Hormonal daily variation co-varies with immunity in captive male bullfrogs (Lithobates catesbeianus)

Titon, Stefanny Christie Monteiro; Titon, Braz; Assis, Vania Regina; Vasconcelos-Teixeira, Ronyelle; Neto, Patrício Getúlio Garcia; Lima, Alan Siqueira; Ferreira, Letícia de França; Fernandes, Pedro Augusto Carlos Magno; Gomes, Fernando Ribeiro; Markus, Regina Pekelmann

doi:10.1016/j.ygcen.2020.113702

Cited by 19 publications

(8 citation statements)

References 71 publications

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“…Interestingly, differences in the BKA for the saline group were observed in experiment 4, in which increased BKA values were described at night. Daily variations in immunity are described for mammals ( Scheiermann et al., 2013 ) and frogs ( Titon et al., 2021 ), with increased immune functions observed at night for nocturnal species. Thus, increased BKA in the saline group at 10 p.m. could be associated with circadian variation in R. icterica toads.…”

Section: Discussionmentioning

confidence: 99%

Short-term stressors and corticosterone effects on immunity in male toads (Rhinella icterica): A neuroimmune-endocrine approach

Titon

Gomes

et al. 2021

Brain, Behavior, & Immunity - Health

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In the last decades, it is growing the idea that stress-induced immunomodulation is bimodal: with acute stress associated with enhancing effects while chronic stress with suppressive effects. However, the immune-endocrine interactions and its implications are often overlooked in ectotherms. We investigated the impact of corticosterone (CORT) treatment and short-term stressors on CORT plasma levels and the immunity of male toads ( Rhinella icterica ), using three distinct protocols: restraint, immune challenge (with lipopolysaccharide, LPS), and CORT transdermal application (TA). Our results showed increased CORT and neutrophil: lymphocyte ratio (NLR) regardless of the stress input (restraint, LPS challenge) or CORT TA. In the meantime, the bacterial killing ability (BKA) was not affected by any treatment, suggesting this immune parameter might be a more constitutive and robust response. Interestingly, the cellular immune response showed distinct patterns. Increased phagocytosis of blood leukocytes and phytohemagglutinin edema followed LPS and CORT TA (15 μg), respectively. In contrast, the phagocytosis of peritoneal leukocytes decreased after CORT TA (1 and 10 μg), indicating that short-term increases in CORT levels might impair local immune function. Such differences in cellular immunity might also be associated with CORT doses or the interaction between CORT and other immune mediators, such as melatonin, testosterone, and cytokines. Overall, our results highlight the immune-enhancing effects of the acute stress response and CORT TA, and the complexity of the immune-endocrine interaction in anurans. It also highlights the relevance of investigating distinct contexts for CORT increase arising from different situations, as well as diverse immune components for a better understanding of the stress-induced immunomodulation.

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Section: Discussionmentioning

confidence: 99%

Short-term stressors and corticosterone effects on immunity in male toads (Rhinella icterica): A neuroimmune-endocrine approach

Titon

Gomes

et al. 2021

Brain, Behavior, & Immunity - Health

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“…Usually, immune responses have a short time scale. For example, under physiological stress, the bactericidal activity in plasma responds relatively quickly (within 15 to 24 h) [ 59 , 60 ], and the white blood cell levels respond within one to two hours under acute stress [ 61 , 62 ]. These immunoassays are applied in ecoimmunology or macroimmunology to help us understand the process of disease epidemiology and the adaptive response of immune function to the environment and on a specific spatial scale [ 63 ].…”

Section: Discussionmentioning

confidence: 99%

Reference Intervals in Combined Veterinary Clinical Examinations of Male Black-Spotted Pond Frogs (Pelophylax nigromaculatus)

