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Wild sea turtle populations are currently listed as threatened and endangered as a result of both natural and anthropogenic factors. These include predation, disease, starvation, pollution, fisheries interaction and habitat degradation. Many natural threats including disease outbreaks have been exacerbated by human interaction. One disease of incre...
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... starvation, pollution, fisheries interaction and habitat degradation. Many natural threats including disease outbreaks have been exacerbated by human interaction (Dos Santos et al. 2010;Jones et al. 2016;Whilde et al. 2017). One disease of increasing threat to marine turtle populations worldwide is fibropapillomatosis (FP), a virulent cancer ( Fig. 1), thought to be triggered by a chelonian-specific herpes virus, ChHV5 (Herbst et al. 1995;Jones et al. 2016;Work et al. 2017;Morrison et al. ...
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... datasets primarily only contain visual records of tumour growth, so, if found to be an applicable approach, two-dimensional surface area measurement would then be retroactively applicable to a large cohort of patient data. Each tumour is assigned to a 'cluster' to enable analysis of tumour growth in designated locations on the turtle anatomy ( Fig. 1 and Table 2). Each cluster was photographed by a member of the Whitney Sea Turtle Hospital veterinary team on arrival, at each check-up and after each surgery. These images were analysed in ImageJ in order to plot the growth (surface area) and post-surgical regrowth of each cluster. Table 2. Body location and abbreviations of tumour ...
Citations
... However, this hypothesis that progression and regression relate to tumor morphology has not been further tested or verified in a controlled setting. Generally, FP tumor growth-rate patterns in hospitalized green turtles might have a role in disease severity and outcome [33]. To our knowledge, there have been no clinical studies on FP tumor growth rates with active differentiation of lesions based on morphological characteristics. ...
... Generally, FP tumor growth-rate patterns in hospitalized green turtles might have a role in disease severity and outcome [33]. To our knowledge, there have been no clinical studies on FP tumor growth rates with active differentiation of lesions based on morphological characteristics. ...
... Our study is based on previously described methodology that used ImageJ to track FP tumor growth rates in hospitalized individuals [33]. We calculated FP tumor growth based on measurements from photographs of nine rehabilitating green turtles (Cm 1-9) hospitalized at the UFWLSTH during 2015-2021. ...
Fibropapillomatosis (FP) is a neoplastic disease most often found in green turtles (Chelonia mydas). Afflicted turtles are burdened with potentially debilitating tumors concentrated externally on the soft tissues, plastron, and eyes and internally on the lungs, kidneys, and the heart. Clinical signs occur at various levels, ranging from mild disease to severe debilitation. Tumors can both progress and regress in affected turtles, with outcomes ranging from death due to the disease to complete regression. Since its official description in the scientific literature in 1938, tumor growth rates have been rarely documented. In addition, FP tumors come in two very different morphologies; yet, to our knowledge, there have been no quantified differences in growth rates between tumor types. FP tumors are often rugose in texture, with a polypoid to papillomatous morphology, and may or may not be pedunculated. In other cases, tumors are smooth, with a skin-like surface texture and little to no papillose structures. In our study, we assessed growth-rate differences between rugose and smooth tumor morphologies in a rehabilitation setting. We measured average biweekly tumor growth over time in green turtles undergoing rehabilitation at the University of Florida Whitney Laboratory Sea Turtle Hospital in St. Augustine, Florida, and compared growth between rugose and smooth tumors. Our results demonstrate that both rugose and smooth tumors follow a similar active growth progression pattern, but rugose tumors grew at significantly faster rates (p = 0.013) than smooth ones. We also documented regression across several examined tumors, ranging from −0.19% up to −10.8% average biweekly negative growth. Our study offers a first-ever assessment of differential growth between tumor morphologies and an additional diagnostic feature that may lead to a more comprehensive understanding and treatment of the disease. We support the importance of tumor morphological categorization (rugose versus smooth) being documented in future FP hospital- and field-based health assessments.
... Elevated chronic stress conditions resulting from human activities from highly urbanized areas can potentially suppress wildlife immune systems and trigger or exacerbate infection [73]. Sea turtle populations dwelling in urbanized coastal environments have been repeatedly found to present elevated FP prevalence [61,[74][75][76][77][78][79]. Habitat loss, human presence, fishing, boating, and encroachment resulting from proximity to anthropogenic areas can significantly stress sea turtle populations. ...
