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Infectious disease and red Wolf conservation: Assessment of disease occurrence and associated risks

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  • Point Defiance Zoo & Aquarium

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Infectious diseases pose a significant threat to global biodiversity and may contribute to extinction. As such, establishing baseline disease prevalence in vulnerable species where disease could affect persistence is important to conservation. We assessed potential disease threats to endangered red wolves (Canis rufus) by evaluating regional (southeastern United States) disease occurrences in mammals and parasite prevalence in red wolves and sympatric coyotes (Canis latrans) in North Carolina. Common viral pathogens in the southeast region, such as canine distemper and canine parvovirus, and numerous widespread endoparasites could pose a threat to the red wolf population. The most prevalent parasites in red wolves and sympatric coyotes were heartworm (Dirofilaria immitis), hookworm (Ancylostoma caninum), and Ehrlichia spp.; several red wolves and coyotes were also positive for bacteria causing Lyme disease (Borrelia burgdorferi). Coyotes had a more species-rich parasite community than red wolves, suggesting they could harbor more parasites and act as a disease reservoir. Species identity and sex did not significantly affect parasite loads, but young canids were less likely to have heartworm and more likely to have high levels of endoparasites. Continued disease monitoring is important for red wolf recovery because low levels of genetic variability may compromise the wolves’ abilities to combat novel pathogens from closely related species, such as domestic dogs and coyotes.
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... 10 Prior studies have identified disease exposure and mortality in both captive and free-ranging red wolves. 2,9 A survey of mortality in captive red wolves examined postmortem between 1997 and 2012 identified neoplasia and gastrointestinal disease as the most common causes of death in adult animals. 9 Infectious disease (primarily bacterial pathogens) contributed to 9% of adult mortality. ...
... 9 A recent analysis of infectious diseases affecting free-ranging red wolves identified exposure to ectoparasites (ticks, biting lice, mange mites), endoparasites (hookworm, heartworm), viral disease (canine distemper, canine parvovirus, rabies), and tick-borne disease (Lyme disease, ehrlichiosis, and Rocky Mountain spotted fever). 2 Prior determination that free-ranging red wolves are exposed to vector-borne organisms (VBOs) raises the question whether these pathogens affect the ex situ population. The goal of this study was to assess the prevalence of selected VBOs in captive red wolves to evaluate their potential as threats to species survival and to provide a baseline that may facilitate ongoing disease monitoring and the detection of emergent threats from such VBOs. ...
... were detected in 72% of sampled free-ranging red wolves, and at least one red wolf tested positive for Rocky Mountain spotted fever. 2 Closely related canids such as coyotes (Canis latrans), gray wolves (Canis lupus), and domestic dogs (Canis lupus familiaris) experience exposure, infection, or both to multiple VBOs at nonzero rates. [2][3][4]7 Alternatively, rather than lack of exposure or susceptibility, red wolves may be capable of clearing infection by these VBOs, or they may experience infection with blood pathogen levels below the detection thresholds of the referenced qPCR assays, which range from one to five pathogen DNA target copies. ...
Article
The red wolf (Canis rufus) is a critically endangered North American canid, with surviving conspecifics divided between a captive breeding population and a reintroduced free-ranging population. The goal of this study was to assess the prevalence of selected vector-borne pathogens in captive red wolves. Whole blood samples were collected from 35 captive red wolves. Quantitative polymerase chain reaction (PCR) assays were performed on extracted DNA to identify infection by Trypanosoma cruzi and vector-borne organisms within the following genera: Anaplasma, Babesia, Bartonella, Ehrlichia, Mycoplasma, Neoehrlichia, Neorickettsia, and Rickettsia. All red wolves sampled were PCR-negative for all tested organisms. These pathogens are unlikely to constitute threats to red wolf conservation and breeding efforts under current captive management conditions. The results of this study establish a baseline that may facilitate ongoing disease monitoring in this species.
