The effect of environmental temperature on reptilian peripheral blood B cell functions

Palackdharry, Sarah; Sadd, Ben M.; Vogel, Laura A.; Bowden, Rachel M.

doi:10.1016/j.yhbeh.2016.10.008

Cited by 16 publications

(12 citation statements)

References 54 publications

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“…Temperature plays an important role in the general physiology of ectotherms, including the efficacy of the innate and acquired immune systems (Goessling et al, 2016; Goessling, Guyer, & Mendonça, 2017; Goessling, Ward, & Mendonça, 2019; Palackdharry, Sadd, Vogel, & Bowden, 2017). Eastern and ornate box turtle plasma antibacterial activity peaked between 30 and 40°C, corresponding to body temperatures attained during behavioral fever in this genus (do Amaral, Marvin, & Hutchison, 2002a; Monagas & Gatten, 1983).…”

Section: Discussionmentioning

confidence: 99%

“…We therefore expected EBT to have superior plasma antibacterial activity at a broader range of lower temperatures, and OBT to have optimal performance at higher temperatures. However, previous studies in ectothermic vertebrates indicate that different components of the immune system are variably temperature‐dependent, and thermal optima may vary for separate immune responses within the same organism (Butler et al, 2013; Palackdharry et al, 2017). The robust plasma antibacterial activity of OBT across a wide temperature range may represent a species‐specific trade‐off with other portions of the immune system, which would require further research to document and characterize.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2020

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Chelonians are one of the most imperiled vertebrate taxa and many species are increasingly threatened by disease, however, the immune response in this group is understudied. We quantified the innate immune response of eastern (Terrapene carolina; EBT) and ornate (Terrapene ornate; OBT) box turtles using plasma antibacterial activity assays. Plasma from both species abolished or significantly reduced the growth of all eight bacterial species evaluated, including Salmonella typhimurium, Escherichia coli, Enterobacter cloacae, Citrobacter freundi, Bacillus subtilis, Staphylococcus epidermidis, and Staphylococcus aureus. Bactericidal capacity was greater in OBT compared to EBT, and OBT plasma retained high antibacterial activities at a broader temperature range (20-40°C) compared to EBT (30-40°C). Plasma antibacterial activity was abolished following treatment with heat, protease, and ethylenediaminetetraacetic acid, indicating that complement is likely responsible for the observed effects. Further characterization of the box turtle immune response may provide insight into the importance of infectious diseases for species conservation, enabling the development of more efficient and effective population management strategies. K E Y W O R D S box turtle, chelonian, innate immunity, reptile, Terrapene

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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

et al. 2020

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“…Although temperature is a factor known to alter immune activity among ectotherms (Butler et al, 2013; Moretti et al, 2019; Wright & Cooper, 1981), unvarying BKA with respect to T body in U. stansburiana uniformis indicates certain immune pathways may be sufficiently maintained across their thermal range. Particular immune functions (e.g., phagocytosis, agglutination) can be tolerant of environmental temperature shifts that occur within and outside the natural climates of reptiles (Johnson et al, 1999; Palackdharry et al, 2017; Refsnider et al, 2015). Yet constant or fluctuating exposure to temperature extremes may become a stressor that in turn suppresses immunity (Fabrício‐Neto et al, 2019; Glassman & Bennett, 1978; McNally & Innis, 2020; Turton et al, 1997).…”

Section: Discussionmentioning

confidence: 99%

Glucocorticoids, energy metabolites, and immunity vary across allostatic states for plateau side‐blotched lizards (Uta stansburiana uniformis) residing in a heterogeneous thermal environment

2020

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Reptiles rely on thermal heat exchange to achieve body temperatures (Tbody) conducive to maintaining homeostasis. Diurnal changes in the thermal environment are therefore liable to influence allostatic mediation of survival processes (e.g., immunity) during environmental challenges or stressors. However, the extent to which Tbody prompts individual variation in physiology remains largely unexplored in reptiles. Our study tested how circulating energy‐mobilizing hormone, energy metabolites, and immunity can vary across basal and stress‐induced allostatic states for plateau side‐blotched lizards (Uta stansburiana uniformis) residing in a heterogeneous thermal environment. We collected baseline and acute stress blood samples from male lizards to compare changes in plasma corticosterone (CORT), glucose, and bacterial killing ability (BKA) in relation to each other and Tbody. We hypothesized each physiological parameter differs between allostatic states, whereby stress‐induced activity increases from baseline. At basal and stress‐induced states, we also hypothesized circulating CORT, glucose, and BKA directly correspond with each other and Tbody. We found both CORT and BKA increased while glucose instead decreased from acute stress. At basal and stress‐induced allostatic states, we found CORT to be directly related to Tbody while BKA was inversely related to CORT. We also found BKA and glucose were directly related at baseline, but inversely related following acute stress. Overall, these results demonstrate allostatic outcomes from acute stress in a free‐living reptile and the role of temperature in mediating energetic state and immunity. Future research on reptilian allostasis should consider multiple environmental conditions and their implications for physiological performance and survival.

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“…While flow cytometry is quick, generates the largest sample size ( Figure 2) and has been used in all current studies of phagocytosis by B cells (e.g. Gao et al, 2012;Li et al, 2006;Muñoz et al, 2014;Palackdharry et al, 2017;Zimmerman, Vogel, Edwards, et al, 2010), it cannot distinguish between cells with beads bound to the surface versus cells that have ingested beads.…”

Section: F I G U R Ementioning

confidence: 99%

Quantifying phagocytic lymphocytes in ectothermic vertebrates: A simplified technique for assessing immune function

et al. 2020

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Ecoimmunology assesses immune function across taxa within a physiological, ecological and evolutionary framework (Martin et al., 2011; Sheldon & Verhulst, 1996). While the toolbox of vertebrate ecoimmunologists is expanding (Brown et al., 2011; Martin et al., 2006), interpretations of immune parameters are often based on endothermic species (Davis et al., 2008; Murphy, 2012). One example is the interpretation of differential white blood cell counts (Davis & Durso, 2009; Davis et al., 2008). In general, lymphocyte numbers indicate adaptive immunity and shifts in lymphocyte to neutrophil/heterophil ratios are interpreted as changes in chronic stress and the balance between specific, induced immune functions and non-specific, constitutive responses (Davis et al., 2008; Goessling et al., 2015). Immune function within ectothermic vertebrates relies heavily on B1 lymphocytes, a subclass of B cells contributing to innate, rather than adaptive, immunity (Ochsenbein & Zinkernagel, 2000; Zimmerman, Vogel, & Bowden., 2010). B1 lymphocytes often constitute a significant portion of circulating lymphocytes (Zimmerman et al., 2017), suggesting that differential white blood cell counts may overestimate adaptive immunity within taxa of ectothermic vertebrates. Further, B1 lymphocytes directly control pathogens through phagocytosis, as demonstrated in all ectothermic species studied to date (fish, an amphibian and three reptiles:

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The effect of environmental temperature on reptilian peripheral blood B cell functions

Cited by 16 publications

References 54 publications

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

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

Glucocorticoids, energy metabolites, and immunity vary across allostatic states for plateau side‐blotched lizards (Uta stansburiana uniformis) residing in a heterogeneous thermal environment

Quantifying phagocytic lymphocytes in ectothermic vertebrates: A simplified technique for assessing immune function

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