Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 October 2021 | 13(12): 19808–19812
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
https://doi.org/10.11609/jott.5777.13.12.19808-19812
#5777 | Received 13 February 2020 | Final
received 11 September 2021 | Finally accepted 25 September 2021
Is release of rehabilitated
wildlife with embedded lead ammunition advisable? Plumbism in a Jaguar Panthera
Onca (Mammalia: Carnivora: Felidae), survivor of
gunshot wounds
Eduardo A. Díaz 1,
Carolina Sáenz 2, E. Santiago Jiménez
3, David A. Egas 4 & Kelly Swing
5
1 Universidad San Francisco de
Quito, Colegio de Ciencias
de la Salud, Escuela de Medicina
Veterinaria, Diego de Robles s/n, Quito 170901,
Ecuador.
1,2 Universidad San Francisco de
Quito, Hospital de Fauna Silvestre TUERI, Diego de Robles s/n, Quito 170901,
Ecuador.
3,4 Universidad San Francisco de
Quito, Colegio de Ciencias
e Ingeniería, Departamento
de Ingeniería Química, Diego
de Robles s/n, Quito 170901, Ecuador.
5 Universidad San Francisco de
Quito, Colegio de Ciencias Biológicas y Ambientales, Estación de Biodiversidad Tiputini, Diego de Robles s/n, Quito 170901, Ecuador.
1 eadiaz@usfq.edu.ec (corresponding
author), 2 csaenz@usfq.edu.ec, 3 eder.jimenez@estud.usfq.edu.ec,
4 degas@usfq.edu.ec, 5 kswing@usfq.edu.ec
Editor: N.V.K. Ashraf, Wildlife Trust of
India, Noida, India. Date of publication: 26 October
2021 (online & print)
Citation: Díaz, E.A., C. Sáenz, E.S. Jiménez, D.A. Egas
& K. Swing(2021). Is release of rehabilitated
wildlife with embedded lead ammunition advisable? Plumbism in a Jaguar Panthera
Onca (Mammalia: Carnivora: Felidae), survivor of
gunshot wounds. Journal of Threatened Taxa 13(12): 19808–19812. https://doi.org/10.11609/jott.5777.13.12.19808-19812
Copyright: © Díaz et al. 2021. Creative Commons Attribution
4.0 International License. JoTT allows unrestricted use, reproduction, and
distribution of this article in any medium by providing adequate credit to the
author(s) and the source of publication.
Funding: Publication of this article was
funded by the Universidad San Francisco de Quito Research Publication Fund.
Competing interests: The authors
declare no competing interests.
Acknowledgements: The authors thank the Ministerio del Ambiente, Inmobiliar, Unidad de Protección
del Medio Ambiente and the Tiputini
Biodiversity Station for supporting this research. This study was conducted
under official agreement and permit issued by Ecuador’s Ministry of the
Environment (permit 019-2018-IC-FAU-DNB/MAE) and authorized by the animal ethics
committee of Universidad San Francisco de Quito (permit 2018-011). Publication
of this article was funded by the Universidad San Francisco de Quito Research
Publication Fund.
Abstract: Lead poisoning is a threat to
wildlife, particularly after ingestion of lead ammunition derived from hunting
activities. Little information, however, is available concerning plumbism in wild animals that survive the trauma associated
with gunshot wounds. This study presents a possible example of lead
intoxication by embedded pellets in a Jaguar Panthera
onca nineteen months after being injured by a
shotgun blast. In addition, the possible path of incorporation of lead into the
trophic chain after the eventual release and death of an impacted animal,
thereby expanding and prolonging the toxic effects of lead ammunition, is
discussed. Direct intoxication by ammunition retained in the body of wild
animals, as well as the indirect impacts on predators and scavengers that
consume their flesh, should be sufficient reasons to reconsider the release of
individuals with embedded lead ammunition into the wild.
Keywords: Blood lead levels, endangered
species, lead-free ammunition, trophic web.
The Jaguar Panthera
onca, is the largest American felid, and the only
living representative of the genus Panthera
in the New World (Caragiulo et al. 2016). Historically distributed from the
southwestern United States to southern Argentina, Jaguars inhabit a wide range
of ecological zones, from tropical moist forests, to xeric shrublands, to
tropical dry forests, to grasslands and savannas (Sanderson et al. 2002). The IUCN Red List classifies the species
globally as Near Threatened since 2002; the population trend is decreasing due
to habitat loss and direct human persecution (Quigley et al. 2017). Currently,
although the species is included in Appendix I of the Convention on
International Trade in Endangered Species (CITES 2019), threats have continued
or intensified at local and regional scales, and Jaguars have already
disappeared from 55% of their historical range. The majority of subpopulations
are Endangered or Critically Endangered (De la Torre et al. 2018). In Ecuador,
where hunting remains one of the main threats to the species, two subspecies
are separated by the Andean highlands, the Endangered Panthera
onca onca from Amazon
rainforest (Espinosa et al. 2011a), and the Critically Endangered P. onca centralis from the western coast (Espinosa et al.