... Several carnivores have been described as heartworm definitive hosts in wildlife: coyote (Canis latrans); red fox (V. vulpes); grey fox (Urocyon cinereoargenteus) [5,11,12]; golden jackal (Canis aureus) [7,9,13]; red wolf (Canis rufus) [14]; European wildcat (Felis silvestris) [13]; and Eurasian otter (Lutra lutra) [13,15]. Data on heartworm infection in the grey wolf (Canis lupus), the closest wild relative of the domestic dog, are still scarce, having been reported only sporadically in Europe since 2001 [7,[16][17][18][19][20][21][22][23]. ...
... In addition, the size of adult nematodes from wolves was similar as reported in dogs (mean length: 25.5 cm) [3]. In contrast, studies on red foxes showed that the majority of female worms were small-sized immature individuals [5,14]. A fox-like pattern was revealed recently in the golden jackal, a canid currently spreading from the Balkans into central Europe, including northern Italy [14]. ...
... In contrast, studies on red foxes showed that the majority of female worms were small-sized immature individuals [5,14]. A fox-like pattern was revealed recently in the golden jackal, a canid currently spreading from the Balkans into central Europe, including northern Italy [14]. Overall, the similarity with dogs and the substantial difference with other wild canids, suggest that wolves are fully competent hosts of D. immitis and in the future may represent a complementary reservoir of this parasite, aside unprotected dogs. ...
Article
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Background: Wild carnivores such as the grey wolf (Canis lupus), red fox (Vulpes vulpes) and golden jackal (Canis aureus) are recognized hosts of Dirofilaria immitis. However, few studies have focused on their actual role in the epidemiology of heartworm infection. This study describes the prevalence and distribution of D. immitis in wolves in a heartworm-endemic area in northern Italy where wolves have recently returned after long-time eradication, and investigates the fertility status of the collected adult nematodes. Methods: In the frame of a long-term wolf monitoring programme in northwestern Italy, 210 wolf carcasses from four provinces were inspected for the presence of filarioid nematodes in the right heart and pulmonary arteries. Female heartworms were measured, and their uterine content analyzed according to a previously described "embryogram" technique. Results: Three wolves, all originating from a single province (Alessandria), were positive for D. immitis (1.42%, 95% CI: 0.48-4.11%, in the whole study area; 13.6%, 95% CI: 4.7-33.3%, limited to the single province from which infected wolves originated). Mean intensity was 5 worms (range: 3-7) and the female worms measured 21-28 cm in length. Six out of 9 female worms harbored uterine microfilariae: 5 were classified as gravid; 1 showed a "discontinuous gradient"; and 3 were non-gravid. Conclusions: The present data show that heartworm infection is already prevalent in wolves that have recolonized the known heartworm-endemic area. Based on "embryogram" results, wolves were shown suitable heartworm hosts. Interestingly, investigated wolves appeared similarly exposed to heartworm infection as sympatric unprotected dogs (owned dogs that have never received any heartworm prevention treatment) sampled at the beginning of the wolf return process.
... Parasites have detrimental effects on host health and fitness (Soares, Gozzelino, & Weis, 2014), driving infectious disease (Simpson, Johnson, & Carver, 2016) and posing major conservation threats, particularly to endangered or isolated host species (Pedersen, Jones, Nunn, & Altizer, 2007;Wikelski, Foufopoulos, Vargas, & Snell, 2004). At the population level, high infection intensity can disrupt group dynamics and substantially limit population growth and size (Albon et al., 2002;Eira, Vingada, Torres, & Miquel, 2006;Watson, 2013), sometimes accelerating population crashes or elevating extinction risk (Brzeski et al., 2015;Gulland, 1992;Johnson et al., 2012). At the individual level, heavy burdens can be highly pathological, increasing risk of infectious disease and secondary illnesses (Beldomenico et al., 2008;Day, Graham, Read, & Kl, 2007), and stimulating immunopathology (Graham, Allen, & Read, 2005). ...