... River discharge from densely populated areas accounts for high amounts of pollution affecting nearshore water quality, showing a positive correlation with FP prevalence in green turtles [66,86]. The negative impact of environmental contaminants from wastewater on sea turtle health has been discussed since 1995 [59], and there has been increasing evidence and support on the matter [61,74,[76][77][78][79]84]. Findings from Brazil, for example, support the association between water quality and FP as degraded habitats reported higher prevalence (58.3%) compared to other areas of the country (15.4%) [74]. ...
... Herbst et al. observed that higher water temperatures experimentally promoted FP tumor growth, while lower temperatures delayed their onset [59]. Moreover, in rehabilitation facilities, green turtles have a higher chance of FP development during the warmer months [79]. Therefore, climate change and consequent extreme sea water temperatures are potentially additional anthropogenic contributions behind FP dynamics. ...
Emerging infectious diseases of wildlife have markedly increased in the last few decades. Unsustainable, continuous, and rapid alterations within and between coupled human and natural systems have significantly disrupted wildlife disease dynamics. Direct and indirect anthropogenic effects, such as climate change, pollution, encroachment, urbanization, travel, and trade, can promote outbreaks of infectious diseases in wildlife. We constructed a coupled human and natural systems framework identifying three main wildlife disease risk factors behind these anthropogenic effects: (i) immune suppression, (ii) viral spillover, and (iii) disease propagation. Through complex and convoluted dynamics, each of the anthropogenic effects and activities listed in our framework can lead, to some extent, to one or more of the identified risk factors accelerating disease outbreaks in wildlife. In this review, we present a novel framework to study anthropogenic effects within coupled human and natural systems that facilitate the emergence of infectious disease involving wildlife. We demonstrate the utility of the framework by applying it to Fibropapillomatosis disease of marine turtles. We aim to articulate the intricate and complex nature of anthropogenically exacerbated wildlife infectious diseases as multifactorial. This paper supports the adoption of a One Health approach and invites the integration of multiple disciplines for the achievement of effective and long-lasting conservation and the mitigation of wildlife emerging diseases.
... Temperatures in our Florida in-water dataset ranged from 24.7 • C to 27.3 • C, with an FP prevalence of 50-60% observed mostly around 26 • C. Studies witnessing higher water temperature effects on tumor growth of hospitalized sea turtles had a similar temperature range in rehabilitation tanks (23 • C to 27 • C) [60]. Further studies in rehab facilities observed the same pattern of a higher likelihood of green turtles' FP development during the warmer months [22]. This pattern could be attributable to pathogenic behavior, often showing a trend of higher growth rate and reproductive output at higher temperatures [25]. ...
... For sea turtles, the negative effects of environmental contaminants from wastewater were already discussed in 1995, as research indicated environmental pollutants greatly impact turtle health [19,76]. Sea turtle populations living in heavily polluted coastal environments were repeatedly found to present elevated FP prevalence [15,22,[28][29][30][31]50]. Research observed a substantially lower FP prevalence in open ocean sites compared to a coastal lagoon (Indian River Lagoon) which is heavily degraded by urban development and polluted from local drainage system inputs [4]. ...
Fibropapillomatosis is a neoplastic disease of marine turtles, with green turtles (Chelonia mydas) being the most affected species. Fibropapillomatosis causes debilitating tumor growths on soft tissues and internal organs, often with lethal consequences. Disease incidence has been increasing in the last few decades and the reason is still uncertain. The potential viral infectious agent of Fibropapillomatosis, chelonid herpesvirus 5, has been co-evolving with its sea turtle host for millions of years and no major mutation linked with increased disease occurrence has been detected. Hence, frequent outbreaks in recent decades are likely attributable to external drivers such as large-scale anthropogenic changes in the green turtle coastal marine ecosystem. This study found that variations in sea surface temperature, salinity, and nutrient effluent discharge from nearby rivers were correlated with an increased incidence of the disease, substantiating that these may be among the significant environmental drivers impacting Fibropapillomatosis prevalence. This study offers data and insight on the need to establish a baseline of environmental factors which may drive Fibropapillomatosis and its clinical exacerbation. We highlight the multifactorial nature of this disease and support the inclusion of interdisciplinary work in future Fibropapillomatosis research efforts.
