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Organisms have evolved diverse strategies to manage parasite infections. Broadly, hosts may avoid infection by altering behaviour, resist infection by targeting parasites or tolerate infection by repairing associated damage. The effectiveness of a strategy depends on interactions between, for example, resource availability, parasite traits (virulence, life-history) and the host itself (nutritional status, immunopathology). To understand how these factors shape host parasite-mitigation strategies, we developed a mathematical model of within-host, parasite-immune dynamics in the context of helminth infections. The model incorporated host nutrition and resource allocation to different mechanisms of immune response: larval parasite prevention; adult parasite clearance; damage repair (tolerance). We also considered a non-immune strategy: avoidance via anorexia, reducing intake of infective stages. Resources not allocated to immune processes promoted host condition, whereas harm due to parasites and immunopathology diminished it. Maximising condition (a proxy for fitness), we determined optimal host investment for each parasite-mitigation strategy, singly and combined, across different environmental resource levels and parasite trait values. Which strategy was optimal varied with scenario. Tolerance generally performed well, especially with high resources. Success of the different resistance strategies (larval prevention or adult clearance) tracked relative virulence of larval and adult parasites: slowly maturing, highly damaging larvae favoured prevention; rapidly maturing, less harmful larvae favoured clearance. Anorexia was viable only in the short term, due to reduced host nutrition. Combined strategies always outperformed any lone strategy: these were dominated by tolerance, with some investment in resistance. Choice of parasite mitigation strategy has profound consequences for hosts, impacting their condition, survival and reproductive success. We show that the efficacy of different strategies is highly dependent on timescale, parasite traits and resource availability. Models that integrate such factors can inform the collection and interpretation of empirical data, to understand how those drivers interact to shape host immune responses in natural systems.
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Ageing is associated with profound changes in behaviour that could influence exposure and susceptibility to infectious disease. As well as determining emergent patterns of infection across individuals of different ages, behavioural ageing could interact with, confound, or counteract age-related changes in other traits. Here, we examine how behavioural ageing can manifest and influence patterns of infection in wild animals. We discuss a range of age-related changes that involve interactions between behaviour and components of exposure and susceptibility to infection, including social ageing and immunosenescence, acquisition of novel parasites and pathogens with age, changes in spatial behaviours, and age-related hygiene and sickness behaviours. Overall, most behavioural changes are expected to result in a reduced exposure rate, but there is relatively little evidence for this phenomenon, emerging largely from a rarity of explicit tests of exposure changes over the lifespan. This review offers a framework for understanding how ageing, behaviour, immunity, and infection interact, providing a series of hypotheses and testable predictions to improve our understanding of health in ageing societies.
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Envejecimiento , Enfermedades Transmisibles , Humanos , Animales , LongevidadRESUMEN
Here, we report the first known outbreak of clinical protozoal myeloencephalitis in naturally infected raccoons by the parasite Sarcocystis neurona. The North American opossum (Didelphis virginiana) and the South American opossum (Didelphis albiventris) are its known definitive hosts. Several other animal species are its intermediate or aberrant hosts. The raccoon (Procyon lotor) is considered the most important intermediate host for S. neurona in the USA. More than 50% of raccoons in the USA have sarcocysts in their muscles, however clinical sarcocystosis in raccoons is rare. In 2014, 38 free-living raccoons were found dead or moribund on the grounds of the Saint Louis Zoo, Missouri, USA. Moribund individuals were weak, lethargic, and mildly ataxic; several with oculo-nasal discharge. Seven raccoons were found dead and 31 were humanely euthanized. Postmortem examinations were conducted on nine raccoons. Neural lesions compatible with acute sarcocystosis were detected in eight raccoons. The predominant lesions were meningoencephalitis and perivascular mononuclear cells. Histologic evidence for the Canine Distemper Virus was found in one raccoon. Schizonts and merozoites were present in the encephalitic lesions of four raccoons. Mature sarcocysts were present within myocytes of five raccoons. In six raccoons, S. neurona schizonts and merozoites were confirmed by immunohistochemical staining with S. neurona-specific polyclonal antibodies. Viable S. neurona was isolated from the brains of two raccoons by bioassay in interferon gamma gene knockout mice and in cell cultures seeded directly with raccoon brain homogenate. Molecular characterization was based on raccoon no. 68. Molecular characterization based on multi-locus typing at five surface antigens (SnSAG1-5-6, SnSAG3 and SnSAG4) and the ITS-1 marker within the ssrRNA locus, using DNA isolated from bradyzoites released from sarcocysts in a naturally infected raccoon (no. 68), confirmed the presence of S. neurona antigen type I, the same genotype that caused a mass mortality event in which 40 southern sea otters stranded dead or dying within a 3 week period in April 2004 with S. neurona-associated disease. An expanded set of genotyping markers was next applied. This study reports the following new genotyping markers at 18S rRNA, 28S rRNA, COX1, ITS-1, RON1, RON2, GAPDH1, ROP20, SAG2, SnSRS21 and TUBA1 markers. The identity of Sarcocystis spp. infecting raccoons is discussed.