2011b).
Lead ammunition is highly toxic for wildlife,
especially in long-lived scavengers and predators (Gil-Sánchez et al.
2018). Intoxication of wildlife following ingestion of lead ammunition has
long been recognized (Pain et al. 2019), contributing to population decline of
some threatened species (Fernandez et al. 2011; Finkelstein et al. 2012;
Garbett et al. 2018). Nonetheless, little is known about the impact of retained
lead projectiles from gunshot wounds, despite a high incidence of embedded lead
in wild animals secondary to hunting injuries (LaDoucer
et al. 2015, Berny et al. 2017). This study describes lead poisoning through
retained ammunition in an Endangered Amazon Jaguar subsequent to its recovery
from multiple firearm injuries, and the possible incorporation of lead into the
trophic chain after incidental ingestion by scavengers.
Material and Methods
On 31 October 2016, a juvenile female Jaguar was
transferred from the province of Sucumbíos in northeastern Ecuador to the
Wildlife Hospital TUERI of Universidad San Francisco de Quito (USFQ) for
evaluation of injuries caused by a shotgun blast. Radiographic series (Sharp
Ray LWX-20P) revealed the presence of 18 pellets scattered dorso-anteriorly;
six of these were removed surgically (Image 1). The patient gradually improved
and was transferred to the recovery center to complete the rehabilitation
process two months after admission. In the following nine months, the Jaguar
exhibited natural behaviors in terms of hunting and fishing, as well as
aversion to and flight from human presence, which indicated excellent potential
for successful release into the wild. Eleven months after her original
injuries, the Jaguar was captured from its enclosure for clinical evaluation
and to assess the possible reabsorption of embedded lead; blood lead levels
(BLL) were measured by atomic absorption spectrophotometry (Buck Scientific
210VGP).
Showing no indications of complicating factors, the
patient was clinically discharged but still held in natural-setting captivity
while her eventual release into a remote area of Yasuní
Biosphere Reserve was planned. In the following eight months, she was captured
twice more, specifically for the placement of a satellite collar (Telonics TGW-4577-4) for post-release monitoring, and
ultimately to evaluate her overall condition for transfer to the release site.
Following release on 21 May 2018, the Jaguar was tracked for four days after
which the satellite device stopped transmitting movements; the animal was found
dead four days later. The carcass presented an advanced state of decomposition
and was being scavenged by vultures at the time of encounter. Remains were
transferred to Wildlife Hospital TUERI for forensic analysis, including
radiology (Sharp Ray LWX-20P) and scanning electron microscopy (JEOL
JSM-IT300LA) of bones. Blood samples collected on the day of release were
analyzed post-mortem by atomic absorption spectrophotometry (Buck Scientific
210VGP) to determine the possible reabsorption of embedded lead into general
circulation.
Results
As previously mentioned, after surgery, twelve lead
pellets remained embedded in the Jaguar’s body; none within the digestive
system or skeletal articulations (Image 1), sites classically considered to
present elevated risks (Eward et al. 2011). Eleven
months later, no clinical symptoms of lead intoxication were identified, and
BLL measurement was negative to the sensitivity limit 0.001 μg/dl.
After release, satellite tracking showed movement for four days – 2.7, 1.5,
1.2, and 0.3 km/day, respectively. The advanced state of decomposition
presented by the carcass when located only allowed radiological examination; no
superficial evidence of the cause of death could be ascertained due to the
putrefied condition of the body. None of the 12 pellets remaining in the
animal’s body were detected by radiographic series. Scanning electron
microscopy showed no traces of lead in the bone samples. Atomic absorption
spectrophotometry analysis of blood samples collected on the day of the release
revealed high BLL (1,223 µg/dl) in noteworthy contrast to earlier samples.
Discussion
Embedded lead has been identified as a risk factor
causing plumbism in humans and experimental animals,
but it has been poorly investigated in wildlife (LaDoucer
et al. 2015; Berny et al. 2017). According to our knowledge, there are no data
that relate the presence of embedded projectiles with BLL in wild mammals, but
in humans, values greater than 25-40 μg/dL can cause symptoms that range from quite mild to coma
and death (Bustamante & Macias-Konstantopoulos
2016). In the present study, no obvious outward symptoms were identified during
the time that the Jaguar remained in captivity. Nevertheless, although BLL were
not detected during the first eleven months, eight months later they reached
one of the highest values recorded to date for a wild felid (Burco et al. 2012; North et al. 2015). This could be due to
the type of exposure. In the case of chronic exposure, symptoms appear
progressively and become incrementally more severe as time passes. Conversely,
severe symptoms can erupt suddenly in acute exposures (Kim et al. 2015).
