Investigation of multiple mortality events in eastern box turtles (Terrapene carolina carolina)

Abstract

Wildlife mortality investigations are important for conservation, food safety, and public health; but they are infrequently reported for cryptic chelonian species. Eastern box turtles (Terrapene carolina carolina) are declining due to anthropogenic factors and disease, and while mortality investigations have been reported for captive and translocated individuals, few descriptions exist for free-living populations. We report the results of four natural mortality event investigations conducted during routine health surveillance of three Illinois box turtle populations in 2011, 2013, 2014, and 2015. In April 2011, over 50 box turtles were found dead and a polymicrobial necrotizing bacterial infection was diagnosed in five survivors using histopathology and aerobic/anaerobic culture. This represents the first reported occurrence of necrotizing bacterial infection in box turtles. In August 2013, paired histopathology and qPCR ranavirus detection in nine turtles was significantly associated with occupation of moist microhabitats, identification of oral plaques and nasal discharge on physical exam, and increases in the heterophil count and heterophil to lymphocyte ratio (p < 0.05). In July 2014 and 2015, ranavirus outbreaks reoccurred within a 0.2km radius of highly-disturbed habitat containing ephemeral ponds used by amphibians for breeding. qPCR ranavirus detection in five individuals each year was significantly associated with use of moist microhabitats (p < 0.05). Detection of single and co-pathogens (Terrapene herpesvirus 1, adenovirus, and Mycoplasma sp.) was common before, during, and after mortality events, but improved sample size would be necessary to determine the impacts of these pathogens on the occurrence and outcome of mortality events. This study provides novel information about the causes and predictors of natural box turtle mortality events. Continued investigation of health, disease, and death in free-living box turtles will improve baseline knowledge of morbidity and mortality, identify threats to survival, and promote the formation of effective conservation strategies.

Plasma antibacterial activities in ornate (Terrapene ornata) and eastern box turtles (Terrapene carolina)

“…Immune function has not been well studied in turtles of the family Emydidae, despite their susceptibility to infectious diseases (ranavirus, Terrapene herpesvirus 1 & 2, Terrapene adenovirus, Mycoplasma sp.) that may threaten individual survival and population viability (Adamovicz et al, 2018; Johnson et al, 2008; Kane et al, 2017; Yonkers et al, 2015). Box turtles ( Terrapene spp .)…”

“…The two species also differ in habitat usage, with OBTs relying largely on prairie habitats and EBTs utilizing forested areas and adjacent fields (van Dijk, 2011; van Dijk & Hammerson, 2011). Disease‐related mortality events are reported more frequently in EBT compared to OBT, but it is unclear if this is due to differences in disease susceptibility, exposure to pathogens, or research effort (Adamovicz et al, 2018; Agha, Price, Nowakowski, Augustine, & Todd, 2017; Johnson et al, 2008).…”

Temperature affects the host hematological and cytokine response following experimental ranavirus infection in red-eared sliders (Trachemys scripta elegans)

“…This may be because transcription does not reflect true circulating cytokine concentration or the timing of sampling did not detect key changes that would improve the statistical models. Frog virus 3-like virus outbreaks in the wild have occurred in the relatively hotter months in North America of June and July [ 13 ], and mortality is likely influenced by both select host and pathogen factors. While ranavirus replication occurs across a range from 12–32°C with the highest growth at 30°C [ 6 ], the host immune response is also increased at the higher end of their preferred optimum temperature zone [ 19 , 46 ].…”

Intestinal B cells in the red‐eared slider turtle, Trachemys scripta: Anatomical distribution and implications for ecological interactions with pathogenic microbes

“…Many reptile species inhabit microbe‐rich environments, such as wetlands, which are also experiencing an increase in the presence of potential pathogens due to global climate change and human needs for land and natural resources (Derne, Weinstein, & Lau, ). Recent studies have identified numerous pathogens associated with mortality events in turtles, including necrotizing bacterial infections, frog virus‐3‐like ranavirus, terrapene herpesvirus 1, adenovirus, Mycoplasma , Salmonella, and Leptospira (Adamovicz et al, ; McKenzie et al, ; Rockwell, Thompson, Maddox, & Mitchell, ). Many of these pathogens are spread by contact with mucosal surfaces; thus, an understanding of threats to turtles and conservation efforts may be enhanced with a more detailed understanding of mucosal immune protection.…”