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Didelphis , Sarcocystis , Sarcocistosis , Animales , Ratones , Sarcocistosis/epidemiología , Sarcocistosis/veterinaria , Sarcocistosis/parasitología , Mapaches/parasitología , Esquizontes , Genotipo , MerozoítosRESUMEN
Gastrointestinal nematode (GIN) parasites play an important role in the ecological dynamics of many animal populations. Recent studies suggest that fine-scale spatial variation in GIN infection dynamics is important in wildlife systems, but the environmental drivers underlying this variation remain poorly understood. We used data from over two decades of GIN parasite egg counts, host space use, and spatial vegetation data from a long-term study of Soay sheep on St Kilda to test how spatial autocorrelation and vegetation in an individual's home range predict parasite burden across three age groups. We developed a novel approach to quantify the plant functional traits present in a home range to describe the quality of vegetation present. Effects of vegetation and space varied between age classes. In immature lambs, strongyle parasite faecal egg counts (FEC) were spatially structured, being highest in the north and south of our study area. Independent of host body weight and spatial autocorrelation, plant functional traits predicted parasite egg counts. Higher egg counts were associated with more digestible and preferred plant functional traits, suggesting the association could be driven by host density and habitat preference. In contrast, we found no evidence that parasite FEC were related to plant functional traits in the host home range in yearlings or adult sheep. Adult FEC were spatially structured, with highest burdens in the north-east of our study area, while yearling FEC showed no evidence of spatial structuring. Parasite burdens in immature individuals appear more readily influenced by fine-scale spatial variation in the environment, highlighting the importance of such heterogeneity for our understanding of wildlife epidemiology and health. Our findings support the importance of fine-scale environmental variation for wildlife disease ecology and provides new evidence that such effects may vary across demographic groups within a population.
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Nematodos , Infecciones por Nematodos , Parásitos , Enfermedades de las Ovejas , Animales , Ovinos , Herbivoria , Infecciones por Nematodos/epidemiología , Infecciones por Nematodos/veterinaria , Animales Salvajes , Heces/parasitología , Enfermedades de las Ovejas/parasitología , Factores de EdadRESUMEN
Next-generation sequencing (NGS) and metabarcoding approaches are increasingly applied to wild animal populations, but there is a disconnect between the widely applied generalized linear mixed model (GLMM) approaches commonly used to study phenotypic variation and the statistical toolkit from community ecology typically applied to metabarcoding data. Here, we describe the suitability of a novel GLMM-based approach for analyzing the taxon-specific sequence read counts derived from standard metabarcoding data. This approach allows decomposition of the contribution of different drivers to variation in community composition (e.g., age, season, individual) via interaction terms in the model random-effects structure. We provide guidance to implementing this approach and show how these models can identify how responsible specific taxonomic groups are for the effects attributed to different drivers. We applied this approach to two cross-sectional data sets from the Soay sheep population of St. Kilda. GLMMs showed agreement with dissimilarity-based approaches highlighting the substantial contribution of age and minimal contribution of season to microbiota community compositions, and simultaneously estimated the contribution of other technical and biological factors. We further used model predictions to show that age effects were principally due to increases in taxa of the phylum Bacteroidetes and declines in taxa of the phylum Firmicutes. This approach offers a powerful means for understanding the influence of drivers of community structure derived from metabarcoding data. We discuss how our approach could be readily adapted to allow researchers to estimate contributions of additional factors such as host or microbe phylogeny to answer emerging questions surrounding the ecological and evolutionary roles of within-host communities. IMPORTANCE NGS and fecal metabarcoding methods have provided powerful opportunities to study the wild gut microbiome. A wealth of data is, therefore, amassing across wild systems, generating the need for analytical approaches that can appropriately investigate simultaneous factors at the host and environmental scale that determine the composition of these communities. Here, we describe a generalized linear mixed-effects model (GLMM) approach to analyze read count data from metabarcoding of the gut microbiota, allowing us to quantify the contributions of multiple host and environmental factors to within-host community structure. Our approach provides outputs that are familiar to a majority of field ecologists and can be run using any standard mixed-effects modeling packages. We illustrate this approach using two metabarcoding data sets from the Soay sheep population of St. Kilda investigating age and season effects as worked examples.
