Early swelling response to phytohemagglutinin is lower in older toads

Abstract

The effects of age on performance of life-history traits are diverse, but a common outcome is senescence, an irreversible deterioration of physical and physiological capabilities of older individuals. Immune response is potentially bound to senescence. However, little is known about immune response ageing in amphibians. In this work, we test the hypothesis that amphibian early immune response is reduced in older individuals. To this end, we captured adult natterjack toads (Epidalea calamita) and inoculated them with phytohemagglutinin, an innocuous protein that triggers a skin-swelling immune response whose magnitude is directly proportional to the ability of the individual to mount an immune response. We measured early swelling immune response (corresponding to an innate-response stage) hourly, for six hours, and we calculated the area under the curve (AUC) for each individual’s time series, as a measure of immune response magnitude incorporating time. We estimated toad age by means of phalanx skeletochronology. Swelling and AUC decreased with age. Therefore, in accordance with our predictions, early immune response seems subject to senescence in these toads. Reduced ability to get over infections due to senescence of immune respose might be—together with a worse functioning of other organs and systems—among the causes of lower survival of older specimens.

Age structure of a lizard along an elevational gradient reveals nonlinear lifespan patterns with altitude

“…2011 ). In fact, senescence often implies a deterioration of the immune system ( Zamora-Camacho and Comas 2018 ), which also leads to higher mortality due to pathogens and parasites. However, senescence is strongly determined by telomere length ( Haussmann and Marchetto 2010 ) and, in our study population, telomeres lengthen up to 4 years old, and then shorten ( Burraco et al.…”

Critical review of the phytohemagglutinin assay for assessing amphibian immunity

“…Only two studies have directly compared age and swelling responses from PHA, while two others compared development time and PHA response ( Abu Bakar et al , 2016 ; Zamora-Camacho and Comas, 2018 ). Abu Bakar et al (2016) found that PHA-induced oedema in Litoria aurea exposed to Bd was higher in adults than in either subadults or juveniles.…”

“…In general, larval immune systems are less developed and robust than adult immune systems, and aspects of the immune system are suppressed during metamorphosis in anurans, although much less is known about urodeles ( Rollins-Smith, 1998 ; Abu Bakar et al , 2016 ; Grogan et al , 2018 ). Another study on Epidalea calamita performed on adults exclusively found that swelling decreased with age, leading study authors to suggest that senescence may reduce immunocompetence after reaching adulthood ( Zamora-Camacho and Comas, 2018 ). Two studies looking at the relationship between development time and immunocompetence found that increased development time in response to stress is associated with reduced PHA response ( Gervasi and Foufopoulos, 2008 ; Seiter, 2009 ).…”

“…Body size variation within species may also affect PHA-related swelling, which experts have suggested may be due to either differing spleen size ( Fites et al , 2014 ; Vasconcelos-Teixeira et al , 2022 ) or the higher cost of immune activation in smaller individuals ( Venesky and Laskey, 2022 ). Six studies assessed the effect of conspecific body size on swelling response with mixed results: three studies reported no effect of body size on oedema ( Brown and Shine, 2014 ; Brown et al , 2015 ; Clulow et al , 2015 ; Zamora-Camacho and Comas, 2018 ); two studies found that increased body size was associated with increased swelling ( Brown et al , 2015 ; Titon et al , 2019 ); and one study found that decreased body size was associated with increased swelling ( Bakewell et al , 2021 ). Generally, increased body size would be expected to be associated with an increased immune response ( Fites et al , 2014 ; Vasconcelos-Teixeira et al , 2022 ; Venesky and Laskey, 2022 ).…”

“…Meanwhile, many other studies reported millimetres of swelling without providing a starting or ending thickness measure to allow comparison with percentage-based reporting ( Gilbertson et al , 2003 ; Gervasi and Foufopoulos, 2008 ; Seiter, 2009 ; Venesky et al , 2012 ; Young et al , 2014 ; Desprat et al , 2015 , 2017 ; Ceccato et al , 2016 ; Szuroczki et al , 2016 , 2019 ; Titon et al , 2016 ; Troïanowski et al , 2017 ; Wang et al , 2019 ; Zamora-Camacho, 2019 ; Zamora-Camacho et al , 2022 ). Other methodologies have been used less often; for example, Zamora-Camacho and Comas (2018) calculated the ‘area under the curve’, by integrating swelling response measurements over multiple time points.…”