Variation in the seasonal patterns of innate and adaptive immunity in the red-eared slider (Trachemys scripta)

Abstract

SUMMARYThe primary function of the immune system is to protect the organism from invading pathogens. In vertebrates, this has resulted in a multifaceted system comprised of both innate and adaptive components. The immune system of all jawed vertebrates is complex, but unlike the endothermic vertebrates, relatively little is known about the functioning of the ectothermic vertebrate immune system, especially the reptilian system. Because turtles are long-lived ectotherms, factors such as temperature and age may affect their immune response, but comprehensive studies are lacking. We investigated variation in immune responses of adult male and female red-eared sliders (Trachemys scripta) across the entire active season. We characterized seasonal variation in innate, cell-mediated and humoral components via bactericidal capacity of plasma, delayed-type hypersensitivity and total immunoglobulin levels, respectively. Results indicate that all immune measures varied significantly across the active season, but each measure had a different pattern of variation. Interestingly, temperature alone does not explain the observed seasonal variation. Immune measures did not vary between males and females, but immunoglobulin levels did vary with age. This study demonstrates the highly dynamic nature of the reptilian immune system, and provides information on how biotic and abiotic factors influence the immune system of a long-lived ectotherm.

State-dependent physiological maintenance in a long-lived ectotherm, the painted turtle (Chrysemys picta)

“…Painted turtles showed marked seasonal fluctuations in immune function, consistent with findings on other reptiles (Zapata et al, 1992;Muñoz and de la Fuente, 2004;Zimmerman et al, 2010). Several components of immune function were reduced during hibernation and in the spring.…”

“…Although we found no correlations between immune function and hemogregarine infection, we cannot rule out the possibility of hemogregarines or unmeasured pathogens contributing to age-related immune patterns. The absence of lysis and any age effect on agglutination in response to foreign antigens in painted turtles contrasts with research in other reptiles, which has demonstrated robust lytic activity against foreign antigens [crocodiles (Merchant and Britton, 2006); garter snakes (Sparkman and Palacios, 2009)] and increasing antibody activity with age [water pythons (Madsen et al, 2007); red-eared sliders (Zimmerman et al, 2010)]. It is possible that similar patterns may occur in painted turtles during the main active season (summer), if immune activity is more robust at that time.…”

“…Whereas immune function and cellular maintenance are generally depressed by reproductive effort (Zuk and Stoehr, 2002;Alonso-Alvarez et al, 2004a;Martin et al, 2006;Martin et al, 2008), sex differences in these measures are not consistently found (e.g. Zuk and Stoehr, 2002;Hausmann et al, 2005;Bertrand et al, 2006;Martin et al, 2006;Beldomenico et al, 2008;Zimmerman et al, 2010). Instead, sex, season, reproductive state, prior pathogen exposure, and recent stress may interact to produce complicated patterns in immune function between the sexes, making it difficult to predict sex differences over more limited sampling efforts (Beldomenico et al, 2008;Davis et al, 2008).…”

“…Physiological maintenance in a long-lived ectotherm Physiological maintenance has been widely studied in birds, mammals and invertebrate model systems, but much less is known about maintenance in ectothermic vertebrates [e.g. reptiles (Saad and El Ridi, 1988;Patnaik, 1994;Nelson and Demas, 1996;Zapata et al, 1992;Muñoz and de la Fuente, 2004;Madsen et al, 2007;Martin et al, 2008;Pitol et al, 2008;Les et al, 2009;Paitz et al, 2009;Sparkman and Palacios, 2009;Zimmerman et al, 2010)]. Ectothermic vertebrates have traits that suggest physiological maintenance patterns should deviate from those seen in previously studied endothermic vertebrates.…”

Field Investigation of Innate Immunity in Passerine Birds in Suburban Chicago, Illinois, Usa

“…In particular, the assay measures different humoral and cellular components of constitutive innate immunity, which represents an organism's first defense against invading pathogens (Matson et al, 2005). Microbicidal assays have been used to study differences in constitutive innate immunity among vertebrate species (Matson et al, 2006a, b) and under different environmental conditions (Allen et al, 2009;Zimmerman et al, 2010), physiologic conditions (Forsman et al, 2010), and infection profiles (Wilcoxen et al, 2010b;Beechler, pers. comm.…”