Park

Kim

2021

Animals

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In conservation physiology, analyzing the physiological response of an organism to understand its ability to adapt to environmental changes is a key technique in establishing a successful conservation strategy. Veterinary clinical examinations determine the physiological condition of animals accurately and safely, and this examination is synergistic when combined. The accuracy and safety of a clinical examination makes it advantageous for use in amphibians with high species diversity and numerous endangered species. However, it is necessary to establish a reference interval (RI) for precise interpretations and identification of animals with abnormalities through individual unit testing. We have established RIs for the immunity, serum components, bone mineral density (BMD), and body composition of black-spotted pond frogs (Pelophylax nigromaculatus). Black-spotted pond frogs are a common species and are widely distributed in East Asia, with suitable characteristics for environmental monitoring. Serum was extracted from 151 male frogs to establish the RI for bacterial killing ability in order to represent immunity. We also used the serum to establish an RI of ten additional serum components to determine the nutritional status, organ function status, body osmotic pressure, and homeostasis conditions. The BMD and three body composition measures for diagnosing food intake status and nutritional condition were measured using dual energy X-ray absorptiometry. The RI was recorded as the mean ± standard deviation, median, first (25%) to third (75%) quantile range, 95% confidence interval of the mean and median, and the 95% percentile (2.5%–97.5% range) of all components. The use of combined clinical veterinary examinations aids our understanding of the physiological conditions of an individual according to biotic and abiotic factors on a complex spatiotemporal scale in an ecosystem.

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“…The phagocytosis assay was performed only for the toads from the experimental T manipulation, according to [42,53]. The leucocytes were isolated from 150 µl of blood.…”

Section: Methodsmentioning

confidence: 99%

“…Interestingly, increased inflammatory response was observed in T-treated adult male treefrogs, particularly in individuals with a higher body mass [46], suggesting that body condition can modulate the trade-offs between T and immunity. Also, plasma T levels and immune function positively covary under laboratory conditions in Lithobates catesbeianus [42]. These studies point to T-induced immune stimulation in anurans, contrasting with the data from a meta-analysis across several vertebrate species suggesting that T has immunosuppressive effects [3].…”

Section: Introductionmentioning

confidence: 99%

Testosterone immunomodulation in free-living and captive Rhinella icterica male toads

Titon

Assis

et al. 2023

Phil. Trans. R. Soc. B

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Testosterone (T) regulates immune function, with both immunostimulatory and immunosuppressive effects on several vertebrates. We investigated the covariation between plasma T and corticosterone (CORT) levels and immunity (plasma bacterial killing ability (BKA), and neutrophil to lymphocyte ratio (NLR)) in free-living Rhinella icterica male toads inside and outside the reproductive season. We found an overall positive correlation between steroids and immune traits, with toads during the reproductive season displaying increased T, CORT and BKA. We also investigated the T transdermal application effects on T, CORT, phagocytosis of blood cells, BKA and NLR in captive toads. Toads were treated with T (1, 10 or 100 µg) or vehicle (sesame oil) for eight consecutive days. Animals were bled on the first and eighth days of treatment. Increased plasma T was observed on the first and last day of T-treatment, while increased BKA was observed following all T doses on the last day, with a positive correlation between T and BKA. Plasma CORT, NLR and phagocytosis increased on the last day for all T-treated and vehicle groups. Overall, we demonstrated a positive covariation between T and immune traits in the field and T-induced augmented BKA in captive toads, indicating a T immunoenhancing effect in R. icterica males. This article is part of the theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’.

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Hormonal daily variation co-varies with immunity in captive male bullfrogs (Lithobates catesbeianus)

Cited by 19 publications

References 71 publications

Short-term stressors and corticosterone effects on immunity in male toads (Rhinella icterica): A neuroimmune-endocrine approach

Short-term stressors and corticosterone effects on immunity in male toads (Rhinella icterica): A neuroimmune-endocrine approach

Reference Intervals in Combined Veterinary Clinical Examinations of Male Black-Spotted Pond Frogs (Pelophylax nigromaculatus)

Testosterone immunomodulation in free-living and captive Rhinella icterica male toads

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