... While sea turtle species' ranges and distributions have altered over the years, so too have those of their pathogens, including fibropapillomatosis (FP), now afflicting every sea turtle species in every ocean globally Farrell et al., 2018;Farrell, Yetsko, et al., 2021;Jones et al., 2016;Smith & Coates, 1938;Williams et al., 1994;Yetsko et al., 2021). We recently employed eDNA-based approaches to study the shedding of the virus (ChHV5) associated with this disease, and these results, combined with the results of this study, can provide insight into the health and population status of wild sea turtles inhabiting our study sites Yetsko et al., 2020). ...
... Indeed, some of the rehabilitation water and sand eDNA samples utilized for sea turtle detection in the present study, were also simultaneously utilized to quantify a viral pathogen of sea turtles . This pathogen is a turtlespecific ChHV5 virus and can result in the tumor disease, fibropapillomatosis (FP) (Chaves et al., 2017;Farrell et al., 2018;Farrell, Yetsko, et al., 2021;Page-Karjian et al., 2015Work et al., 2015Work et al., , 2020Yetsko et al., 2021). We previously adapted the eDNA methodology described here to successfully detect, quantify, and temporally track the concentration of ChHV5 DNA in water (qPCR and shotgun sequencing) and sand (qPCR only) samples in a controlled rehabilitation setting Yetsko et al., 2021). ...
Elusive aquatic wildlife, such as endangered sea turtles, are difficult to monitor and conserve. As novel molecular and genetic technologies develop, it is possible to adapt and optimize them for wildlife conservation. One such technology is environmental (e)DNA – the detection of DNA shed from organisms into their surrounding environments. We developed species‐specific green (Chelonia mydas) and loggerhead (Caretta caretta) sea turtle probe‐based qPCR assays, which can detect and quantify sea turtle eDNA in controlled (captive tank water and sand samples) and free ranging (oceanic water samples and nesting beach sand) settings. eDNA detection complemented traditional in‐water sea turtle monitoring by enabling detection even when turtles were not visually observed. Furthermore, we report that high throughput shotgun sequencing of eDNA sand samples enabled sea turtle population genetic studies and pathogen monitoring, demonstrating that non‐invasive eDNA techniques are viable and efficient alternatives to biological sampling (e.g. biopsies and blood draws). Genetic information was obtained from sand many hours after nesting events, without having to observe or interact with the target individual. This greatly reduces the sampling stress experienced by nesting mothers and emerging hatchlings, and avoids sacrificing viable eggs for genetic analysis. The detection of pathogens from sand indicates significant potential for increased wildlife disease monitoring capacity and viral variant surveillance. Together, these results demonstrate the potential of eDNA approaches to ultimately help understand and conserve threatened species such as sea turtles.
... Many of these ailments are due to anthropogenic interactions such as boat strikes, fishing line/hook entanglements, and ingestion of large quantities of plastic (Bjorndal et al. 1994;Chaloupka et al. 2008;Barreiros 2015;Eastman et al. 2020). Marine turtles, particularly green sea turtles (Chelonia mydas), also strand afflicted by virulent tumours, fibropapillomatosis (FP) (Foley et al. 2007;Chaloupka et al. 2008;Page-Karjian et al. 2014;Duffy et al. 2018;Farrell et al. 2018;Whilde et al. 2019;Yetsko et al. 2021), the incidence of which correlated to humaninduced alterations to inshore habitats (Van Houtan et al. 2010;Hargrove et al. 2016;Jones et al. 2016). Currently, surgery is the primary treatment for turtles with FP, but post-surgical tumour regrowth is common, prolonging rehabilitation (Page-Karjian et al. 2012;Duffy et al. 2018;Farrell et al. 2018;Whilde et al. 2019). ...
