Interplay among steroids, body condition and immunity in response to long-term captivity in toads

Abstract

Stressful experiences can promote harmful effects on physiology and fitness. However, stress-mediated hormonal and immune changes are complex and may be highly dependent on body condition. Here, we investigated captivity-associated stress effects, over 7, 30, 60, and 90 days on plasma corticosterone (CORT) and testosterone (T) levels, body index, and innate immunity (bacterial killing ability and phagocytosis of peritoneal cells) in toads (Rhinella icterica). Toads in captivity exhibited elevated CORT and decreased T and immunity, without changes in body index. The inter-relationships between these variables were additionally contrasted with those obtained previously for R. schneideri, a related species that exhibited extreme loss of body mass under the same captive conditions. While T and phagocytosis were positively associated in both species, the relationship between CORT and bacterial killing ability was dependent on body index alterations. While CORT and bacterial killing ability were positively associated for toads that maintained body index, CORT was negatively associated with body index in toads that lost body mass over time in captivity. In these same toads, body index was positively associated with bacterial killing ability. These results demonstrate that steroids-immunity inter-relationships arising from prolonged exposure to a stressor in toads are highly dependent on body condition.

Time-related immunomodulation by stressors and corticosterone transdermal application in toads

“…Meanwhile, for the individuals in the field displaying high baseline CORT, we observed a tendency to decrease CORT plasma levels following 24h restraint. These toads were already displaying high CORT in the field probably due to reproductive behavior (calling activity) [27], precluding the assessment of increased CORT values 24h post-restraint [11]. Moreover, the trend to decreased CORT 24h post-restraint in these toads also corroborates the observation that the peak of GC release in response to restraint occurs before 24h of exposure to this stressor.…”

“…Toads displaying high CORT levels in the field (those exhibiting calling behavior at the moment of capture [27]) showed a tendency to decrease CORT after restraint for 24h (S1 Table, P = 0.082, Fig 1A). Meanwhile, toads characterized by low CORT levels at time 0h (before initiating restraint) showed increased CORT plasma levels after 1 and 24h post-restraint (S1 Table, P = 0.003, Fig 1B).…”

“…In amphibians an array of stress protocols have been used in order to investigate stress-induced CORT changes, including restraint, captivity and exogenous CORT administration [12,20–27], with recent studies also investigating stress-induced immunomodulation [12,20–23,27]. Restraint and captivity stress-induced changes include increased CORT along with both immune- enhancing or suppressive effects in anurans, depending on the studied immune parameter, as well as variation in stress duration and intensity [11,12,21,23,27]. The NLR, for example, increased following restraint without movement restriction, but even higher values were observed after restraint with movement restriction, indicating the NLR changes are correlated with intensity of the stressor [11].…”

“…Phagocytosis activity is also up-regulated following acute restraint and CORT exogenous application [12,23]. Additionally, changes in cellular and non-cellular aspects of immune response are not synchronized following long-term captivity in toads, with down-regulation of phagocytic activity and bacterial killing ability (BKA) being observed at different time-points of captivity [27,28]. Although evidences of stress-induced immunomodulation in anurans has been provided, they are generally derived from different combinations of experimental protocols (i.e., restraint, captivity, hormonal exogenous administration), and immune parameters, such as, NLR, phagocytosis, BKA, phytohemaglutinin (PHA) swelling response, among others [4,20,21,28,29].…”

Physiological condition of amphibians exposed to historical industrial pollution in a Brazilian biodiversity hotspot

“…To evaluate R. ornata individuals' health, we assessed morphological and physiological traits generally used as indicators of physiological condition and exposure to contaminants: individuals' body condition, proportional organ masses and white blood cell counts. Body condition, which ultimately expresses the mass-to-length relationship, is widely used as an indicator of individual nutritional condition and has been shown to be positively correlated with fecundity (Reading and Clarke, 1995), individual fitness (Jakob, Marshall, and Uetz, 1996) and habitat quality (Janin, Léna, and Joly, 2011), and negatively associated with chronic stress response (Titon et al, 2017). In turn, proportional increases in liver and kidneys masses have been shown to reflect increased detoxification function (e. g. Arrieta et al, 2004), whereas proportional 6 decrease in gonads has been shown to indicate reduced fertility (e. g. Rie et al, 2005).…”