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Microbioma Gastrointestinal , Microbiota , Animales , Ovinos , Estudios Transversales , Microbioma Gastrointestinal/genética , Animales Salvajes , HecesRESUMEN
Arboviruses receive heightened research attention during major outbreaks or when they cause unusual or severe clinical disease, but they are otherwise undercharacterized. Global change is also accelerating the emergence and spread of arboviral diseases, leading to time-sensitive questions about potential interactions between viruses and novel vectors. Vector competence experiments help determine the susceptibility of certain arthropods to a given arbovirus, but these experiments are often conducted in real time during outbreaks, rather than with preparedness in mind. We conducted a systematic review of reported mosquito-arbovirus competence experiments, screening 570 abstracts to arrive at 265 studies testing in vivo arboviral competence. We found that more than 90% of potential mosquito-virus combinations are untested in experimental settings and that entire regions and their corresponding vectors and viruses are undersampled. These knowledge gaps stymie outbreak response and limit attempts to both build and validate predictive models of the vector-virus network.
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Aedes , Infecciones por Arbovirus , Arbovirus , Culicidae , Animales , Humanos , Arbovirus/fisiología , Mosquitos Vectores , Infecciones por Arbovirus/epidemiología , Brotes de EnfermedadesRESUMEN
The growing threat of vector-borne diseases, highlighted by recent epidemics, has prompted increased focus on the fundamental biology of vector-virus interactions. To this end, experiments are often the most reliable way to measure vector competence (the potential for arthropod vectors to transmit certain pathogens). Data from these experiments are critical to understand outbreak risk, but - despite having been collected and reported for a large range of vector-pathogen combinations - terminology is inconsistent, records are scattered across studies, and the accompanying publications often share data with insufficient detail for reuse or synthesis. Here, we present a minimum data and metadata standard for reporting the results of vector competence experiments. Our reporting checklist strikes a balance between completeness and labor-intensiveness, with the goal of making these important experimental data easier to find and reuse in the future, without much added effort for the scientists generating the data. To illustrate the standard, we provide an example that reproduces results from a study of Aedes aegypti vector competence for Zika virus.
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Aedes , Infección por el Virus Zika , Virus Zika , Animales , Infección por el Virus Zika/epidemiología , Mosquitos Vectores , Brotes de EnfermedadesRESUMEN
Monitoring the prevalence and abundance of parasites over time is important for addressing their potential impact on host life histories, immunological profiles and their influence as a selective force. Only long-term ecological studies have the potential to shed light on both the temporal trends in infection prevalence and abundance and the drivers of such trends, because of their ability to dissect drivers that may be confounded over shorter time scales. Despite this, only a relatively small number of such studies exist. Here, we analysed changes in the prevalence and abundance of gastrointestinal parasites in the wild Soay sheep population of St. Kilda across 31 years. The host population density (PD) has increased across the study, and PD is known to increase parasite transmission, but we found that PD and year explained temporal variation in parasite prevalence and abundance independently. Prevalence of both strongyle nematodes and coccidian microparasites increased during the study, and this effect varied between lambs, yearlings and adults. Meanwhile, abundance of strongyles was more strongly linked to host PD than to temporal (yearly) dynamics, while abundance of coccidia showed a strong temporal trend without any influence of PD. Strikingly, coccidian abundance increased 3-fold across the course of the study in lambs, while increases in yearlings and adults were negligible. Our decades-long, intensive, individual-based study will enable the role of environmental change and selection pressures in driving these dynamics to be determined, potentially providing unparalleled insight into the drivers of temporal variation in parasite dynamics in the wild.