Therefore, absence of evident clinical symptoms, and sudden death of the
Jaguar, may have been due to acute absorption of lead.
Pain, weakened muscle strength, sensory abnormalities
and brain inflammation can appear as acute symptoms in plumbism.
More severe manifestations occur at very concentrated exposures, and symptoms
abruptly worsen to include delirium, loss of muscular coordination,
convulsions, ataxia, paralysis, coma and death (Sanders et al. 2009; Flora et
al. 2012). Following release, satellite tracking revealed that the distance
moved by the animal progressively decreased in the subsequent days (2.7, 1.5,
1.2, and 0.3 km/day).
In an effort to corroborate the hypothesis of acute
exposure, a bone analysis was performed seeking to determine the presence of
lead. The accumulation of lead in bones is indicative of long-term exposure due
to its extended residence time, in contrast to BLL that is used to measure recent
exposure because of the short half-life of lead in the blood (Green & Pain
2019). Scanning electron microscopy did not detect lead residues in
bone samples, confirming that the embedded reabsorption would not have been
chronic.
In most
cases of plumbism, lead is ingested and absorbed into
the bloodstream through the intestinal tract. Acute onset of nervous symptoms is a potential
condition of captive felids fed hunted game animals (North et al. 2015). In our
case, the Jaguar did not receive hunted meat or any other type of food that
could contain traces of lead, making it is impossible that the poisoning
occurred in this way; any BLL should come through reabsorption from the
ammunition embedded in its body. In human cases, lead toxicity with intra-articular
retained ammunition is indeed considered a risk, but extra-articular embedded
lead, when difficult to extract, is routinely permitted to remain in tissues
indefinitely without surveillance for lead toxicity. However, lead toxicity
associated with extra-articular retained ammunition, although uncommon, may be
asymptomatic and difficult to diagnose yet debilitating and potentially lethal
(Eward et al. 2011; Grasso et al. 2017). This fact
could corroborate our findings in the present case. Although there seems to be
no clear relationship between the amount of lead retained, residence time or
location in the human body, embedded lead cannot be considered inert or safe
(De Araújo et al. 2015).
Primary treatment in cases of retained lead ammunition
usually includes chelation, followed by complete surgical removal of retained
projectiles, in order to prevent systemic toxicity (Bustamante & Macias-Konstantopoulos 2016). Nevertheless, sometimes the
elimination of projectiles would require complicated surgical approach
resulting in extensive tissue dissection and high morbidity in a patient
weakened by trauma (De Araújo et al. 2015). When surgical removal of ammunition
fragments is contra-indicated, there are currently no long-term treatment
methods available, since the source of exposure remains in the body, and
prolonged chelation would cause adverse health effects such as hepatotoxicity
or nephrotoxicity (McQuirter et al. 2004; Flora &
Pachauri 2010). Therefore, these patients should be considered at chronic risk
for lead poisoning and monitored periodically (Moazeni
et al. 2014).
Finally, in the radiological tests performed on the
Jaguar carcass, none of the 12 embedded pellets was detected. A likely
explanation is incidental ingestion by scavengers; three species of vultures
were identified next to the Jaguar cadaver: the American Black Vulture Coragyps atratus,
the Greater Yellow-headed Vulture Cathartes
melambrotus, and the King Vulture Sarcoramphus papa. Therefore, lead
projectiles retained in the Jaguar’s body could have had devastating effects
not only for the Jaguar itself, but also for other species upon entering the
trophic web through carrion consumers. In South America, with lead poisoning
being a major widespread conservation threat for the Andean Condor Vultur gryphus (and
probably for other sympatric carnivores also), urgent conservation actions to
reduce this toxin in the wild are necessary (Wiemeyer
et al. 2017). In this sense, evidence on the adverse effects of the use of lead
ammunition on wildlife is ample. Because the change to non-toxic alternatives
is possible and would allow important benefits for nature conservation (Kanstrup et al. 2018; Cromie et
al. 2019), the strategy should be considered and implemented on a much broader
scale.
In conclusion, some limitations of this work have been
the lack of more thorough BLL monitoring during the time that the patient
remained in captivity due to the difficult handling of the species, and the
impossibility of assessing the presence of lead in other soft tissues after
death because of the advanced state of decomposition in which the carcass was
found. According to the authors’ knowledge, the present study suggests for the
first time that the presence of embedded pellets can be associated with a significant
blood lead concentration in a wild felid. This situation reinforces the need
for better understanding of the toxic effects of lead in wildlife surviving
gunshot wounds. Until then, each patient with lead ammunition retained in its
body should be considered at chronic risk for itself and a potential danger to
other species that may eventually feed on it. Therefore, release of individuals
with embedded lead projectiles should be carefully considered by wildlife
managers when complete removal of lead fragments is not possible.
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