Physiological and Ecological Correlates of the Cellular and Humoral Innate Immune Responses in an Insular Desert Bat: The Fish-Eating Myotis (Myotis vivesi)

Abstract

The immune response is affected by aridity, but it has been rarely examined in desert-dwelling bats. For two consecutive years, we examined the seasonal variation in the innate immune response of an insular desert bat, the fish-eating myotis (Myotis vivesi), in relation to its reproductive activity and ectoparasite load. We evaluated the reproductive activity based on external morphological traits and testosterone levels in the plasma for males and progesterone and estradiol for females. We injected phytohemagglutinin (PHA) into the footpads of the bats to estimate the innate cellular response, and we measured the bacterial killing ability (BKA) of the blood plasma to determine the innate humoral response. Both the external morphological traits and hormone levels indicate that the females were pregnant in spring and lactating in summer, and that the males were reproductively active in autumn, when mating probably occurred. The swelling response of the female and male bats was lower in spring. The BKA in the males did not vary seasonally; the BKA in the females varied seasonally but only in the first year of the study, with lower values in spring and summer. The BKA in spring was lower in the first year of the study, when the females appeared to be in early pregnancy, compared to the second year, when the females were in advanced pregnancy. The swelling increased as the body mass and body conditions of the males increased, but the BKA was not correlated with body mass or body condition in either sex. Ectoparasite abundance and prevalence did not vary among seasons. Ectoparasite abundance was not correlated with the PHA response in both sexes; it was not correlated with the BKA in females, but it was inversely correlated in males. Of the three hormones measured, only estradiol was correlated with the immune response: females with higher estradiol levels had a higher PHA response and BKA. Our findings indicate that the cellular and humoral innate immune responses of the fish-eating myotis varied throughout the year, following the seasonal reproductive pattern of the species. Our evaluation of the proximal factors affecting the expression of the immune response points to the potential immunoregulatory role of sex hormones and body mass.

Season and host-community composition inside roosts may affect host-specificity of bat flies

“…Milk-production and breast feeding are highly demanding in terms of energy and time invested, Ref. 35 and most females are not able to invest the same level of energy in grooming or avoidance, while also showing lower levels of cellular and innate immunity in this period 36 . In consequence, the largest prevalence and intensity of bat flies is recorded in the post-reproductive period (e.g.…”

Ecological drivers of host-specificity among bat flies: the importance of season and presence of multi-species bat community inside roosts

“…schreibersii), thus bat y populations synchronize their reproductive output with the hosts' reproduction 23 . The large groups of nursing females and their young make easy targets to exploit because their reproductive activity requires high effort (milk-production and breast feeding are highly demanding in terms of energy and time invested, 38 and most females are not able to invest the same level of energy in grooming or avoidance, while also showing lower levels of cellular and innate immunity in this period 39 ). In consequence, the largest prevalence and intensity of bat ies is recorded in the post-reproductive period (e.g.…”

Constitutive Innate Immunity of Migrant and Resident Long-Nosed Bats (Leptonycteris yerbabuenae) in the Drylands of Mexico

“…Cloud, MN, USA) using the spectrophotometric method described by Liebl and Martin [54] and French and Neuman-Lee [55] with some modifications. This Gram-negative bacteria stimulates the constitutive immune response [33], and it has previously been used in several bat studies [24][25][26][56][57][58]. The constitutive immunity is a combination of the humoral (e.g., natural antibodies, complement, and acute phase proteins) and cellular components (e.g., macrophages, heterophils, and thrombocytes) of the immune system that establish the first line of defense against invading pathogens.…”

“…Migratory male silver-haired bats (Lasionycteris noctivagans) have lower IgG levels, higher neutrophil levels, and higher neutrophil/lymphocyte ratios than resident males, yet the bacteria-killing ability (BKA) is similar between the migratory and resident males [22]. Similarly scarce are studies examining the link between reproductive activity and the immune response in bats in general [22][23][24][25]. The inflammatory responses of Myotis myotis [23] and M. vivesi [24] and the BKA of M. vivesi [24] are lower in pregnant females, and females have higher IgG concentrations during pregnancy and higher hemolysis during lactation in Myotis daubentonii [25].…”

“…Similarly scarce are studies examining the link between reproductive activity and the immune response in bats in general [22][23][24][25]. The inflammatory responses of Myotis myotis [23] and M. vivesi [24] and the BKA of M. vivesi [24] are lower in pregnant females, and females have higher IgG concentrations during pregnancy and higher hemolysis during lactation in Myotis daubentonii [25]. Non-reproductive males have higher concentrations of white blood cells in M. daubentonii [25], higher inflammatory responses in M. vivesi [24], and lower BKAs in Desmodus rotundus [26] than reproductive males.…”