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Coccidios , Enfermedades Transmisibles , Enfermedades Gastrointestinales , Parasitosis Intestinales , Nematodos , Parásitos , Ovinos , Animales , Parasitosis Intestinales/epidemiología , Parasitosis Intestinales/veterinaria , Parasitosis Intestinales/parasitología , Oveja Doméstica , Enfermedades Gastrointestinales/epidemiología , Enfermedades Gastrointestinales/veterinariaRESUMEN
The world is rapidly urbanizing, inviting mounting concern that urban environments will experience increased zoonotic disease risk. Urban animals could have more frequent contact with humans, therefore transmitting more zoonotic parasites; however, this relationship is complicated by sampling bias and phenotypic confounders. Here we test whether urban mammal species host more zoonotic parasites, investigating the underlying drivers alongside a suite of phenotypic, taxonomic and geographic predictors. We found that urban-adapted mammals have more documented parasites and more zoonotic parasites: despite comprising only 6% of investigated species, urban mammals provided 39% of known host-parasite combinations. However, contrary to predictions, much of the observed effect was attributable to parasite discovery and research effort rather than to urban adaptation status, and urban-adapted species in fact hosted fewer zoonotic parasites than expected on the basis of their total parasite richness. We conclude that extended historical contact with humans has had a limited impact on zoonotic parasite richness in urban-adapted mammals; instead, their greater observed zoonotic richness probably reflects sampling bias arising from proximity to humans, supporting a near-universal conflation between zoonotic risk, research effort and synanthropy. These findings underscore the need to resolve the mechanisms linking anthropogenic change, sampling bias and observed wildlife disease dynamics.
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Interacciones Huésped-Parásitos , Parásitos , Animales , Animales Salvajes/parasitología , MamíferosRESUMEN
Within-year variation in infection is a ubiquitous feature of natural populations, but is determined by a complex interplay of environmental, parasitological and host factors. At the same time, co-infection is the norm in the wild. Longitudinal dynamics of co-infecting parasites may therefore be further complicated by covariation across multiple parasites. Here, we used fecal parasite egg and oocyst counts collected repeatedly from individually marked wild Soay sheep to investigate seasonal dynamics of six gastrointestinal parasite groups. Prevalence and abundance tended to be higher in spring and summer, and abundance was higher in lambs compared to adults. We found that within-year variation in highly prevalent strongyle nematode counts was dependent on adult reproductive status, where reproductive ewes had distinct dynamics compared to males and barren ewes. For similarly prevalent coccidia we found an overall peak in oocyst counts in spring but no differences among males, barren and pregnant ewes. Using multivariate mixed-effects models, we further show that apparent positive correlation between strongyle and coccidia counts was driven by short-term within-individual changes in both counts rather than long-term among-individual covariation. Overall, these results demonstrate that seasonality varies across demographic and parasite groups and highlight the value of investigating co-infection dynamics over time.