... Consequently, studies suggest that sex differences in infection exist because of differing optimal fitness strategies, mediated by competitive trade-offs between reproduction and self-maintenance, with males favoring paternity and females longevity (Folstad & Karter, 1992;Hamilton & Zuk, 1982;Hayward, 2013;Mills et al., 2009;Zahavi, 1975). Within a host population, juveniles, and juvenile males in particular (Clutton-Brock & Pemberton, 2004;Wilson, Grenfell, Pilkington, Boyd, & Gulland, 2004), often experience the heaviest parasite loads (Brzeski et al., 2015;Jones, Crawley, Pilkington, & Pemberton, 2005). This may be due in part to the fact that immune function is not yet fully developed in maturing individuals (Simon, Hollander, & Mcmichael, 2015), as well as potential trade-offs arising between growth and immunity (Medley, 2002;Tschirren & Richner, 2006). ...
... While parasites have been implicated in the regulation of certain populations of red grouse Lagopus lagopus scotica (Hudson, Dobson, & Newborn, 1998), Arctic charr (Knudsen et al., 2002), and Svalbard reindeer Rangifer tarandus platyrhynchus (Albon et al., 2002), studies describing the frequency of parasite-induced mortality and identifying the individuals within populations with the highest risk of parasite-induced mortality are exceptionally rare. In addition, while studies have shown that infection intensities within wild populations are consistently increased in certain groups, for example, juveniles (Brzeski et al., 2015) and males (Craig et al., 2006;Harrison et al., 2010;Klein, 2004), links between these groups and elevated mortality risk have rarely been made. Arguably in many wild vertebrate populations, individual mortality is likely to be due to a synergy of factors, for example, interactions between infection and weight loss, hormone differences, and poor diet. ...
... Parasites have detrimental effects on host health and fitness (Soares, Gozzelino, & Weis, 2014), driving infectious disease (Simpson, Johnson, & Carver, 2016) and posing major conservation threats, particularly to endangered or isolated host species (Pedersen, Jones, Nunn, & Altizer, 2007;Wikelski, Foufopoulos, Vargas, & Snell, 2004). At the population level, high infection intensity can disrupt group dynamics and substantially limit population growth and size (Albon et al., 2002;Eira, Vingada, Torres, & Miquel, 2006;Watson, 2013), sometimes accelerating population crashes or elevating extinction risk (Brzeski et al., 2015;Gulland, 1992;Johnson et al., 2012). At the individual level, heavy burdens can be highly pathological, increasing risk of infectious disease and secondary illnesses (Beldomenico et al., 2008;Day, Graham, Read, & Kl, 2007), and stimulating immunopathology (Graham, Allen, & Read, 2005). ...
... Consequently, studies suggest that sex differences in infection exist because of differing optimal fitness strategies, mediated by competitive trade-offs between reproduction and self-maintenance, with males favoring paternity and females longevity (Folstad & Karter, 1992;Hamilton & Zuk, 1982;Hayward, 2013;Mills et al., 2009;Zahavi, 1975). Within a host population, juveniles, and juvenile males in particular (Clutton-Brock & Pemberton, 2004;Wilson, Grenfell, Pilkington, Boyd, & Gulland, 2004), often experience the heaviest parasite loads (Brzeski et al., 2015;Jones, Crawley, Pilkington, & Pemberton, 2005). This may be due in part to the fact that immune function is not yet fully developed in maturing individuals (Simon, Hollander, & Mcmichael, 2015), as well as potential trade-offs arising between growth and immunity (Medley, 2002;Tschirren & Richner, 2006). ...
... While parasites have been implicated in the regulation of certain populations of red grouse Lagopus lagopus scotica (Hudson, Dobson, & Newborn, 1998), Arctic charr (Knudsen et al., 2002), and Svalbard reindeer Rangifer tarandus platyrhynchus (Albon et al., 2002), studies describing the frequency of parasite-induced mortality and identifying the individuals within populations with the highest risk of parasite-induced mortality are exceptionally rare. In addition, while studies have shown that infection intensities within wild populations are consistently increased in certain groups, for example, juveniles (Brzeski et al., 2015) and males (Craig et al., 2006;Harrison et al., 2010;Klein, 2004), links between these groups and elevated mortality risk have rarely been made. Arguably in many wild vertebrate populations, individual mortality is likely to be due to a synergy of factors, for example, interactions between infection and weight loss, hormone differences, and poor diet. ...
