An ecoimmunological approach to disease in tortoises reveals the importance of lymphocytes

Abstract

We quantified the severity of upper respiratory tract disease (URTD) and immunological metrics (differential white blood cell counts and bacteria‐killing ability of blood plasma) in relation to climatic variables in 20 populations of Mojave desert tortoise (Gopherus agassizii). Prevalence and infection intensity of Mycoplasma agassizii, an etiological agent of URTD, have previously been quantified for these populations (Weitzman et al. ). Immunological variables were reduced by principal component analyses and separated into cells involved in inflammation (PC1) and cellular functions mediated by lymphocytes and basophils (PC2). In population‐level models, the mean number of lymphocytes per individual was associated with mean annual number of days below freezing. Lymphocytes were also positively associated with mean infection intensity of M. agassizii. Additionally, prevalence of URTD was closely associated with PC1 (cells associated with inflammation). This suggests that at least two immunological strategies are involved in responding to M. agassizii, one that involves primarily lymphocytes and one that involves inflammatory mechanisms. Recent studies on immunology in Testudines suggest that a large proportion of lymphocytes in this taxon are similar to B‐1 lymphocytes of mammals and have phagocytic properties. Controlled experiments are needed to understand the disease mitigation of these lymphocytes in desert tortoises.

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

“…Repeated exposure to potentially pathogenic bacteria via the fecal‐oral route may explain the more robust plasma antibacterial ability of ornate box turtles against these organisms. This activity is similar to that observed in Komodo dragons (Merchant, Henry, et al, 2013), yellow‐bellied sliders ( Trachemys scripta ; Haskins, Hamilton, Jones, et al, 2017; Haskins, Hamilton, Stacy, Finger, & Tuberville, 2017), and eastern mud turtles ( Kinosternon subrubrum ; Cochran et al, 2018), and superior to values reported for red‐eared sliders (Zimmerman, Paitz, et al, 2010), common snapping turtles (Baker, Kessler, & Merchant, 2019), alligator snapping turtles (Baker, Kessler, & Merchant, 2019), gopher tortoises ( Gopherus polyphemus ; Goessling, Guyer, & Mendonça, 2016; Goessling, Guyer, & Mendonça, 2017; Goessling, Koler, et al, 2017; Sandmeier et al, 2016; Sandmeier et al, 2018) and prairie rattlesnakes (Baker & Merchant, 2018a).…”

“…However, heparin is the preferred anticoagulant for most chelonians, including box turtles, due to the occurrence of hemolysis in whole blood samples anticoagulated with EDTA (Heatley & Russell, 2010; Muro, Cuenca, Pastor, Vinas, & Lavin, 1998). Furthermore, many existing chelonian innate immune function studies (including those focused on complement activity) use plasma samples containing heparin at approximately 20 USP/ml (Baker, Kessler, Darville‐Bowleg, et al, 2019; Baker, Kessler, & Merchant, 2019; Beck et al, 2017; Cochran et al, 2018; Ferronato et al, 2009; Goessling et al, 2016; Goessling, Guyer, & Mendonça, 2017; Goessling, Koler, et al, 2017; Goessling et al, 2019; Haskins, Hamilton, Jones, et al, 2017; Haskins, Hamilton, Stacy, et al, 2017; Refsnider et al, 2015; Sandmeier et al, 2016, 2018). While our findings may be biased by the use of heparinized samples, they are comparable to the existing chelonian innate immune function literature, which also relies heavily upon this anticoagulant.…”

“…(e.g. Goessling, Guyer, & Mendonça, 2017; Sandmeier, Horn, & Tracy, 2016; Sandmeier, Weitzman, & Tracy, 2018), Chinese soft‐shelled turtles ( Pelodiscus sinensis ; e.g. Ji et al, 2019; Liu, Han, Chen, & Zhao, 2019; Shi et al, 2019), and, to a lesser extent, red‐eared sliders ( Trachemys scripta elegans ; e.g.…”

Complex immune responses and molecular reactions to pathogens and disease in a desert reptile (Gopherus agassizii)

“…It is also plausible that levels of transcription were also modulated by environmental or behavioral factors that were not addressed in this study (Boei et al, 2017). We did not quantify the activity levels, internal body temperatures, or metabolic rates for individual tortoises, but realize that temperature changes can have profound effects on metabolism and immunity by modulating important triggers and regulators of immune pathways (Ferguson, Kortet, & Sinclair, 2018;Sandmeier, Weitzman, & Tracy, 2018).…”

Host species, pathogens and disease associated with divergent nasal microbial communities in tortoises

“…This respiratory disease describes signs including nasal exudate and lesions on the nasal epithelium, with extreme cases resulting in lethargy or even death [ 22 ]. Disease and transmission are thought to be pathogen load-dependent, and they are associated with increased levels of M. agassizii [ 26 – 28 ]. A closely related microbe, M. testudineum , is also associated with tortoise URTD, but its role in disease is less studied or understood [ 29 – 31 ].…”