... Marine turtles, particularly green sea turtles (Chelonia mydas), also strand afflicted by virulent tumours, fibropapillomatosis (FP) (Foley et al. 2007;Chaloupka et al. 2008;Page-Karjian et al. 2014;Duffy et al. 2018;Farrell et al. 2018;Whilde et al. 2019;Yetsko et al. 2021), the incidence of which correlated to humaninduced alterations to inshore habitats (Van Houtan et al. 2010;Hargrove et al. 2016;Jones et al. 2016). Currently, surgery is the primary treatment for turtles with FP, but post-surgical tumour regrowth is common, prolonging rehabilitation (Page-Karjian et al. 2012;Duffy et al. 2018;Farrell et al. 2018;Whilde et al. 2019). As captive environments are more restrictive and simplistic than natural ones, longer rehabilitation periods further curtail turtles' abilities to exhibit their full range of natural behaviours. ...
Wild sea turtles that are admitted to turtle hospitals and rehabilitation centers suffering from illnesses and injuries may be held for extended periods of months to years, until they are recovered and ready for release back to the wild. During this time, natural behaviors may be limited, potentially adversely affecting the long-term rehabilitation success, however, little research has been carried out on the behavior of hospitalized sea turtles. Here we report that environmental enrichment can be an effective means of encouraging natural behaviors in turtles in hospital/rehabilitation and aquarium settings, but find that enrichment should be monitored and tailored to individual turtles to achieve positive results.
... First described in the scientific literature in the 1930 s [9], This disease is most prevalent in green turtles (Chelonia mydas), which also tend to be the most severely afflicted; however, FP has been documented, to a lesser extent, in all other species [5,7,10,11]. Fibropapillomatosis manifests as multiple tumours that primarily arise from the soft tissues of sea turtles, including: cutaneous, ocular and visceral tumours (fibromas, fibrosarcomas, mixofibromas and mixomas), which can vary in size and distribution [12,13]. These tumours can be severely debilitating; impairing vision, locomotion, feeding, predator evasion and other natural behaviours, and preventing affected turtles from providing their valuable ecosystem services and keystone species functions [1,11,12,14,15]. ...
... Fibropapillomatosis is one of the most significant transmissible diseases known in sea turtles and remains a persistent health concern despite conservation successes and significant growth of some affected populations [17]. The FP epizootic has been identified as one of the five major threats to sea turtles, which has been reflected in the renewed scientific interest in this disease in the last decade [5,7,11,13,[18][19][20][21][22][23][24][25][26]. Prevalence statistics reveal the rapid establishment of FP among many sea turtle populations, with reported increases from 13.3 to 42% in Florida, USA (2005-2016), 13.2 to 35.3% in northeastern Brazil (2012)(2013)(2014)(2015), 0% to 33% in Guinea-Bissau (2009-2019) and 0.6% to 35.2% in Texas, USA (2010USA ( -2018 [7,17,[27][28][29][30][31]. ...
The spreading global sea turtle fibropapillomatosis (FP) epizootic is threatening some of Earth’s ancient reptiles, adding to the plethora of threats faced by these keystone species. Understanding this neoplastic disease and its likely aetiological pathogen, chelonid alphaherpesvirus 5 (ChHV5), is crucial to understand how the disease impacts sea turtle populations and species and the future trajectory of disease incidence.
We generated 20 ChHV5 genomes, from three sea turtle species, to better understand the viral variant diversity and gene evolution of this oncogenic virus. We revealed previously underappreciated genetic diversity within this virus (with an average of 2035 single nucleotide polymorphisms (SNPs), 1.54% of the ChHV5 genome) and identified genes under the strongest evolutionary pressure. Furthermore, we investigated the phylogeny of ChHV5 at both genome and gene level, confirming the propensity of the virus to be interspecific, with related variants able to infect multiple sea turtle species. Finally, we revealed unexpected intra-host diversity, with up to 0.15% of the viral genome varying between ChHV5 genomes isolated from different tumours concurrently arising within the same individual.
These findings offer important insights into ChHV5 biology and provide genomic resources for this oncogenic virus.
... Fibropapillomatosis manifests as multiple tumours that primarily arise from the soft tissues of sea turtles including: cutaneous, ocular and visceral tumours, which can vary in size and distribution [12,13]. These tumours can be severely debilitating; impairing vision, locomotion, feeding, predator evasion and other natural behaviours, and preventing affected turtles from providing their valuable ecosystem services and keystone species functions [1,11,12,14,15]. ...