Article
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Parasites can cause severe host morbidity and threaten survival. As parasites are generally aggregated within certain host demographics, they are likely to affect a small proportion of the entire population, with specific hosts being at particular risk. However, little is known as to whether increased host mortality from parasitic causes is experienced by specific host demographics. Outside of theoretical studies, there is a paucity of literature concerning dynamics of parasite-associated host mortality. Empirical evidence mainly focuses on short-lived hosts or model systems, with data lacking from long-lived wild or semi-wild vertebrate populations. We investigated parasite-associated mortality utilizing a multigenerational database of mortality, health, and reproductive data for over 4,000 semi-captive timber elephants (Elephas maximus), with known causes of death for mortality events. We determined variation in mortality according to a number of host traits that are commonly associated with variation in parasitism within mammals: age, sex, and reproductive investment in females. We found that potentially parasite-associated mortality varied significantly across elephant ages, with individuals at extremes of lifespan (young and old) at highest risk. Mortality probability was significantly higher for males across all ages. Female reproducers experienced a lower probability of potentially parasite-associated mortality than females who did not reproduce at any investigated time frame. Our results demonstrate increased potentially parasite-associated mortality within particular demographic groups. These groups (males, juveniles, elderly adults) have been identified in other studies as susceptible to parasitism, stressing the need for further work investigating links between infection and mortality. Furthermore, we show variation between reproductive and non-reproductive females, with mothers being less at risk of potentially parasite mortality than nonreproducers.
... Infatti, questi potrebbero agire da "sentinelle" della comparsa e/o la diffusione della parassitosi in aree indenni, o addirittura da reservoir, in particolar modo laddove i fenomeni di interazione domestico--selvatico sono frequenti e le condizioni climatiche consentono ai vettori lunghi periodi di attività. Attualmente, gli ospiti definitivi descritti nella fauna selvatica sono il coyote, la volpe rossa e grigia (rispettivamente, Canis latrans, Vulpes vulpes, Urocyon cinereoargenteus) (Wixsom et al., 1991;Criado et al., 2000), il lupo (Canis lupus, Canis rufus) (Brzeski et al., 2015), lo sciacallo dorato (Canis aureus) (Tolnai et al., 2014) e la lontra euro--asiatica (Lutra lutra) (Torres et al., 2004). I casi di dirofilariosi descritti in Europa nella volpe e nello sciacallo dorato hanno evidenziato una prevalenza relativamente bassa (rispettivamente 2,9% e 7,4%) ed una microfilariemia sporadica associata ad una predominanza di infestazioni con pochi adulti in sede cardiaca (Gradoni et al., 1980;Marconcini et al., 1996;Magi et al., 2008;Tolnai et al., 2014). ...
... Questi studi suggeriscono che volpe e sciacallo non rappresentano, almeno nelle aree relative agli studi, ospiti ideali per il completamento del ciclo biologico del nematode. In altri carnivori selvatici, risultati più recenti dagli Stati Uniti (Brzeski et al., 2015) descrivono una prevalenza più elevata (45%) di dirofilariosi cardiopolmonare nel lupo rosso (Canis rufus) e nel coyote (7%) (Wixsom et al., 1991). Nel lupo europeo la prima infestazione è stata segnalata nel 2001 da Segovia in Spagna con la presenza di un'unica filaria adulta (a seguito di 47 necroscopie eseguite su lupi provenienti dal nord--est della Spagna), mentre in Italia risale al 2007 (Pascucci et al., 2007) in una regione del centro--sud in cui la dirofilariosi è presente solo in maniera sporadica. ...
Presentation
La filariosi cardiopolmonare è una patologia causata dalla Dirofilaria immitis e colpisce primariamente il cane. I carnivori selvatici come lupo (Canis lupus) e volpe (Vulpes vulpes) rappresentano ospiti potenzialmente validi per il completamento del ciclo vitale del parassita, tuttavia esistono pochi studi che ne descrivano il ruolo epidemiologico effettivo. Lo scopo del nostro studio è quello di analizzare la capacità riproduttiva delle filarie adulte isolate da lupi del nord Italia dal 2016 al 2019, e di inquadrare la situazione epidemiologica di volpe e lupo in una zona endemica del Piemonte confrontandola con quella del cane descritta da altri autori.
