Rapid thermal immune acclimation in common musk turtles (<i>Sternotherus odoratus</i>)

Goessling, Jeffrey M.; Ward, Chad; Mendonça, Mary T.

doi:10.1002/jez.2252

Cited by 17 publications

(16 citation statements)

References 26 publications

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“…The observed shift in circulating leukocytes indicated that the experimental treatment was successful in eliciting an acute immune response across reproductive categories. The leukocyte response was similar to the observed cellular response to LPS treatment in chelonians (Goessling et al, 2017(Goessling et al, , 2019 and crocodilians (Merchant et al, 2006). The effect of LPS on plasma bactericidal capacity was not consistent with experimental predictions.…”

Section: Immune Responses To Lps Challengementioning

confidence: 55%

The metabolic response to an immune challenge in a viviparous snake, Sistrurus miliarius

Lind

Agugliaro

Farrell

2020

Journal of Experimental Biology

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Mounting an immune response may be energetically costly and require the diversion of resources away from other physiological processes. Yet, both the metabolic cost of immune responses and the factors that impact investment priorities remain poorly described in many vertebrate groups. For example, although viviparity has evolved many times in vertebrates, the relationship between immune function and pregnancy has been disproportionately studied in placental mammals. To examine the energetic costs of immune activation and the modulation of immune function during pregnancy in a nonmammalian vertebrate, we elicited an immune response in pregnant and non-pregnant pygmy rattlesnakes, Sistrurus miliarius, using lipopolysaccharide (LPS). Resting metabolic rate (RMR) was measured using flow-through respirometry. Immune function was examined using bactericidal assays and leukocyte counts. The RMR of pygmy rattlesnakes increased significantly in response to LPS injection. There was no statistically significant difference in the metabolic response of non-reproductive and pregnant snakes to LPS. Mean metabolic increments for pregnant females, non-reproductive females, and males were 13%, 18% and 26%, respectively. The ratio of heterophils to lymphocytes was elevated in response to LPS across reproductive categories; however, LPS did not impact plasma bactericidal ability in non-reproductive snakes. Although pregnant females had significantly higher plasma bactericidal ability compared with non-reproductive snakes prior to manipulation, their bactericidal ability declined in response to LPS. LPS administration also significantly reduced several litter characteristics, particularly when administrated relatively early in pregnancy. Our results indicate that immune performance is energetically costly and is altered during pregnancy, and that immune activation during pregnancy may result in tradeoffs that affect offspring in a viviparous reptile.

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Section: Immune Responses To Lps Challengementioning

confidence: 55%

The metabolic response to an immune challenge in a viviparous snake, Sistrurus miliarius

Lind

Agugliaro

Farrell

2020

Journal of Experimental Biology

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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%

“…Thermal acclimation and season also influence chelonian plasma antimicrobial activity, which generally decreases in winter, is maximal during the summer active period, and varies in response to acute temperature fluctuations based on acclimation status (Goessling et al, 2016; Goessling, Guyer, & Mendonça, 2017; Goessling, Koler, et al, 2017; Goessling et al, 2019; Refsnider, Palacios, Reding, & Bronikowski, 2015; Sandmeier et al, 2016; Schwanz, Warner, McGaugh, Di Terlizzi, & Bronikowski, 2011; Zimmerman, Paitz, et al, 2010). Changes in innate immunity can occur rapidly, for example, Zimmerman, Paitz, et al (2010) found that red‐eared slider plasma antibacterial capacity increased significantly over a 3‐week period during the month of May, then declined over a 2‐week period at the end of June.…”

Section: Discussionmentioning

confidence: 99%

“…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.…”

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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“…Further, complement and NAb levels could both be further upregulated once Salmonella enters the blood stream. In support of this idea, previous studies in reptiles have found that LPS exposure resulted in an increased bactericidal ability (Goessling, Ward, & Mendonca, ). If complement is responsible for the killing in the bactericidal assay, we may have expected to find a positive correlation between killing and avidity (Rajnavölgyi et al, ).…”

Section: Discussionmentioning

confidence: 59%

Mucosal antibody quantity but not avidity predicts likelihood of Salmonella infection in red‐eared slider turtles (Trachemys scripta)

et al. 2019

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Natural antibodies (NAbs) are polyreactive, have low avidity, and are a product of B‐1 cells. Evidence suggests that NAbs may play a key role in immune defense in turtles, as increased total mucosal antibodies are associated with a decreased number of extracellular intestinal parasites. However, it is unknown if this trend extends to other types of pathogens and if avidity of the NAb to the pathogen is a factor in protection. We examined the relationship between a common intracellular bacteria in turtles—Salmonella—and NAbs. Plasma and mucosal samples were taken from red‐eared slider turtles. We measured levels and avidity of antibodies that bound to lipopolysaccharide (LPS), a component of Salmonella cell wall. We examined the relationship between these measures and the ability of plasma to kill Salmonella as well as infection status. Higher mucosal antibody levels were significantly associated with a decrease in likelihood of infection with Salmonella; however, plasma antibody levels were not. There was a trend for bactericidal ability of the plasma to be positively correlated with plasma antibody levels bound to LPS, but not mucosal antibody levels. Avidity was not significantly related to either killing capacity or likelihood of infection suggesting that only increased quantity and not better binding is responsible for the decreased likelihood of infection. These findings suggest that NAb regulation was sufficient to isolate the infection to the gastrointestinal tract of the turtles, allowing it to be cleared with the mucus layer. Our results add further evidence that turtles use a general, nonspecific NAb response to combat pathogens.

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Rapid thermal immune acclimation in common musk turtles (Sternotherus odoratus)

Cited by 17 publications

References 26 publications

The metabolic response to an immune challenge in a viviparous snake, Sistrurus miliarius

The metabolic response to an immune challenge in a viviparous snake, Sistrurus miliarius

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

Mucosal antibody quantity but not avidity predicts likelihood of Salmonella infection in red‐eared slider turtles (Trachemys scripta)

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