... Fibropapillomatosis is one of the most significant transmissible diseases known in marine turtles and remains a persistent health concern despite conservation successes and significant growth of some affected populations [17]. The FP epizootic has been identified as one of the five major threats to marine turtles, which has been reflected in the renewed scientific interest in this disease in the last decade [5,7,11,13,[18][19][20][21][22][23][24][25][26]. Prevalence statistics reveal the rapid establishment of FP among many sea turtle populations; with reported increases from 13.3 to 42% in Florida, USA (2005-2016), 13.2 to 35.3% in northeastern Brazil (2012)(2013)(2014)(2015), 0% to 33% in Guinea-Bissau and 0 to 35.2% in Texas, USA [7,17,[27][28][29][30][31]. ...
The spreading global sea turtle fibropapillomatosis (FP) epizootic is threatening some of Earth’s ancient reptiles, adding to the plethora of threats faced by these keystone species. Understanding this neoplastic disease, and its likely aetiological pathogen, chelonid alphaherpesvirus 5 (ChHV5), is crucial to understand how the disease impacts sea turtle populations and species and the future trajectory of disease incidence. We generated 20 ChHV5 genomes, from three sea turtle species, to better understand the viral variant diversity and gene evolution of this oncogenic virus. We revealed previously underappreciated genetic diversity within this virus (with an average of 2,035 single nucleotide polymorphisms [SNPs], 1.54% of the ChHV5 genome) and identified genes under the strongest evolutionary pressure. Furthermore, we investigated the phylogeny of ChHV5 at both genome and gene level, confirming the propensity of the virus to be interspecific with related variants able to infect multiple sea turtle species. Finally, we revealed unexpected intra-host diversity, with up to 0.15% of the viral genome varying between ChHV5 genomes isolated from different tumours concurrently arising within the same individual. These findings offer important insights into ChHV5 biology and provide genomic resources for this oncogenic virus.
... S ea turtle fibropapillomatosis (FP) is an epizootic (animal epidemic) tumor disease, affecting endangered sea turtles worldwide [1][2][3][4][5] . The disease is characterized by the formation of cutaneous and internal fibro-epithelial tumors, which can lead to debilitation and death. ...
... However, Koch's postulates to confirm its causative role have yet to be fulfilled, because ChHV5 is extremely difficult to isolate and propagate in the laboratory 3,5,[34][35][36][37] . Similarly, despite advances in FP tumor research 1,3,5,30,31,[38][39][40][41][42][43][44][45][46] , many open questions remain regarding the role of ChHV5 in driving FP tumorigenesis, including whether it is a cause of the disease or an opportunistic pathogen, exploiting immunocompromised tumor-afflicted turtles 3,5,31 . Interestingly, levels of ChHV5 (ChHV5 gB and UL30 gene DNA detected by qPCR, and ChHV5 glycoprotein H peptides detected by ELISA) in clinically healthy turtles are closer to that of FP tumors, than in non-tumored tissue of FP-afflicted turtles 34,47 . ...
Pathogen-induced cancers account for 15% of human tumors and are a growing concern for endangered wildlife. Fibropapillomatosis is an expanding virally and environmentally co-induced sea turtle tumor epizootic. Chelonid herpesvirus 5 (ChHV5) is implicated as a causative virus, but its transmission method and specific role in oncogenesis and progression is unclear. We applied environmental (e)DNA-based viral monitoring to assess viral shedding as a direct means of transmission, and the relationship between tumor burden, surgical resection and ChHV5 shedding. To elucidate the abundance and transcriptional status of ChHV5 across early, established, regrowth and internal tumors we conducted genomics and transcriptomics. We determined that ChHV5 is shed into the water column, representing a likely transmission route, and revealed novel temporal shedding dynamics and tumor burden correlations. ChHV5 was more abundant in the water column than in marine leeches. We also revealed that ChHV5 is latent in fibropapillomatosis, including early stage, regrowth and internal tumors; higher viral transcription is not indicative of poor patient outcome, and high ChHV5 loads predominantly arise from latent virus. These results expand our knowledge of the cellular and shedding dynamics of ChHV5 and can provide insights into temporal transmission dynamics and viral oncogenesis not readily investigable in tumors of terrestrial species.