... To keep the analyses at a reasonable level of complexity, the following pathogen groups were considered: bacteria (including rickettsia), viruses (including prions), ectoparasites (mites, ticks, lice and fleas), and protozoa. Only one fungus (Batrachochytrium dendrobatidis) and two parasitic helminths (meningeal worm Parelaphostrongylus tenuis and heartworm Dirofilaria immitis) were considered, based on their proven capacity to affect populations of wild amphibians (Skerratt et al. 2007), cervids (Lankester 2010) and canids (Brzeski et al. 2015), respectively. ...
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... We used mixed-effects modeling to contextualize genetic diversity within the broad range of factors that may influence infection severity in YNP wolves. Input data were derived from annual observa- (Almberg et al., 2015;Brzeski et al., 2015) and observation year (Stahler et al., 2013). As numerous wolves changed pack membership across years, we fitted these variables as partially crossed random intercepts. ...
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Population genetic theory posits that molecular variation buffers against disease risk. Although this “monoculture effect” is well supported in agricultural settings, its applicability to wildlife populations remains in question. In the present study, we examined the genomics underlying individual‐level disease severity and population‐level consequences of sarcoptic mange infection in a wild population of canids. Using gray wolves (Canis lupus) reintroduced to Yellowstone National Park (YNP) as our focal system, we leveraged 25 years of observational data and biobanked blood and tissue to genotype 76,859 loci in over 400 wolves. At the individual level, we reported an inverse relationship between host genomic variation and infection severity. We additionally identified 410 loci significantly associated with mange severity, with annotations related to inflammation, immunity, and skin barrier integrity and disorders. We contextualized results within environmental, demographic, and behavioral variables, and confirmed that genetic variation was predictive of infection severity. At the population level, we reported decreased genome‐wide variation since the initial gray wolf reintroduction event and identified evidence of selection acting against alleles associated with mange infection severity. We concluded that genomic variation plays an important role in disease severity in YNP wolves. This role scales from individual to population levels, and includes patterns of genome‐wide variation in support of the monoculture effect and specific loci associated with the complex mange phenotype. Results yielded system‐specific insights, while also highlighting the relevance of genomic analyses to wildlife disease ecology, evolution, and conservation.
... Understanding the relationship between inbreeding and disease is critical to the conservation of small or fragmented populations, in which the probability of inbreeding is elevated (Pertoldi et al. 2007, Smith et al. 2009, Brzeski et al. 2015. Our results illustrate the elevated risk that both endemic and emerging vector-borne diseases (WNV and-in nestlings-Plasmodium) can pose for inbred individuals and populations, underscoring the need to buffer small populations against infectious disease. ...
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... The low vaccination coverage concept utilised in conserving endangered species can also protect a core group of individuals during a disease outbreak (Prager et al. 2011;Vial et al. 2006). The prophylactic use of vaccines can increase a population's resistance to a disease, especially when herd immunity has been attained (Aguirre et al. 2002;Brzeski et al. 2015;Fine 1993). Inoculating animals can also be utilised as a remedial treatment for individuals that have been exposed to a particular pathogen, see Hofmeyr et al. (2000). ...
Thesis
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Code
Tools for performing model selection and model averaging. Automated model selection through subsetting the maximum model, with optional constraints for model inclusion. Model parameter and prediction averaging based on model weights derived from information criteria (AICc and alike) or custom model weighting schemes. [Please do not request the full text - it is an R package. The up-to-date manual is available from CRAN].
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Canine and Feline Infectious Diseases is a practical, up-to-date resource covering the most important and cutting-edge advances in the field. Presented by a seasoned educator in a concise, highly visual format, this innovative guide keeps you current with the latest advances in this ever-changing field. 80 case studies illustrate the clinical relevance of the major infectious disease chapters.
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Present range of Canis latrans in the US Southeast is outlined, a distribution facilitated by, or locally a direct result of releases by man. Spread, which has been notable since 1972, has been expedited by the merging of local populations. -P.J.Jarvis