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The adaptive immune system is critical to an effective response to infection in vertebrates, with T-helper (Th) cells pivotal in orchestrating these responses. In natural populations where co-infections are the norm, different Th responses are likely to play an important role in maintaining host health and fitness, a relationship which remains poorly understood in wild animals. In this study, we characterised variation in functionally distinct Th responses in a wild population of Soay sheep by enumerating cells expressing Th-subset specific transcription factors and quantifying Th-associated cytokines. We tested the prediction that raised Th1 and Th2 responses should predict reduced apicomplexan and helminth parasite burdens, respectively. All measures of Th-associated cytokine production increased with age, while Th17- and regulatory Th-associated cytokine production increased more rapidly with age in males than females. Independent of age, sex, and each other, IL-4 and Gata3 negatively predicted gastro-intestinal nematode faecal egg count, while IFN-γ negatively predicted coccidian faecal oocyst count. Our results provide important support from outside the laboratory that Th1 and Th2 responses predict resistance to different kinds of parasites, and illustrate how harnessing specific reagents and tools from laboratory immunology will illuminate our understanding of host-parasite interactions in the wild.
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Parásitos/inmunología , Enfermedades Parasitarias/inmunología , Ovinos/sangre , Ovinos/inmunología , Ovinos/parasitología , Linfocitos T Colaboradores-Inductores/inmunología , Inmunidad Adaptativa , Animales , Citocinas/sangre , Heces/parasitología , Femenino , Factor de Transcripción GATA3/sangre , Factor de Transcripción GATA3/metabolismo , Interacciones Huésped-Parásitos , Interleucina-4/sangre , Masculino , Enfermedades Parasitarias/parasitología , Fenotipo , Pronóstico , Células TH1/inmunología , Células Th17/inmunología , Células Th2/inmunología , Factores de Transcripción/sangreRESUMEN
Ecologists increasingly recognise coinfection as an important component of emergent epidemiological patterns, connecting aspects of ecoimmunology, behaviour, ecosystem function and even extinction risk. Building on syndemic theory in medical anthropology, we propose the term 'synzootics' to describe co-occurring enzootic or epizootic processes that produce worse health outcomes in wild animals. Using framing from syndemic theory, we describe how the synzootic concept offers new insights into the ecology and evolution of infectious diseases. We then recommend a set of empirical criteria and lines of evidence that can be used to identify synzootics in nature. We conclude by exploring how synzootics could indirectly drive the emergence of novel pathogens in human populations.
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Coinfección , Enfermedades Transmisibles , Animales , Ecología , EcosistemaRESUMEN
Gastrointestinal (GI) helminths are common parasites of humans, wildlife, and livestock, causing chronic infections. In humans and wildlife, poor nutrition or limited resources can compromise an individual's immune response, predisposing them to higher helminth burdens. This relationship has been tested in laboratory models by investigating infection outcomes following reductions of specific nutrients. However, much less is known about how diet supplementation can impact susceptibility to infection, acquisition of immunity, and drug efficacy in natural host-helminth systems. We experimentally supplemented the diet of wood mice (Apodemus sylvaticus) with high-quality nutrition and measured resistance to the common GI nematode Heligmosomoides polygyrus. To test whether diet can enhance immunity to reinfection, we also administered anthelmintic treatment in both natural and captive populations. Supplemented wood mice were more resistant to H. polygyrus infection, cleared worms more efficiently after treatment, avoided a post-treatment infection rebound, produced stronger general and parasite-specific antibody responses, and maintained better body condition. In addition, when applied in conjunction with anthelmintic treatment, supplemented nutrition significantly reduced H. polygyrus transmission potential. These results show the rapid and extensive benefits of a well-balanced diet and have important implications for both disease control and wildlife health under changing environmental conditions.
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Nematospiroides dubius , Preparaciones Farmacéuticas , Animales , Suplementos Dietéticos , Interacciones Huésped-Parásitos , Ratones , MurinaeRESUMEN
Individuals are often co-infected with several parasite species, yet measuring within-host interactions remains difficult in the wild. Consequently, the impacts of such interactions on host fitness and epidemiology are often unknown. We used anthelmintic drugs to experimentally reduce nematode infection and measured the effects on both nematodes and the important zoonosis Sin Nombre virus (SNV) in its primary reservoir (Peromyscus spp.). Treatment significantly reduced nematode infection, but increased SNV seroprevalence. Furthermore, mice that were co-infected with both nematodes and SNV were in better condition and survived up to four times longer than uninfected or singly infected mice. These results highlight the importance of investigating multiple parasites for understanding interindividual variation and epidemiological dynamics in reservoir populations with zoonotic transmission potential.