... Examples of the use of species-specific PCR in marine biosecurity include application to the Atlantic wedge clam (Rangia cuneata), the soft-shell clam (Mya arenaria), and the Australian tubeworm (Ficopomatus enigmaticus; Zaiko et al. 2018). Therefore, it is evident that eDNA has already been successfully implemented in numerous scientific studies, including one of our two case studies, the fibropapillomatosis panzootic in green sea turtles (Chelonia mydas; Work et al. 2015, Chaves et al. 2017, Page-Karjian et al. 2017, Farrell et al. 2018, Yetsko et al. 2021. ...
... One pathogen of particular concern in relation to the conservation of endangered marine turtle species and the monitoring of harmful pathogens is the turtle-specific DNA virus, chelonid herpesvirus 5 (ChHV5; Chaves et al. 2017, Yetsko et al. 2021. This alphaherpesvirus has been identified as the most likely etiological agent of a devastating neoplastic disease, fibropapillomatosis, affecting all seven species of sea turtle, particularly juvenile green sea turtles (Chelonia mydas) found in tropical and subtropical oceans worldwide (Chaves et al. 2017, Farrell et al. 2018. Fibropapillomatosis can result in fatalities through both direct and indirect mechanisms. ...
Novel forensics-inspired molecular approaches have revolutionized species detection in the wild and are particularly useful for tracing endangered or invasive species. These new environmental DNA or RNA (eDNA or eRNA)-based techniques are now being applied to human and animal pathogen surveillance, particularly in aquatic environments. They allow better disease monitoring (presence or absence and geographical spread) and understanding of pathogen occurrence and transmission, benefitting species conservation and, more recently, our understanding of the COVID-19 global human pandemic. In the present article, we summarize the benefits of eDNA-based monitoring, highlighted by two case studies: The first is a fibropapillomatosis tumor-associated herpesvirus (chelonid herpesvirus 5) driving a sea turtle panzootic, and the second relates to eRNA-based detection of the SARS-CoV-2 coronavirus driving the COVID-19 human pandemic. The limitations of eDNA-or eRNA-based approaches are also summarized, and future directions and recommendations of the field are discussed. Continuous eDNA-or eRNA-based monitoring programs can potentially improve human and animal health by predicting disease outbreaks in advance, facilitating proactive rather than reactive responses.
... While advances in our understanding of the FP tumor disease epizootic in sea turtles continue to be made 10,28,33,[36][37][38][39][40][41][42][43] , many questions remain unanswered in relation to this enigmatic disease. There is virtually no molecular information about the relationship (e.g., primary/metastatic) between the numerous tumors, which can range from tens to hundreds, arising on a single individual turtle. ...
... No treatments exist for internal tumors, with current practice (including Florida Fish and Wildlife Conservation Commission guidelines) indicating euthanasia for such turtles, regardless of their health status otherwise 68 . Furthermore, surgical excision of external FP tumors often results in high rates of tumor regrowth/ recurrence 13,28,36,69 . Therefore, it is imperative that chemotherapeutic approaches are developed to augment surgical removal of external tumors and to provide first-line therapy for applicable internal tumors. ...
Sea turtle populations are under threat from an epizootic tumor disease (animal epidemic) known as fibropapillomatosis. Fibropapillomatosis continues to spread geographically, with prevalence of the disease also growing at many longer-affected sites globally. However, we do not yet understand the precise environmental, mutational and viral events driving fibropapillomatosis tumor formation and progression.
Here we perform transcriptomic and immunohistochemical profiling of five fibropapillomatosis tumor types: external new, established and postsurgical regrowth tumors, and internal lung and kidney tumors. We reveal that internal tumors are molecularly distinct from the more common external tumors. However, they have a small number of conserved potentially therapeutically targetable molecular vulnerabilities in common, such as the MAPK, Wnt, TGFβ and TNF oncogenic signaling pathways. These conserved oncogenic drivers recapitulate remarkably well the core pan-cancer drivers responsible for human cancers. Fibropapillomatosis has been considered benign, but metastatic-related transcriptional signatures are strongly activated in kidney and established external tumors. Tumors in turtles with poor outcomes (died/euthanized) have genes associated with apoptosis and immune function suppressed, with these genes providing putative predictive biomarkers.
Together, these results offer an improved understanding of fibropapillomatosis tumorigenesis and provide insights into the origins, inter-tumor relationships, and therapeutic treatment for this wildlife epizootic.
