works to
                                                                 particular interest in the marine environment. He is Professor
                          better understand the many drivers
                                                                 Emeritus       of     Anatomic
                          that influence health and the
                                                                 Pathology      and Wildlife
interconnections between humans, animals and our shared
                                                                 Pathology in the Department
environments.
                                                                 of         Pathology          &
  Scott McBurney used his BSc
                                                                 Microbiology,           Atlantic
(Honors) in wildlife biology,
                                                                 Veterinary              College,
University of Guelph during a 6-
                                                                 University of Prince Edward
yr resource conservation career
                                                                 Island, and former Director of
as a National Park Warden.
                                                                 the Atlantic regional centre of
Despite a love for National
                                                                 the Canadian Wildlife Health Cooperative.
Parks, he continued to have a
passion to apply veterinary                                      Received 22 April 2020 – Accepted 20 July 2020
medicine to the field of wildlife
health. Therefore, Scott returned to university, graduating
with a DVM in the first veterinary class of the Atlantic
Veterinary College (AVC). Subsequently, he returned to the
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