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Nematodos , Parásitos , Enfermedades de los Roedores , Virus Sin Nombre , Animales , Anticuerpos Antivirales , Masculino , Ratones , Peromyscus , Enfermedades de los Roedores/epidemiología , Roedores , Estudios SeroepidemiológicosRESUMEN
Lay Summary: Competition often occurs among diverse parasites within a single host, but control efforts could change its strength. We examined how the interplay between competition and control could shape the evolution of parasite traits like drug resistance and disease severity.
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Toxoplasma gondii causes lifelong chronic infection in both feline definitive hosts and intermediate hosts. Multiple exposures to the parasite are likely to occur in nature due to high environmental contamination. Here, we present data of high seroprevalence and multiple T. gondii strain co-infections in individual bobcats (Lynx rufus). Unfrozen samples (blood, heart, tongue and faeces) were collected from 35 free ranging wild bobcats from Mississippi, USA. Toxoplasma gondii antibodies were detected in serum by the modified agglutination test (1:≥200) in all 35 bobcats. Hearts from all bobcats were bioassayed in mice and viable T. gondii was isolated from 21; these strains were further propagated in cell culture. Additionally, DNA was extracted from digests of tongues and hearts of all 35 bobcats; T. gondii DNA was detected in tissues of all 35 bobcats. Genetic characterisation of DNA from cell culture-derived isolates was performed by multiplex PCR using 10 PCR-RFLP markers. Results showed that ToxoDB genotype #5 predominated (in 18 isolates) with a few other types (#24 in two isolates, and #2 in one isolate). PCR-DNA sequencing at two polymorphic markers, GRA6 and GRA7, detected multiple recombinant strains co-infecting the tissues of bobcats; most possessing Type II alleles at GRA7 versus Type X (HG-12) alleles at GRA6. Our results suggest that individual bobcats have been exposed to more than one parasite strain during their life time.
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Coinfección/veterinaria , Lynx/parasitología , Toxoplasma/aislamiento & purificación , Toxoplasmosis Animal/epidemiología , Toxoplasmosis Animal/parasitología , Animales , Anticuerpos Antiprotozoarios/sangre , Antígenos de Protozoos/genética , Secuencia de Bases , Gatos , Chlorocebus aethiops , Coinfección/parasitología , ADN Protozoario/genética , Femenino , Genotipo , Masculino , Ratones , Mississippi/epidemiología , Polimorfismo Genético , Proteínas Protozoarias/genética , Estudios Seroepidemiológicos , Toxoplasma/clasificación , Toxoplasma/genética , Toxoplasmosis Animal/diagnósticoRESUMEN
Protozoal infections have been widely documented in marine mammals and may cause morbidity and mortality at levels that result in population level effects. The presence and potential impact on the recovery of endangered Hawaiian monk seals Neomonachus schauinslandi by protozoal pathogens was first identified in the carcass of a stranded adult male with disseminated toxoplasmosis and a captive monk seal with hepatitis. We report 7 additional cases and 2 suspect cases of protozoal-related mortality in Hawaiian monk seals between 2001 and 2015, including the first record of vertical transmission in this species. This study establishes case definitions for classification of protozoal infections in Hawaiian monk seals. Histopathology and immunohistochemistry were the primary diagnostic modalities used to define cases, given that these analyses establish a direct link between disease and pathogen presence. Findings were supported by serology and molecular data when available. Toxoplasma gondii was the predominant apicomplexan parasite identified and was associated with 100% of mortalities (n = 8) and 50% of suspect cases (n = 2). Incidental identification of sarcocysts in the skeletal muscle without tissue inflammation occurred in 4 seals, including one co-infected with T. gondii. In 2015, 2 cases of toxoplasmosis were identified ante-mortem and shared similar clinical findings, including hematological abnormalities and histopathology. Protozoal-related mortalities, specifically due to toxoplasmosis, are emerging as a threat to the recovery of this endangered pinniped and other native Hawaiian taxa. By establishing case definitions, this study provides a foundation for measuring the impact of these diseases on Hawaiian monk seals.